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481 uef.fi
PUBLICATIONS OF THE UNIVERSITY OF EASTERN FINLAND
Dissertations in Health Sciences
ISBN 978-952-61-2871-9ISSN 1798-5706
Dissertations in Health Sciences
PUBLICATIONS OF THE UNIVERSITY OF EASTERN FINLAND
LEENA MARIA JAUHIAINEN
DIET AND PERIODONTAL CONDITION- AN EPIDEMIOLOGICAL STUDY
The aim of this thesis was to study the role of single polyunsaturated fatty acids and diet quality based on Nordic food culture and Finnish dietary recommendations in
periodontal diseases among Finnish adults. In this study, no consistent associations were
observed between a daily intake of omega-3 or omega-6 polyunsaturated fatty acids or their ratios and gingival bleeding or periodontal
pocketing. However, the results suggested that a healthy diet may be beneficial in preventing
the development of infectious periodontal diseases such as gingivitis and periodontitis.
LEENA MARIA JAUHIAINEN
30886310_UEF_Vaitoskirja_NO_481_Leena_Jauhiainen_Terveystiede_kansi_18_09_10.indd 1 10.9.2018 15.36.27
Diet and Periodontal Condition
- an Epidemiological Study
LEENA MARIA JAUHIAINEN
Diet and Periodontal Condition
- an Epidemiological Study
To be presented by permission of the Faculty of Health Sciences, University of Eastern Finland for
public examination in Snellmania SN201, Kuopio, on Friday, October 12th 2018, at 14 noon
Publications of the University of Eastern Finland
Dissertations in Health Sciences
Number 481
Institute of Dentistry, Faculty of Health Sciences,
University of Eastern Finland
Kuopio
2018
Grano
Jyväskylä, 2018
Series Editors:
Professor Tomi Laitinen, M.D., Ph.D.
Institute of Clinical Medicine, Clinical Physiology and Nuclear Medicine
Faculty of Health Sciences
Associate Professor Tarja Kvist, Ph.D.
Department of Nursing Science
Faculty of Health Sciences
Professor Kai Kaarniranta, M.D., Ph.D.
Institute of Clinical Medicine, Ophthalmology
Faculty of Health Sciences
Associate Professor (Tenure Track) Tarja Malm, Ph.D.
A.I. Virtanen Institute for Molecular Sciences
Faculty of Health Sciences
Lecturer Veli-Pekka Ranta, Ph.D. (pharmacy)
School of Pharmacy
Faculty of Health Sciences
Distributor:
University of Eastern Finland
Kuopio Campus Library
P.O.Box 1627
FI-70211 Kuopio, Finland
http://www.uef.fi/kirjasto
ISBN (print): 978-952-61-2871-9
ISBN (pdf): 978-952-61-2872-6
ISSN (print): 1798-5706
ISSN (pdf): 1798-5714
ISSN-L: 1798-5706
III
Author’s address: Department of Periodontology/Institute of Dentistry/University of Eastern
Finland
KUOPIO
FINLAND
Supervisors: Professor Pekka Ylöstalo, DDS, Ph.D.
Department of Periodontology/Institute of Dentistry/University of Oulu
OULU
FINLAND
Professor Anna Liisa Suominen, DDS, Ph.D.
Department of Oral Public Health/Institute of Dentistry/University of Eastern
Finland
KUOPIO
FINLAND
Reviewers: Title of docent Mervi Gürsoy, DDS, Ph.D.
Department of Periodontology/Institute of Dentistry/University of Turku
TURKU
FINLAND
Title of docent Anu Ruusunen, Ph.D.
IMPACT Strategic Research Centre/Food and Mood Centre, School of
Medicine/Deakin University
VICTORIA
AUSTRALIA
Opponent: Professor Marja L. Laine, DDS, Ph.D.
Halitosis and Saliva Clinic/Department of Periodontology/Academic Centre
for Dentistry Amsterdam (ACTA)
AMSTERDAM
NETHERLANDS
IV
V
Jauhiainen, Leena
Diet and Periodontal Condition – an Epidemiological Study
University of Eastern Finland, Faculty of Health Sciences
Publications of the University of Eastern Finland. Dissertations in Health Sciences 481. 2018. 68 p.
ISBN (print): 978-952-61-2871-9
ISBN (pdf): 978-952-61-2872-6
ISSN (print): 1798-5706
ISSN (pdf): 1798-5714
ISSN-L: 1798-5706
ABSTRACT
Earlier studies have suggested that single nutrients have both beneficial (omega-3 polyunsaturated fatty acids and antioxidants, for example) and detrimental (saturated fats and sugar, for example) effects on periodontium, but the knowledge on whether whole diets have an effect on periodontium is still lacking. The aim of this thesis was to study whether single polyunsaturated fatty acids or diet quality indices based on Nordic food culture and Finnish dietary recommendations are associated with the presence and development of infectious periodontal diseases. Articles I, II and III were based on the cross-sectional data from the nationally representative Health 2000 Survey and manuscript IV on the longitudinal data from the Health 2000 and Health 2011 Surveys. Articles I and II included 30–79-year-old non-smokers (30–49 years, n=1210; 50–79 years, n=977), article III included 30–79-year-old daily smokers (30–49 years, n=704; 50–79 years, n=267) and manuscript IV included 30–49-year-old non-smokers and smokers (n=587). Information on polyunsaturated fatty acids and diet quality indices based on Nordic food culture and Finnish dietary recommendations was collected by a 128-item validated food frequency questionnaire and information on periodontal condition was based on a clinical oral health examination. In this study, no consistent associations were observed between a daily intake of omega-3 or omega-6 polyunsaturated fatty acids or their ratios and gingival bleeding or periodontal pocketing. In the cross-sectional data, diet quality indices based on Nordic food culture and Finnish dietary recommendations were found to be associated with less gingival bleeding among non-smokers with poor oral hygiene, whereas among daily smokers, no consistent associations were observed. Among 30–49-year-old smoking subjects with good oral hygiene, a diet based on Finnish dietary recommendations associated with a lower number of teeth with deepened periodontal pockets. In the longitudinal data, non-adherence to diet quality indices based on Nordic food culture and Finnish dietary recommendations was associated with the deterioration of periodontal condition and the development of deepened periodontal pockets after an 11-year follow-up. The results of this study support the conception that a healthy diet is beneficial in preventing the development of infectious periodontal diseases such as gingivitis and periodontitis. National Library of Medicine Classification: QT 235, QU 90, WU 240, WU 242.
Medical Subject Headings: Cross-Sectional Studies; Diet; Epidemiologic Studies; Fatty Acids, Omega-3; Fatty
Acids, Omega-6; Fatty Acids, Unsaturated; Finland; Follow-Up Studies; Gingival Hemorrhage; Gingivitis;
Longitudinal Studies; Oral Hygiene; Periodontal Diseases; Periodontal Pocket; Periodontitis; Periodontium;
Smoking.
VI
VII
Jauhiainen, Leena
Ruokavalio ja hampaiden kiinnityskudosten kunto – epidemiologinen tutkimus
Itä-Suomen yliopisto, terveystieteiden tiedekunta
Publications of the University of Eastern Finland. Dissertations in Health Sciences 481. 2018. 68 s.
ISBN (print): 978-952-61-2871-9
ISBN (pdf): 978-952-61-2872-6
ISSN (print): 1798-5706
ISSN (pdf): 1798-5714
ISSN-L: 1798-5706
TIIVISTELMÄ
Aiemmissa tutkimuksissa on havaittu, että yksittäisillä ravintoaineilla on sekä hyödyllisiä (esimerkiksi omega-3 monityydyttymättömät rasvahapot ja antioksidantit) että haitallisia (esimerkiksi tyydyttyneet rasvahapot ja sokeri) vaikutuksia parodontiumiin eli hampaan ien- ja kiinnityskudoksiin, mutta näyttö ruokavalion kokonaisuuden merkityksestä parodontiumin kuntoon on vielä puutteellista. Tämän väitöstutkimuksen tavoitteena oli selvittää, onko monityydyttymättömien rasvahappojen saannilla ja pohjoismaiseen ruokakulttuuriin sekä suomalaisiin ravitsemussuosituksiin perustuvan ruokavalion noudattamisella yhteys parodontaalisairauksien esiintymiseen tai niiden kehittymiseen. Väitöstyön osajulkaisut I, II ja III perustuvat aikuisväestöä edustavan Terveys 2000 -tutkimuksen poikkileikkausaineistoon ja osajulkaisu IV Terveys 2000 - ja Terveys 2011 -tutkimusten seuranta-aineistoon. Osajulkaisut I ja II koostuivat 30–79-vuotiaista henkilöistä, jotka eivät olleet koskaan tupakoineet (30–49 vuotiaat, n=1210; 50–79 vuotiaat, n=977). Osajulkaisu III koostui 30–79-vuotiaista henkilöistä, jotka tupakoivat päivittäin (30–49-vuotiaat, n=704; 50–79-vuotiaat, n=267). Osajulkaisu IV koostui 30–49-vuotiaista tupakoivista ja tupakoimattomista henkilöistä (n=587). Tiedot monityydyttymättömien rasvahappojen saannista ja ruokavaliosta kerättiin validoidulla 128-kohtaisella ruoankäytön frekvenssikyselyllä, kun taas ienverenvuoto- ja ientaskutiedot perustuivat kliiniseen tutkimukseen. Yksittäisten omega-3 tai omega-6 rasvahappojen saannilla tai niiden suhteilla ei havaittu johdonmukaista yhteyttä ienverenvuodon tai syventyneiden ientaskujen esiintymiseen. Tupakoimattomia henkilöitä sisältävässä poikkileikkausaineistossa pohjoismaiseen ruokakulttuuriin ja ravitsemussuosituksiin perustuvaa ruokavaliota noudattavilla oli vähemmän ienverenvuotoa. Tämä yhteys tuli esille erityisesti niillä henkilöillä, joiden suuhygienia oli riittämätön. Tupakoivia henkilöitä sisältävässä poikkileikkausaineistossa terveellinen ruokavalio ei ollut yhteydessä ienverenvuotoon tai ientaskuhampaiden määrään, vaikkakin ravitsemussuosituksiin perustuvaa ruokavaliota noudattavilla 30–49-vuotiailla tupakoitsijoilla, joilla oli hyvä suuhygienia, näytti olevan vähemmän ientaskuhampaita. Seurantatutkimuksessa havaittiin, että ravitsemussuosituksista poikkeavaa ruokavaliota noudattavilla oli huonompi hampaiden kiinnityskudosten kunto ja heille kehittyi runsaammin ientaskuja 11 vuoden seurannan aikana. Tämän tutkimuksen mukaan terveellisen ruokavalion noudattaminen saattaa olla hyödyksi ientulehduksen ja hampaan kiinnityskudossairauksien kehittymisen ehkäisyssä. Luokitus: QT 235, QU 90, WU 240, WU 242.
Yleinen suomalainen asiasanasto: iensairaudet; ientulehdus; ikenet; omegarasvahapot; parodontiitti;
pitkittäistutkimus; poikittaistutkimus; rasvahapot; ruokavaliot; seurantatutkimus; Suomi; suuhygienia; suun
ja hampaiston taudit; suun terveys; tupakointi; verenvuoto.
VIII
IX
Acknowledgements
This study was carried out at the Institute of Dentistry, University of Eastern Finland between 2012–2018 and was conducted in co-operation with the National Institute for Health and Welfare (THL), especially with the organisations of the Health 2000 and 2011 Surveys and their expert groups. First and foremost, I deeply thank my main supervisor, Professor Pekka Ylöstalo for his devotion to this project. He has taugh me a lot about periodontology by helping me with my patients during my specialization studies and during our discussions about periodontology. Furthermore, he has tirelessly answered my questions about epidemiology and statistics, and especially he has been a great example in the excellence of scientific writing. Likewise, I express my warmest gratitude to my second supervisor, Professor Liisa Suominen. I admire her excellence in statistics and I am deeply grateful for her contribution to the statistical work of this thesis. From time to time during this process, I have been very tired and during those days Professor Suominen encouraged me to take a small break from the studies and advised to continue once feeling ready. This advice, together with Professor Suominen´s positive and constructive feedback during the whole process encouraged me to continue reaching my target. I am also grateful for Docent Anu Ruusunen and Docent Mervi Gürsoy for their work as reviewers of this thesis. Their constructive comments helped me to improve the quality of the thesis. Furthermore, I express my warm thanks to my co-authors, Professor Emeritus Matti Knuuttila, Docent Satu Männistö and Docent Noora Kanerva. Professor Knuuttila´s long experience in science brought new perspectives to each article and he helped me forward by thoroughly explaining his points of view. Docent Männistö´s and Docent Kanerva´s expertise in the science of nutrition has been essentially needed during the writing of the articles. I am honored that Professor Marja Laine agreed to act as opponent during the public examination. I also thank MA Merja Fleming for revising the language of three articles and one manuscript, and MA Sanna Turunen for revising the language of this thesis. Furthermore, I thank Coordinator Perttu Suhonen for his help with IT issues. It has been a great privilege to have friends and colleagues writing their own theses at the same time. I thank Ulla Kotiranta, Ritva Eskeli and Anniina Haro for all the profound conversations about studies and life, and their support during this process. I feel privileged to have such a good friend as Maija Tiihonen in my life. Since our studies in Oulu, we have spent countless memorable moments together. During the writing process, our weekly visits to the swimming hall (mainly to talk ) really helped me to relax. I warmly thank my family from the bottom of my heart for all their love and support. My younger sister Helena for always having such a positive attitude, for her constructive comments during discussions about various topics and for all the fun moments when travelling together. Finally, I express my deepest gratitude to my parents, Hellevi and
X
Paavo, for always being there for me. Their encouragement since I was a little girl made me believe in me and helped me to complete these studies. They set me an example of great attitude towards work by being the most hardworking people I know. In addition, their practical help during the writing process helped me to manage with my everyday tasks. This study was financially supported by personal grants from the Finnish Dental Society Apollonia, the Olvi-foundation and the Northern Savo Dental Society, which are gratefully acknowledged. Kuopio, August 2018 Leena Jauhiainen
XI
List of the original publications
This dissertation is based on the following original publications:
I Jauhiainen L, Ylöstalo P, Männistö S, Kanerva N, Knuuttila M and Suominen AL.
Periodontal condition in relation to intake of omega-3 and omega-6
polyunsaturated fatty acids. Journal of Clinical Periodontology 43: 901–908, 2016.
II Jauhiainen L, Suominen AL, Kanerva N, Männistö S, Knuuttila M and Ylöstalo P.
Periodontal pocketing and gingival bleeding in relation to Nordic diet – results
from a population-based survey. Journal of Clinical Periodontology 43: 1013–1023,
2016.
III Jauhiainen L, Suominen AL, Männistö S, Knuuttila M and Ylöstalo P. Periodontal
condition in relation to the adherence to nutrient recommendations in daily
smokers. Journal of Clinical Periodontology, 45: 636–649, 2018.
IV Jauhiainen L, Ylöstalo P, Knuuttila M, Männistö S, Kanerva N and Suominen AL.
Poor diet predicts periodontal disease in 11-year follow-up study. Submitted.
The publications were reprinted with the permission of the copyright owners.
XII
XIII
Contents
1 INTRODUCTION 1 2 REVIEW OF THE LITERATURE 3
2.1 Periodontal pathogenesis ....................................................................... 3 2.1.1 Neutrophils as part of innate immunity ......................................... 3 2.1.2 Oxidative stress in the periodontal pathogenesis .......................... 3 2.1.3 Smoking and neutrophil function .................................................... 4
2.2 The potential role of nutrition in the pathogenesis of periodontitis ............................................................................................. 5
2.2.1 Polyunsaturated fatty acids (PUFAs) ............................................... 5 2.2.2 Accelaration of oxidative stress and antioxidants ......................... 5
2.3 Earlier studies on single nutrients, foods/food groups or whole diet and periodontal diseases ................................................................ 6
2.3.1 Polyunsaturated fatty acids and periodontal condition ............... 6 2.3.2 Antioxidants and periodontal condition ........................................ 6 2.3.3 Foods/food groups and periodontal condition .............................. 7 2.3.4 Whole diet approach and periodontal condition .......................... 7
2.4 Different ways to measure dietary intakes, diet quality and nutrient status ........................................................................................ 18
2.4.1 Methods based on reporting ........................................................... 18 2.4.2 Biochemical measures ...................................................................... 20
3 AIMS OF THE STUDY 22 4 MATERIAL AND METHODS 23
4.1 Study populations ................................................................................. 23 4.1.1 The Health 2000 Survey ................................................................... 23 4.1.2 The Health 2011 Survey ................................................................... 24 4.1.3 Subjects .............................................................................................. 25
4.2 Methods .................................................................................................. 28 4.2.1 Periodontal condition ...................................................................... 28 4.2.2 Dietary assessments ......................................................................... 29 4.2.3 Confounding variables .................................................................... 31
4.3 Statistical methods ................................................................................ 39 4.4 Ethical considerations........................................................................... 39
5 RESULTS 40 5.1 Associations of polyunsaturated fatty acids with periodontal
condition ................................................................................................. 40 5.2 Associations of diets based on Nordic food culture and Finnish
dietary recommendations with periodontal condition ................... 42 5.3 Associations of diets based on Nordic food culture and Finnish
dietary recommendations with the number of teeth with deepened periodontal pockets after 11 years follow-up and with the development of periodontal disease .................................. 45
XIV
6 DISCUSSION 47
6.1 Diet and periodontal condition .......................................................... 47
6.1.1 Associations between polyunsaturated fatty acids and
periodontal condition ...................................................................... 47
6.1.2 Associations of diets based on Nordic food culture and
Finnish dietary recommendations with periodontal condition 48
6.1.3 Associations of diets based on Nordic food culture and
Finnish dietary recommendations with periodontal disease
development and future periodontal condition .......................... 49
6.2 Possible explanations for the findings ............................................... 49
6.3 Methodological considerations ........................................................... 51
6.3.1 Study design ..................................................................................... 51
6.3.2 Variables ............................................................................................ 52
6.4 Clinical implications and future perspectives .................................. 55
7 CONCLUSION 56
REFERENCES 57
ORIGINAL PUBLICATIONS (I–IV) 69
XV
Abbreviations
AA Arachidonic acid
AHEI Alternate Healthy
Eating Index
ALA Alphalinoleic acid
α-carotene Alpha-carotene
α-linoleic acid Alpha-linoleic acid
ASA Acetylsalicylic acid
α-tocopherole Alpha-tocopherole
β–carotene Beta-carotene
β–cryptoxanthin Beta-cryptoxanthin
BMI Body mass index
BOP Bleeding on
probing
BSDS Baltic Sea Diet
Score
CAL Clinical attachment
level/loss
CI Confidence
interval
COX Cyclooxygenase
CRP C-reactive protein
DFDBA Demineralized
freeze-dried bone
allograft
DHA Docosahecsaenoic
acid
DPA Docosapentaenoic
acid
DQI Diet Quality Index
EPA Eicosapentaenoic
acid
E% Percentage of the
total energy intake
Fc-γ Fc-gamma
FFQ Food frequency
questionnaire
GCF Gingival crevice
fluid
HbA1c Hemoglobin A1c
HDL High-density
lipoprotein
HEI Healty Eating
Index
Hs-CRP High-sensitivity C-
reactive protein
IL-6 Interleukin 6
IL-1β Interleukin 1-beta
IL-10 Interleukin 10
IRR Incidence rate ratio
LA Linoleic acid
LDL Low-density
lipoprotein
LTB4 Leukotriene B4
MCP-3 Monocyte
chemoattractant
protein-3
MDS Mediterranean Diet
Score
XVI
MMP Matrix
metalloproteinase
MUFA Monounsaturated
fatty acids
NADPH Nicotinamide
adenine
dinucleotide
phosphatase
oxidase
NFI Nordic Food Index
NF-κB Nuclear factor
kappa-beta
NHANES National Health
and Nutrition
Examination
Survey
NSAID Nonsteroidal anti-
inflammatory
drugs
NTx N-terminal
telopeptide
8-OHdG 8-hydroxy-2-
deoxyguoanosine
PBMCs Peripheral blood
mononuclear cells
PD Pocket depth
PGE2 Prostaglandin E2
PRR Prevalence rate
ratio
PUFA Polyunsaturated
fatty acid
PMNs Polymor-
phonuclear
neutrophilic
leucocytes
RANKL Receptor activator
of nuclear factor
kappa-Β ligand
RCT Randomized
controlled trial
RFDS Recommended
Finnish Diet Score
ROS Reactive oxygen
species
SFA Saturated fatty acid
TAOC Total antioxidant
capacity
TAS Total antioxidant
status
t-PAI1 Tissue
plasminogen
activator 1
TBARS Thiobarbituric acid
reactive
substances
USA United States
VCAM Vascular cell
adhesion molecule
WC Waist
circumference
1 Introduction
Periodontal diseases are common infectious and inflammatory diseases in the oral cavity
that affect a majority of the adult population. The prevalence of periodontitis varies
between 45–65 % according to national surveys made in the United States, the United
Kingdom and Finland (Morris et al. 2001, Knuuttila and Suominen-Taipale 2008, p. 51, Eke
et al. 2015) and worldwide 11% suffer from severe form of chronic periodontitis
(Kassebaum et al. 2014).
The accumulation of plaque on the tooth surface initiates inflammation in the supra-
alveolar soft tissues, which is clinically observed as gingival bleeding. If a periodontal
examination reveals a deepened periodontal pocket of ≥ 4 mm, gingival bleeding and
radiographical bone loss, periodontitis is diagnosed.
Although pathogenic bacteria in the dental plaque have an important role as initiators
and regulators of inflammation, both innate and acquired immunity play key roles in the
pathogenesis of periodontal diseases. Indeed, the destruction of connective tissue and
alveolar bone is mainly caused by immune response, of which principal target is good, to
kill bacteria (Nicu and Loos 2016). In particular, most of the tissue destruction seem to be
mediated by one cell type, the polymorphonuclear granulocytes, also called as neutrophils
(Summers et al. 2010). It is known that individual susceptibility to periodontal diseases
varies according to genetic background, but the susceptibility is modified by lifestyle and
health related risks, such as smoking, diabetes and obesity (Genco and Borgnakke 2013).
The term “Nordic diet” describes a healthy local diet that is based on Nordic food culture.
