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DOI: 10.1542/peds.2011-2825; originally published online July 9, 2012; 2012;130;211Pediatrics
Keski-NisulaEija Bergroth, Sami Remes, Juha Pekkanen, Timo Kauppila, Gisela Büchele and Leea
ContactsRespiratory Tract Illnesses During the First Year of Life: Effect of Dog and Cat
http://pediatrics.aappublications.org/content/130/2/211.full.html
located on the World Wide Web at: The online version of this article, along with updated information and services, is
of Pediatrics. All rights reserved. Print ISSN: 0031-4005. Online ISSN: 1098-4275.Boulevard, Elk Grove Village, Illinois, 60007. Copyright © 2012 by the American Academy published, and trademarked by the American Academy of Pediatrics, 141 Northwest Pointpublication, it has been published continuously since 1948. PEDIATRICS is owned, PEDIATRICS is the official journal of the American Academy of Pediatrics. A monthly
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Respiratory Tract Illnesses During the First Year ofLife: Effect of Dog and Cat Contacts
WHAT’S KNOWN ON THIS SUBJECT: Respiratory infectioussymptoms are common during the first year of life. Day careattendance, older siblings, and lack of breastfeeding have beenconsidered as possible factors influencing early respiratory tractinfections.
WHAT THIS STUDY ADDS: Children with early dog contacts seemto have fewer infectious respiratory symptoms and diseases,especially otitis, during the first year of life.
abstractOBJECTIVES: To investigate the effect of dog and cat contacts on thefrequency of respiratory symptoms and infections during the firstyear of life.
METHODS: In this birth cohort study, 397 children were followed upfrom pregnancy onward, and the frequency of respiratory symptomsand infections together with information about dog and cat contactsduring the first year of life were reported by using weekly diaries anda questionnaire at the age of 1 year. All the children were born in east-ern or middle Finland between September 2002 and May 2005.
RESULTS: In multivariate analysis, children having dogs at home werehealthier (ie, had fewer respiratory tract symptoms or infections) thanchildren with no dog contacts (adjusted odds ratio, [aOR]: 1.31; 95%confidence interval [CI]: 1.13–1.52). Furthermore, children havingdog contacts at home had less frequent otitis (aOR: 0.56; 95% CI:0.38–0.81) and tended to need fewer courses of antibiotics (aOR:0.71; 95% CI: 0.52–0.96) than children without such contacts. In uni-variate analysis, both the weekly amount of contact with dogs andcats and the average yearly amount of contact were associated withdecreased respiratory infectious disease morbidity.
CONCLUSIONS: These results suggest that dog contactsmay have a pro-tective effect on respiratory tract infections during the first year of life.Our findings support the theory that during the first year of life, animalcontacts are important, possibly leading to better resistance to infec-tious respiratory illnesses during childhood. Pediatrics 2012;130:211–220
AUTHORS: Eija Bergroth, MD,a Sami Remes, MD, PhD,a
Juha Pekkanen, MD, PhD,b,c Timo Kauppila, MSc,b GiselaBüchele, PhD,d and Leea Keski-Nisula, MD, PhDb,e
Departments of aPediatrics and eObstetrics and Gynecology,Kuopio University Hospital, Kuopio, Finland; bDepartment ofEnvironmental Health, National Institute for Health and Welfare,Kuopio, Finland; cInstitute of Public Health and Clinical Nutrition,University of Eastern Finland, Kuopio, Finland; and dInstitute ofEpidemiology and Medical Biometry, University of Ulm, Ulm,Germany
KEY WORDScat, dog, pets, respiratory infections
ABBREVIATIONSaOR—adjusted odds ratioCI—95% confidence intervalGEE—generalized estimating equations
Dr Bergroth substantially contributed to analysis andinterpretation of data, drafted the article, and approved the finalversion to be published; Dr Remes substantially contributed todesign and interpretation of data, revised the article forimportant intellectual content, and approved the final version;Dr Pekkanen substantially contributed to conception, design andinterpretation of data, revised the article for importantintellectual content, and approved the final version; Mr Kauppilasubstantially contributed to design and acquisition of data,revised the article for important intellectual content, andapproved the final version; Dr Büchele substantially contributedto conception, design and interpretation of data, revised thearticle for important intellectual content, and approved the finalversion; and Dr Keski-Nisula substantially contributed toanalysis and interpretation of data, revised the article forimportant intellectual content, and approved the final version.
www.pediatrics.org/cgi/doi/10.1542/peds.2011-2825
doi:10.1542/peds.2011-2825
Accepted for publication Apr 5, 2012
Address correspondence to Eija Bergroth, MD, Department ofPediatrics, Kuopio University Hospital, Puijonlaaksontie 2, 70210Kuopio, Finland. E-mail: [email protected]
PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).
Copyright © 2012 by the American Academy of Pediatrics
FINANCIAL DISCLOSURE: The authors have indicated they haveno financial relationships relevant to this article to disclose.
FUNDING: This study was supported by Foundation for PediatricResearch, Kerttu and Kalle Viikki, Päivikki and Sakari Sohlberg,and Juho Vainio Foundations, EVO funding, Farmers’ SocialInsurance Institution–Mela, Academy of Finland (grant 139021),and Kuopio University Hospital, Finland and European Union(QLK4-2001-00250 and FP7-211911).