Initially, nutritionists in the Nordic countries raised the local perspective to counterpart the
fashionable Mediterranean diet consisting of components that are widely used in the
Mediterranean countries (Bere and Brug 2009). This led the University of Eastern Finland,
the Finnish Heart Association and the Finnish Diabetic Association to launch the Baltic Sea
Diet Pyramid in 2011 (Uusitupa and Schwab 2011). Based on this Pyramid, eating local
foods, including apples and berries; roots and cabbages; rye, oat and barley; low-fat milk
products; rapeseed oil; and salmon and freshwater fish; as well as avoiding red and
processed meat and keeping the consumption of alcohol as moderate, is recommended. In
order to study whether the local diet in the Nordic countries would have similar health
effects as the well-studied Mediterranean diet, the Baltic Sea Diet Score (BSDS) was
developed to measure quality of diet in epidemiological studies (Kanerva et al. 2014a). A
more comprehensive way to describe a healthy diet is to emphasize the dietary
recommendations at a more general level. An example of such a measurement in
epidemiological settings is the Recommended Finnish Diet Score (RFDS) (Kanerva et al.
2013a). The Nordic diet has been reported to associate inversely with low-grade
inflammation (Kanerva et al. 2013b, Kanerva et al. 2014b, Kolehmainen et al. 2015, Lankinen
et al. 2016).
The potential anti-inflammatory properties of different nutrients and the acceleration of
inflammation by others together with the systemic nature of periodontal inflammation have
raised a question whether a healthy diet improves periodontal health and a poor diet
compromises it. Several studies have suggested that single nutrients, such as antioxidants
and omega-3 polyunsaturated fatty acids (PUFAs) are related to periodontal health.
However, single nutrients are not eaten separately but as a part of a diet, and at the
2
moment, there is a lack of knowledge on the relation between whole diets and periodontal
health. The aim of this study was to provide evidence on the role that diets based on Nordic
food culture and Finnish dietary recommendations have on periodontal health.
3
2 Review of the Literature
2.1 PERIODONTAL PATHOGENESIS
2.1.1 Neutrophils as part of innate immunity
The synthesization of neutrophils takes place in the bone marrow from where they are
transferred into circulation and periodontal tissues with the aid of cytokines produced
during acute inflammation (Summers et al. 2010, Nicu and Loos 2016). Neutrophils are
primed during their first exposure with cytokines or bacterial antigens (Summers et al.
2010), after which they are ready to act against pathogens efficiently (Guthrie et al. 1984,
Colotta et al. 1992).
Neutrophils are specialized to phagocytose and kill microbes intracellularly. In order to
recognize microbes, they carry two main receptors on their surface: toll-like receptors bind
microbe-associated molecular patterns and Fc-γ-receptors bind immunoglobulins (Cooper
et al. 2013). After binding, a microbe is taken into a phagosome inside the cell membranes
(Nicu and Loos 2016) and is killed by granular proteases, which are activated with the aid
of reactive oxygen species (ROS) (Roos et al. 2003). ROS are generated by nicotinamide
adenine dinucleotide phosphatase oxidase (NADPH), which has four subunits, p47phox,
p67phox, p40phox and cytochrome b558. The subunits form an active NADPH-molecule when
stimulated by opsonized microbes or high amounts of chemochines. NADPH molecule
transfers electrons to molecular oxygen and generates superoxide, which can later convert
into hydrogen peroxide and hydroxyl radical (Roos et al. 2003, Chapple and Matthews
2007). This process is called the ”respiratory burst” of neutrophils (Cooper et al. 2013). In
addition, NADPH has a role as an activator of granular proteases (Reeves et al. 2002) and
extracellular traps, which are able to immobilize microbes, neutralize virulence factors and
kill microbes directly (Cooper et al. 2013). Due to the fact that neutrophils contain large
amounts of matrix metalloproteinases (MMPs) and ROS, it is essential that they are
removed safely from the site of inflammation (Nicu and Loos 2016). It has been suggested
that the release of extracellular traps may be a part of this process by initiating apoptosis
(Brinkmann et al. 2004).
To maintain tissue homeostasis, neutrophils react to the increased levels of pro-
inflammatory prostaglandin E2 (PGE2) adjacent to them, and consequently begin to
generate anti-inflammatory mediators called lipoxins, protectins, resolvins and maresins
(Gronert et al. 2001, Freire and Van Dyke 2013). These molecules initiate the resolution of
inflammation. In that process, both the number of infiltrating neutrophils and the levels of
pro-inflammatory cytokines reduce, and macrophages are stimulated to phagocytose
apoptotic neutrophils (Freire and Van Dyke 2013).
2.1.2 Oxidative stress in the periodontal pathogenesis
Oxidative stress is an imbalance between oxidants and antioxidants, in favour of oxidants
(Sies 1985, Sies 1986). Oxidants, such as oxygen-derived ROS, are generated during normal
4
physiologic processes, whereas antioxidants are agents that are able to reduce and resist
oxidative stress. In a healthy state, there is an equilibrum between oxidants and
antioxidants, but during infection and inflammation, oxidative stress increases, partly due
to the actions of neutrophils (Chapple and Matthews 2007).
Currently, there is some evidence that periodontitis patients have neutrophils that are
both hyperactive and hyper-reactive in their release of ROS. Earlier studies have reported
of small, but significant differences in intra- and extracellular ROS generation between
periodontitis patients and periodontally healthy controls both with FC-γ-stimulation
(Fredriksson et al. 2003) and without it (Matthews et al. 2007a). Furthermore, the
unstimulated extracellular ROS generation was reported to be at a higher level after
peridontal treatment in periodontitis patients, compared to the levels in healthy controls
(Matthews et al. 2007b), which suggests that the higher ROS production is an innate
property of neutrophils in individuals with periodontitis.
Despite the essential role in the phagocytosis, ROS have detrimental effects on
periodontal tissues. Firstly, they are able to activate protein transcription factors, such as
nuclear factor kappa-beta (NF-κB) or activating protein-1, thus accelarating the production
of pro-inflammatory cytokines. Secondly, ROS are able to degrade proline-rich collagens in
the extracellular matrix. Thirdly, ROS can cause direct damages to macromolecules, such as
proteins and lipids. Furthermore, it has been suggested that these violated macromolecules
can cause prolongued transit times of neutrophils through periodontal tissues and in this
way increase the risk of excess oxidative load in the tissues (Chapple and Matthews 2007).
2.1.3 Smoking and neutrophil function
The negative contribution of smoking on periodontal health is largely related to its
influence on host response. It has been observed that the chemotaxis of neutrophils is
reduced (Kraal et al. 1977) and the number of neutrophils in the periodontal pocket is lower
in smokers than in non-smokers (Pauletto et al. 2000). Additionally, the neutrophil transfer
from blood vessels to the surrounding connective tissue is enhanced among smokers and
this is most likely related to the upregulation of the expression adhesion of integrins and
the downregulation of the surface expression of integrins (Ryder et al. 1998b). At the tissue
level, neutrophils are less efficient to phagocytose and kill bacteria in smokers than in non-
smokers (Kenney et al. 1977).
Earlier studies focussing on neutrophil function have suggested that cigarette smoke
increases the release of ROS in unstimulated neutrophils. However, when neutrophils are
stimulated first by bacterial lipopolysaccaride or phorbol myristate acetate, the ability to
produce ROS is reduced (Ryder et al. 1998a, Matthews et al. 2011). These findings can be
interpreted in a way that there is a constant release of ROS among smokers, but during
bacterial infection, the ability to create oxidative burst and kill bacteria is reduced
(Zappacosta et al. 2001). Moreover, it has been observed that antioxidant storages,
measured by vitamin C concentration in the serum (Faruque et al. 1995, Schleicher et al.
2009), as well as, the levels of superoxide dismutase enzyme in gingival crevice fluid and
saliva are lower in smokers than in non-smokers, (Agnihotri et al. 2009) indicating an
increased use of antioxidants in the body among smokers.
5
2.2 THE POTENTIAL ROLE OF NUTRITION IN THE PATHOGENESIS OF PERIODONTITIS
2.2.1 Polyunsaturated fatty acids (PUFAs)
There are two essential fatty acids, namely alpha-linoleic acid (ALA, omega-3 PUFA) and
linoleic acid (LA, omega-6 PUFA) that are not synthesized in the body. Thus, their intake
from diet is important. The dietary sources for LA are corn, peanut, cottonseed, soybean,
and many plant oils (Mayes 2000a), whereas those for ALA are flaxseed-, canola-, pernilla-,
rapeseed- and soybean oils (Ratnayake & Galli 2009, Valtion Ravitsemusneuvottelukunta
2014), respectively. LA, in turn, can be converted into arachidonic acid (AA, omega-6
PUFA), which is an important component of the cell membrane phospholipids (Mayes
2000b, pp. 250, 252). Besides this conversion, AA can be obtained from animal fats, liver,
eggs, lipids and fish (Ratnayake and Galli 2009). Moreover, ALA can be converted into
other omega-3 fatty acids: docosahecsaenoic acid (DHA) and eicosapentaenoic acid (EPA).
However, this conversion rate in general is low, and also inefficient especially in men and
older people compared to women and younger people, respectively (Burdge and Wootton
2002, Burdge et al. 2002). One explanation for this difference is that the conversion is partly
dependent on oestrogen, the primary female sex hormone. Due to their potential anti-
inflammatory properties and the low conversion rate, intake of preformed EPA and DHA
from fish is important. EPA and DHA are able to incorporate in the cell membranes of
inflammatory cells and thus partly replace AA in case of a high dietary intake (Calder et al.
2002).
Eicosanoids are hormones that regulate many physiological processes, including
inflammation. They are produced by cyclooxygenase (COX) and lipooxygenase enzymes
from LA, ALA, AA and EPA (Mayes 2000b, pp. 250, 254). From eicosanoid family, PGE2 is
an important pro-inflammatory mediator of periodontal tissue destruction. It is synthesized
by COX-2 enzyme from AA (Mayes 2000b, p. 254) and is mainly released from
macrophages and fibroblasts during the activation of innate immunity. PGE2 causes MMP
release and activation of osteoclasts (Preshaw and Taylor 2012, p. 203). On the other hand,
the resolution of inflammation is regulated by AA derived lipoxins, EPA derived resolvins
and DHA derived resolvins, maresins and protectins (Freire and Van Dyke 2013).
2.2.2 Accelaration of oxidative stress and antioxidants
Postprandially, there are free fatty acids, amino acids and glucose in the circulation. Fatty
acids and glucose are metabolized into acetylCoA, which is converted into energy in the
Krebs cycle. The oxidation of AcetylCoA in the cycle generates reducing equivalents, which
enter the respiratory chain in the mitochondria and take part in the generation of adenosine
triphosphate. If the eaten meal contains lots of energy, carbohydrates with a high glycemic
index and a certain lipid profile (triglycerides, saturated fatty acids (SFA) and high omega-
6/omega-3 PUFA ratio), the electron transport chain gets oveloaded, and this in turn leads
to increased oxidative stress and activation of redox-sensitive signal transduction pathways
and the generation of pro-inflammatory cytokines (Mayes 2000c, pp. 137, 138, Margioris
2009, Muñoz and Costa 2013).
6
Nutrition is able to resist oxidative stress through the beneficial effects of antioxidants. The human antioxidant system consists of enzymatic antioxidants that are endogenously generated, for example superoxide dismutase and glutathione peroxidase, and non-enzymatic antioxidants that are obtained from foods, such as vitamin C, vitamin E, carotenoids and polyphenols (Ruiz-Núñez et al. 2013). The food-derived antioxidants are mainly chain-breaking, i.e. scavenging antioxidants, although a single antioxidant can have several actions. The food-derived antioxidants locate in the extracellular environment: the lipid-soluble vitamin E and carotenoids at the cell membrane level and the water-soluble vitamin C and polyphenols in the extracellular fluids (Chapple and Matthews 2007). A diet rich in berries, fruits and vegetables is a good source of dietary antioxidants.
2.3 EARLIER STUDIES ON SINGLE NUTRIENTS, FOODS/FOOD GROUPS OR WHOLE DIET AND PERIODONTAL DISEASES
2.3.1 Polyunsaturated fatty acids and periodontal condition
The association between dietary intake of, or supplementation with, omega-3 or omega-6 PUFAs and periodontal disease has been studied in at least one cross-sectional study, three longitudinal studies and seven randomized controlled trials. Evidence from observational studies supports the positive association between the intake of omega-3 PUFAs and periodontal health. In the cross-sectional study made among American population, it was reported that dietary DHA associated inversely with periodontal disease, although the observed association was not linear (Naqvi 2010). Furthermore, longitudinal cohort studies reported that a high dietary omega-6/omega-3 ratio and low intake of DHA were associated with periodontal disease progression (Iwasaki et al. 2010, Iwasaki et al. 2011). (Table 1). The results of randomized controlled trials examining the effects of omega-3 fatty acid supplementations on periodontal condition are contradictory (Campan et al. 1997, Rosenstein et al. 2003, Deore et al. 2014). However, interventions with omega-3 PUFAs and acetylsalicylic acid (ASA) enhanced periodontal healing and decreased the amount of inflammatory markers in the gingival crevice fluid (El-Sharkawy et al. 2010, Elkhouli 2011, Naqvi et al. 2014, Elwakeel and Hazaa 2015). (Table 1).
2.3.2 Antioxidants and periodontal condition
Antioxidants (carotenoids (α- and β–carotene, β–cryptoxanthin, zeaxanthin, lutein and lycopene); green tea supplement; selenium; vitamins A including retinol; vitamin C; and E including α- and γ-tocopherol) are the most studied nutrients in relation to periodontal diseases. The association between dietary antioxidants or serum/plasma/gingival crevice fluid/saliva levels of antioxidant and periodontal diseases has been studied in at least six cross-sectional, six case-control and three longitudinal studies. In addition, there are two randomized controlled trials on the topic. In an earlier cross-sectional study by Nishida and co-workers, the intake of vitamin C was found to be associated with periodontal health (Nishida et al. 2000). Moreover, in several cross-sectional (Amarasena et al. 2005, Amaliya et al. 2007, Chapple et al. 2007, Linden et al.
7
2009) and case/control studies (Väänänen et al. 1993, Brock et al. 2004, Panjamurthy et al. 2005, Konopka et al. 2007, Kuzmanova et al. 2012, Baser et al. 2015) it was observed that the serum/plasma/gingival crevice fluid/saliva levels of antioxidants were associated with periodontal health. However, Konopka reported that the antioxidant levels did not associate with the severity of the disease (Konopka et al. 2007). In contrast to these studies, a recent cross-sectional study reported no association between plasma vitamin C and alveolar bone loss (Amaliya et al. 2015). This divergent finding may be explained by the fact that in that study, vitamin C levels were measured from fasting blood, which reflects not only the uptake capacity of vitamin C, but also the levels of vitamin C after distribution. (Table 2). Regarding longitudinal studies, it has been reported that higher serum levels (Iwasaki et al. 2012a) and dietary intakes (Iwasaki et al. 2012b, Dodington et al. 2015) of antioxidants were associated with slower periodontal disease progression and better periodontal healing. The results of randomized controlled trials are contradictory as supplementation with vitamin C (Sulaiman and Shehadeh 2010) had no beneficial effect on periodontal healing while supplementation with green tea supplement was reported to benefit the healing of the periodontium. (Table 2). 2.3.3 Foods/food groups and periodontal condition The association between foods/food groups and periodontitis has been studied in at least three cross-sectional studies, two longitudinal studies and one randomized controlled trial. The results of those studies are contradictory, although most of the studies suggest that consumption of foods that contain antioxidants (fruits, vegetables and green tea) is associated with periodontal health. In the cross-sectional studies, it was reported that the consumption of green tea was associated with lower prevalence of periodontitis (Kushiyama et al. 2009), and the consumption of fruits with a lower risk to have deepened periodontal pockets (Blignaut and Grobler 1992) and alveolar bone loss (Amaliya et al. 2015). Longitudinal studies reported that dark green and yellow vegetables were inversely associated, and cereals, nuts and seeds, sugar, sweeteners and confectioneries were associated with the loss of attachment (Yoshihara et al. 2009), and that the consumption of fruits and vegetables were associated with periodontal healing (Dodington et al. 2015). However, the results of a randomized controlled trial showed that increased consumption of fruits, vegetables and whole grains did not improve periodontal healing compared to the control group (Zare Javid et al. 2014). (Table 3). 2.3.4 Whole diet approach and periodontal condition The association between diet and periodontal condition has been studied in at least two cross-sectional studies, three interventional studies and one randomized controlled trial. In two cross-sectional studies, adherence to a healthy diet (measured by healthy eating index (HEI)) was reported to reduce the odds of having periodontal disease by 16% compared to those with non-adherence to a healthy diet (Al-Zahrani et al. 2005) and non-adherence to a healthy diet to increase the odds for periodontitis to 3.5 fold compared to those adherent to healthy diet (Bawadi et al. 2011). (Table 4).
8
Beneficial effects of a healthy diet on periodontal condition has also been found in
interventional studies. In those studies, a wholesome nutrition intervention (plenty of
vegetables, fruits, whole-grain products, potatoes, legumes and dairy products; limited
consumption of meat, fish and eggs) was reported to reduce the signs and markers of
inflammation (Jenzsch et al. 2009) and ready-made meals (soybeans, white fish, seaweed,
vegetables, potato and brown rice) to improve the periodontal condition without any
simultaneous periodontal treatment (Kondo et al. 2014). These studies included participants
who either had metabolic syndrome or were at a high risk to develop it. In a similar
fashion, adherence to a Stone Age diet (barley, wheat, spelt, salt, herbs, honey, milk, meat
from goat and hens, berries, edible plants from nature and fish) (Baumgartner et al. 2009)
and a diet low in carbohydrates and omega-6 PUFAs and high in omega-3 PUFAs, vitamins
C and D, antioxidants and fiber (Woelber et al. 2016) were reported to be associated with
reduced inflammation of the gingiva. (Table 4).
9
Table
1.
Stu
die
s o
n t
he inta
ke o
f or
supple
menta
tion w
ith o
mega-3
and o
mega-6
poly
unsatu
rate
d fatt
y a
cid
s in r
ela
tion t
o p
eri
odontitis
Stu
dy
S
tud
y p
op
ula
tio
n
Ag
e D
esig
n a
nd
du
rati
on
Exp
osu
re
Ad
dit
ion
al
per
iod
on
tal
trea
tmen
t o
r
inst
ruct
ion
s
Ou
tco
me
var
iab
les
Re
sult
s
Do
din
gto
n e
t al
.
2015
No
n-s
mo
ker
s (n
=63)
an
d s
mo
ker
s
(n=2
3) w
ith
ch
ron
ic p
erio
do
nti
tis
(at
leas
t 30
% o
f si
tes
wit
h P
D o
f ≥
4 m
m)
in C
anad
a
34–9
0
yea
rs
Lo
ng
itu
din
al
stu
dy
, 8–1
6
wee
ks
Die
tary
α-l
ino
leic
aci
d, E
PA
and
DH
A
Ora
l h
yg
ien
e
inst
ruct
ion
s,
scal
ing
an
d r
oo
t
pla
nin
g
Per
cen
tag
e o
f si
tes
wit
h a
PD
of
> 3
mm
In n
on
-sm
ok
ers,
an
in
ver
se a
sso
ciat
ion
bet
wee
n t
he
per
cen
tag
e o
f si
tes
wit
h >
3
mm
PD
s an
d E
PA
an
d D
HA
Elw
akee
l &
Haz
aa
2015
Su
bje
cts
wit
h t
yp
e II
dia
bet
es
mel
litu
s an
d m
od
erat
e to
sev
ere
per
iod
on
titi
s in
Eg
yp
t, n
=40
24–5
8
yea
rs
RC
T, s
ix
mo
nth
s
Tre
atm
ent
gro
up
: om
ega
-3
PU
FA
1 g
x 3
+ 7
5 m
g A
SA
.
Pla
ceb
o g
rou
p: c
oco
nu
t o
il +
lact
ose
tab
let
Ora
l h
yg
ien
e
inst
uct
ion
s,
scal
ing
an
d r
oo
t
pla
nin
g
Pla
qu
e in
dex
, gin
giv
al
ind
ex,
PD
, CA
L.
GC
F: I
L-1
β a
nd
MC
P-3
.
Blo
od
: Hb
A1c
A s
ign
ific
antl
y b
ette
r im
pro
vem
ent
in t
he
clin
ical
par
amet
ers
in t
he
trea
tmen
t g
rou
p
tha
n i
n t
he
pla
ceb
o g
rou
p.
IL-1
β a
nd
MC
P-3
sig
nif
ican
tly
lo
wer
in
th
e
trea
tmen
t g
rou
p t
ha
n i
n t
he
con
tro
l g
rou
p
Deo
re e
t al
. 201
4 S
ub
ject
s w
ith
mo
der
ate
to s
ever
e
per
iod
on
titi
s in
In
dia
, tre
atm
ent
gro
up
(n
=29
) an
d p
lace
bo
gro
up
(n=2
9)
30–6
0
yea
rs
RC
T, t
hre
e
mo
nth
s
Tre
atm
ent
gro
up
: om
ega
-3
PU
FA
300
mg
x 1
(180
mg
EP
A
and
120
mg
DH
A).
Pla
ceb
o g
rou
p:
300
mg
of
liq
uid
par
affi
n x
1
Ora
l h
yg
ien
e
inst
ruct
ion
s,
scal
ing
an
d r
oo
t
pla
nin
g
Pla
qu
e in
dex
, gin
giv
al
ind
ex, o
ral
hy
gie
ne
ind
ex-
sim
pli
fied
, B
OP
, PD
an
d
CA
L, s
ulc
us
ble
edin
g i
nd
ex.
Blo
od
: CR
P
In t
he
trea
tmen
t g
rou
p a
sig
nif
ican
tly
hig
her
red
uct
ion
in
gin
giv
al i
nd
ex, s
ulc
us
ble
edin
g i
nd
ex a
nd
PD
, an
d g
ain
in
CA
L
com
par
ed w
ith
th
e p
lace
bo
gro
up
.
A s
ign
ific
antl
y h
igh
er r
edu
ctio
n i
n o
ral
hy
gie
ne
ind
ex-s
imp
lifi
ed in
th
e p
lace
bo
gro
up
co
mp
ared
wit
h t
he
trea
tmen
t g
rou
p
Naq
vi
et a
l. 2
014
Su
bje
cts
wit
h m
od
erat
e p
erio
do
nti
tis
in t
he
US
A, t
reat
men
t g
rou
p (
n=2
7)
and
pla
ceb
o g
rou
p (
n=2
8)
≥ 40
yea
rs
RC
T, t
hre
e
mo
nth
s
Tre
atm
ent
gro
up
: DH
A 2
g +
AS
A 8
1 m
g /
day
.
Pla
ceb
o g
rou
p: 9
50 m
g x
4
corn
oil
an
d s
oy
bea
n o
il +
AS
A
81 m
g
Ora
l h
yg
ien
e
inst
ruct
ion
s
PD
, CA
L, m
od
ifie
d g
ing
ival
ind
ex, B
OP
, pla
qu
e in
dex
.
GC
F: I
L-1
β, I
L-6
, hs-
CR
P.