PEDIATRICS Volume 130, Number 2, August 2012 211
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Respiratory infectious symptoms anddiseasesare frequent during thefirst ofyear life. They are usually caused by avirus, with human rhinovirus being themost common pathogen.1–3 In previousreports, the frequency of respiratorytract infections has been estimated tovary between 3 and 6 episodes withinthe first year of life.4–6
A variety of factors, such as day careattendance,7,8 older siblings7,9,10 andlack of breastfeeding,10–12 have beenconsidered as possible risk factors forearly respiratory tract infections. In ad-dition, a parental history of asthma13,14
and smoking10,15–18 are thought to havea role in the child’s susceptibility to in-fections and to respiratory symptoms.Earlier reports on the role of animalcontacts on the prevalence of respir-atory tract infections are sparse. Someprevious studies have shown that dogcontacts,19,20 although not cat contacts,15
seem to decrease the number of com-mon cold episodes during childhood.However, pet ownership has also beenconsidered a possible risk factor forfrequent childhood respiratory tractinfections in some reports.21
In the last 10 years, a large body ofliteraturehasevaluated theroleofearlychildhood animal exposure, includinghousehold pets, in the risk of asthma orallergy in children.22–24 We have pre-viously reported a decreased tumornecrosis factor a–producing capacityat birth and in the first year of life inchildren exposed to indoor dogs inearly life,25 suggesting that exposure todogs during early life may reduce in-nate immune responses already atbirth. At the same time, virologicalstudies have shown large differencesin immune responses among the chil-dren exposed to viruses that cause acommon cold, such as human rhinovi-rus; it seems to cause common coldsfor most children during childhood,whereas atopic children with the higherrisk of persistent asthma have hadmore
frequently severe infections with wheez-ing and altered immune response.26
Thus, a better understanding of the in-terplay between pet-related exposuresand the development of early respiratorytract infections may provide indirectinsight regarding the factors affectingthe maturation of immune responsesand its disturbances, such as asthma.In addition, recognizing the risk fac-tors for respiratory tract infectionsduring childhood is important becausethere might be a connection betweenchildhood respiratory tract infectionsand chronic airway diseases later inadulthood.21
Theaimof this studywas todescribe theeffect of domestic animal contacts onrespiratory tract infection morbidityduring the first year of life. The studywas based on a prospective birth co-hort study with diary-based data onrespiratory tract infections and animalexposures during the first year of life.
METHODS
The primary study population con-sisted of Finnish participants in a pro-spective birth cohort study, PASTURE(Protection Against Allergy in RuralEnvironments), which is an ongoing in-ternational study in 5 different Europeancountries (Austria, Finland, France,Germany, and Switzerland). The Finnishstudy population consists of 208 chil-dren whose mothers were followed upfrom the third trimester of pregnancy.The mothers lived in rural areas, eitheron a farm or in a nonfarming environ-ment. The cohort has been described inmore detail elsewhere.27 Another 216mothers and their children (the ex-tended Finnish cohort) were followedup through the same extensive pro-tocol as the primary study population.The mothers lived in either rural orsuburban environments, and all gavebirth at Kuopio University Hospital. Allthe study children were born betweenSeptember 2002 and May 2005.
The children’s parents were given diaryquestionnaires consisting of questionsrelated to infectious symptoms andhealth care attendance as well as onthe children’s dog and cat contacts. Thediary questionnaires were filled inweekly, beginning from the ninth post-natal week and continuing up to the52ndweek, providing a total of 44 weeksof diary entries. In the diary ques-tionnaires, parents were asked if theirchildren had been “hale and hearty”during the previous 7 days. If the childhad not been completely healthy, theparents also filled in a weekly ques-tionnaire concerning different infecti-ous diseases and symptoms (whetherthe child had had cough, wheezing ofbreath, rhinitis, fever $38.5°C, middleear infection, diarrhea, urinary tractinfection, itchy rash, or some other ill-ness during these last 7 days). In thisanalysis, we evaluated respiratory in-fectious symptoms (cough, wheezing ofbreath, rhinitis, and fever) and infec-tions (middle ear infection). Any chil-dren for whom there were less thanone-half the number of possible diaryentries during the study period (,23weeks) were excluded (n = 27). Thus,397 children were included in the fol-lowing analyses.
Families were asked in the weeklyquestionnaires whether they had a dogor a cat at home and how much time ithad spent inside daily. For the followinganalysis, dog and cat contacts indoor athomewere grouped into: (1) no contactatall; (2) lowcontact (pet insideathomeup to a maximum of 6 hours daily); (3)medium contact (pet inside from 6–16hours daily); and (4) high contact (petinside.16 hours daily). Breastfeedingwas reported in 3 categories weekly:the child had either been solely breast-fed, partly breastfed, or not breastfedat all.
We further evaluated the estimatedaverage amount of daily dog and catcontacts during the study period by
212 BERGROTH et al at Indonesia:AAP Sponsored on October 10, 2012pediatrics.aappublications.orgDownloaded from
using a self-administered retrospec-tively collected 1-year questionnaire,which was collected from the motherswhen the children were 12 months old.The estimated average amount of dailydog and cat contacts was grouped asfollows: (1) no dog/cat at all or dog/catnever inside at home; (2) dog/cat oc-casionally inside at home; (3) dog/catoften inside at home; or (4) dog/catmostly inside at home. The analysisalso included those children with bothdog and cat contacts.
Additional data were collected fromquestionnaires during pregnancy andearly childhood. Children were di-vided into 4 groups depending on thebirth month: summer (June–August),autumn (September–November), win-ter (December–February), and spring(March–May). The birth weight wascategorized into tertiles: ,3480g, 3480to,3810 g, and$3810 g. The number ofolder siblings was also categorized into3 groups: no siblings, 1 sibling, or $2siblings. Information concerning ma-ternal smoking 2 months after deliverywas requested in the 2- month ques-tionnaire: yes versus no. Parental atopywas categorized as yes if the mother orfather had ever been diagnosed withasthma, allergic eczema, or rhinitis, orno if neither of the parents had ever hadany of those diagnoses. The choice offamilies of whether to keep pets wascategorized yes versus no. Both mater-nal and paternal educational levelswere categorized into 3 groups: (1) el-ementary or vocational school; (2) highschool or college; or (3) university.
When data on animal contacts or in-formation on the health, respiratorysymptoms, and infectionsweremissingfrom a diary, the week in question wasexcluded from the analysis. The samewas done with other missing data if theinformation was not reliably derivablefrom other sources (eg, missing breast-feeding status from previous or subse-quent weeks).
Statistical Methods
Data analysis was performed by usingPASW statistics version 18.0 (SPSS Inc,Chicago, IL). The comparison of thefrequencies of the healthy weeks andduration of the various respiratory dis-eases or symptoms with different base-line and risk factors was performed byusing the x2 test or the Kruskall-Wallistest. Generalized estimating equations(GEE) were used to investigate the rela-tionships between the prevalence of re-spiratory disease or symptoms duringthe follow-up and various predictivefactors. The working correlation matrixwas AR(1). In the multivariate GEE mod-els, potential confounding variableswere selected a priori on the basis of
biological plausibility. These variablesincluded: gender (male versus female),living environment (farm, rural non-farming versus suburban), number ofsiblings (0, 1, vs.1), maternal smoking(yes versus no), parental atopy (yesversus no), breastfeeding (solely, partlyversus no), birth weight (,3480, 3480 to,3810 vs $3810 g), season of birth(winter, spring, summer, autumn), diarymonth, and cohort (Finnish PASTURE[Protection Against Allergy in RuralEnvironments] versus extended Finnishcohort). Contacts with dogs or cats athome were also determined accordingto the amount of the time that the animalshad spent inside the housedaily. The cutofflevel for significance was set at 0.05.
TABLE 1 Baseline Characteristics of Study Population in Relation to Living Environment
Characteristic Farm Rural Nonfarming Suburban All P
No. of diary weeks 5002 8133 3989 17 124Gender, % male 46.0 52.5 48.6 49.7 ,.001Gestational weeks at birth 39.5 6 1.2 39.6 6 1.1 39.4 6 1.3 39.6 6 1.2 ,.001Birth weight (g) 3714 6 444 3650 6 469 3559 6 463 3648 6 464 ,.001Birth season ,.001Winter 30.6 30.0 23.4 28.6Spring 33.6 30.1 23.1 29.5Summer 8.7 13.9 30.8 16.3Autumn 27.1 26.0 22.7 25.6
No. of siblings 1.4 6 1.5 1.3 6 1.8 0.8 6 1.1 1.2 6 1.6 ,.001Parental atopy 46.5 53.0 68.8 54.8 ,.001Maternal education ,.001Elementary/vocational school 33.7 33.7 27.8 32.3High school/college 48.1 46.4 45.8 46.8University 18.2 19.8 26.4 20.9
Paternal education ,.001Elementary/vocational school 69.3 58.7 48.4 59.6High school/college 26.6 28.0 25.2 27.0University 4.1 13.2 26.4 13.4
Maternal smoking at 2 mo 3.5 8.0 7.4 6.5 ,.001Breastfeeding .04Solely 14.1 15.0 13.5 14.4Partly 42.4 40.2 42.2 41.3No 43.6 44.7 44.3 44.3
Dog contacts at home ,.001No dog or dog not inside 65.4 66.3 76.4 68.4Dog inside ,6 h/d 11.2 4.3 4.2 6.3Dog inside 6–16 h/d 12.1 9.0 1.4 8.1Dog inside .16 h/d 11.3 20.3 18.0 17.2
Cat contacts at home ,.001No cat or cat not inside 56.5 86.2 84.3 77.2Cat inside,6 h/d 18.2 2.3 1.8 6.8Cat inside 6–16 h/d 15.0 5.5 1.5 7.3Cat inside.16 h/d 10.3 5.9 12.5 8.7
Contacts with other children 47.5 56.3 55.5 53.6 ,.001Day care attendance at age 1 y 13.7 16.5 21.4 16.8 ,.001
Data are presented as the mean6 SD or percentage. P values were obtained by using Pearson x2 or Kruskal-Wallis tests.
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Ethical Approval
The parents of all the children involvedin the study gave their written informedconsent. The research protocol wasapproved by the Research Ethics Com-mittee of the Hospital District ofNorthern Savo (Kuopio, Finland).
RESULTS
In total, information was received fora total of 17 124 follow-up weeks re-corded from the 397 children. More
weekly questionnaires were completedat the beginning of the follow-up: thenumber varied from 396 forms in weeks7, 11, 12, 17, and 18 to 347 forms in week44. Of the 44 follow-up weeks, the meannumber of completed weeks was 43.0per child (range: 23–44 weeks), with94.2% of families filling in at least 40forms.
Table 1 shows the baseline character-istics and animal contacts of the 397study children presented as diaryweeksin relation to living environment. There
were significant differences in all shownconfounding variables between differentliving environments, and thus the livingenvironment variable was further se-lected as a confounder in the multivari-ate analysis.