Blo
od
: co
mp
lete
blo
od
cou
nt,
fas
tin
g l
ipid
pan
el,
hs-
CR
P, I
L-6
an
d V
CA
M.
Uri
ne:
NT
x
A s
ign
ific
antl
y h
igh
er r
edu
ctio
n i
n P
Ds,
gin
giv
al i
nd
ex, G
CF
hs-
CR
P a
nd
IL
-1β
in
the
trea
tmen
t g
rou
p c
om
par
ed w
ith
th
e
pla
ceb
o g
rou
p
Elk
ho
uli
201
1 S
ub
ject
s w
ith
mo
der
ate
to s
ever
e
chro
nic
per
iod
on
titi
s an
d a
t le
ast
on
e g
rad
e II
fu
rcat
ion
def
ect
in
Eg
yp
t, n
=40
35–6
0
yea
rs
RC
T, s
ix
mo
nth
s
Tre
atm
ent
gro
up
: om
ega
-3
PU
FA
1 g
x 3
(30
0 m
g D
HA
and
150
mg
EP
A)
+ 75
mg
AS
A.
Pla
ceb
o g
rou
p: p
lace
bo
pil
ls
Ora
l h
yg
ien
e
inst
ruct
ion
s,
scal
ing
an
d r
oo
t
pla
nin
g.
Reg
ener
ativ
e
ther
apy
of
the
furc
atio
n d
efec
t
wit
h D
FD
BA
Pla
qu
e in
dex
, gin
giv
al
ind
ex, g
ing
ival
ble
edin
g
ind
ex,
PD
, CA
L.
GC
F: I
L-1
β a
nd
IL
-10
In t
he
trea
tmen
t g
rou
p a
sig
nif
ican
tly
gre
ater
red
uct
ion
in
gin
giv
al i
nd
ex,
gin
giv
al b
leed
ing
in
dex
, PD
, IL
-1β
an
d
gai
n i
n t
he
CA
L c
om
par
ed w
ith
th
e
pla
ceb
o g
rou
p
T
able
1 t
o b
e c
ontinued
10
Table
1 c
ontinues
Iwas
aki
et a
l. 2
011
Su
bje
cts
in J
apan
, n=
235
75 y
ears
at
bas
elin
e
Lo
ng
itu
din
al
stu
dy
, th
ree
yea
rs
Die
tary
om
ega
-3 a
nd
om
ega
-6
PU
FA
s
- T
he
nu
mb
er o
f te
eth
wit
h a
chan
ge
in t
he
CA
L o
f ≥
3
mm
in
on
e y
ear
A h
igh
om
ega
-6/o
meg
a-3
rat
io w
as
asso
ciat
ed w
ith
pro
gre
ssio
n o
f
per
iod
on
titi
s
El-
Sh
ark
awy
201
0 S
ub
ject
s w
ith
ch
ron
ic p
erio
do
nti
tis
in E
gy
pt,
tre
atm
ent
gro
up
(n
=40)
and
pla
ceb
o g
rou
p (
n=4
0)
32–6
6
yea
rs
RC
T, s
ix
mo
nth
s
Inte
rven
tio
n g
rou
p: o
meg
a-3
PU
FA
1 g
x 3
(90
0 m
g f
ish
oil
(EP
A/D
HA
30
%),
100
mg
wh
eat-
ger
m o
il)
+ 81
mg
AS
A.
Pla
ceb
o g
rou
p: p
lace
bo
pil
ls
Ora
l h
yg
ien
e
inst
ruct
ion
s,
scal
ing
an
d r
oo
t
pla
nin
g
Pla
qu
e in
dex
, mo
dif
ied
gin
giv
al i
nd
ex, B
OP
, PD
an
d
CA
L.
Sal
iva
sam
ple
s: M
MP
-8 a
nd
RA
NK
L
In t
he
trea
tmen
t g
rou
p a
hig
her
red
uct
ion
in t
he
PD
s, M
MP
-8, R
AN
KL
an
d g
ain
in
the
CA
L c
om
par
ed w
ith
th
e p
lace
bo
gro
up
Iwas
aki
et a
l. 2
010
Su
bje
cts
in J
apan
, n=
36
74 y
ears
at
bas
elin
e
Lo
ng
itu
din
al
stu
dy
, fiv
e
yea
rs
Die
tary
EP
A a
nd
DH
A
- T
he
nu
mb
er o
f te
eth
wit
h a
chan
ge
in t
he
CA
L o
f ≥
3
mm
in
on
e y
ear
Lo
w i
nta
ke
of
DH
A i
ncr
ease
d t
he
risk
of
atta
chm
ent
loss
to
1.5
fo
ld c
om
par
ed w
ith
a h
igh
in
tak
e
Naq
vi
et a
l. 2
010
Su
bje
cts
fro
m N
HA
NE
S i
n t
he
USA
,
n=
9182
≥ 20
yea
rs
Cro
ss-
sect
ion
al
stu
dy
Die
tary
EP
A, D
HA
an
d
lin
ole
ic a
cid
(in
clu
din
g
gam
mal
ino
leic
an
d A
LA
, bo
th
om
ega
-3 a
nd
om
ega
-6 P
UF
As)
- P
erio
do
nti
tis
was
def
ined
as
hav
ing
a P
D o
f ≥
4 m
m a
nd
CA
L o
f ≥
3 m
m i
n a
t le
ast
on
e to
oth
Hig
h i
nta
ke
of
DH
A f
rom
th
e d
iet
wa
s
inv
erse
ly a
sso
ciat
ed w
ith
per
iod
on
titi
s
Ro
sen
stei
n e
t al
.
2003
Men
wit
h m
ild
, mo
der
ate
or
sev
ere
per
iod
on
titi
s d
ivid
ed i
nto
fo
ur
trea
tmen
t g
rou
ps,
n=
24
25–5
7
yea
rs
RC
T, t
hre
e
mo
nth
s
EP
A 5
00 m
g x
2 x
3 o
r
EP
A 5
00 m
g x
3 a
nd
bo
rag
e o
il
500
mg
x 3
or
bo
rag
e o
il 5
00
mg
x 2
x 3
or
pla
ceb
o x
2 x
3
Ora
l h
yg
ien
e
inst
ruct
ion
s
Mo
dif
ied
gin
giv
al i
nd
ex,
pla
qu
e in
dex
, P
D.
GC
F: β
-g
lucu
ron
idas
e
A s
ign
ific
ant
dif
fere
nce
bet
wee
n b
ora
ge
oil
gro
up
an
d p
lace
bo
gro
up
in
mo
dif
ied
gin
giv
al i
nd
ex a
nd
PD
s
Cam
pan
et
al.
1997
Su
bje
cts
in t
he
trea
tmen
t g
rou
p
(n=1
8) a
nd
su
bje
cts
in t
he
pla
ceb
o
gro
up
(n
= 19
)
18–2
8
yea
rs
RC
T, f
ive
wee
ks
Tre
atm
ent
gro
up
: om
ega
-3
(18%
EP
A, 1
2% D
HA
) 1.
8 g
x
3.
Pla
ceb
o g
rou
p: o
liv
e o
il 6
g
dai
ly (
1% o
meg
a-3
PU
FA
)
Ref
rain
ing
fro
m
ora
l h
yg
ien
e
pro
ced
ure
s
Gin
giv
al i
nd
ex, p
apil
lary
ble
edin
g i
nd
ex, p
laq
ue
ind
ex.
Gin
giv
al s
amp
les:
EP
A,
DP
A, D
HA
, AA
, PG
E2,
LT
B4
No
sig
nif
ican
t d
iffe
ren
ce b
etw
een
th
e tw
o
gro
up
s in
cli
nic
al p
aram
eter
s. A
sig
nif
ican
tly
hig
her
am
ou
nt
of
EP
A i
n t
he
gin
giv
al b
iop
sies
in
th
e tr
eatm
ent
gro
up
tha
n i
n t
he
pla
ceb
o g
rou
p
Abbre
via
tions:
AA,
ara
chid
onic
acid
; ALA,
alp
halinole
ic a
cid
; ASA,
acety
lsalicylic a
cid
; BO
P,
ble
edin
g o
n p
robin
g;
CAL,
clinic
al att
achm
ent
level/
loss;
CRP,
C-r
eactive p
rote
in;
DFD
BA,
dem
inera
lized f
reeze-d
ried b
one a
llogra
ft;
DH
A,
docosahecsaenoic
acid
; D
PA,
docosapenta
enoic
acid
; EPA,
eic
osapenta
enoic
acid
; G
CF,
gin
giv
al cre
vic
e f
luid
; H
bA1c,
hem
oglo
bin
A1c;
Hs-C
RP,
hig
h-s
ensitiv
ity C
-reactive p
rote
in;
IL-1
β,
inte
rleukin
1-b
eta
; IL
-
6,
inte
rleukin
-6;
IL-1
0,
inte
rleukin
-10;
LTB
4, le
ukotr
iene-B
4; M
CP-3
, m
onocyte
chem
oatt
racta
nt
pro
tein
-3;
MM
P-8
, m
atr
ix m
eta
llopro
tein
ase-8
; N
Tx,
N-t
erm
inal te
lopeptide;
PD
depth
; PG
E2, pro
sta
gla
ndin
E2; PU
FA,
poly
unsatu
rate
d fatt
y a
cid
; RAN
KL,
recepto
r activato
r of
nucle
ar
facto
r
kappa-Β
lig
and;
RCT,
random
ized c
ontr
olled t
rial;
USA,
United S
tate
s;
VCAM
, vascula
r cell a
dhesio
n m
ole
cule
11
Table
2.
Stu
die
s o
n a
ntioxid
ant
levels
in t
he g
ingiv
al cre
vic
e flu
id,
pla
sm
a,
seru
m o
r saliva;
die
tary
antioxid
ant
inta
ke o
r supple
menta
tion w
ith
antioxid
ants
and p
eri
odontitis
Stu
dy
S
tud
y p
op
ula
tio
n
Ag
e
Des
ign
an
d
du
rati
on
Exp
osu
re
Ad
dit
ion
al
per
iod
on
tal
trea
tmen
t
Ou
tco
me
var
iab
les
Res
ult
s
Ch
op
ra e
t al
. 201
6 S
ub
ject
s w
ith
mil
d t
o
mo
der
ate
per
iod
on
titi
s in
Ind
ia, d
ivid
ed i
nto
tre
atm
ent
gro
up
(n
= 56
) an
d c
on
tro
l
gro
up
(n
= 59
)
20–5
0
yea
rs
RC
T, t
hre
e
mo
nth
s
Tre
atm
ent
gro
up
:
gre
en t
ea s
up
ple
men
t
Co
ntr
ol
gro
up
:
cell
ulo
se
Sca
lin
g a
nd
roo
t p
lan
ing
Gin
giv
al i
nd
ex,
pla
qu
e in
dex
, PD
,
CA
L a
nd
BO
P%
.
GC
F: T
AO
C.
Pla
sma:
TA
OC
A s
ign
ific
antl
y g
reat
er r
edu
ctio
n i
n a
ll
clin
ical
par
amet
ers
and
ric
e in
TA
OC
of
GC
F a
nd
pla
sma
in t
he
trea
tmen
t
gro
up
co
mp
ared
wit
h t
he
con
tro
l
gro
up
Am
aliy
a et
al.
201
5 T
ea p
lan
tati
on
wo
rker
s in
Ind
on
esia
, n=
98
39–5
0
yea
rs
Cro
ss-
sect
ion
al
stu
dy
Vit
amin
C i
n p
lasm
a -
Alv
eola
r b
on
e lo
ss
No
ass
oci
ati
on
bet
wee
n p
lasm
a
vit
amin
C l
evel
an
d a
lveo
lar
bo
ne
loss
Bas
er e
t al
. 201
5 S
ub
ject
s w
ith
ag
gre
ssiv
e
per
iod
on
titi
s (n
=15)
an
d
hea
lth
y c
on
tro
ls (
n=2
1);
sub
ject
s w
ith
ch
ron
ic
per
iod
on
titi
s (n
=36)
an
d
hea
lth
y c
on
tro
ls (
n=1
6) i
n
Tu
rkey
21–5
0
yea
rs
Cas
e-co
ntr
ol
stu
dy
TA
OC
of
the
pla
sma
and
sal
iva
- P
laq
ue
ind
ex,
gin
giv
al i
nd
ex, B
OP
,
PD
, CA
L
A s
ign
ific
antl
y l
ow
er T
AO
C o
f th
e
pla
sma
in s
ub
ject
s w
ith
bo
th t
yp
es o
f
per
iod
on
titi
s th
an
in
co
ntr
ols
. TA
OC
of
the
sali
va
was
sig
nif
ican
tly
lo
wer
in
sub
ject
s w
ith
ch
ron
ic p
erio
do
nti
tis
than
in
th
e co
ntr
ol
gro
up
. In
ver
se
asso
cia
tio
n b
etw
een
sa
liv
a T
AO
C, a
nd
neg
ativ
e co
rrel
atio
ns
bet
wee
n p
lasm
a
TA
OC
an
d B
OP
, PD
an
d C
AL
Do
din
gto
n e
t al
.
2015
No
n-s
mo
ker
s (n
=63)
an
d
smo
ker
s (n
=23)
wit
h c
hro
nic
per
iod
on
titi
s (a
t le
ast
30%
of
site
s w
ith
po
cket
dep
th o
f ≥
4
mm
) in
Can
ada
34–9
0
yea
rs
Lo
ng
itu
din
al
stu
dy
, 8–1
6
wee
ks
Die
tary
β–c
aro
ten
e,
vit
amin
C, α
-
toco
ph
ero
le
Ora
l
hy
gie
ne
inst
ruct
ion
s,
scal
ing
an
d
roo
t p
lan
ing
Per
cen
tag
e o
f si
tes
wit
h a
PD
of
> 3
mm
In n
on
-sm
ok
ers,
an
in
ver
se
asso
cia
tio
n b
etw
een
th
e p
erce
nta
ge
of
site
s w
ith
> 3
mm
PD
s an
d β
–
caro
ten
e, v
itam
in C
an
d α
-
toco
ph
ero
le
Iwas
aki
et a
l. 2
012a
Su
bje
cts
in J
apan
, n=2
24
71 y
ears
at
bas
elin
e
Lo
ng
itu
din
al
stu
dy
of
eig
ht
yea
rs
Vit
amin
C a
nd
α-
toco
ph
ero
l in
ser
um
- S
um
of
teet
h w
ith
CA
L ≥
3 m
m d
uri
ng
the
foll
ow
-up
Inv
erse
ass
oci
ati
on
bet
wee
n s
eru
m
lev
el o
f v
itam
in C
, α
-to
cop
her
ol
an
d
the
sum
of
teet
h w
ith
CA
L ≥
3 m
m
Table
2 t
o b
e c
ontinued
12
Table
2 c
ontinues
Iw
asak
i et a
l. 20
12b
Su
bjec
ts in
Japa
n, n
=264
75
yea
rs
at
base
line
Long
itudi
nal
stud
y, tw
o ye
ars
Die
tary
α- a
nd β
–ca
rote
ne, v
itam
ins C
an
d E
- Su
m o
f tee
th w
ith
CA
L ≥
3 m
m d
urin
g th
e fo
llow
-up
Inve
rse
asso
ciat
ion
betw
een
the
inta
ke
of β
–car
oten
e, v
itam
ins
C a
nd E
and
th
e su
m o
f tee
th w
ith C
AL
≥ 3
mm
Kuz
man
ova
et a
l. 20
12
Subj
ects
with
per
iodo
ntiti
s (n
=21)
and
con
trol
s (n
=21)
in
the
Net
herl
ands
≥ 21
yea
rs
Cas
e-co
ntro
l st
udy
Vita
min
C s
tatu
s in
pl
asm
a, p
olym
or-
phon
ucle
ar
neut
roph
ilic
leuc
ocyt
es (P
MN
s)
and
peri
pher
al b
lood
m
onon
ucle
ar
cells
(PBM
Cs)
- BO
P, P
D, C
AL,
bon
e lo
ss
No
diffe
renc
e in
the
diet
ary
inta
ke, o
r co
ncen
trat
ion
of v
itam
in C
in P
MN
s or
PBM
Cs,
but
low
er le
vel o
f vita
min
C
in p
lasm
a of
sub
ject
s with
pe
riod
ontit
is th
an o
f con
trol
s. In
vers
e as
soci
atio
n be
twee
n vi
tam
in C
leve
l in
PMN
s and
PD
in s
ubje
cts
with
pe
riod
ontit
is
Sula
iman
&Sh
ehad
eh
2010
Su
bjec
ts w
ith c
hron
ic
peri
odon
titis
(n=3
0 (1
5 +
15))
and
cont
rols
(n=3
0) in
Syr
ia
23–6
5 ye
ars
RCT,
thre
e m
onth
s Su
bjec
ts w
ith
peri
odon
titis
, gro
up 1
(n
=15)
: 2
g vi
tam
in C
/ da
y +
peri
odon
tal t
reat
men
t, gr
oup
2 (n
=15)
pe
riod
onta
l tre
atm
ent
only
Ora
l hy
gien
e in
stru
ctio
ns,
scal
ing
and
root
pla
ning
PD, C
AL,
BO
P%,
plaq
ue in
dex,
gi
ngiv
al in
dex
TAO
C w
as lo
wer
in su
bjec
ts w
ith
peri
odon
titis
than
in c
ontr
ols
at
base
line.
Am
ong
subj
ects
with
pe
riod
ontit
is, v
itam
in C
su
pple
men
tatio
n di
d no
t enh
ance
he
alin
g of
per
iodo
ntal
tiss
ues
Lind
en e
t al.
2009
M
en fr
om a
ll so
cial
cla
sses
in
the
Nor
ther
n Ir
elan
d, n
=125
8 60
–70
year
s C
ross
-se
ctio
nal
stud
y
Retin
ol, α
- and
γ-
toco
pher
ol,
α- a
nd β
–ca
rote
ne,
β–cr
ypto
xant
hin,
ze
axan
thin
, lut
ein
and
lyco
pene
in s
erum
- Lo
w-th
resh
old
peri
odon
titis
(at l
east
tw
o in
terp
roxi
mal
si
tes
with
CA
L ≥
6 m
m a
nd o
ne P
D o
f ≥
5 m
m);
hig
h-th
resh
old
peri
odon
titis
(15%
of
site
s C
AL
≥ 6
mm
, at
leas
t one
PD
of ≥
6
mm
)
Inve
rse
asso
ciat
ion
betw
een
low
-th
resh
old
peri
odon
titis
and
α- a
nd β
–ca
rote
ne a
nd β
–cry
ptox
anth
in in
se
rum
, inv
erse
ass
ocia
tion
betw
een
high
-thre
shol
d pe
riod
ontit
is a
nd β
–ca
rote
ne a
nd β
–cry
ptox
anth
in in
se
rum
Table
2 t
o be
continued
13
Table
2 c
ontinues
A
mal
iya
et a
l. 20
07
Tea
plan
tatio
n w
orke
rs in
In
done
sia,
n=
123
33–4
3 ye
ars
Cro
ss-
sect
iona
l st
udy
Vita
min
C in
pla
sma
- C
AL
Lo
w le
vel o
f vita
min
C in
pla
sma
was
as
soci
ated
CA
L
Cha
pple
et a
l. 20
07
Subj
ects
from
NH
AN
ES II
I in
the
USA
, n=1
1 48
0 ≥
20 y
ears
C
ross
-se
ctio
nal
stud
y
α- a
nd β
–car
oten
e,
sele
nium
, lut
ein,
uri
c ac
id,
β–cr
ypto
xant
hine
, vita
min
s A
, C, E
and
bili
rubi
n of
the
seru
m. T
AO
C (u
ric
acid
an
d vi
tam
ins
A, C
and
E)
- M
ild p
erio
dont
itis
(at
leas
t one
site
with
bo
th P
D a
nd C
AL
≥ 4
mm
), se
vere
pe
riod
ontit
is (a
t lea
st
two
site
s w
ith C
AL
≥ 5
mm
and
at l
east
one
si
te w
ith P
D ≥
4 m
m)
Α- a
nd β
–car
oten
e, β
–cry
ptox
anth
ine,
vi
tam
in C
, bili
rubi
n an
d TA
OC
wer
e in
vers
ely
asso
ciat
ed w
ith m
ild
peri
odon
titis
. In
the
mod
el re
stri
cted
to
neve
r sm
oker
s, a
n in
vers
e as
siat
ion
rem
aine
d be
twee
n vi
tam
in C
, bili
rubi
n an
d TA
OC
and
mild
per
iodo
ntiti
s. Β
–ca
rote
ne, v
itam
in C
, bili
rubi
n an
d TA
OC
w
ere
inve
rsel
y as
soci
ated
with
sev
ere
peri
odon
titis
, but
the
asso
ciat
ion
betw
een
β–ca
rote
ne a
nd s
ever
e pe
riod
ontit
is w
as lo
st in
the
mod
el
rest
rict
ed to
nev
er-s
mok
ers
K
onop
ka e
t al
. 200
7
Subj
ects
with
agg
ress
ive
peri
odon
titis
(n=2
6) o
r chr
onic
pe
riod
ontit
is (n
=30)
, and
co
ntro
ls (n
=25)
in P
olan
d
18–5
5 ye
ars
Cas
e-co
ntro
l To
tal a
ntio
xida
nt s
tatu
s (T
AS)
of t
he s
erum
, 8-
hydr
oxy-
2-de
oxyg
uano
sine
(8
-OH
dG)
- Pl
aque
inde
x,
appr
oxim
alra
um
plaq
ue in
dex,
pa
pilla
ry b
leed
ing
inde
x, m
odifi
ed
sulc
ular
ble
edin
g in
dex,
PD
, alv
eola
r bo
ne lo
ss
The
leve
l of 8
-OH
dG in
the
ging
ival
bl
ood
was
sig
nific
antly
hig
her i
n su
bjec
ts
with
per
iodo
ntiti
s th
an in
con
trol
s an
d al
so in
sub
ject
s with
chr
onic
pe
riod
ontit
is th
an w
ith a
ggre
ssiv
e pe
riod
ontit
is. T
AS
leve
ls in
the
ging
ival
bl
ood
of c
hron
ic p
erio
dont
itis
patie
nts
wer
e si
gnifi
cant
ly lo
wer
com
pare
d w
ith
cont
rols
. A s
igni
fican
t diff
eren
ce in
TA
S le
vels
of p
erip
hera
l blo
od b
etw
een
subj
ects
with
per
iodo
ntiti
s an
d co
ntro
ls
and
also
in s
ubje
cts w
ith c
hron
ic
peri
odon
titis
and
agg
ress
ive
peri
odon
titis
. No
corr
elat
ion
betw
een
8-O
HdG
or T
AS
and
clin
ical
par
amet
ers
in
eith
er p
atie
nt g
roup
Table
2 t
o be
continued
14
Table
2 c
ontinues
Am
aras
ena
et
al. 2
005
Co
mm
un
ity
-dw
elli
ng
su
bje
cts
in
Jap
an, n
=413
70 y
ears
C
ross
-
sect
ion
al
stu
dy
Ser
um
lev
el o
f v
itam
in C
-
CA
L
Lo
w l
evel
of
vit
amin
C i
n s
eru
m w
as
wea
kly
ass
oci
ate
d w
ith
CA
L
Pan
jam
urt
hy
et a
l. 2
005
Men
wit
h c
hro
nic
per
iod
on
titi
s
(n=2
5) a
nd
mal
e co
ntr
ols
(n
=25)
in I
nd
ia
25–3
5
yea
rs
Cas
e-
con
tro
l
Vit
amin
C a
nd
E a
nd
red
uce
d g
luta
thio
ne
(no
n-
enzy
mat
ic a
nti
ox
idan
ts);
cata
lase
, glu
tath
ion
e
per
ox
idas
e an
d s
up
ero
xid
e
dis
mu
tase
(en
zym
atic
anti
ox
idan
ts).