Infectious Respiratory Symptoms
Four children were reported as havingbeen healthy during the whole studyperiod, and 15.6% of the children (n =62) were healthy for less than one-halfof the follow-up weeks. In total, 285(71.8%) children had had fever, 157(39.5%) a middle ear infection, 384(96.7%) rhinitis, 335 (84.4%) cough,and 128 (32.2%) wheezing during anytime of the study period. In addition,nearly one-half of the children (n = 189[47.6%]) needed systemic antibiotics inthe course of the 44-week study period.The most frequently reported diseasewas rhinitis, which occurred in 17.0%of the follow-up weeks. Cough occurredin 10.4%, fever in 4.0%, wheezing in2.0%, and middle ear infection in 2.5%of the follow-up weeks. Two childrenhad pneumonia during the follow-up.
Cat and Dog Contacts
Of 397 children, 245 (61.7%) had had dogand 136 (34.3%) had had cat contact athome at some time during the study
TABLE 2 Healthy Weeks and Weeks With Different Respiratory Tract Symptoms and Infections and Use of Antibiotics During Follow-up in Relation to Dogand Cat Contacts Based on Weekly Diary Data
Dog or Cat Contact Healthy Fever Antibiotics Wheezing Cough Otitis Rhinitis
N n (%) N n (%) N n (%) N n (%) N n (%) N n (%) N n (%)
Dog contacts at homeNo dog or dog not
inside11 569 7500 (64.8) 11143 493 (4.4) 11569 471 (4.1) 11143 231 (2.1) 11142 1256 (11.3) 11143 339 (3.0) 11143 2045 (18.4)
Dog inside ,6 h/d 1063 805 (75.7) 1047 34 (3.2) 1063 20 (1.9) 1047 19 (1.8) 1047 88 (8.4) 1047 9 (0.9) 1047 142 (13.6)Dog inside 6–16 h/d 1374 1020 (74.2) 1361 48 (3.5) 1374 45 (3.3) 1361 17 (1.2) 1361 132 (9.7) 1361 17 (1.2) 1361 202 (14.8)Dog inside .16 h/d 2909 2101 (72.2) 2865 105 (3.7) 2909 86 (3.0) 2865 67 (2.3) 2865 286 (10.0) 2865 60 (2.1) 2865 502 (17.5)P ,.001 .06 ,.001 .12 .006 ,.001 ,.001
Cat contacts at homeNo cat or cat not
inside13 061 8628 (66.1) 12632 526 (4.2) 13061 497 (3.8) 12632 269 (2.1) 12631 1400 (11.1) 12632 339 (2.7) 12632 2300 (18.2)
Cat inside ,6 h/d 1144 895 (78.2) 1131 38 (3.4) 1144 20 (1.7) 1131 16 (1.4) 1131 68 (6.0) 1131 16 (1.4) 1131 131 (11.6)Cat inside 6–16 h/d 1236 858 (69.4) 1198 50 (4.2) 1236 50 (4.0) 1198 22 (1.8) 1198 140 (11.7) 1198 28 (2.3) 1198 217 (18.1)Cat inside .16 h/d 1474 1044 (70.8) 1455 68 (4.7) 1474 57 (3.9) 1455 28 (1.9) 1455 153 (10.5) 1455 44 (3.0) 1455 242 (16.6)P ,.001 .43 .004 .38 ,.001 .046 ,.001
N, total number of weeks with particular animal exposure; n, total number of weeks with specific symptom or infection and percentage (%) of weeks with specific symptom or infection fromthe total population with particular animal exposure; P values are obtained by Pearson Chi-Square test.
FIGURE 1The percentage of healthy weeks in relation to average amount of dog or cat contacts at home. *P, .01;**P , .05.
214 BERGROTH et al at Indonesia:AAP Sponsored on October 10, 2012pediatrics.aappublications.orgDownloaded from
period (range: 1–44 weeks). However,dog contacts at home were not stable:during the study weeks 1, 22, and 44, thepercentages of children living with nodog or no cat contact in the home variedfrom 66.1% to 69.3% and 76.1% to 77.4%,respectively. According to the 1-yearretrospective questionnaire at the end
of the study period, 65.2% of the chil-dren lived mainly in homes with no dogcontact and 75.5% in homes with no catcontact. During the pregnancy, 22.7% offamilies reported pet animal avoidancedue to allergic symptoms in the family.
If children had dog or cat contacts athome, they were significantly healthier
during the study period in univariatetests (both P , .001) (Table 2, Fig 1)and had fewer weeks with cough, otitis,and rhinitis and also needed fewercourses of antibiotics than childrenwith no cat or dog contacts at all. Thenumber of study weeks with differ-ent respiratory tract symptoms and
TABLE 3 Healthy Weeks and the Weeks With Different Respiratory Tract Symptoms and Infections and Use of Antibiotics During Follow-up in Relation toDog and Cat Contacts Based on Retrospective Cross-Sectional Data of Average Animal Contacts During the Study
Dog or Cat Contact Healthy Fever Antibiotics Wheezing Cough Otitis Rhinitis
N n (%) N n (%) N n (%) N n (%) N n (%) N n (%) N n (%)
Dog contacts at homeNo dog or dog
not inside10 798 6878 (63.7) 10361 447 (4.3) 10798 468 (4.3) 10 361 231 (2.2) 10360 1193 (11.5) 10 361 331 (3.2) 10 361 1918 (18.5)
Dog occasionallyinside
1278 953 (74.6) 1269 57 (4.5) 1278 14 (1.1) 1269 20 (1.6) 1269 135 (10.6) 1269 7 (0.6) 1269 225 (17.7)
Dog often inside 1391 1132 (81.4) 1390 53 (3.8) 1391 36 (2.6) 1390 16 (1.2) 1390 109 (7.8) 1390 12 (0.9) 1390 155 (11.2)Dog mostly inside 3113 2229 (71.6) 3066 102 (3.3) 3113 93 (3.0) 3066 59 (1.9) 3066 313 (10.2) 3066 65 (2.1) 3066 537 (17.5)P ,.001 .08 ,.001 .03 ,.001 ,.001 ,.001
Cat contacts at homeNo cat or cat
not inside12 643 8278 (65.5) 12191 500 (4.1) 12643 511 (4.0) 12 191 263 (2.2) 12190 1369 (11.2) 12 191 342 (2.8) 12 191 2233 (18.3)
Cat occasionallyinside
884 726 (82.1) 884 32 (3.6) 884 12 (1.4) 884 14 (1.6) 884 57 (6.4) 884 9 (1.0) 884 101 (11.4)
Cat often inside 1734 1239 (71.5) 1705 77 (4.5) 1734 45 (2.6) 1705 32 (1.9) 1705 179 (10.5) 1705 35 (2.1) 1705 301 (17.7)Cat mostly inside 1451 1039 (71.6) 1438 59 (4.1) 1451 49 (3.4) 1438 24 (1.7) 1438 159 (11.1) 1438 33 (2.3) 1438 237 (16.5)P ,.001 .74 ,.001 .40 ,.001 .004 ,.001
N, total number of weeks with particular animal exposure; n, total number of weeks with specific symptom or infection and percentage (%) of weeks with specific symptom or infection fromthe total population with particular animal exposure; P values are obtained by Pearson Chi-Square test.
TABLE 4 Multivariate Results of the Association Between Animal Contacts and Overall Healthiness, Fever, and Antibiotic Usage Based on Collection ofWeekly Diary Data
Dog or Cat Contact Healthy Fever Antibiotics
N n (%) aOR (95% CI)a P N n (%) aOR (95% CI)a P N n (%) aOR (95% CI)a P
Dog contact at homeNo 11 569 7500 (64.8) 1 11 143 493 (4.4) 1 11 569 471 (4.1) 1Yes 5346 3926 (73.4) 1.31 (1.13–1.52) ,.001 5273 187 (3.5) 0.80 (0.66–0.98) .03 5346 151 (2.8) 0.71 (0.52–0.96) .03
Amount of dog contactsat homeNo dog or dog
not inside11 569 7500 (64.8) 1 11 143 493 (4.4) 1 11 569 471 (4.1) 1
Dog inside ,6 h/d 1063 805 (75.7) 1.25 (1.04–1.50) .02 1047 34 (3.2) 0.63 (0.41–0.97) .04 1063 20 (1.9) 0.54 (0.34–0.87) .01Dog inside 6–16 h/d 1374 1020 (74.2) 1.21 (0.93–1.57) .16 1361 48 (3.5) 0.85 (0.63–1.15) .30 1374 45 (3.3) 0.91 (0.52–1.59) .73Dog inside .16 h/d 2909 2101 (72.2) 1.41 (1.14–1.74) .001 2865 105 (3.7) 0.87 (0.68–1.11) .25 2909 86 (3.0) 0.72 (0.49–1.04) .08
Cat contact at homeNo 13 061 8628 (66.1) 1 12 632 526 (4.2) 1 13 061 497 (3.8) 1Yes 3854 2797 (72.6) 1.06 (0.88–1.29) .53 3784 156 (4.1) 1.00 (0.79–1.27) ..99 3854 127 (3.3) 0.98 (0.61–1.59) .95
Amount of cat contactsat homeNo cat or cat
not inside13 061 8628 (66.1) 1 12 632 526 (4.2) 1 13 061 497 (3.8) 1
Cat inside,6 h/d 1144 895 (78.2) 1.13 (0.86–1.47) .38 1131 38 (3.4) 0.83 (0.56–1.24) .37 1144 20 (1.7) 0.65 (0.37–1.17) .15Cat inside 6–16 h/d 1236 858 (69.4) 1.01 (0.77–1.32) .94 1198 50 (4.2) 0.97 (0.69–1.38) .87 1236 50 (4.0) 1.06 (0.48–2.33) .88Cat inside.16 h/d 1474 1044 (70.8) 1.06 (0.81–1.38) .69 1455 68 (4.7) 1.13 (0.83–1.55) .44 1474 57 (3.9) 1.13 (0.67–1.90) .65
Values are aORs and 95% CIs obtained by using GEE analysis, working correlationmatrix AR(1). N, total number of weekswith particular animal exposure; n, total number of weeks with specificsymptom or infection and percentage (%) of weeks with specific symptom or infection from the total population with particular animal exposure.a All the aORs were adjusted for gender, birth weight, season of birth, parental atopy, number of siblings, cohort, maternal smoking, breastfeeding, living environment, and diary month.
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infections was also compared with 1-year questionnaire data on cat anddog contacts (Table 3), and the resultswere comparable to the results of theanimal contact data from the diary(Table 2).
Themultivariateanalysiswasconductedlongitudinally (Tables 4 and 5) andcross-sectionally (Tables 6 and 7), byusing GEE models. Even after adjustingfor possible confounders, children hav-ing a dog at home were significantlyhealthier, had less frequent otitis, andtended to need fewer courses of anti-biotics during the study period thanchildren without dog contacts. Both theweekly amount of dog contacts (ac-cording to diary data) and the averageamount of yearly contact (according to1-year questionnaire data) with dogswas associated similarly with de-creasing respiratory infectious diseasemorbidity. The highest protective asso-ciation between dog ownership andhealthiness, as well as lower risk forantibiotic use, otitis and rhinitis wasdetected among children who had a doginside at home for ,6 hours daily(according to diary data) or had a dogtemporally or often inside (accordingto retrospective data) compared withthosewho did not have any dogs ordogswere not inside (Tables 4, 5, 6, and 7). Insensitivity analysis, the associations didnot change after we removed fromanalysis those children whose familiesreported avoidance of pets due to someallergic causes (data not shown).