Th
iob
arb
itu
ric
acid
rea
ctiv
e
sub
stan
ces
(TB
AR
S)
in
pla
sma
- -
Men
wit
h p
erio
do
nti
tis
had
sig
nif
ican
tly
hig
her
TB
AR
S a
nd
en
zym
atic
anti
ox
idan
t ac
tiv
itie
s an
d l
ow
er l
evel
s o
f
vit
amin
C a
nd
E t
han
co
ntr
ols
Bro
ck e
t al
.
2004
Su
bje
cts
wit
h c
hro
nic
per
iod
on
titi
s (n
=17)
an
d c
on
tro
ls
(n=1
7) i
n t
he
Gre
at-B
rita
in
23–6
3
yea
rs
Cas
e-
con
tro
l
TA
OC
of
the
seru
m,
pla
sma,
GC
F a
nd
sal
iva
- P
erio
do
nti
tis
(at
leas
t
two
sit
es p
er
qu
adra
nt
wit
h P
Ds
of
≥ 5
mm
dem
on
stra
tin
g b
oth
BO
P a
nd
30%
bo
ne
loss
(n
ot
firs
t m
ola
rs
or
inci
sors
)
Su
bje
cts
wit
h p
erio
do
nti
tis
had
sig
nif
ican
tly
lo
wer
TA
OC
in
GC
F a
nd
pla
sma
than
co
ntr
ols
Nis
hid
a et
al.
2000
Su
bje
cts
fro
m N
HA
NE
S I
II i
n
the
US
A, n
=12
419
≥ 20
yea
rs
Cro
ss-
sect
ion
al
stu
dy
Die
tary
vit
amin
C
- P
erio
do
nti
tis
was
def
ined
as
mea
n C
AL
≥ 1.
5 m
m
Inv
erse
ass
oci
ati
on
bet
wee
n v
itam
in C
inta
ke
and
per
iod
on
titi
s
Vää
nän
en e
t
al. 1
993
Su
bje
cts
wit
h a
lo
w v
itam
in C
pla
sma
lev
el (
case
, n=7
5) a
nd
sub
ject
s w
ith
a h
igh
vit
amin
C
pla
sma
lev
el (
con
tro
l, n
=75)
in
Fin
lan
d
20–6
4
Cas
e-
con
tro
l
Vit
amin
C i
n p
lasm
a -
Pla
qu
e, c
alcu
lus,
fill
ing
ov
erh
ang
s,
BO
P, P
D a
nd
gin
giv
al
rece
ssio
n
Cas
es h
ad m
ore
BO
P a
nd
dee
pen
ed
per
iod
on
tal
po
cket
s th
an c
on
tro
ls
Abbre
via
tions:
BO
B,
ble
edin
g o
n p
robin
g;
CAL,
clinic
al att
achm
ent
level/
loss;
8-O
HdG
, 8-h
ydro
xy-2
-deoxyguanosin
e;
GCF,
gin
giv
al cre
vic
e f
luid
;
NH
AN
ES,
National H
ealth a
nd N
utr
itio
n E
xam
ination S
urv
ey;
PBM
Cs,
peri
phera
l blo
od m
ononucle
ar
cells;
PD
depth
; PM
Ns,
poly
morp
honucle
ar
neutr
ophilic
leucocyte
s;
RC
T,
random
ized c
ontr
olled t
rial;
TAO
C,
tota
l antioxid
ant
capacity;
TAS,
tota
l antioxid
ant
sta
tus;
TBARS,
thio
barb
ituric a
cid
reactive s
ubsta
nces
15
Table
3.
Stu
die
s o
n t
he c
onsum
ption o
f fo
ods/f
ood g
roups in r
ela
tion t
o p
eri
odontitis
Stu
dy
S
tud
y p
op
ula
tio
n
Ag
e
Des
ign
an
d
du
rati
on
Exp
osu
re
Ad
dit
ion
al
per
iod
on
tal
trea
tmen
t o
r
inst
ruct
ion
s
Ou
tco
me
var
iab
les
Re
sult
s
Am
aliy
a et
al.
2015
Tea
pla
nta
tio
n w
ork
ers
in
Ind
on
esia
, n=
98
39–5
0 y
ears
C
ross
-sec
tio
nal
stu
dy
Gu
ava
fru
it s
erv
ing
s
- A
lveo
lar
bo
ne
loss
A
n i
nv
erse
ass
oci
atio
n b
etw
een
gu
ava
fru
it s
erv
ing
s an
d a
lveo
lar
bo
ne
loss
Do
din
gto
n e
t al
.
2015
No
n-s
mo
ker
s (n
=63)
an
d
smo
ker
s (n
=23)
wit
h
chro
nic
per
iod
on
titi
s (a
t
leas
t 30
% o
f si
tes
wit
h P
D
of
≥ 4
mm
) in
Can
ada
34–9
0 y
ears
L
on
git
ud
inal
stu
dy
, 8–1
6
wee
ks
Fru
its
and
veg
etab
les
Ora
l
hy
gie
ne
inst
ruct
ion
s,
scal
ing
an
d
roo
t p
lan
ing
Per
cen
tag
e o
f si
tes
wit
h a
PD
s
of
> 3
mm
In n
on
-sm
ok
ers,
an
in
ver
se
asso
ciat
ion
bet
wee
n t
he
per
cen
tag
e
of
site
s w
ith
> 3
mm
PD
s an
d f
ruit
s
and
veg
etab
les
Zar
e Ja
vid
et
al.
2013
Su
bje
cts
in t
he
trea
tmen
t
gro
up
(n
=18)
an
d s
ub
ject
s
in t
he
con
tro
l g
rou
p (
n=1
9)
in t
he
Un
ited
Kin
gd
om
30–6
5 y
ears
R
CT
, six
mo
nth
s D
ieta
ry i
nte
rven
tio
n w
ith
th
e
aim
to
in
crea
se t
he
com
sum
pti
on
of
fru
its,
veg
eta
ble
s an
d w
ho
le g
rain
s
Ora
l
hy
gie
ne
inst
ruct
ion
s,
scal
ing
an
d
roo
t p
lan
ing
Pla
qu
e in
dex
, P
D, g
ing
ival
rece
ssio
n, b
leed
ing
in
dex
,
CA
L.
Inta
ke
of
fru
its,
veg
etab
les
and
fib
re. T
AO
C o
f p
lasm
a an
d
sali
va
No
sig
nif
ican
t d
iffe
ren
ce i
n
per
iod
on
tal
par
amet
ers
bet
wee
n
the
two
gro
up
s. T
he
inta
ke
of
fru
its
and
veg
etab
les
and
wh
ole
gra
ins
and
th
e T
AO
C o
f p
lasm
a in
crea
sed
sig
nif
ican
tly
in
th
e in
terv
enti
on
gro
up
Ku
shiy
ama
et a
l.
2009
Men
of
Sel
f-D
efen
ce F
orc
e
in J
apan
, n=
940
49–5
9 y
ears
C
ross
-sec
tio
nal
stu
dy
Co
nsu
mp
tio
n o
f g
reen
tea
-
BO
P, P
D, C
AL
In
ver
se a
sso
ciat
ion
bet
wee
n g
reen
tea
inta
ke
and
BO
P, P
D a
nd
CA
L
Yo
shih
ara
et a
l
2009
Su
bje
cts
in J
apan
, n=6
00
70 y
ears
at
bas
elin
e
Lo
ng
itu
din
al
stu
dy
, six
yea
rs
Fis
h, s
hel
lfis
h, m
eat,
bea
ns
and
egg
s; m
ilk
an
d m
ilk
pro
du
cts;
dar
k g
reen
an
d y
ello
w
veg
eta
ble
s; o
ther
veg
etab
les
and
fru
its;
cer
eals
, nu
ts a
nd
seed
s, s
ug
ar a
nd
sw
eete
ner
s,
con
fect
ion
ery
; an
d f
ats
and
oil
s
- P
erio
do
nta
l d
isea
se e
ven
t (t
he
nu
mb
er o
f te
eth
wit
h a
ch
ang
e
of
CA
L ≥
3 m
m d
uri
ng
th
e
foll
ow
-up
)
Da
rk g
reen
an
d y
ello
w v
eget
able
s
wer
e in
ver
sely
an
d c
erea
ls, n
uts
and
see
ds,
su
gar
, sw
eete
ner
s an
d
con
fect
ion
erie
s w
ere
po
siti
vel
y
asso
ciat
ed w
ith
per
iod
on
tal
dis
ease
even
ts
Bli
gn
aut
&
Gro
ble
r 19
92
Wo
rker
s o
f fr
uit
- (a
pp
le,
gra
pe,
cit
rus
and
mix
ed-
va
riet
y f
ruit
) an
d g
rain
farm
s, n
= 31
3
15–7
6 y
ears
C
ross
-sec
tio
nal
stu
dy
Bei
ng
a f
ruit
or
a g
rain
far
m
wo
rker
- C
om
mu
nit
y p
erio
do
nta
l in
dex
of
trea
tmen
t n
eed
s
Th
e w
ork
ers
of
the
fru
it f
arm
s
con
sum
ed h
igh
er a
mo
un
ts o
f fr
uit
s
com
par
ed w
ith
th
e g
rain
far
m
wo
rker
s. W
ork
ers
fro
m c
itru
s fa
rm
had
few
er p
erio
do
nta
lly
hea
lth
y
sex
tan
ts, b
ut
had
mo
re r
arel
y d
eep
po
cket
s th
an w
ork
ers
fro
m o
ther
farm
s
Abbre
via
tions:
BO
B,
ble
edin
g o
n p
robin
g;
CAL,
clinic
al att
achm
ent
level/
loss;
PD
depth
; RCT,
random
ized c
ontr
olled t
rial;
TAO
C,
tota
l
antioxid
ant
capacity
16
Table
4.
Stu
die
s o
n t
he w
hole
die
t appro
ach in r
ela
tion t
o p
eri
odontitis
Stu
dy
S
tud
y p
op
ula
tio
n
Ag
e D
esi
gn
an
d d
ura
tio
n
Exp
osu
re
Ad
dit
ion
al
perio
do
nta
l
trea
tmen
t o
r
inst
ru
cti
on
s
Ou
tco
mes
Resu
lts
Wo
elb
er e
t al
. 201
7 S
ub
ject
s in
th
e
trea
tmen
t g
rou
p (
n=1
0)
and
su
bje
cts
in t
he
con
tro
l g
rou
p (
n=5
)
wit
h g
ing
ivit
is a
nd
a
die
t b
ased
pri
mar
ily
on
carb
oh
yd
rate
s in
Ger
man
y
23–7
0 y
ears
R
CT
, eig
ht
wee
ks
Tre
atm
ent
gro
up
: a d
iet
low
in
car
bo
hy
dra
tes
and
om
ega
-6 P
UF
As,
and
hig
h i
n o
meg
a-3
PU
FA
s, v
ita
min
C a
nd
D, a
nti
oxi
dan
ts a
nd
fib
re.
Co
ntr
ol
gro
up
: a d
iet
hig
h i
n c
arb
oh
yd
rate
s
Ref
rain
ing
fro
m
inte
rden
tal
hy
gie
ne
pro
ced
ure
s
Pla
qu
e in
dex
, gin
giv
al
ind
ex, B
OP
, to
tal
per
iod
on
tal
infl
amed
area
In t
he
trea
tmen
t g
rou
p, a
sig
nif
ican
t re
du
ctio
n i
n t
he
gin
giv
al i
nd
ex, B
OP
an
d t
ota
l
per
iod
on
tal
infl
amed
are
a
com
par
ed w
ith
th
e co
ntr
ol
gro
up
Ko
nd
o e
t al
. 201
4 S
ub
ject
s w
ith
a b
od
y
mas
s in
dex
of
≥25
or
pla
sma
glu
cose
lev
el ≥
120
mg
/dl
2 h
ou
rs a
fter
a 75
-g o
ral
glu
cose
tole
ran
ce t
est
in J
apan
,
n=1
7
35–6
0 y
ears
In
terv
enti
on
al s
tud
y (
no
con
tro
l g
rou
p),
35
wee
ks
A h
igh
-fib
re a
nd
lo
w-f
at
die
t in
clu
din
g s
oy
bea
ns,
wh
ite
fish
, sea
wee
d,
veg
eta
ble
s, p
ota
to a
nd
bro
wn
ric
e (t
ota
l en
erg
y
30 k
cal/
kg
of
idea
l b
od
y
wei
gh
t)
- P
D, C
AL
, BO
P, G
CF
,
bo
dy
wei
gh
t, B
MI,
WC
, blo
od
pre
ssu
re.
Fro
m b
loo
d: H
bA
1c,
glu
cose
, in
suli
n, H
DL
,
LD
L, t
rig
lyse
rid
es,
fib
rin
og
en, t
-PA
I1, h
s-
CR
P, a
dip
on
ecti
n a
nd
lep
tin
All
per
iod
on
tal
par
amet
ers
wer
e
sig
nif
ican
tly
lo
wer
at
the
end
of
the
exp
erim
ent
than
at
the
beg
inn
ing
. A s
ign
ific
ant
red
uct
ion
in
wei
gh
t, B
MI,
WC
,
Hb
A1c
, glu
cose
, LD
L,
trig
lyse
rid
es, t
-PA
I1, h
s-C
RP
,
and
lep
tin
. In
crea
se i
n s
eru
m
adip
on
ecti
n
Baw
adi
et a
l. 2
011
Ran
do
mly
sel
ecte
d
pat
ien
ts o
f th
e Jo
rdan
Un
iver
sity
of
Sci
ence
and
Tec
hn
olo
gy
med
ical
cen
ter
in J
ord
an, n
=340
18–7
0 y
ears
C
ross
-sec
tio
nal
stu
dy
T
he
hea
lth
ines
s o
f th
e
die
t w
as a
sses
sed
by
usi
ng
th
e H
ealt
hy
Eat
ing
In
dex
(H
EI)
.
Th
e le
vel
of
ph
ysi
cal
acti
vit
y
- T
he
pre
sen
ce o
f
per
iod
on
titi
s w
as
det
erm
ined
as
hav
ing
fou
r o
r m
ore
tee
th
wit
h b
oth
a P
D o
f ≥
4
mm
an
d C
AL
of
≥ 3
mm
In t
ho
se c
on
sum
ing
a p
oo
r d
iet
had
3.5
hig
her
od
ds
for
hav
ing
per
iod
on
titi
s th
an i
n t
he
on
es
com
sum
ing
a g
oo
d d
iet.
In
th
ose
hav
ing
a l
ow
lev
el o
f p
hy
sica
l
acti
vit
y h
ad 3
.8 h
igh
er o
dd
s fo
r
hav
ing
per
iod
on
titi
s th
an i
n t
he
on
es h
avin
g a
hig
h l
evel
of
ph
ysi
cal
acti
vit
y
Table
4 t
o b
e c
ontinued
17
Table
4 c
ontinues
Bau
mg
artn
er e
t al
.
2009
Su
bje
cts
liv
ing
in
con
dit
ion
s si
mil
ar t
o
Sto
ne
Ag
e in
S
wit
zerl
and
, n=1
0
8–46
yea
rs
Inte
rven
tio
nal
stu
dy
, fo
ur
wee
ks
Sto
ne
Ag
e d
iet
incl
ud
ed
bar
ley
, wh
eat,
sp
elt,
salt
, her
bs,
ho
ney
, mil
k,
mea
t fr
om
go
at a
nd
hen
s, b
erri
es, e
dib
le
pla
nts
fro
m t
he
nat
ure
and
fis
h
Ref
rain
ing
fro
m
ora
l h
yg
ien
e
pro
ced
ure
s
Mic
rob
iolo
gic
al
sam
pli
ng
, pla
qu
e in
dex
,
gin
giv
al i
nd
ex, B
OP
, PD
A s
ign
ific
ant
incr
ease
in
pla
qu
e
ind
ex w
hil
e a
sig
nif
ican
t
dec
reas
e in
BO
P. I
ncr
ease
s in
sub
gin
giv
al b
acte
rial
co
un
ts i
n
spec
ies
no
t as
soci
ated
wit
h
per
iod
on
titi
s, w
hil
e a
dec
reas
e o
f
ton
gu
e b
act
eria
l co
un
ts
Jen
zsch
et
al. 2
009
Wo
men
wit
h
met
ab
oli
c sy
nd
rom
e
and
ch
ron
ic
per
iod
on
titi
s in
Ger
man
y, n
=20
Mea
n a
ge
55
yea
rs
Inte
rven
tio
nal
stu
dy
, 12
mo
nth
s
Die
tary
in
terv
enti
on
wit
h t
he
aim
to
ch
ang
e
fro
m t
he
com
sum
pti
on
of
Ger
man
mix
ed d
iet
to w
ho
leso
me
nu
trit
ion
(veg
eta
ble
s, f
ruit
s,
wh
ole
-gra
in p
rod
uct
s,
po
tato
es, l
egu
mes
an
d
dai
ry p
rod
uct
s; l
imit
ed
con
sum
pti
on
on
mea
t,
fish
an
d e
gg
s)
- P
D, g
ing
ival
in
dex
,
pla
qu
e in
dex
.
GC
F: I
L-1
β a
nd
IL
-6,
gra
nu
locy
te e
last
ase
,
per
iod
on
top
ath
og
ens.
Sti
mu
late
d s
aliv
a:
ox
idat
ive
and
anti
oxi
dat
ive
var
iab
les
A s
ign
ific
ant
red
uct
ion
in
gin
giv
al i
nd
ex, w
ho
le m
ou
th
PD
s, I
L-1
β a
nd
IL
-6
Al-
Zah
ran
i et
al.
200
5 S
ub
ject
s fr
om
NH
AN
ES
III
-stu
dy
in
the
US
A, n
=12
110
≥18
yea
rs
Cro
ss-s
ecti
on
al s
tud
y
Die
t m
easu
red
by
HE
I.
Mai
nta
inin
g n
orm
al
wei
gh
t.
Ph
ysi
cal
acti
vit
y
- T
he
pre
sen
ce o
f
per
iod
on
titi
s w
as
det
erm
ined
as
hav
ing
at
leas
t o
ne
site
wit
h b
oth
a P
D o
f ≥
4 m
m a
nd
CA
L o
f ≥
3 m
m
Hav
ing
all
th
ree
hea
lth
enh
anci
ng
beh
avio
urs
red
uce
d
the
risk
of
hav
ing
per
iod
on
titi
s
40 %
. On
e h
ealt
h e
nh
anci
ng
beh
avio
ur
red
uce
d t
he
risk
16
%
Abbre
via
tions:
BM
I, b
ody m
ass index;
BO
P,
ble
edin
g o
n p
robin
g;
CAL,
clinic
al att
achm
ent
level/
loss;
GCF,
gin
giv
al cre
vic
e flu
id;
HbA1c,
hem
oglo
bin
A1c;
HD
L,
hig
h-d
ensity lip
opro
tein
; H
EI,
Healthy E
ating I
ndex;
hs-C
RP,
hig
h-s
ensitiv
ity C
-reactive p
rote
in;
IL-1
β,
inte
rleukin
1β;
IL-6
, in
terl
eukin
6;
LD
L,
low
-density lip
opro
tein
; N
HAN
ES,
National H
ealth a
nd N
utr
itio
n E
xam
ination S
urv
ey;
PD
depth
; PU
FA,
poly
unsatu
rate
d f
att
y a
cid
; RCT,
random
ized c
ontr
olled t
rial;
t-P
AI1
, tissue p
lasm
inogen a
ctivato
r 1;
USA,
United S
tate
s;
WC
, w
ais
t cir
cum
fere
nce
18
2.4 DIFFERENT WAYS TO MEASURE DIETARY INTAKES, DIET QUALITY AND NUTRIENT STATUS
2.4.1 Methods based on reporting
The methods in assessing dietary intake can be divided into short-term and long-term
methods and they can be based on real time recording or memory. The three most
commonly used methods are diet records, 24-hour recalls and food frequency
questionnaires (FFQ). The traditional paper-based methodologies have recently been
complemented with innovative technologies that use mobile phones or internet in the
reporting of dietary intake (Illner et al. 2012).
Diet records
The only prospective method to collect dietary data is the use of diet records. In this
method, a person records the use of all foods on a specific day or period of days in real-time
(Baranowski 2013, p. 53). The portion sizes are estimated by using either weighting, or by
using household measures or pictures of different portion sizes (Thompson and Byers
1994). The advantage of diet records is that they enable the recording of any kind of foods
and preparation methods, because of their open-ended form (Baranowski 2013, p. 54). The
data from diet records are thought to represent absolute intakes of foods and nutrients
(Baranowski 2013, p. 54), but validation studies have shown that diet records may
underestimate the dietary intake, especially in less motivated individuals (Black et al. 1993,
Livingstone et al. 1990). In addition, eating may be more conscious, which may lead to
changes in food consumption (Thompson and Byers 1994). Although diet records are not
based on memory, it is possible that people forget either intentionally or unintentionally to
record all eaten foods. Furthermore, this method is burdensome both for the participant
and also the researcher, who has to check the records for completeness (Thompson and
Byers 1994) and store information by hand. To obtain extensive data within a long time
frame, diet records need to be repeated in different seasons and days of the week. Diet
records are not the main method in collecting dietary data in epidemiological studies, but
they are frequently used to validate other methods, especially FFQ (Baranowski 2013, pp.
49, 56).
24-hour recall
A short-term, retrospective and memory-based method to collect dietary data is 24-hour
recall. In the interview, the researcher assists the participant to memorize all foods and
drinks consumed within the previous 24 hours (Thompson and Byers 1994). Estimation of
portion sizes is done by using pictures of different portion sizes, household measures or
package sizes of well-known products, but the estimation of portion sizes is nevertheless
based on memory (Baranowski 2013, p. 51). In this method, it is important to use well-
trained interviewers who are able to ask versatile and open-ended questions in a neutral
atmosphere to help the participant to remember the eaten foods. As a dietary assessment
method, 24-hour recall enables the recording of any kind of foods and its advantage is that
19
it does not usually change the food consumption. However, due to errors in memory, there
may be either under- or overreporting. Similar to diet records, this method needs to be
repeated to capture usual long-term dietary intake and it aims to measure absolute rather
than relative intakes (Baranowski 2013, pp. 51, 54–56). In both diet records and 24-hour
recall, it is helpful if the participants have been trained beforehand, because training leads
to more accurate recording of energy content and portion size estimation during the data
collection period (Martin et al. 2007). Validation studies have suggested that 24-hour recall
describes well the mean intakes of nutrients at a group level, but there may be some
variation at an individual level due to misreporting (Madden et al. 1976, Gersovitz et al.
1978).
Food frequency questionnaire (FFQ)
FFQ is the most commonly used method in large epidemiological studies to estimate
average long-term food consumption (weeks, months, years) (Willett 2013a, p. 71). It
includes a list of foods and the frequencies of consumption, in semiquantitative
questionnaires there are also portion size estimates present (Thompson and Byers 1994).
The list of foods in the questionnaire is composed by taking into account several facts: first,
the food has to be used often enough by most people; second, the food must contain
nutrients of interest and third there has to be between-person variation in the use of foods.
Furthermore, there may be some preliminary information of foods and their association
with the diseases under interest (Willett 2013a, p. 72). FFQ is mainly used to rank
individuals by consumption of foods rather than measuring absolute intakes of nutrients,
although semiquantitative questionnaires can be used to estimate relative or absolute
nutrient intakes. An advantage of FFQ is that it is self-admistered, requires little time to
complete, is not especially burdensome for the researcher and is inexpensive compared to
other methods. The calibration of FFQ is performed using repeated diet records or recalls
(Thompson and Byers 1994). Keeping in mind that diet records and recalls may
underestimate dietary intake (Mertz et al. 1991, Lichtman et al. 1992), the correlations for
most foods and nutrients between these short-term and long-term methods range from 0.4
to 0.7. A FFQ with a very long food list tends to overestimate the dietary intake of foods,
nutrients and total calories (Thompson and Byers 1994).
Independent of the method that has been used, the data of eaten foods are converted to
nutrients using food composition tables or databases and usually these nutrients are later
energy-adjusted to reflect the intake of a nutrient independent of body size.
Diet quality scores as a method to assess diet quality
During the last years, scientific interest has moved besides studying single nutrients
towards whole diet approaches in order to better assess the complexity of a diet. In Table 5
different indices used to evaluate the whole diet in studies are presented. This kind of
methodology is based on an a priori method. In that method, a predefined dietary pattern
based on dietary recommendations or typical to a certain geographical area, is used as a
template to calculate an index or a score, which reflects the healthiness of the diet. Each
20
score component is defined as positive or negative and summarized accordingly (Waijers et
al. 2007).
Three of the most studied dietary scores, the Diet Quality Index (DQI), the Healthy Eating
Index (HEI) and the Alternative Healthy Eating Index (AHEI) are based on the North
American dietary recommendations. Other indices that are based on the national dietary
recommendations are for example the Recommended Finnish Diet Score (RFDS) and the
Diet Quality Index (DQI) (Swedish dietary recommendations). (Table 5).
In addition to dietary recommendations, indices may also be based on local food cultures.
The Mediterranean diet score (MDS) is composed to describe a diet traditionally eaten in
the Mediterranean countries. However, as the Mediterranean diet is regionally derived and
adhering to it may be culturally problematic in other parts of the Europe, nutritionists have
compiled two corresponding dietary scores, the Baltic Sea Diet Score (BSDS) and the Nordic
Food Index (NFI), which consist of locally produced foods commonly used in the Nordic
countries. (Table 5).
2.4.2 Biochemical measures
Biochemical measures of nutrient status reflect the level of nutrient in the tissues after
phases of absorbtion, transport, distribution, metabolism and excretion. These measures
can be used to measure dietary intake of certain nutrients and to validate the methods that
are based on self-reporting. Although biochemical measures are considered to be an
objective assessment of nutrient intake, the values are a contribution of nutrient intake and
endogenous production of a nutrient, and are also influenced by lifestyle factors, such as
smoking and physical activity, genetic factors, and pathophysiological processes.
Furthermore, usability of a biochemical measure as a marker of food consumption may be
distorted by storage and cooking methods as well as the soil where the food has been
grown (van Dam and Hunter 2013, pp. 150–151). A limitation of biomarkers is that they are
available only for a small number of nutrients (for example omega-3 PUFAs, selenium, and
vitamins C and D) (van Dam and Hunter 2013, pp. 151–152).
Biomarkers can be detected from different body tissues and the optimal tissue type to
observe a biomarker depends on the biomarker in question. The most typical tissues to
measure a biomarker are serum and plasma, other possibilities are also erythrocytes, urine,
adipose tissue, and hair and nail specimens. Usually in epidemiological studies, there is an
interest to measure food consumption and nutrient intake over long time periods and
therefore, in some cases, the use of other specimen types than serum and plasma may be
favourable, because of their better time integration (van Dam and Hunter 2013, p. 159). For
example, serum cholesterol esthers reflect the intake of EPA over a few weeks, whereas
erythrocytes over a few months and adipose tissue over a few years (Katan et al. 1997).
21
Table
5.
Die
t quality
indic
es d
escri
bin
g e
ither
adhere
nce t
o d
ieta
ry r
ecom
mendati
ons o
r lo
cal fo
od c
ulture
Ind
ice
Ref
eren
ce
Co
mp
on
ents
S
cori
ng
Die
t Q
ual
ity
In
dex
(D
QI)
(No
rth
Am
eric
an d
ieta
ry
reco
mm
end
atio
ns)
(Pat
ters
on
et
al. 1
994,
Hai
nes
et
al.
1999
, up
dat
e)
To
tal
fat,
SF
A, c
ho
lest
ero
l, p
rote
in, c
alci
um
, so
diu
m, f
ruit
s an
d
veg
etab
les,
gra
ins
and
leg
um
es
Ea
ch c
om
po
nen
t 0
–2 p
oin
ts.
Sco
re: 0
(h
ealt
hy
die
t)–1
6 (p
oo
r d
iet)
Hea
lth
y E
atin
g I
nd
ex (
HE
I)
(Ken
ned
y e
t al
. 199
5, G
uen
ther
200
8,
up
dat
e, G
uen
ther
et
al. 2
013,
up
dat
e)
To
tal
fat,
SF
A, c
ho
lest
ero
l, s
od
ium
, gra
ins,
veg
etab
les,
fru
its,
mil
k, m
eat,
th
e am
ou
nt
of
var
iety
in
th
e d
iet
Ea
ch c
om
po
nen
t 0
–10
po
ints
.
Sco
re: 0
(p
oo
r d
iet)
–100
(h
ealt
hy
die
t)
Alt
ern
ativ
e H
ealt
hy
Eat
ing
In
dex
(AH
EI)
(McC
ull
ou
gh
et
al. 2
002,
Ch
iuv
e et
al.
2012
, up
dat
e)
Th
e ra
tio
of
MU
FA
an
d P
UF
A t
o S
FA
, tra
ns-
fatt
y a
cid
s, c
erea
l
fib
er, f
ruit
s, v
eget
able
s, n
uts
an
d s
oy
pro
tein
, alc
oh
ol,
rat
io o
f
wh
ite
mea
t to
red
mea
t, d
ura
tio
n o
f m
ult
ivit
amin
use
Ea
ch c
om
po
nen
t 0
–10
po
ints
, ex
cep
t
mu
ltiv
itam
in u
se 2
.5–7
.5 p
oin
ts.
Sco
re: 2
.5 (
po
or
die
t)–8
7.5
(hea
lth
y d
iet)
Rec
om
men
ded
Fin
nis
h D
iet
Sco
re
(RF
DS
)
(Kan
erv
a et
al.
201
3a)
Fru
its
(in
clu
din
g b
erri
es),
veg
etab
les,
th
e ra
tio
of
wh
ite
mea
t to
red
an
d p
roce
ssed
mea
t, r
ye,
th
e ra
tio
of
PU
FA
to
SF
A a
nd
tran
s-fa
tty
aci
ds,
sal
t, s
ucr
ose
an
d a
lco
ho
l
Ea
ch c
om
po
nen
t 0
–3 p
oin
ts.
Sco
re: 0
(p
oo
r d
iet)
–24
(hea
lth
y d
iet)
Die
t Q
ual
ity
In
dex
(D
QI)
(Sw
edis
h d
ieta
ry
reco
mm
end
atio
ns)
(Dra
ke
et a
l. 2
011)
S
FA
, PU
FA
, fib
re, s
ucr
ose
, fis
h a
nd
sh
ellf
ish
, fru
its
and
veg
etab
les
Ea
ch c
om
po
nen
t 0
–1 p
oin
ts.
Sco
re: 0
(p
oo
r d
iet)
–6 (
hea
lth
y d
iet)
Med
iter
ran
ean
Die
t S
core
(M
DS
) (T
rich
op
ou
lou
et
al. 1
995)
R
atio
of
MU
FA
to
SF
A, a
lco
ho
l (r
ed w
ine)
, cer
eals
, leg
um
es,
fru
its
and
nu
ts, v
eget
able
s, m
eat
and
mea
t p
rod
uct
s, d
airy
pro
du
cts
Ea
ch c
om
po
nen
t 0
–1 p
oin
t.
Sco
re 0
(p
oo
r d
iet)
–8 (
hea
lth
y d
iet)
Bal
tic
Sea
Die
t S
core
(B
SD
S)
(Kan
erv
a et
al.
201
4a)
Fru
its
and
ber
ries
, veg
etab
les,
cer
eals
, lo
w-f
at m
ilk
, fis
h, m
eat
pro
du
cts,
alc
oh
ol,
rat
io o
f P
UF
A t
o S
FA
an
d t
ran
s-fa
tty
aci
ds,
tota
l fa
t
Ea
ch c
om
po
nen
t 0
–3 p
oin
ts, e
xcep
t fo
r al
coh
ol
0–1
po
ints
.
Sco
re: 0
(p
oo
r d
iet)
–25
(hea
lth
y d
iet)
No
rdic
Fo
od
In
dex
(N
FI)
(O
lsen
et
al. 2
011)
F
ish
, cab
bag
e, a
pp
les
and
ber
ries
, ry
e b
read
, oat
mea
l, r
oo
t
veg
etab
les
Ea
ch c
om
po
nen
t 0
–1 p
oin
ts.
Sco
re: 0
(p
oo
r d
iet)
–6 (
hea
lth
y d
iet)
Abbre
via
tions:
AH
EI,
Altern
ative H
ealthy E
ating I
ndex;
BSD
S,
Baltic
Sea D
iet
Score
; D
QI,
Die
t Q
uality
Index;
HEI,
Healthy E
ating I
ndex;
MD
S,
Mediterr
anean D
iet
Score
; M
UFA,
monounsatu
rate
d fatt
y a
cid
; N
FI,
Nord
ic F
ood I
ndex;
PU
FA,
poly
unsatu
rate
d fatt
y a
cid
; RFD
S,
Recom
mended F
innis
h D
iet
Score
; SFA,
satu
rate
d fatt
y
acid
22
3 Aims of the Study
The general aim of this study was to provide evidence on the role of certain nutrients and
diet quality indices in periodontal diseases and, in addition, to compare the associations of
the two diet quality indices, the BSDS and the RFDS with periodontal condition. The more
specific aims are presented below.
1. To study whether omega-3 and omega-6 fatty acids and their ratios are related to the
number of sextants with gingival bleeding and the number of teeth with deepened
periodontal pockets (I).
2. To study the associations of diets based on Nordic food culture and Finnish dietary
recommendations, measured by the Baltic Sea Diet Score (BSDS) and the
Recommended Finnish Diet Score (RFDS), with the number of sextants with gingival
bleeding and the number of teeth with deepened periodontal pockets (II, III).
3. To study the role of diets based on Nordic food culture and Finnish dietary
recommendations, measured by the BSDS and RFDS, in predicting future
periodontal condition and in the development of deepened periodontal pockets (IV).
23
4 Material and Methods 4.1 STUDY POPULATIONS 4.1.1 The Health 2000 Survey The Health 2000 Survey was conducted in Finland in 2000 and 2001 by the National Institute for Health and Welfare (THL) (formerly the National Public Health Institute (KTL) of Finland). The aim of the survey was to get information on public health and functional capacity. The target population consisted of 18-year-old or older people from the mainland of Finland living either at home or at an institution (Laiho et al. 2008, p. 13). The Statistics Finland planned the two-stage, stratified cluster sampling design. First stratification was made according to five university hospital regions (Helsinki, Turku, Tampere, Kuopio, Oulu), each containing about one million inhabitants. Then 80 health centre districts out of 249 were chosen in the Survey. The propability of the 15 largest health centre districts to be chosen in the Survey was 1, and the rest 65 districts were chosen by systematic PPS (Probability-Proportional-to-Size) sampling in each stratum. The Social Insurance of Finland selected the final sample, which was done by systematic sampling, proportioned to the size of the population in the district from these 80 health centre districts. The final samples consisted of 18–29 year-old-people (n=1894) and over 30-year-old people (n=8028) (Aromaa and Koskinen 2004, p. 11). The Health 2000 Survey consisted of a home interview (90 minutes), health examination and interviews about symptoms and mental health. The health examination took about 3 hours and 15 minutes and included measurements (height, body circumference, electrocardiography, blood pressure, spirometry, bioimpedance body composition analysis, heel bone density), laboratory testing, oral health examination, functional capacity tests (physical and cognitive capacity, vision and hearing) and a clinical examination. In addition, participants filled in three questionnaires and a dietary questionnaire. If participants were not able to attend the health examination at the health centre, a home health examination was carried out (100 minutes). At the home interview, background information, data on health and illnesses, medications, use of health care services, lifestyle, living environment, functional capacity, employment, ability to work and need for help and rehabilitation were collected. Those who were not able to attend the home interview, were tried to reach by the telephone and were sent a postal questionnaire. (Figure 1). Due to the activity in reaching participants, some information was obtained from 93% of the sample (Aromaa and Koskinen 2004, pp. 16–20, 22). More information on the protocol of the Health 2000 Survey is presented in the methodology report (Heistaro 2008).
24
Figure 1. The research protocol of the Health 2000 Survey (≥30-year-old adult population). The picture is originally published in the Methodology Report – Health 2000 Survey, p. 17. Printed with the permission of the National Institute for Health and Welfare (THL). 4.1.2 The Health 2011 Survey The Health 2011 Survey was carried out as a follow-up study for the Health 2000 Survey. All living participants of the original sample of the Health 2000 Survey (18 years or older in 2000), who lived in Finland and had not refused to take part in the follow-up studies were invited. The sample of 30-year-old or older adults was 7964 in 2011. Of those, 5806 (73%) took part in at least one part of the Survey and 4218 (53%) in the health examination. The Health 2011 Survey was carried out in outline the same way as the Health 2000 Survey. However, due to the limited resources, interview was implemented in the facilities of the field research instead of home, clinical examination by physicians was not conducted and the oral health examination was conducted only in the southern part (Hospital districts of Helsinki and Uusimaa) and northern part (Hospital districts of Kainuu, Keski-Pohjanmaa, Pohjois-Pohjanmaa, Lappi, Länsipohja, Pohjois-Savo and Vaasa) of Finland. The participation rate in the oral health examinations was 41% (n=1496). The scheme for the health examination in 2011 is presented in the methodology report (Mäki-Opas et al. 2016, p. 37).
25
4.1.3 Subjects
The main sample of 30-year-old and older people consisted of 8028 participants. Of this
sample, 6986 participants were interviewed, 6354 took part in a health examination, 6335 in
the oral health examination and 5998 filled in a FFQ. A more precise description of the
participants in each stage of the Health 2000 Survey is presented in the methodology report
(Koskinen et al. 2008, p. 139). The study populations in each article and manuscript were
composed of the participants who had attended both the oral health examination and filled
in an FFQ. In manuscript IV, the study population consisted of participants who had
attended the oral health examination in both 2000 and 2011. In all studies, (articles I–III,
manuscript IV), participants who had diabetes, rheumatoid arthritis, or inadequate
information on nutrition or periodontal parameters were excluded from the study. In
addition to above mentioned restrictions, articles I and II included only non-smokers and
article III only daily smokers, whereas in manuscript IV, the study population included
both non-smokers and smokers. (Table 6).
Due to the differences in non-oral conditions, such as illnesses and medications, and in
oral conditions such as the number of teeth and the number of teeth with deepened
periodontal pockets, study populations were divided into two age groups: 30–49-year-old
and 50–79-year-old participants (articles I, II and III) (Table 6, Figures 2, 3). The study
population in manuscript IV consisted of 30–49-year-old (baseline) participants, who had
attended oral health examination both in 2000 and 2011. (Table 6).
26
Table
6.
The n
um
ber
of
part
icip
ants
in e
ach s
tudy p
opula
tion in a
rtic
les I
–II
I and m
anuscri
pt
IV
Art
icle
S
tud
y d
esig
n
Th
e n
um
ber
of
30–7
9-
yea
r-o
ld p
arti
cip
an
ts
afte
r re
stri
ctio
ns*
Par
tici
pan
ts i
n t
he
yo
un
ger
ag
e g
rou
p (
30–
49 y
ears
)
Par
tici
pan
ts i
n t
he
old
er
age
gro
up
(50–7
9 y
ears
)
Str
atif
icat
ion
s:
Go
od
ora
l h
yg
ien
e /
po
or
ora
l h
yg
ien
e (3
0–4
9
yea
rs)
Str
atif
icat
ion
s:
Go
od
ora
l h
yg
ien
e /
po
or
ora
l h
yg
ien
e (5
0–7
9
yea
rs)
I C
ross
-sec
tio
nal
, dat
a fr
om
th
e
Hea
lth
200
0 S
urv
ey
2192
no
n-s
mo
ker
s 12
12
980
- -
II
Cro
ss-s
ecti
on
al, d
ata
fro
m t
he
Hea
lth
200
0 S
urv
ey
2187
no
n-s
mo
ker
s 12
10
977
513/
694
391/
569
III
Cro
ss-s
ecti
on
al, d
ata
fro
m t
he
Hea
lth
200
0 S
urv
ey
971
smo
ker
s 70
4 26
7 21
7/48
6 62
/200
Th
e n
um
ber
of
30–4
9-
yea
r-o
ld p
arti
cip
an
ts
afte
r re
stri
ctio
ns*
Th
e n
um
ber
of
30–4
9-
yea
r-o
ld p
arti
cip
ants
in
the
inci
den
ce d
ata
IV
Lo
ng
itu
din
al, d
ata
fro
m t
he
Hea
lth
200
0 an
d 2
011
Su
rvey
s
587
no
n-s
mo
ker
s an
d
smo
ker
s
240
no
n-s
mo
ker
s an
d
smo
ker
s
- -
-
* r
estr
ictions:
dia
bete
s,
rheum
ato
id a
rthri
tis,
inadequate
info
rmation o
n d
iet,
the n
um
ber
of
sexta
nts
with g
ingiv
al ble
edin
g o
r th
e n
um
ber
of
teeth
with d
eepened p
eri
odonta
l pockets
27
Figure 2. The number of teeth and the number of teeth with ≥4 mm deep periodontal pockets in
10-year age groups of the non-smoking study population (articles I and II)
Figure 3. The number of teeth and the number of teeth with ≥4 mm deep periodontal pockets in
10-year age groups of the smoking study population (article III)
28
4.2 METHODS
Oral health examination
A dentist, assisted by a nurse, performed the oral health examination as part of the health
examination and it took about 15 minutes per participant. The examination was conducted
in a portable dental treatment unit (Dentronic Mini-Dent®, Planmeca Oy, Helsinki, Finland),
with the aid of a headlamp (Tekmala Oy) and fibre optic light (Novar). A dental mirror and
a WHO periodontal probe was used in the examination.The examination of the
periodontium was done for every participant with teeth during the oral health examination,
except for those who would have needed antibiotic prophylaxis (Suominen-Taipale and
Vehkalahti 2008, pp. 13–14). In 2011, the oral health examination was slightly modified
when compared to the oral health examination in 2000. However, the periodontal pocket
measurements were identical in both years (Vehkalahti and Suominen 2016, p. 128).
4.2.1 Periodontal condition
Measurement of periodontal pockets
Periodontal pocket depths (PD) were measured on every tooth except wisdom teeth and
tooth remnants using 20 g force. The clinical examination was performed on four surfaces
of every tooth: distobuccal, buccal, mesiolingual and lingual surfaces. Measurements were
registered as follows:”no periodontal pocket”, ”a PD of 4–5 mm” and ”a PD of ≥ 6 mm”.
Only the deepest pocket of each tooth was recorded (Knuuttila and Suominen-Taipale 2008,
p. 49). In all articles, the latter two categories were combined to represent a tooth with a PD
of ≥ 4 mm. The distribution of the number of teeth with a PD of ≥ 4 mm among non-
smoking and smoking study populations is presented in Figure 4.
Measurement of gingival bleeding
Gingival bleeding was assessed based on bleeding on probing (BOP) that was observed
immediately after probing. In the Health 2000 Survey, it was recorded on a maximum of
three sextants per upper jaw and three sextants per lower jaw (Knuuttila and Suominen-
Taipale 2008, p. 49). The recording was done, if there were at least two teeth per sextant. In
2011, the recording of gingival bleeding was done by tooth (yes/no) (Vehkalahti and
Suominen 2016, p. 130).
The level of oral hygiene
The presence of dental plaque was observed in the examination with a modified form of
Silness-Löe plaque index (Silness and Löe 1964). During the Health 2000 Survey, plaque
was measured on one surface of three teeth: the buccal surface of the most posterior tooth
on the upper right side; the lingual surface of the most posterior tooth on the lower left side
and the buccal surface of tooth 33. The presence of plaque was recorded as no visible
plaque, visible plaque in gingival margins and visible plaque elsewhere. The highest value
29
of the indicator teeth was used to describe the level of oral hygiene (Vehkalahti and
Knuuttila 2008, p. 26). In articles II ja III, a stratified analysis was conducted by the level of
oral hygiene: those who had no visible plaque on the teeth were categorized as having good
oral hygiene, and the ones with visible plaque on gingival margins or visible plaque
elsewhere on the teeth as having poor oral hygiene. During the Health 2011 Survey, the
presence of plaque was measured and recorded on the buccal surface of every tooth
(yes/no) (Vehkalahti and Suominen 2016, p. 130).