DISCUSSION
According to our results, dog and catcontacts during early infancy may beassociated with less morbidity in gen-eral (indicated as more healthy weeks)and concomitantly may have a protect-ive effect on respiratory tract symp-toms and infections. In comparisonsbetween cat and dog contacts, dogcontacts showed a more significantprotective role on respiratory infectiousTA
BLE5
Multivariate
Results
oftheAssociationBetweenAnimal
Contacts
andDifferent
RespiratoryTractSymptom
sandInfections
Basedon
WeeklyDiaryData
Collection
Dogor
CatContact
Wheezing
Cough
Otitis
Rhinitis
Nn(%
)aOR(95%
CI)a
PN
n(%
)aOR(95%
CI)a
PN
n(%
)aOR(95%
CI)a
PN
n(%
)aOR(95%
CI)a
P
Dogcontactathome
No11
143
231(2.1)
111142
1256
(11.3)
111143
339(3.0)
111
143
2045
(18.4)
1Yes
5273
103(2.0)
0.87
(0.61–1.24)
.44
5273
506(9.6)
0.85
(0.70–1.03)
.10
5273
86(1.6)
0.56
(0.38–0.81)
.002
5273
846(16.0)
0.92
(0.79–1.07)
.26
Amount
ofdogcontactsathome
Nodogor
dognotinside
11143
231(2.1)
111
142
1256
(11.3)
111143
339(3.0)
111
143
2045
(18.4)
1Doginside
,6h/d
1047
19(1.8)
0.84
(0.53–1.33)
.46
1047
88(8.4)
0.75
(0.55–1.01)
.06
1047
9(0.9)
0.38
(0.18–0.82)
.01
1047
142(13.6)
0.81
(0.64–1.03)
.08
Doginside
6–16
h/d
1361
17(1.2)
0.61
(0.29–1.27)
.18
1361
132(9.7)
1.00
(0.70–1.42)
.99
1361
17(1.2)
0.53
(0.29–0.97)
.04
1361
202(14.8)
0.93
(0.73–1.19)
.56
Doginside
.16
h/d
2865
67(2.3)
0.99
(0.60–1.64)
.97
2865
286(10.0)
0.87
(0.68–1.10)
.24
2865
60(2.1)
0.67
(0.41–1.08)
.10
2865
502(17.5)
0.99
(0.81–1.21)
.91
Catcontactathome
No12
632
269(2.1)
112
631
1400
(11.1)
112632
339(2.7)
112
632
2300
(18.2)
1Yes
3784
66(1.7)
1.02
(0.66–1.57)
.95
3784
361(9.5)
1.07
(0.84–1.35)
.60
3784
88(2.3)
1.02
(0.67–1.55)
.92
3784
590(15.6)
0.95
(0.79–1.14)
.57
Amount
ofcatcontactsathome
Nocatorcatn
otinside
12632
269(2.1)
112
631
1400
(11.1)
112
632
339(2.7)
112
632
2300
(18.2)
1Catinside,6h/d
1131
16(1.4)
0.94
(0.48–1.83)
.85
1131
68(6.0)
0.85
(0.62–1.17)
.32
1131
16(1.4)
0.75
(0.39–1.44)
.39
1131
131(11.6)
0.81
(0.62–1.06)
.13
Catinside6–16
h/d
1198
22(1.8)
0.89
(0.48–1.65)
.71
1198
140(11.7)
1.19
(0.85–1.68)
.31
1198
28(2.3)
0.91
(0.47–1.74)
.76
1198
217(18.1)
1.00
(0.77–1.28)
.97
Catinside.16
h/d
1455
28(1.9)
1.17
(0.66–2.08)
.59
1455
153(10.5)
1.12
(0.82–1.52)
.48
1455
44(3.0)
1.29
(0.77–2.15)
.34
1455
242(16.6)
1.02
(0.79–1.31)
.91
Values
areaORs
and95%CIsobtained
byusingGEEanalysis,w
orking
correlationmatrixAR(1).N,totalnum
berofweeks
with
particular
animalexposure.n,totalnumberofweeks
with
specificsymptom
orinfectionandpercentage
(%)ofweeks
with
specificsymptom
orinfectionfrom
thetotalpopulationwith
particular
animalexposure.
aAllthe
aORs
wereadjusted
forgender,birth
weight,season
ofbirth,parentalatopy,numberofsiblings,cohort,maternalsmoking,breastfeeding,livingenvironm
ent,anddiarymonth.
216 BERGROTH et al at Indonesia:AAP Sponsored on October 10, 2012pediatrics.aappublications.orgDownloaded from
disease morbidity. To our knowledge,this is the first study that has evaluatedthe significance of pet contacts duringchildhood for the development of re-spiratory tract infections and, further-more, has made analyses by using 2different data collection methods forinformation on animal contact. Thisstudy also made possible evaluation ofthe effects of different lengths of animalcontacts, by using short time variations,on the risk of respiratory tract illnesses.
The results support those of Hatakkaet al,20 who reported that furred petswould decrease the risk of recurrentacute respiratory tract symptoms withchildren 1 to 6 years old, although somereports have found no association be-tween respiratory tract infections andpet keeping.28 Our current results alsosupport indirectly those of Grüberet al,19 who found that having a dogat home during the first 2 years of lifedecreased the number of commoncold episodes among 0- to 2-year-olds. We showed that children whohad dog contacts at home had lessotitis and rhinitis and more healthyweeks than children without dogcontacts at home, but having a dog at
home during the first postnatal yearhad no significant role in the occur-rence of wheezing and cough, whichis in line with earlier results,29 eventhough the reason for these findingsis obscure.
Cat ownership seemed to also havean overall protective effect, althoughweaker than dog ownership, on theinfectious health of infants. Similarly, insome earlier studies, exposure to catshas been considered aprotective factortoward wheezing in the first year oflife,13 as well as for croup with olderchildren.30 On the contrary, many stud-ies have shown that cat contacts haveno effect on infectious symptoms15,29 orwheeze among children.31 In line withthis, the association between exposureto cats and respiratory tract symptomsand infections during childhood wasdecreased in our study after confound-ing in multivariate analysis. It is unsurewhy cat exposure is less significantcompared with dog exposure. However,Heyworth et al32 have shown that catand/or dog ownership is also associatedwith a reduced risk of gastroenteritis.This finding could indicate a real relation-ship exists between animal contacts
and the frequency of infections amongchildren.
We also showed that children living inhouses inwhichdogs spendonly part ofthe day inside (defined as,6 hours ortemporally) had the lowest risk of in-fectious symptoms and respiratorytract infections. A possible explanationfor this interesting finding might bethat the amount of dirt brought insidethe home by dogs could be higher inthese families because they spentmore time outdoors. In other words,less dirt is brought indoors by dogswho mainly live indoors. The living en-vironment could also affect the amountof dirt and animal contacts. Hence, wedid a subanalysis and evaluated theeffect of animal contacts on overallhealthiness separately for childrenliving in rural and suburban environ-ments. The directions of associationsdid not change, although some of theassociations weakened slightly, as wellas some got stronger. Furthermore, weincluded the area of living as a cova-riate in the multivariate analysis, andthe associations between dog expo-sure and health variables remained.The amount of dirt is likely to correlate
TABLE 6 Multivariate Results of the Association Between Animal Contacts and Overall Healthiness, Fever, and Antibiotic Usage Based on Collection ofCross-sectional Data of Average Animal Contacts During the Study
Dog or Cat Contact Healthy Fever Antibiotics
N n (%) aOR (95% CI)a P N n (%) aOR (95% CI)a P N n (%) aOR (95% CI)a P
Dog contacts at1 y ageNo dog or dog
not inside10 798 6878 (63.7) 1 10 361 447 (4.3) 1 10 798 468 (4.3) 1
Dog temporallyinside
1278 953 (74.6) 1.46 (1.07–2.00) 0.02 1269 57 (4.5) 1.04 (0.70–1.53) .86 1278 14 (1.1) 0.28 (0.14–0.59) .001
Dog often inside 1391 1132 (81.4) 2.08 (1.44–3.00) ,0.001 1390 53 (3.8) 0.84 (0.62–1.14) .27 1391 36 (2.6) 0.61 (0.28–1.35) .61Dog mostly inside 3113 2229 (71.6) 1.34 (1.05–1.70) 0.02 3066 102 (3.3) 0.86 (0.65–1.14) .29 3113 93 (3.0) 0.74 (0.51–1.08) .12
Cat contacts at1 y ageNo cat or cat
not inside12 643 8278 (65.5) 1 12 191 500 (4.1) 1 12 643 511 (4.0) 1
Cat temporallyinside
884 726 (82.1) 1.64 (1.12–2.39) 0.01 884 32 (3.6) 0.83 (0.53–1.28) .39 884 12 (1.4) 0.37 (0.18–0.76) .007
Cat often inside 1734 1239 (71.5) 1.04 (0.79–1.37) 0.79 1705 77 (4.5) 1.08 (0.79–1.47) .64 1734 45 (2.6) 0.67 (0.39–1.14) .14Cat mostly inside 1451 1039 (71.6) 1.15 (0.85–1.58) 0.37 1438 59 (4.1) 1.06 (0.76–1.49) .72 1451 49 (3.4) 0.93 (0.51–1.70) .82
Values are aORs and 95% CIs obtained by using GEE analysis, working correlationmatrix AR(1). N, total number of weekswith particular animal exposure; n, total number of weeks with specificsymptom or infection and percentage (%) of weeks with specific symptom or infection from the total population with particular animal exposure.a All the aORs were adjusted for gender, birth weight, season of birth, parental atopy, number of siblings, cohort, maternal smoking, breastfeeding, living environment, and diary month.
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PEDIATRICS Volume 130, Number 2, August 2012 217 at Indonesia:AAP Sponsored on October 10, 2012pediatrics.aappublications.orgDownloaded from
with bacterial diversity in the livingenvironment, possibly affecting thematuration of the child’s immune sys-tem and further affecting the risk ofrespiratory tract infections. However,in this article, we could not objectivelyanalyze the actual role of bacterial di-versity, which will have to be the sub-ject of further studies.
There are several possible reasonswhy the reported associations be-tween pet ownership and respiratorytract infections during childhood areinconsistent. First, the different typesof pet animals have not been evaluatedseparately in the analyses.5,16,20,21,28
Second, some studies enrolled olderchildren. For example, Burr et al16 foundthat pet ownership increased the riskof wheezing, rhinitis, and the numberof cold episodes per year for 12- to14-year-olds. Third, studies have eval-uated the associations between re-spiratory tract infections and animalcontacts during childhood retrospec-tively.21 Our study was prospective innature, and we also analyzed resultsby using data collected with 2 differentmethods, thus making our results morereliable.