Figure 4. The distributions (%) of the number of teeth with ≥ 4 mm deep periodontal pockets
among the 30–79-year-old non-smoking (articles I and II) and smoking (article III) study
populations without diabetes or rheumatoid arthritis
4.2.2 Dietary assessments
Food frequency questionnaire (FFQ)
Information on the consumption of foods and intake of nutrients during the past year was
assessed based on the FFQs. Experience from earlier Finnish studies was taken into account
when planning the questionnaire form, which consisted of 128 foods and drinks that were
commonly consumed in Finland. Foods were categorized to represent dairy, cereals, fat
spreads, vegetables, potato, pasta and rice, meat, fish, fruits and berries, desserts, sweets
and other snack foods, and drinks. The frequency of the use of foods ranged from never or
rarely to six or more times a day in nine categories. Fixed portion sizes were illustrated in
the questionnaire form as references. Food consumption was converted into grams per day
so that the frequency of the food item was multiplied by a fixed portion size. Daily food
consumption and nutrient intakes were calculated using the national food composition
database, Fineli® (Reinivuo et al. 2010). When estimating the fat content of dishes,
assumption of fats was based on sales statistics of cooking fats in Finland. The destruction
of nutrients during cooking was not taken into account.
30
Fatty acids
Information on the daily intake of omega-3 PUFAs as a whole (ALA, eicosatetraenoic
acid, EPA, docosapentaenoic acid, DHA) (g/day) and EPA and DHA (mg/day) separately,
as well as omega-6 PUFAs as a whole (LA, gammalinoleic acid, dihomo-gamma-linoleic
acid, AA) (g/day) and AA (mg/day) separately was obtained from the FFQs. In addition to
the afore-mentioned variables, the ratios of EPA/AA, DHA/AA and omega-3/omega-6
PUFAs were used as continuous variables and as categorized into quintiles in article I.
Baltic Sea Diet Score (BSDS)
The BSDS was based on the Nordic food culture, but complied also dietary
recommendations and it included foods that were produced locally in the Nordic countries
(Kanerva et al. 2014a). BSDS consisted of nine components, six of them were food groups
and three represented nutrient intakes. Healthy food items or nutrients were considered as
positive and unhealthy as negative. The score ranged between 0 and 25 and was
interpreted: the higher the score, the healthier the diet. The positive variables were fruits
and berries (apples, pears and berries); vegetables (leafy vegetables, cucumber, tomatoes,
peas, cabbages and roots, excluding potato); cereals (rye, oats and barley); low-fat milk
(low-fat and fat-free milk); fish (salmon and freshwater fish); and fat ratio (the ratio of
PUFA to SFA and trans-fatty acids). The negative variables were red meat (beef, pork,
processed meat products and sausage); total fat intake as a percentage of the total energy
intake (E%); and alcohol (ethanol intake). The score was calculated according to quartiles of
consumption for each score component. For the positive score components, the lowest
quartile was given 0 points, the second one 1 point, the third one 2 points and the highest
quartile of intake 3 points. For the negative score components, points were given in reverse
order, with the exception of alcohol, which was given 0–1 point (one point was given if the
ethanol intake was < 20 g for men and < 10 g for women, otherwise zero points were given).
The points given for each component were summed up for the overall score.
In article II, BSDS was used both as a continuous variable and categorized into quintiles.
In articles III and IV, BSDS was used as a continuous variable and categorized into tertiles.
The category boundaries for BSDS in each subpopulation are presented in the articles.
Recommended Finnish Diet Score (RFDS)
RFDS was based on Finnish dietary recommendations and was more general in nature than
the BSDS, because it consisted of food items and nutrients that are produced either locally
or abroad (Kanerva et al. 2013a). The RFDS consisted of eight components, four of them
were food groups and four represented nutrients. The score ranged between 0 and 24 and
was interpreted: the higher the score, the healthier the diet. The evaluation of the food
items and nutrients and the interpretation of the score was similar to BSDS. The five
positive components were fruits (apples, citruses and other fruits and berries); vegetables
(fruit vegetables, leafy vegetables, roots, cabbages, legumes, mushrooms, excluding potato);
the ratio of white meat (poultry, fish and fish products) to red and processed meat (beef,
pork, lamb, sausage, meat products, game and offal); rye, which was used to represent
dietary fibre intake and is the most common source of fibre in Finland; and the ratio of
31
PUFA to SFA and trans-fatty acids. The three negative components of the score were salt (g/day), sucrose (E%) and alcohol (E%). The score was calculated according to quartiles of consumption of each score component. For the positive score components, the lowest quartile was given 0 points, the second one 1 point, the third one 2 points and the highest quartile of intake 3 points. For the negative score components, points were given in reverse order. The points given for each component were summed up for the overall score. In article II, RFDS was used both as a continuous variable and categorized into quintiles. In article III and manuscript IV, RFDS was used as a continuous variable and categorized into tertiles. The category boundaries for RFDS in each subpopulation are presented in the articles. 4.2.3 Confounding variables Level of education Information on the level of education was asked as a part of the home interview by asking about formal schooling and vocational training. Education was categorized into three categories: basic, intermediate and higher education. Those with no formal vocational training or senior secondary education were classified to have basic education. The ones who had completed vocational training or passed the matriculation examination were considered to have intermediate education. Those with higher education had degrees or diplomas from higher vocational institutions, polytechnics and universities. Dental attendance pattern and toothbrushing frequency
Information on dental attendance pattern was asked as part of the health interview in both 2000 and 2011. In the cross-sectional study, it was categorized into the following categories: visiting a dentist regularly for a check-up vs. visiting a dentist only when experiencing toothache or other symptoms or never. In the longitudinal study, dental attendance pattern was categorized as visiting a dentist regularly in 2000, in 2011, in both years and in neither year. Information on toothbrushing frequency was asked as part of the health interview. It was categorized into the following categories: twice a day or more, once a day, and less than once a day or never. Smoking Information on smoking was asked as part of the home interview in both 2000 and 2011. In articles I and II, participants were considered to be non-smokers, if they did not report any smoking in the past, or they reported having smoked under 100 times in the past, or they reported smoking in the past over 100 times, but the smoking did not continue for one year and the most recent smoking occasion was over one month ago (information from year 2000). In article III, participants were considered to be daily smokers if they reported having smoked daily for at least a year and the latest smoking occasion was on the day of the interview or a day before (information from year 2000). In manuscript IV, participants were considered to be daily smokers if they reported that they smoked cigarettes daily;
32
occasional smokers if they reported that they smoked cigarettes occasionally and non-smokers if they reported that they did not smoke either at the moment or in the past (information from year 2011). Physical exercise Information on physical activity was asked as a part of self-administered questionnaire in 2000 and 2011 by using the Gothenburg scale (Wilhelmsen et al. 1972) and the International Physical Activity Questionnaire scale (Craig et al. 2003) that measure the physical activity during leisure time, household work, walking and sitting. The variable was based on two questions of the frequency of ≥ 30 minutes moderate to hard physical activity on leisure time in a week, and the time used for walking or cycling on the way to work in a day. In the cross-sectional study, the level of physical activity was categorized as physical activity of ≥ 30 minutes 4–7 times a week, 2–3 times a week, once a week, or 2–3 times a month or less. In the longitudinal study, the level of physical activity was categorized as optimal when the participant reported having ≥ 30 minutes leisure time exercise at least four times a week and ≥ 30 minutes walk or cycling on the way to work a day. It was categorized as adequate when the participant reported of ≥ 30 minutes leisure time exercise at least four times a week or ≥ 30 minutes walk or cycling on the way to work a day. The level of physical activity was categorized as uncertain when the participant reported having ≥ 30 minutes leisure time exercise 2–3 times a week and < 30 minutes walk or cycling on the way to work a day. The level of physical activity was categorized as inadequate when the participant reported of ≥ 30 minutes leisure time exercise once a week or less and of < 30 minutes walk or cycling on the way to work a day. Use of supplements Information on the use of any kind of vitamin or trace element supplements was asked in the FFQ. It was categorized as regular use vs. no use (in 2000). Use of non-steroidal anti-inflammatory drugs (NSAID)
Information on the use of medication was asked as part of the health interview in 2000 and 2011. Participants were asked to indicate the names of the medicines they had used during the past seven days, and the responses were checked by the interviewer from packages or prescriptions. Medicines were further classified in accordance with the Pharmaca Fennica prescription medicine compendium. Participants were considered to use NSAID, if they reported having used them in the past seven days. If the information was from year 2000, the use of NSAID was categorized as use, no use, or information missing. If the information was from year 2011, it was used as a dichotomous variable (use vs. no use) in the multivariable models.
33
Diabetes and rheumatoid arthritis Information on whether participants had rheumatoid arthritis or diabetes diagnosed by a physician was asked as part of the health interview in both 2000 and 2011. In 2000 the absence of diabetes was further confirmed in the health examination and from registers and by laboratory measurements (fasting glucose less than 7.0 mmol/l, and/or the results of the glucose tolerance test less than 11.1 mmol/l). Body mass index The body mass index (BMI) is a measure of weight (kilograms) in relation to the square of height (metres) (kg/m2). The weight of the participants was measured as a part of the bioimbedance body composition analysis and the height of the participants by a stadiometer in 2000 and 2011. The information on weight and height was also asked as a part of a self-administered questionnaire. BMI was calculated based on this information and it was used in the multivariable models as a continuous variable in the cross-sectional studies (information from year 2000) and in the longitudinal study (information from year 2000 and the change between 2000 and 2011). C-reactive protein High sensitivity C-reactive protein (Hs-CRP) level was measured as a part of the laboratory testing from the venous blood in 2000 and 2011. The serum samples were first kept on the table for clotting, then sentrifuged, pipetted into smaller tubes and frozen into -20 degrees Celsius. Hs-CRP was quantified using an automated analyser and an immunoturbidimetric test. Hs-CRP was used as a continuous variable in the multivariable models in the cross-sectional studies (information from year 2000) and the longitudinal study (information from year 2011). Due to the skewed distribution of the CRP concentrations, the values were logarithmically transformed. Baseline characteristics and potential counfounders of study populations in articles I–III and manuscript IV are presented in Table 7, and those of non-smoking and smoking study populations according to the tertiles of the Baltic Sea Diet Score (BSDS) and the Recommended Finnish Diet Score (RFDS) in Table 8.
34
Table
7.
Baseline c
hara
cte
ristics o
f th
e s
tudy p
opula
tions in a
rtic
les I
–II
I and m
anuscri
pt
IV
A
rtic
le I
, cro
ss-s
ecti
on
al
(200
0)
A
rtic
le I
I, c
ross
-sec
tio
nal
(200
0)
A
rtic
le I
II, c
ross
-sec
tio
nal
(200
0)
M
anu
scri
pt
IV,
lon
git
ud
inal
(2
000,
201
1)
30–7
9
yea
rs,
n=2
192
no
n-
smo
ker
s
30–4
9 y
ears
,
n=
1212
50–7
9 y
ears
,
n=9
80
30–7
9 y
ears
,
n=2
187
no
n-
smo
ker
s
30–4
9 y
ears
,
n=1
210
50–7
9 y
ears
,
n=9
77
30–7
9 y
ears
,
n=9
71
smo
ker
s
30–4
9 y
ears
,
n=7
04
50–7
9 y
ears
,
n=2
67
30–4
9 y
ears
,
n=
587
no
n-
smo
ker
s
and
smo
ker
s
Inci
den
ce
dat
a, 3
0–49
yea
rs,
n=2
40
n
(%
)
Sex
Mal
e
Fem
ale
786
(36)
1406
(64
)
468
(39)
744
(61)
318
(32)
662
(68)
784
(36)
1403
(64
)
466
(39)
744
(61)
318
(33)
659
(67)
515
(53)
456
(47)
364
(52)
340
(48)
151
(57)
116
(43)
248
(42)
339
(58)
84 (
35)
156
(65)
Ed
uca
tio
n
Bas
ic
Inte
rmed
iate
Hig
her
572
(26)
698
(32)
922
(42)
138
(11)
436
(36)
638
(53)
434
(44)
262
(27)
284
(29)
571
(26)
694(
32)
922
(42)
138
(11)
434
(36)
638
(53)
433
(44)
260
(27)
284
(29)
331
(34)
402
(41)
236
(24)
187
(27)
334
(48)
182
(26)
144
(54)
68 (
26)
54 (
20)
67 (
11)
202
(35)
315
(54)
29 (
12)
61 (
25)
150
(63)
Lev
el o
f o
ral
hy
gie
ne
Go
od
*
Po
or*
*
904
(41)
1268
(59
)
513
(42)
696
(58)
391
(40)
572
(60)
904
(41)
1263
(59
)
513
(42)
694
(58)
391
(40)
569
(60)
279
(29)
686
(71)
217
(31)
486
(69)
62 (
24)
200
(76
)
211
(36)
***
376
(64)
***
114
(48)
***
126
(52)
***
Nu
mb
er o
f te
eth
wit
h d
eep
ened
per
iod
on
tal
po
cket
s
0 1–3
4–6
7–11
12+
915
(42)
614
(28)
296
(14)
244
(11)
123
(5.6
)
581
(48)
342
(28)
130
(11)
113
(9.3
)
46 (
3.8)
334
(34)
272
(28)
166
(17)
131
(13)
77 (
7.9)
913
(42)
613
(28)
294
(13)
244
(11)
123
(6)
580
(48)
342
(28)
129
(11)
113
(9)
46 (
4)
333
(34)
271
(28)
165
(17)
131
(13)
77 (
8)
277
(29)
203
(21)
149
(15)
138
(14)
204
(21)
227
(32)
147
(21)
110
(16)
86 (
12)
134
(19)
50 (
19)
56 (
21)
39 (
15)
52 (
19)
70 (
26)
238
(40)
165
(28)
81 (
14)
47 (
8)
53 (
9)
240
(100
)
0 (0
)
0 (0
)
0 (0
)
0 (0
) *N
o p
laq
ue
on
th
e in
dic
ato
r te
eth
.
**P
laq
ue
on
th
e g
ing
ival
mar
gin
or
else
wh
ere
on
th
e in
dic
ato
r te
eth
. **
* In
yea
r 20
00.
35
Table
8.
Backgro
und c
hara
cte
ristics o
f th
e n
on-s
mokin
g a
nd s
mokin
g s
tudy p
opula
tions in t
ert
iles (
low
indic
ating a
poor
die
t and h
igh indic
ating a
healthy d
iet)
of th
e B
altic
Sea D
iet
Score
and t
he R
ecom
mended F
innis
h D
iet
Score
Bal
tic
Sea
Die
t S
core
N
on
-sm
ok
ers
S
mo
ker
s
Ter
tile
s
Ra
ng
e
Lo
w
3–11
Mid
dle
12–1
4
Hig
h
15–2
5
L
ow
2–11
Mid
dle
12–1
4
Hig
h
15–2
4
30–4
9 y
ears
, n
433
343
434
25
6 19
4 25
4
n
(%
)
Sex
Mal
e
Fem
ale
198
(46)
235
(54)
147
(43)
196
(57)
121
(28)
313
(72)
162
(63)
94 (
37)
97 (
50)
97 (
50)
105
(41)
149
(59)
Ed
uca
tio
n
Bas
ic
Inte
rmed
iate
Hig
her
44 (
10)
174
(40)
215
(50)
50 (
15)
106
(31)
187
(55)
44 (
10)
154
(35)
236
(54)
75 (
29)
131
(51)
50 (
20)
53 8
27)
88 (
45)
53 (
27)
59 (
23)
115
(45)
79 (
31)
Lev
el o
f o
ral
hy
gie
ne
Go
od
*
Po
or*
168
265
138
204
207
225
67 (
26)
188
(74)
59 (
30)
135
(70)
91 (
36)
163
(64)
Nu
mb
er o
f te
eth
wit
h
dee
pen
ed p
erio
do
nta
l
po
cket
s
0 1–3
4–6
7–11
12+
204
(47)
128
(30)
42 (
10)
42 (
10)
17 (
4)
159
(46)
91 (
27)
41 (
12)
38 (
11)
14 (
4)
217
(50)
123
(28)
46 (
11)
33 (
8)
15 (
3)
70 (
27)
46 (
18)
50 (
20)
32 (
13)
58 (
23)
62 (
32)
49 (
25)
27 (
14)
26 (
13)
30 (
15)
95 (
37)
52 (
20)
33 (
13)
28 (
11)
46 (
18)
M
ean
(S
E)
Th
e n
um
ber
of
teet
h
27.5
(0.
2)
27.1
(0.
2)
27.0
(0.
2)
25.5
(0.
4)
25.5
(0.
4)
25.8
(0.
3)
Hs-
CR
P m
g/l
1.5
(0.2
) 1.
3 (0
.1)
1.2
(0.1
)
1.9
(0.3
) 2.
0 (0
.3)
1.7
(0.2
)
BM
I 25
.7 (
0.2)
25
.8 (
0.2)
25
.5 (
0.2)
25.6
(0.
3)
25.7
(0.
3)
26.0
(0.
2)
Table
8 t
o b
e c
ontinued
36
Table
8 c
ontinues
Ter
tile
s
Ra
ng
e
Lo
w
1–10
Mid
dle
11–1
4
Hig
h
15–2
5
L
ow
2–11
Mid
dle
12–1
4
Hig
h
15–2
4
50–7
9 y
ears
, n
284
333
360
93
79
95
n
(%
)
Sex
Mal
e
Fem
ale
123
(43)
161
(57)
116
(35)
217
(65)
79 (
22)
281
(78)
66 (
71)
27 (
29)
43 (
54)
36 (
46)
42 (
44)
53 (
56)
Ed
uca
tio
n
Bas
ic
Inte
rmed
iate
Hig
her
132
(46)
79 (
28)
73 (
26)
145
(44)
83 (
25)
105
(32)
156
(43)
98 (
27)
106
(29)
58 (
62)
19 (
20)
16 (
17)
41 (
52)
20 (
25)
18 (
23)
45 (
48)
29 (
31)
20 (
21)
Lev
el o
f o
ral
hy
gie
ne
Go
od
*
Po
or*
106
(38)
173
(62)
117
(36)
208
(64)
168
(47)
188
(53)
15 (
17)
75 (
83)
12 (
14)
66 (
86)
35 (
37)
59 (
63)
Nu
mb
er o
f te
eth
wit
h
dee
pen
ed p
erio
do
nta
l
po
cket
s
0 1–3
4–6
7–11
12+
93 (
33)
75 (
26)
47 (
17)
37 (
13)
32 (
11)
114
(34)
90 (
27)
53 (
16)
50 (
15)
26 (
8)
126
(35)
106
(29)
65 (
18)
44 (
12)
19 (
5)
14 (
15)
21 (
23)
13 (
14)
14 (
15)
31 (
33)
13 (
17)
13 (
17)
10 (
13)
23 (
29)
20 (
25)
23 (
24)
22 (
23)
16 (
17)
15 (
16)
10 (
20)
M
ean
(S
E)
Th
e n
um
ber
of
teet
h
20.6
(0.
5)
20.9
(0.
4)
20.6
(0.
4)
17.9
(0.
9)
19.2
(0.
8)
18.1
(0.
9)
Hs-
CR
P m
g/l
1.
8 (0
.2)
1.8
(0.2
) 1.
5 (0
.2)
3.
9 (0
.8)
3.0
(0.7
) 1.
7 (0
.3)
BM
I 27
.4 (
0.3)
27.5
(0.
3)
26.9
(0.
2)
26
.6 (
0.4)
26
.6 (
0.4)
26
.4 (
0.4)
Table
8 t
o b
e c
ontinued
37
Table
8 c
ontinues
R
eco
mm
end
ed F
inn
ish
Die
t S
core
Ter
tile
s
Ra
ng
e
Lo
w
0–7
Mid
dle
8–10
Hig
h
11–1
8
L
ow
0–7
Mid
dle
8–10
Hig
h
11–1
8
30–4
9 y
ears
, n
42
6 35
8 42
6
245
213
246
n
(%
)
Sex
Mal
e
Fem
ale
218
(51)
208
(49)
129
(36)
229
(64)
119
(28)
307
(72)
160
(65)
85 (
35)
109
(51)
104
(49)
95 (
39)
151
(61)
Ed
uca
tio
n
Bas
ic
Inte
rmed
iate
Hig
her
60 (
14)
174
(41)
192
(45)
37 (
10)
125
(35)
196
(55)
41 (
10)
135
(32)
250
(59)
73 (
30)
130
(53)
42 (
17)
56 (
26)
99 (
46)
58 (
27)
58 (
24)
105
(43)
82 (
33)
Lev
el o
f o
ral
hy
gie
ne
Go
od
*
Po
or*
167
(39)
258
(61)
149
(42)
208
(58)
197
(46)
228
(54)
62 (
25)
182
(75)
61 (
29)
152
(71)
94 (
38)
152
(62)
Nu
mb
er o
f te
eth
wit
h
dee
pen
ed p
erio
do
nta
l
po
cket
s
0 1–3
4–6
7–11
12+
206
(48)
117
(27)
46 (
11)
43 (
10)
14 (
3)
168
(47)
100
(28)
38 (
11)
35 (
10)
17 (
5)
206
(48)
125
(29)
45 (
11)
35 (
8)
15 (
4)
65 (
27)
47 (
19)
46 (
19)
34 (
14)
53 (
22)
69 (
32)
50 (
23)
31 (
15)
25 (
12)
38 (
18)
93 (
38)
50 (
20)
33 (
13)
27 (
11)
43 (
17)
M
ean
(S
E)
Th
e n
um
ber
of
teet
h
27.2
(0.
2)
27.3
(0.
2)
27.1
(0.
2)
25.1
(0.
4)
25.6
(0.
4)
26.2
(0.
3)
Hs-
CR
P
1.5
(0.2
)
1.2
(0.1
) 1.
4 (0
.1)
2.
0 (0
.3)
1.8
(0.2
) 1.
6 (0
.2)
BM
I 25
.7 (
0.2)
25
.7 (
0.2)
25
.5 (
0.2)
25.1
(0.
3)
25.8
(0.
3)
26.3
(0.