Lastly, it ispossiblethattheeffectofanimalcontacts on the frequency of respiratorytract symptoms is mediated by a choiceamongatopicparentstonotkeeppets.20,33
We included parental atopy as a con-founder in the multivariate analysis, andthe association was not diminished.When we repeated the analyses withoutsubjects with a reported family history ofpet avoidance, associations were notchanged. As a whole, predictions on pet-keeping data are not straightforward,and there are studies showing thatatopic families do not necessarily avoidkeeping pets.34 However, the influenceof possible atopic predisposition of thestudy children on the results cannot becompletely ruled out.
Evidencesuggests thatanimal contacts,especially during early life, might beTA
BLE7
Multivariate
Results
oftheAssociationBetweenAnimal
Contacts
andDifferent
RespiratoryTractSymptom
sandInfections
Basedon
RetrospectiveCross-sectionalData
ofAverageAnimal
Contacts
During
theStudy
Dogor
CatC
ontact
Wheezing
Cough
Otitis
Rhinitis
Nn(%
)aOR(95%
CI)a
PN
n(%
)aOR(95%
CI)a
PN
n(%
)aOR(95%
CI)a
PN
n(%
)aOR(95%
CI)a
P
Dogcontactsat
age1y
Nodogor
dog
notinside
10361
231(2.2)
110
360
1193
(11.5)
110
361
331(3.2)
110
361
1918
(18.5)
1
Dogtemporally
inside
1269
20(1.6)
0.91
(0.49–1.70)
.77
1269
135(10.6)
1.03
(0.69–1.52)
.90
1269
7(0.6)
0.17
(0.07–0.42)
,.001
1269
225(17.7)
0.99
(0.74–1.32)
.93
Dogofteninside
1390
16(1.2)
0.47
(0.20–1.09)
.08
1390
109(7.8)
0.73
(0.44–1.19)
.21
1390
12(0.9)
027
(0.12–0.63)
.003
1390
155(11.2)
0.60
(0.44–0.83)
.002
Dogmostly
inside
3066
59(1.9)
0.86
(0.48–1.51)
.59
3066
313(10.2)
0.95
(0.73–1.25)
.73
3066
65(2.1)
0.75
(0.47–1.18)
.21
3066
537(17.5)
1.02
(0.83–1.26)
.85
Catcontactsat
age1y
Nocatorcatn
otinside
12191
263(2.2)
112
190
1369
(11.2)
112
191
342(2.8)
112
191
2233
(18.3)
1Cattem
porally
inside
884
14(1.6)
0.93
(0.34–2.60)
.90
884
57(6.4)
0.74
(0.41–1.32)
.30
884
9(1.0)
0.41
(0.16–1.01)
.05
884
101(11.4)
0.70
(0.45–1.09)
.11
Catofteninside
1705
32(1.9)
0.99
(0.50–1.96)
.97
1705
179(10.5)
1.09
(0.74–1.61)
.66
1705
35(2.1)
0.76
(0.40–1.46)
.42
1705
301(17.7)
1.07
(0.80–1.41)
.66
Catm
ostly
inside
1438
24(1.7)
0.99
(0.53–1.82)
.96
1438
159(11.1)
1.13
(0.78–1.64)
.51
1438
33(2.3)
0.89
(0.51–1.57)
.69
1438
237(16.5)
0.96
(0.74–1.25)
.76
Values
areaORs
and95%CIsobtained
byusingGEEanalysis,w
orking
correlationmatrixAR(1).N,totalnum
berofweeks
with
particular
animalexposure.n,totalnumberofweeks
with
specificsymptom
orinfectionandpercentage
(%)ofweeks
with
specificsymptom
orinfectionfrom
thetotalpopulationwith
particular
animalexposure.
aAllthe
aORs
wereadjusted
forgender,birth
weight,season
ofbirth,parentalatopy,numberofsiblings,cohort,maternalsmoking,breastfeeding,livingenvironm
ent,anddiarymonth.
218 BERGROTH et al at Indonesia:AAP Sponsored on October 10, 2012pediatrics.aappublications.orgDownloaded from
crucial in immunity developing alonga nonallergic route24,35 and in ensuringeffective responses to respiratory viralinfections in early life.35,36 We speculatethat animal contacts could help tomature the immunologic system, lead-ing to more composed immunologicresponse and shorter duration of in-fections. We offer preliminary evidencethat dog ownership may be protective
against respiratory tract infectionsduring the first year of life.
CONCLUSIONS
To our knowledge, this is the first pro-spective study in which the frequenciesof respiratory infectious symptoms anddiseases are compared with weeklyamounts of pet contacts in a diaryfollow-up manner during early infancy.
Our results suggest that dog contactsprotect children from respiratory tractinfections during the first year of life.
ACKNOWLEDGMENTSWe thank the families for participatingin the study, the field nurses for theirdedicated work, and Pekka Tiittanenfor data management and statisticalassistance.
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DOI: 10.1542/peds.2011-2825; originally published online July 9, 2012; 2012;130;211Pediatrics
Keski-NisulaEija Bergroth, Sami Remes, Juha Pekkanen, Timo Kauppila, Gisela Büchele and Leea
ContactsRespiratory Tract Illnesses During the First Year of Life: Effect of Dog and Cat
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