2)
Table
8 t
o b
e c
ontinued
38
Table
8 c
ontinues
Ter
tile
s
Ra
ng
e
Lo
w
0–7
Mid
dle
8–10
Hig
h
11–1
8
L
ow
1–7
Mid
dle
8–10
Hig
h
11–1
7
50–7
9 y
ears
, n
332
301
344
92
85
90
n
(%
)
Sex
Mal
e
Fem
ale
152
(46)
180
(54)
97 (
32)
204
(68)
69 (
20)
275
(80)
64 (
70)
28 (
30)
48 (
56)
37 (
44)
39 (
43)
51 (
57)
Ed
uca
tio
n
Bas
ic
Inte
rmed
iate
Hig
her
164
(49)
88 (
27)
80 (
24)
135
(45)
68 (
23)
98 (
33)
134
(39)
104
(30)
106
(31)
54 (
59)
22 (
24)
16 (
17)
49 (
58)
18 (
21)
18 (
21)
41 (
46)
28 (
31)
20 (
22)
Lev
el o
f o
ral
hy
gie
ne
Go
od
*
Po
or*
117
(36)
208
(64)
117
(40)
176
(60)
157
(46)
185
(54)
15 (
16)
76 (
84)
17 (
20)
66 (
80)
30 (
34)
58 (
66)
Nu
mb
er o
f te
eth
wit
h
dee
pen
ed p
erio
do
nta
l
po
cket
s
0 1–3
4–6
7–11
12+
110
(33)
85 (
26)
57 (
17)
48 (
14)
32 (
10)
113
(38)
84 (
28)
44 (
15)
41 (
14)
19 (
6)
110
(32)
102
(30)
64 (
19)
42 (
12)
26 (
8)
11 (
12)
21 (
23)
12 (
13)
18 (
20)
30 (
33)
19 (
22)
15 (
18)
13 (
15)
17 (
20)
21 (
25)
20 (
22)
20 (
22)
14 (
16)
17 (
19)
19 (
21)
M
ean
(S
E)
Th
e n
um
ber
of
teet
h
19.8
(0.
5)
20.8
(0.
4)
21.5
(0.
4)
18.0
(0.
9)
18.8
(0.
9)
18.3
(0.
9)
Hs-
CR
P m
g/l
1.9
(0.3
) 1.
6 (0
.1)
1.5
(0.2
)
4.0
(0.8
) 2.
2 (0
.4)
2.3
(0.7
)
BM
I 27
.4 (
0.2)
27
.2 (
0.2)
27
.2 (
0.2)
26.1
(0.
4)
26.3
(0.
4)
27.3
(0.
4)
Abbre
via
tions:
BM
I, b
ody m
ass index;
Hs-C
RP m
g/l
, hig
h-s
ensitiv
ity C
-reactive p
rote
in m
illigra
ms/l
itre
; SE,
sta
ndard
err
or
39
4.3 STATISTICAL METHODS
The sample in the Health 2000 Survey was compiled using a two-stage cluster sampling,
and weighting was used to take into account the non-response, except in manuscript IV.
SAS callable SUDAAN Research Triangle Institute, Raleigh NC, USA (Release 11.0.1.)
software was used in articles I–III to perform data analyses to take into account the
sampling design. In manuscript IV, SAS statistical package, version 9.4., PROC GENMOD,
Cary NC, USA was used to perform the data analyses.
Due to the count data and the skewed distribution of the outcome variable, prevalence
rate ratios (PRR) and 95% confidence intervals (95% CI) in articles I–III and incidence rate
ratios (IRR) and 95% CI (manuscript IV) were estimated using Poisson regression models.
The number of sextants with gingival bleeding was used as an offset variable in the models
with gingival bleeding as an outcome, whereas the number of teeth with deepened
periodontal pockets was used as an offset variable in the models with deepened
periodontal pockets as an outcome.
To take into account the confounding related to total energy intake, all the nutrient
variables except alcohol E% were corrected using the residual method before fitting the
regression models (Willett and Stampfer 1986).
In articles I–III, the study population was stratified into 30–49-year-old and 50–79-year-
old age groups. In articles II and III, data were stratified also according to the level of oral
hygiene.
4.4 ETHICAL CONSIDERATIONS
Ethical approval applications of the Health 2000 Survey and the Health 2011 Survey were
approved by the Ethical Committee for Epidemiology and Public Health of the Hospital
District of Helsinki and Uusimaa and the application of the Health 2000 Survey also by the
Ethical Committee for National Public Health Institute (KTL) of Finland.
Participation to the study was voluntary, although recommended. The participants
received information letters during the home interview and the clinical health examination,
and they were able to ask questions at both occasions. After being informed, they were
asked to sign consent forms. Those who did not contact the project organization, were tried
to reach by phone and mail.
Information security was high during every part of the study: coded information was sent
using protected internet connections and this information contained only identification
numbers, not actual names of the participants. The data were further storaged in a way that
the researchers were not able to identify single persons when analyzing the data.
40
5 Results
5.1 ASSOCIATIONS OF POLYUNSATURATED FATTY ACIDS WITH
PERIODONTAL CONDITION
Daily intake of single PUFAs (AA, EPA, DHA), omega-3 (ALA, eicosatetraenoic acid,
EPA, docosapentaenoic acid, DHA), omega-6 fatty acids (LA, gammalinoleic acid, dihomo-
gamma-linoleic acid, AA), and ratios of omega-3 and omega-6 PUFAs, EPA and AA, and
DHA and AA were analyzed in relation to the number of sextants with gingival bleeding
and the number of teeth with deepened periodontal pockets among 30–49-year-old and 50–
79-year-old participants. In these data, there were no consistent associations between intake
of PUFAs or the ratios of PUFAs and the number of sextants with gingival bleeding or the
number of teeth with deepened periodontal pockets in neither age groups (Figures 5, 6, 7
and 8, article I).
Figure 5. Prevalence rate ratios and 95% confidence intervals for the number of sextants with
gingival bleeding among 30–49-year-old participants. Arachidonic acid (AA) mg/day,
eicosapentaenoic acid (EPA) mg/day and docosahecsaenoic acid (DHA) mg/day as quintiles I–V
were used as explanatory variables.
41
Figure 6. Prevalence rate ratios and 95% confidence intervals for the number of sextants with
gingival bleeding among 50–79-year-old participants. Arachidonic acid (AA) mg/day,
eicosapentaenoic acid (EPA) mg/day and docosahecsaenoic acid (DHA) mg/day in quintiles I–V
were used as explanatory variables.
Figure 7. Prevalence rate ratios and 95% confidence intervals for the number of ≥ 4 mm
deepened periodontal pockets among 30–49-year-old participants. Arachidonic acid (AA)
mg/day, eicosapentaenoic acid (EPA) mg/day and docosahecsaenoic acid (DHA) mg/day in
quintiles I–V were used as explanatory variables.
42
Figure 8. Prevalence rate ratios and 95% confidence intervals for the number of ≥ 4 mm
deepened periodontal pockets among 50–79-year-old participants. Arachidonic acid (AA)
mg/day, eicosapentaenoic acid (EPA) mg/day and docosahecsaenoic acid (DHA) mg/day in
quintiles I–V were used as explanatory variables.
5.2 ASSOCIATIONS OF DIETS BASED ON NORDIC FOOD CULTURE AND
FINNISH DIETARY RECOMMENDATIONS WITH PERIODONTAL CONDITION
Non-smokers
In the total non-smoking study population, a weak inverse association was observed
between BSDS (p=0.04) and RFDS (p=0.01) and the number of sextants with gingival
bleeding in participants aged 30–49 years, but not in those aged 50–79 years. No consistent
association between scores and the number of teeth with deepened periodontal pockets was
observed in 30–79-year-old participants.
In the stratified analysis according to the level of oral hygiene, an inverse association
between scores and the number of sextants with gingival bleeding was observed both in the
younger (BSDS, p=0.06 and RFDS, p=0.01) and the older (BSDS, p=0.02 and RFDS, p=0.01)
age groups with poor oral hygiene. An inverse association was observed between BSDS
(p=0.02) and RFDS (p=0.03) and the number of teeth with deepened periodontal pockets in
the participants aged 50–79 years with poor oral hygiene. (Table 9).
43
Table 9. Prevalence rate ratios and 95% confidence intervals for the number of sextants with
gingival bleeding and the number of teeth with deepened periodontal pockets in quintiles (low
indicating a poor diet and high indicating a healthy diet) of the Baltic Sea Diet Score (BSDS)
and the Recommended Finnish Diet Score (RFDS) first among the total non-smoking study
population and then stratified according to the level of oral hygiene
The number of sextants with gingival
bleeding
The number of teeth with deepened periodontal
pockets
BSDS, quintiles
I (ref.)–V
RFDS, quintiles
I (ref.)–V
BSDS, quintiles
I (ref.)–V
RFDS, quintiles
I (ref.)–V
30–49 years1, n= 1210
ref.
1.12 (0.96–1.30)
1.05 (0.91–1.21)
0.94 (0.83–1.08)
0.89 (0.76–1.04)
p=0.043
ref.
0.91 (0.78–1.07)
0.92 (0.81–1.04)
0.75 (0.63–0.88)
0.80 (0.67–0.95)
p=0.006
ref.
1.33 (0.97–1.83)
1.16 (0.93–1.45)
1.10 (0.87–1.39)
1.20 (0.89–1.61)
p=0.396
ref.
1.19 (0.90–1.58)
1.19 (0.94–1.51)
1.13 (0.84–1.52)
1.16 (0.84–1.60)
p=0.682
Good oral hygiene2,3,
n= 513
ref.
1.15 (0.82–1.62)
1.22 (0.89–1.67)
1.00 (0.73–1.37)
0.94 (0.66–1.33)
p= 0.442
ref.
0.77 (0.55–1.07)
0.82 (0.64–1.07)
0.80 (0.57–1.12)
0.66 (0.46 – 0.94)
p= 0.211
ref.
1.35 (0.72–2.55)
1.47 (0.96–2.24)
1.18 (0.71–1.98)
1.27 (0.81–2.01)
p= 0.503
ref.
0.97 (0.58–1.61)
0.93 (0.54–1.61)
1.15 (0.59 – 2.25)
0.87 (0.50–1.52)
p= 0.851
Poor oral hygiene3,4,
n= 694
ref.
1.08 (0.91–1.29)
0.98 (0.84–1.14)
0.91 (0.78–1.06)
0.85 (0.71–1.02)
p= 0.061
ref.
0.96 (0.80–1.15)
0.94 (0.81–1.10)
0.71 (0.58–0.87)
0.86 (0.70–1.05)
p= 0.013
ref.
1.21 (0.84–1.72)
1.02 (0.77–1.34)
0.99 (0.74–1.32)
1.11 (0.77–1.58)
p= 0.740
ref.
1.16 (0.83–1.61)
1.18 (0.89–1.57)
0.99 (0.73–1.35)
1.15 (0.79–1.66)
p= 0.680
50–79 years1, n= 977
ref.
0.93 (0.81–1.07)
1.00 (0.87–1.14)
0.93 (0.80–1.08)
0.87 (0.74–1.04)
p=0.399
ref.
0.96 (0.84–1.09)
0.88 (0.76–1.02)
0.97 (0.82–1.15)
0.85 (0.71–1.01)
p=0.234
ref.
0.84 (0.67–1.05)
0.85 (0.69–1.05)
0.80 (0.64–0.99)
0.83 (0.64–1.07)
p=0.288
ref.
0.86 (0.71–1.05)
0.69 (0.55–0.88)
0.96 (0.74–1.23)
0.86 (0.64–1.14)
p=0.033
Good oral hygiene2,3,
n= 391
ref.
1.05 (0.78–1.43)
1.22 (0.90–1.65)
0.89 (0.63–1.26)
1.11 (0.79–1.58)
p= 0.402
ref.
1.13 (0.80–1.61)
1.10 (0.79–1.52)
1.19 (0.84–1.70)
1.10 (0.76–1.59)
p= 0.901
ref.
0.56 (0.35–0.89)
0.88 (0.58–1.34)
0.82 (0.50–1.35)
1.04 (0.63–1.71)
p= 0.037
ref.
0.88 (0.57–1.34)
0.74 (0.47–1.18)
1.00 (0.63–1.59)
1.15 (0.69–1.93)
p= 0.403
Poor oral hygiene3,4,
n= 569
ref.
0.87 (0.74–1.03)
0.92 (0.79–1.08)
0.94 (0.78–1.13)
0.77 (0.64–0.91)
p= 0.024
ref.
0.89 (0.78–1.02)
0.82 (0.70–0.97)
0.86 (0.72–1.03)
0.72 (0.59–0.88)
p= 0.010
ref.
0.87 (0.67–1.11)
0.79 (0.62–1.01)
0.73 (0.57–0.94)
0.65 (0.49–0.86)
p= 0.024
ref.
0.85 (0.68–1.06)
0.66 (0.49–0.89)
0.85 (0.64–1.12)
0.64 (0.46–0.88)
p= 0.027 1 Adjusted for age, gender, level of education, plaque, use of supplements, alcohol E%, logarithmically transformed C-reactive protein,
body mass index. 2 No plaque on the reference teeth. 3 Adjusted for age, gender, level of education, use of supplements, alcohol E%, logarithmically transformed C-reactive protein, body mass
index. 4 Plaque on the gingival margin of the reference teeth or plaque elsewhere on the reference teeth.
44
Smokers
In the total study population representing daily smokers, no association between BSDS or
RFDS and sextants with gingival bleeding or teeth with deepened periodontal pockets was
observed in the adjusted models in either age group. Among 30–49-year-old participants
with good oral hygiene, an inverse association between BSDS (p=0.08) and RFDS (p=0.03)
and the number of teeth with deepened periodontal pockets was observed. Among 50–79-
year-old participants with good oral hygiene, either BSDS or RFDS did not associate
consistently with the number of teeth with deepened periodontal pockets. (Table 10).
Table 10. Prevalence rate ratios and 95% confidence intervals for the number of sextants with
gingival bleeding and the number of teeth with deepened periodontal pockets in tertiles (low
indicating a poor diet and high indicating a healthy diet) of the Baltic Sea Diet Score (BSDS)
and the Recommended Finnish Diet Score (RFDS) first in the total smoking study population
and then stratified according to the level of oral hygiene
The number of sextants with gingival
bleeding
The number of teeth with deepened periodontal
pockets
BSDS, tertiles
I (ref.)–III
RFDS, tertiles
I (ref.)–III
BSDS, tertiles
I (ref.)–III
RFDS, tertiles
I (ref.)–III
30–49 years1, n= 704
ref.
1.03 (0.88–1.20)
1.09 (0.94–1.26)
p= 0.5152
ref.
1.01 (0.87–1.16)
0.97 (0.82–1.15)
p= 0.9018
ref.
0.89 (0.71–1.11)
0.97 (0.77–1.21)
p= 0.5641
ref.
0.97 (0.79–1.19)
0.90 (0.74–1.10)
p= 0.5655
Good oral hygiene2,3,
n= 217
ref.
1.10 (0.74–1.64)
1.06 (0.71–1.57)
p= 0.8991
ref.
0.82 (0.52–1.30)
0.84 (0.58–1.21)
p= 0.5791
ref.
0.58 ( 0.35–0.93)
0.78 (0.51–1.20)
p= 0.0781
ref.
0.60 (0.37–0.98)
0.63 (0.43–0.92)
p= 0.0265
Poor oral hygiene3,4,
n= 486
ref.
1.02 (0.84–1.23)
1.07 (0.91–1.27)
p= 0.6818
ref.
1.03 (0.88–1.20)
0.97 (0.80–1.17)
p= 0.8069
ref.
0.95 (0.73–1.22)
0.98 (0.76–1.25)
p= 0.9119
ref.
0.99 (0.79–1.24)
0.91 (0.73–1.14)
p= 0.6805
50–79 years1, n= 267
ref.
1.06 (0.85–1.33)
0.98 (0.76–1.26)
p= 0.7469
ref.
0.90 (0.73–1.11)
0.90 (0.69–1.16)
p= 0.5192
ref.
1.08 (0.86–1.35)
0.97 (0.74–1.29)
p= 0.7048
ref.
0.87 (0.69–1.10)
1.03 (0.80–1.33)
p= 0.3638
Good oral hygiene2,3,
n= 62
ref.
1.26 (0.21–7.56)
1.43 (0.57–3.57)
p= 0.6135
ref.
0.54 (0.20–1.49)
0.77 (0.34–1.76)
p= 0.4619
ref.
0.77 (0.31–1.88)
0.79 (0.38–1.66)
p= 0.7831
ref.
0.50 (0.25–0.98)
0.64 (0.29–1.39)
p= 0.1241
Poor oral hygiene3,4,
n= 200
ref.
1.10 (0.89–1.36)
0.94 (0.74–1.20)
p= 0.4137
ref.
0.98 (0.79–1.22)
0.86 (0.67–1.11)
p= 0.5155
ref.
1.17 (0.94–1.46)
1.06 (0.83–1.35)
p= 0.3717
ref.
0.93 (0.73–1.19)
1.04 (0.79–1.37)
p= 0.7494 1 Adjusted for age, gender, level of education, dental attendance pattern, toothbrushing frequency, plaque, body mass index, number of
cigarettes smoked, logarithmically transformed C-reactive protein, the use of supplements, NSAID use and physical exercise. 2 No plaque on the reference teeth. 3 Adjusted for age, gender, level of education, dental attendance pattern, toothbrushing frequency, body mass index, number of cigarettes
smoked, logarithmically transformed C-reactive protein, the use of supplements, NSAID use and physical exercise. 4 Plaque on the gingival margin of the reference teeth or plaque elsewhere on the reference teeth.
45
5.3 ASSOCIATIONS OF DIETS BASED ON NORDIC FOOD CULTURE AND
FINNISH DIETARY RECOMMENDATIONS WITH THE NUMBER OF TEETH WITH DEEPENED PERIODONTAL POCKETS AFTER 11 YEARS
FOLLOW-UP AND WITH THE DEVELOPMENT OF PERIODONTAL DISEASE
In all dietary tertiles, the average number of teeth with ≥ 4 mm deep periodontal pockets
increased during the follow-up (Figure 9). Among the whole study population consisting of
30–49-year-old non-smokers and smokers, low scores of BSDS and RFDS were associated
with a high number of teeth with deepened periodontal pockets after 11 years follow-up.
Of the used indices, the association was linear between RFDS and the number of teeth with
deepened periodontal pockets, whereas association between BSDS and the number of teeth
with deepened periodontal pockets was not linear. Among those who were periodontally
healthy at baseline, both BSDS and RFDS associated inversely with the number of teeth
with deepened periodontal pockets at follow-up. The observed associations did not follow
an exposure-response pattern. The continuous incidence rate ratios and 95% confidence
intervals (CIs) were 0.94 (0.92–0.96) for BSDS and 0.91 (0.88–0.94) for RFDS. (Table 11).
Figure 9. The average number of teeth with ≥ 4 mm deep periodontal pockets in the tertiles
(low indicating a poor diet and high indicating a healthy diet) of the Baltic Sea Diet Score
(BSDS) and the Recommended Finnish Diet Score (RFDS) in 2000 and 2011 among the whole
study population, n=587 (manuscript IV)
46
Table 11. Incidence rate ratios and 95% confidence intervals for the number of teeth with
deepened periodontal pockets at follow-up. The Baltic Sea Diet Score (BSDS) and the
Recommended Finnish Diet Score (RFDS) (low indicating a poor diet and high indicating a healty
diet) were used as explanatory variables.
Whole study
population (30–49
years), n=587
BSDS RFDS Incidence data (30–
49 years),
n= 240
BSDS RFDS
Continuous 1.00 (0.98–1.01)
p=0.358
0.97 (0.95–0.98)
p= <0.0001
0.94 (0.92–0.96)
p= <0.0001
0.91 (0.88–0.94)
p= <0.0001
Tertiles
Low
Middle
High
1.78 (1.59 – 2.0)
p= < 0.0001
1.90 (1.69–2.14)
p= < 0.0001
ref.
1.24 (1.12–1.39)
p= <0.0001
1.00 (0.89–1.12)
p= 0.984
ref.
1.11 (0.87–1.40)
p=0.399
1.37 (1.07–1.77)
p=0.014
ref.
1.69 (1.29–2.21)
p= 0.0001
0.86 (0.64–1.15)
p=0.310
ref.
The number of teeth was used as an offset variable.
The models were adjusted for: year 2000: age, gender, the level of education, the body mass index (BMI), the use of supplements, plaque;
year 2011: plaque, physical activity, smoking, C-reactive protein, the use of non-steroidal anti-inflammatory drugs; 2000, 2011: change of
BMI, dental attendance pattern. The model of the whole study population was adjusted for the number of teeth with deepened
periodontal pockets in year 2000.
47
6 Discussion
6.1 DIET AND PERIODONTAL CONDITION
In this study, it was observed that a poor-quality diet was associated, although not
strongly, with the early phases of periodontal disease i.e. gingival bleeding and the
development of periodontal pockets. Daily intake of single omega-3 or omega-6 PUFAs or
their ratios were not consistently associated with the periodontal condition.
6.1.1 Associations between polyunsaturated fatty acids and periodontal condition
One of the hypotheses of this thesis was that a high intake of omega-3 PUFAs would be
associated with periodontal health. Contrary to the hypothesis and the results of the earlier
non-experimental studies (Iwasaki et al. 2010, Naqvi 2010, Iwasaki et al. 2011), there were
no essential associations between the daily intake of omega-3 or omega-6 PUFAs or their
ratios and the number of sextants with gingival bleeding or the number of teeth with
deepened periodontal pockets. Besides the apparent conclusion that there is no causal
association between the intake of the studied PUFAs and periodontal condition, some
alternative explanations for the findings exist.
Reasons for the opposite findings between the earlier non-experimental studies with this
study may be explained by the differences in the age of the subjects, in the methods of
collecting dietary information, the definition and the handling of the outcome variable, as
well as the controlling of confounding factors. In addition, the differences in the quality and
quantity of PUFA intakes in different countries may also partly explain the differences
between the findings by Iwasaki and Naqvi and the findings of this study. For example, a
recent review article showed that the intake of seafood-derived omega-3 PUFAs is highest
in Japan, mid-level in Finland and lowest in the USA, while the intake of omega-6 PUFAs is
highest in the USA, mid-level in Japan and lowest in Finland (Micha et al. 2014). Also the
source of omega-3 PUFAs differ between countries; most of the intake of omega-3 PUFAs
were ALA from vegetable sources in Finland (Helldán et al. 2013, p. 58) whereas in Japan,
the proportion of seafood omega-3 PUFAs from the total omega-3 PUFAs is higher than in
Finland (Micha et al. 2014).
The results of this study are also in contradiction with interventional studies, which have
shown positive effects of omega-3 PUFAs (+acetylicsalicylic acid) in periodontal healing
(El-Sharkawy et al. 2010, Elkhouli 2011, Deore et al. 2014, Naqvi et al. 2014, Elwakeel and
Hazaa 2015). However, in those studies, the intake of omega-3 fatty acids was supplemental
daily doses during several months and cannot be compared with intakes solely of the diet.
In addition, the potential positive effect of ASA is difficult to distinguish.
The methodological limitations of article I are discussed later.
48
6.1.2 Associations of diets based on Nordic food culture and Finnish dietary
recommendations with periodontal condition
Another aim of this thesis was to study whether diets based on Nordic food culture and
Finnish dietary recommendations, measured by the BSDS and the RFDS, associate with
periodontal condition.
In this study, it was found that the association between diet and gingival bleeding among
smokers and non-smokers were different. In the non-smoking population, a healthy diet
was inversely associated with gingival bleeding especially among those participants who
had poor oral hygiene (article II). This observation is probably related to the aetiological
role of dental plaque in gingival inflammation. Moreover, these results, which suggest anti-
inflammatory effect of diet, are in line with earlier findings by Woelber and Baumgartner
who both reported of reduced signs of inflammation in an experimental gingivitis model
after an intervention with a diet low in refined sugars and high in fiber, plant-based foods
and omega-3 PUFAs (Baumgartner et al. 2009, Woelber et al. 2016). The fact that among
smokers, no consistent association was observed between a healthy diet and gingival
bleeding can be explained by the vasoconstrictive effect of cigarette smoke (Kumar and
Faizuddin 2011).
Another interesting observation was that among the non-smoking population, a healthy
diet was associated with a low number of teeth with deepened periodontal pockets among
50–79-year-old participants with poor oral hygiene, but not among 30–49-year-old
participants (article II). There may be either true modification by age, related to biological
factors, for example, or this may be a spurious finding. Biological explanation could relate,
for example to an increased need for nutrients to compensate age-related detrimental
changes in immune response. Other possible explanation for this contradictory finding
between age groups may be residual confounding related to differences in the number of
teeth or number of teeth with deepened periodontal pockets, or non-oral illnesses and
medications between the younger and the older age groups. Due to the fact that older
people have on average more non-oral illnesses and medications and a larger variation in
the number of teeth than younger people, it can be expected that risk estimates among
older age group are in larger extent subjected to residual confounding.
Among 30–79-year-old daily smokers, a healthy diet did not consistently associate with
periodontal condition (article III). However, among 30–49-year-old participants with good
oral hygiene, a diet based on Finnish dietary recommendations (RFDS) as well as a diet
based on Nordic food culture and dietary recommendations (BSDS) associated inversely
with the number of teeth deepened periodontal pockets (article III). Besides a positive effect
of diet on periodontium, these findings suggest a weak association between diet and
periodontal pockets among smokers. This is because the inverse association was detected
only in the absence of other risk factors (plaque, diabetes) for periodontal disease. As it was
the case among non-smokers, there was a difference how diet associated with the number
of teeth with periodontal pockets between age groups. Because of a high risk for
confounding among older age group, it is possible that the true effect of diet on
periodontium among older age group remains unobserved.
The inverse associations between a healthy diet and deepened periodontal pockets in this
study were weaker than reported earlier by Bawadi and Al-Zahrani (Al-Zahrani et al. 2005,
Bawadi et al. 2011). Essential differences between those studies and this study are that they
49
used dichotomous classification of the outcome variable; participants in their study
population had on average more risk factors for periodontal disease and they had larger
variation in the age and ethnicity of the subjects.
The methodological limitations of articles II and III are discussed later.
6.1.3 Associations of diets based on Nordic food culture and Finnish dietary
recommendations with periodontal disease development and future periodontal
condition
The lack of knowledge on the role of whole diet in the development and progression of
periodontal disease led to the decision to study this matter in longitudinal study design
(manuscript IV). To date, there are no long follow-up studies made in general population,
while there are two interventional studies focusing on the topic (progression) among
subjects with metabolic syndrome. In those interventional studies, the positive changes in
the periodontal condition were observed among those who followed a healthy diet.
However, the improvement in periodontal condition in those studies may have, at least
partly, been attributed to changes in body weight (Jenzsch et al. 2009, Kondo et al. 2014).
The most important observation of the manuscript IV was that poor-quality diet appears
to predict the deterioration of periodontal condition, including periodontal pocket
formation, which is an initial process, leading to the development of periodontitis. The
findings are partly in line with the results of articles II and III, in which a poor-quality diet
was related to initial signs (gingival bleeding) of periodontal disease. A possible
explanation for differences in the results – in a longitudinal setting poor diet was associated
with periodontal pockets whereas in cross-sectional study the association was not
consistent – could be related to the the fact that in a follow-up study (manuscript IV), non-
smokers and smokers were not studied separately. Combining smokers and non-smokers
together with progressive nature of the periodontal disease along with aging, led to a
higher proportion of teeth with deepened periodontal pockets, which made it easier to
detect the weak beneficial effect of healthy diet on periodontium. Regarding the study
population in manuscript IV, it is worth noting that the effect of smoking was taken into
account using multivariable models.
6.2 POSSIBLE EXPLANATIONS FOR THE FINDINGS
The biological explanation for why diet could play a role on tissue homeostasis or
processes, which lead to periodontal tissue destruction, is based on the knowledge that
components of diet have anti-inflammatory properties. It is known, for example that
omega-3 PUFAs are precursors for anti-inflammatory molecules that are secreted during
the resolution of inflammation, whereas certain pro-inflammatory molecules are made of
omega-6 PUFAs. In addition, high-energy foods, such as sugars and SFAs, are able to
accelerate, and on the contrary, antioxidants from fruits, vegetables and berries are able to
resist oxidative stress in the body. The anti-inflammatory effect of a diet based on Nordic
food culture and dietary recommendations has been observed earlier, as it was associated
with a lower hs-CRP concentration in a Finnish study (Kanerva et al. 2014b). The fact that
50
diet associated with gingival bleeding among non-smokers (article II) support the
conception that the presumed beneficial effect of the diet is related to inflammation.
The purpose of this study was to assess whether diet associated independently with
periodontal condition. However, it is worth noting that it is likely that diet has also an
indirect effect on periodontium through body composition. In this study, it was not
possible to control thoroughly the possible mediating effect of body composition on
periodontium, because BMI is not necessarily an ideal way to measure body composition.
Diets based on Nordic food culture and Finnish dietary recommendations have earlier been
associated with lower waist circumference and body fat percentage in two Finnish studies
(Kanerva et al. 2013a, b). As it is known that BMI (Ylöstalo et al. 2008, Saxlin et al. 2011) and
waist circumference (Kangas et al. 2017) have been found to associate with poor
periodontal condition in these Health 2000 data, it is possible that high body fat
composition and its changes in longitudinal study mediates partly the effect of diet on
periodontal condition.
It is known that periodontal diseases are common among people who are in a poor
socioeconomic position. The facts through which socioeconomic position may have effect
on periodontal health are related to either material or behavioural factors. For example,
diet, smoking, oral hygiene practices and ability to use dental health care services are
somewhat dependent on disposable income (Thomson et al. 2012). This kind of clustering
was observed also in these Health 2000 data (Table 8). Regardless of the fact that the
socioeconomic factors and closely related behavioural factors such as level of education,
dental attendance pattern and smoking, for example, were taken into account in the
analyses using multivariate regression models, it is possible that clustering of health habits
partly explains the findings between diet and periodontal condition.
The seemingly contradictory findings related to the effect of the diet on periodontal
condition between age groups, the inverse association between a healthy diet and deepened
periodontal pockets among 50–79-year-old non-smokers with poor oral hygiene and in 30–
49-year-old smokers with good oral hygiene may relate to the simultaneous absence of
important risk factors. In a respective manner, a lack of consistent association between
healthy diet and deepened periodontal pockets among 50–79-year-old smokers could be
explained by the cumulative effect of smoking and simultaneous presence of other risk
factors, which easily overwhelm the weak beneficial effect of a healthy diet.
The occurrence of periodontal disease is determined by a number of disease
determinants, which include constitutional, behavioural and environmental factors. In the
absence of risk factors, periodontal disease prevalence is rather low, indicating that the
number of teeth with deepened periodontal pockets in a non-risk population, such as
young or middle-aged non-smoking and non-diabetic population, is rather low. A low
number of teeth with deepened periodontal pockets make it difficult to observe the
association between the risk factor and periodontal disease, especially in a case where the
association between the risk factor and periodontal condition is weak. In addition, the low
number of teeth with periodontal pockets increases the possibility of a chance finding.
These aspects could explain the lack of consistent association between a healthy diet and
deepened periodontal pockets among 30–49-year-old non-smokers.
When compiling the indices (BSDS and RFDS), it was observed that the average scores
among those belonging to the highest category were rather low, which means that even
those in the highest category did not eat according to the Nordic diet or the Finnish dietary
51
recommendations. In addition, a part of those belonging to the lowest category had a
reasonably good diet. The limited variation in the exposure variable, i.e. diet, due to the
categorization into tertiles, may have led to smaller risk estimates compared to the situation
where there was large variation in the exposure variable, or alternatively more categories in
the explanatory variable. However, due to the relatively small study population, the
alternative categorization was not feasible. Related possibly to chance finding, it was found
that inverse association between a healthy diet and periodontal condition did not always
follow an exposure-response pattern. One additional reason for deviations from linearity
may be the fact that those with the same score may have gathered their points from
different foods or nutrients. The associations of single components of the scores with
periodontal condition were not analysed separately in this study.
6.3 METHODOLOGICAL CONSIDERATIONS
6.3.1 Study design
The objectives of epidemiological studies are to describe the distribution of health-related
states and events, to find hypotheses for causal relations between exposures and outcomes,
and to test hypotheses at a population level. The Health 2000 Survey was a population-
based study (with main sample of 8028 subjects), in which 79% of the enrolled subjects
participated in both the interview and the health examination (Koskinen et al. 2008, p. 139).
This fairly high participation rate lowers the possibility for selection bias. In order to reduce
further the selection bias related to a low participation rate of older people, over 80-year-old
people were taken to the sample twice as many than younger ones.
A stratified cluster sampling design and the use of sample weights based on age, gender
and region in the analyses were used to minimize the effect of lost information during the
survey and to ensure that the final sample was representative. After 11 years, a follow-up
Survey was conducted where all living participants of the Health 2000 Survey were invited.
In that survey, oral health examination was carried out due to the limited resources only in
two out of five university hospital regions, which naturally lowers the national
representativeness of the follow-up sample.
The Health 2000 Survey has a cross-sectional study design, in which the temporal
sequence between the exposure and the outcome cannot, in many cases, be verified. It is
important to consider that despite the fact that FFQ gives information on individuals diets
over one year and it is also known that people do not make sudden changes in their diets,
rather they evolve over long time periods (Willett 2013b, p. 2), it has to be kept in mind that
the development of periodontitis is a slow process (Löe et al. 1986, Rosling et al. 2001).
Therefore it is clear that the temporal sequence between diet and the presence of
periodontal pockets cannot be reliably assessed (articles I–III). However, it is worth noting
that gingival bleeding represents the current inflammatory condition of the gums and it
develops in about one week from the beginning of the plaque accumulation. In articles I–III
(gingival bleeding as outcome), the requirement for temporal sequence between the
exposure and outcome can therefore be considered fulfilled.
52
Statistical methods
SAS Callable SUDAAN Research Triangle Institute, Raleigh NC, USA (Release 11.0.1.) was
used to take into account the weighting and two-stage cluster sampling in the data.
Regarding the statistical methods, it should be pointed out that Poisson regression models
may have led to too large confidence intervals and too low p-values. This is related to the
skewed distribution of the outcome variable, which is partly a consequence of a number of
restrictions (risk factors for periodontal disease) that were used to control for confounding.
However, in an earlier paper of the Health 2000 Survey, it was found that risk estimates
obtained from Poisson regression models and those from the negative binomial regression
models were fairly similar (Saxlin et al. 2009). Therefore, it can be concluded that the risk
estimates, confidence intervals or p-values were not essentially biased.
6.3.2 Variables
Periodontal variables
The information of periodontal variables was based on a clinical examination and the
possible sources of bias are related to inaccuracies in the measurements during the
examinations. In the validation study (the Health 2000 Survey), the percentual agreement
for measurements of gingival bleeding between the reference dentist and the field-dentists
was 66% (ҡ-value 0.36) and for pocket depth measurements 77% (ҡ-value 0.41), respectively
(Vehkalahti et al. 2004, p. 28). These inter-examiner values indicate that field-dentists
reported of fewer teeth with deepened periodontal pockets and less gingival bleeding than
the reference-dentist, which may have caused bias towards zero. The repeatability among
the field-dentists showed a ҡ-value of 0.66 for gingival bleeding and 0.83 for periodontal
pocketing (Vehkalahti et al. 2004, p. 29). However, the intra-examiner kappa-values were
relatively high, which mean that the repeatability among fields-dentists was at a good level.
The number of sextants with gingival bleeding was used as an outcome variable to
measure the extent of inflammation in the gingival tissues. Despite the robust manner of
the measurement, the variable can be considered suitable enough to rank participants by
the extent of gingival bleeding. On the other hand, it is not clear whether it measures
reliably the presence of gingivitis, especially in those who have only few teeth per sextant.
Because the measurement in the Health 2000 Survey and its follow-up was based solely on
the clinical measurement of the probing depths rather than a combination of a pocket depth
measurement and attachment level measurement, or radiographs or bacteriological data, it
is possible that the presence of PDs ≥ 4 mm in some cases does not refer to the presence of
periodontitis, but rather to gingival swelling or overgrowth. In order to minimize the effect
of a measurement error and to reflect the true pattern of periodontal disease, the outcome
variables were used as continuous variables. An alternative way would be classifying
participants into healthy and diseased groups using more or less arbitrary cut-off points.
This would have caused loss of sensitivity of the outcome variable and increased the effect
of misclassification. Because the number of teeth with deep periodontal pockets was low
and the number of participants in each study was rather low, it was not possible to use the
number of teeth with deep (≥ 6 mm) periodontal pockets as the outcome variable. Lastly, it
53
should be noted that the measurement of gingival bleeding as well as the measurement of
periodontal pockets were not site-spesific and PD on each tooth was measured only at
predetermined sites. Both these most likely have caused bias towards zero.
Dietary variables
FFQ is the most used method in large epidemiological studies in collecting data of the
whole diet and in enabling the ranking of individuals by intake. The validated FFQ
(Männistö et al. 1996, Paalanen et al. 2006) that was used in the Health 2000 Survey,
collected data on the use of foods and drinks in the previous 12 months. The reliability of
the questionnaire was examined and the intraclass correlation coefficients, which measure
the repeatability of the method, ranged mainly between 0.32–0.68 for food groups and 0.40–
0.69 for nutrients and were considered as acceptable. In addition, the validity of the FFQ
was studied and the participants in the validation study represented well the population of
the Health 2000 Survey, but were slightly younger. Observations of the validation study
showed that mean nutrient intakes were overreported in the FFQ when they were
compared to diet records. Highest differences between the methods were observed in
PUFAs, carotenoids, vitamin E, and vitamin C in both men and women. For example, the
correlation for omega-3 fatty acids was 0.20 for women and 0.35 for men when FFQ was
compared to a three-day food diary (Paalanen et al. 2006).
FFQ can be considered suitable in collecting data for indices that estimated the quality of
the whole diet (articles II–III, manuscript IV). However, it is not a good method to measure
the intake of PUFAs (Willett and Lenart 2013, pp. 100–112), which can be considered as a
limitation, especially related to the ability to collect data on the absolute intakes of PUFAs
in article I. For example, instead of asking cooking fats separately, the assumption of the fat
content of dishes was based on sales statistics of cooking fats in Finland. That, together with
the possible overreporting of the consumption of healthy foods, such as fish and
underreporting of unhealthy foods, may have led participants ending up in the adjacent
quintiles than would have been intended. This may indicate that the true variation in the
intake of PUFAs in this population was smaller than it was reported based on the FFQ.
Consequently, these inaccuracies in the measurement of PUFAs may have caused bias
towards zero in article I. It could be speculated that a more accurate way to collect data on
PUFAs would have been by measuring nutrient concentrations from erythrocytes or
adipose tissue samples.
Absolute nutrient intakes are usually dependent on the total energy intake, which is
inturn dependent on body size, physical activity and metabolic efficiency. In order to
reduce the effect of these factors on the nutrient intake, the residual method was used to
correct all nutrient intake variables, except alcohol E%, before fitting regression models. It
has been suggested that body weight and physical activity could be used as adjustments to
represent energy consumption, instead of using total energy intake estimated from FFQ or
diet records (Jakes et al. 2004). However, in another study, the residual method was
concluded to be more suitable than the use of body weight and physical activity as a
method to adjust for total energy intake (Rhee et al. 2014). Despite the fact that all models in
this study were adjusted for BMI, and models in article III and manuscript IV also for
physical activity (a rough measurement), only nutrient intake variables, but not the food
54
consumption variables were adjusted for the total energy intake. This may have led to
residual confounding related to total energy intake. This, in turn, could be interpreted in a
way that participants with higher energy consumption due to body size or physical activity
may have received higher scores of BSDS and RFDS than they would have if the food
consumption had been energy-adjusted. Consequently, the true variation in the intake of
nutrients may have been smaller than it was reported, which may have led to bias towards
zero.
Potential confounders and modifiers of the association
In epidemiology, true causal relations, if present, are more reliably observed in a situation
where the study population is as homogenous as possible. To increase the homogeneity of
the study population, the data was restricted to non-diabetic and non-rheumatoid
participants and stratified according to age, oral hygiene and smoking, which were possible
due to the large sample and the high participation rate.
In relation to age, the Health 2000 Survey is not at all homogeneous, because it represents
the total Finnish adult population. This means that age, itself and age-related factors, are
among factors, which may cause biases. Due to confounding effect of age, age-related risks
are often studied using stratification method. In line with this principle and based on
earlier experience in the Health 2000 Survey, the data were analysed separately in two age
groups: 30–49-year-olds and 50–79-year-olds (articles I–III). As expected, it was observed
that there were differences between age groups. For example, there was a fairly clear
difference in the number of teeth and the number of teeth with ≥ 4 mm deepened
periodontal pockets between those who were below 50 years and above 50 years. Analysing
the data separately among those who were below 50 years and above 50 years can also be
justified by the fact that older people have more non-oral illnesses and medications than
younger people.
Although the number of teeth was taken into account in the analyses, it is possible that
some residual confounding related to the number of teeth with deepened periodontal
pockets exists, due to the position of lost teeth, for example. However, if selective loss of
teeth exists, it is probably the periodontally most vulnerable teeth that have been extracted,
which improves the periodontal condition. That, in turn, causes again bias towards zero.
However, it is worth noting that the variation in tooth loss during the follow-up period in
different categories of diets was quite small, which indicates that the biasing effect of tooth
loss is most likely minimal.
In the Health 2000 data, the level of oral hygiene was measured by observing dental
plaque on three indicator teeth and the oral hygiene level was based on the highest value of
the indicator teeth. Despite the rough level of the measurement, dental plaque has been
found to fairly strongly associate with the number of teeth with deepened periodontal
pockets (Saxlin et al. 2008), which suggest that the oral hygiene variable can be considered
to be quite reliable.
55
6.4 CLINICAL IMPLICATIONS AND FUTURE PERSPECTIVES
In this study, it was observed that adherence to healthy diets based on Nordic food
culture and Finnish dietary recommendations were associated with periodontal health and
non-adherence to dietary recommendations with gingival bleeding and periodontal
pocketing. These findings can be interpreted in a way that a healthy diet has potential to be
beneficial in the prevention of the development of periodontal diseases. This study showed
that this potential beneficial effect is, on the other hand, most likely limited, as the
association between diet and periodontal condition was not detected in the presence of
simultaneuous risk factors for periodontal disease, such as plaque and smoking.
One of the aims of this study was to compare two diets: the local Nordic diet, measured
by the BSDS, and a more general diet based on Finnish dietary recommendations,
measured by the RFDS. The RFDS showed to be slightly more strongly associated with
gingival bleeding and pocketing, which may be explained by the larger selection of healthy
components in it. The most notable differences in diet quality indices were fruits and
vegetables (only locally produced fruits vs. fruits produced both locally and abroad) as well
as the intake of sugar, which was not measured in the BSDS at all. It may not be
coincidental that these are components that have been associated with periodontal disease
in earlier studies (Yoshihara et al. 2009, Lula et al. 2014).
This study was among the first studies examining the relation of a whole diet with
periodontal condition and the first to study the role of a whole diet with the development
of periodontal disease. Due to the non-experimental study design, it is self-evident that no
clinical recommendations can be given based on this thesis. However, based on this study
and the earlier literature, it can be concluded that eating a diet that consists mainly of fruits,
vegetables and berries; whole grain cereals; low-fat milk; and fish and poultry; and includes
limited amounts of salt; sucrose; saturated fats and trans-fatty acids; red and processed
meat products; and alcohol could be useful in preventing inflammation in the
periodontium and consequently the development of periodontal diseases.
Future studies should provide evidence on:
1. The effect of dietary counselling intervention, as part of other health education, on
the development of periodontal diseases.
2. The relation of a diet based on dietary recommendations and periodontal healing,
preferably using experimental study design and patients with different age groups.
3. The role of single components of RFDS in relation to periodontal healing could be
studied separately.
56
7 Conclusion
The aim of this thesis was to examine the relation of diets based on Nordic food culture and Finnish dietary recommendations to periodontal condition and the development of periodontal disease. Another aim was to study single polyunsaturated fatty acids and their ratios in relation to periodontal condition. Lastly, the third aim was to compare the associations of two diet quality indices, the BSDS and the RFDS, with periodontal condition. In this study it was observed that:
1. Single polyunsaturated fatty acids or their ratios were not associated with periodontal condition.
2. Adherence to diets based on Nordic food culture and Finnish dietary recommendations were inversely associated with inflammation especially in participants with poor oral hygiene, but not consistently with periodontal pocketing among 30–79-year-old non-smoking population.
3. Diets based on Nordic food culture and Finnish dietary recommendations were not consistently associated with periodontal condition among 30–79-year-old daily smokers. The association between diet and periodontal pocketing was dependent on age and oral hygiene.
4. Non-adherence to diets based on Nordic food culture and Finnish dietary recommendations was associated with the deterioration of periodontal condition and the development of periodontal disease.
5. The RFDS was more strongly associated with periodontal health than the BSDS.
57
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PUBLICATIONS OF THE UNIVERSITY OF EASTERN FINLAND
Dissertations in Health Sciences
ISBN 978-952-61-2871-9ISSN 1798-5706
Dissertations in Health Sciences
PUBLICATIONS OF THE UNIVERSITY OF EASTERN FINLAND
LEENA MARIA JAUHIAINEN
DIET AND PERIODONTAL CONDITION- AN EPIDEMIOLOGICAL STUDY
The aim of this thesis was to study the role of single polyunsaturated fatty acids and diet quality based on Nordic food culture and Finnish dietary recommendations in
periodontal diseases among Finnish adults. In this study, no consistent associations were
observed between a daily intake of omega-3 or omega-6 polyunsaturated fatty acids or their ratios and gingival bleeding or periodontal
pocketing. However, the results suggested that a healthy diet may be beneficial in preventing
the development of infectious periodontal diseases such as gingivitis and periodontitis.
LEENA MARIA JAUHIAINEN
30886310_UEF_Vaitoskirja_NO_481_Leena_Jauhiainen_Terveystiede_kansi_18_09_10.indd 1 10.9.2018 15.36.27
