Diet and nutrition for the management and prevention of ...€¦ · Diet and nutrition for the management and prevention of type 2 diabetes Standfirst: Common ground on dietary approaches

Confidential: For Review Only

Diet and nutrition for the management and prevention of

type 2 diabetes

Standfirst: Common ground on dietary approaches for the

prevention, management and potential for remission of type 2 diabetes can be defined, argue Nita G. Forouhi and

colleagues

Journal: BMJ

Manuscript ID BMJ.2017.042272

Article Type: Analysis

BMJ Journal: BMJ

Date Submitted by the Author: 08-Nov-2017

Complete List of Authors: Forouhi, Nita; University of Cambridge School of Clinical Medicine, MRC Epidemiology Unit Misra, Anoop; Fortis Hospitals, Fortis-C-DOC Centre of Excellence for Diabetes, Metabolic Diseases and Endocrinology Mohan, D; Dr. Mohan’s Diabetes Specialities Centre and Madras Diabetes

Research Foundation Taylor, Roy; University of Newcastle, Magnetic Resonance Centre, Institute of Cellular Medicine Yancy, William; Duke University Diet and Fitness Center; Duke University School of Medicine, Department of Medicine

Keywords: Type 2 diabetes, management, prevention, remission, consensus, controversy

https://mc.manuscriptcentral.com/bmj

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Diet and nutrition for the management and prevention of type 2 diabetes

Standfirst: Common ground on dietary approaches for the prevention, management

and potential for remission of type 2 diabetes can be defined, argue Nita G. Forouhi

and colleagues

Nita G. Forouhi1, Anoop Misra

2, Viswanathan Mohan

3, Roy Taylor

4, William Yancy

5,6,7

1. MRC Epidemiology Unit, University of Cambridge School of Clinical Medicine,

Cambridge

2. Fortis-C-DOC Centre of Excellence for Diabetes, Metabolic Diseases and

Endocrinology, New Delhi, India

3. Dr. Mohan’s Diabetes Specialities Centre and Madras Diabetes Research

Foundation, Chennai, India

4. MR Centre, Institute of Cellular Medicine, Newcastle University, UK

5. Duke University Diet and Fitness Center, Durham, NC

6. Department of Medicine, Duke University School of Medicine, Durham, NC

7. Center for Health Services Research in Primary Care, Department of Veterans

Affairs, Durham, NC

Corresponding author:

Professor Nita G. Forouhi

MRC Epidemiology Unit, University of Cambridge School of Clinical Medicine,

Cambridge CB2 0QQ, United Kingdom

Email: [email protected]

Tel: +44 1223 330315

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Why diet matters for diabetes and why dietary management is difficult to

implement

Diabetes is one of the biggest global public health issues of our time, with a

relentless escalation in its estimated prevalence rising from 415 million people in

2015 to 642 million by 2040, and its related health, social and economic costs.1

Clearly, urgent solutions for slowing, even reversing this trend are warranted and

must come from investment in modifiable factors including diet, physical activity and

weight. Indeed, diet is overwhelmingly the predominant factor accounting for

morbidity and mortality according to the Global Burden of Disease Study across 188

countries.2 The enormous importance of nutrition in both the management and

prevention of type 2 diabetes (T2D) through its impact on weight and metabolic

control is clear. Yet, nutrition is also one of the most controversial and least adhered

to aspects of the management of T2D. There are multiple reasons for this; we

consider some of these.

The concept of being on a ‘diet’ for a chronic life-long condition like diabetes is

enough to put many people off, as knowing what to eat, and maintaining an optimal

eating pattern is challenging. Concepts of “Nutrition Therapy” or “Medical Nutrition

Therapy” were introduced to guide a systematic and evidence-based approach, and

Box: Scene setting: Diet and nutrition are undoubtedly of paramount importance in the

management and prevention of diabetes, and progress has been made in formulating

evidence-based dietary guidance in the past decade. Yet, there are ongoing areas of

controversy fueling polarised debate among scientists, leading to widespread

confusion. In this article, we examine the evidence for areas of consensus as well as

ongoing uncertainty or controversy about dietary guidelines for diabetes. What is the

best dietary approach? Is it possible to achieve remission of type 2 diabetes with

lifestyle or is it inevitably a condition causing progressive health decline? We also

examine the influence of nutrition transition and population-specific issues in the global

context and discuss future directions for optimal effectiveness and implementation of

diet and nutrition approaches for diabetes.

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their effectiveness has been demonstrated,3 but challenges remain. Although most

diabetes guidelines recommend starting pharmacotherapy only after an initial trial

of nutritional and exercise lifestyle advice, this is rarely followed in practice,

particularly in a global context. Most physicians are not trained in the principles of

nutrition interventions, and this inadequate knowledge and skill pose major barriers

to counselling patients, and innovative solutions are warranted.4 5 Moreover, talking

to patients about nutrition is time consuming. In many settings, except at some

specialized diabetes centres where trained nutritionists/educators are available,

advice regarding nutrition for diabetes, at best, remains a sheet of paper with a

printed menu which is handed over to the patient. In such resource poor settings, at

the point of T2D diagnosis, often the patient leaves the clinic with a list of new

medications and little else.

The cost of generic anti-diabetic drugs is very low in most developing countries like

India. Metformin is available for 1 rupee (about one pence) and some

sulphonylureas are also low-cost. Since the doctor is also better trained in

pharmacotherapy, the first, and often only, therapy offered to the person with

diabetes is a drug prescription, with fewer than 5-10% of patients with T2D being

treated only with lifestyle modification in settings like India.6 In contrast, 31% of the

primary care population with T2D was being managed solely with diet in a report

from the U.K., but process of care measures risk factors were less frequently

managed in this group than in the medication treated group.7 A particular point that

has not received priority is capturing of dietary information in patient medical

records, alongside other process measures, yet it is very difficult to achieve adequate

glycaemic control without at least modest attention to dietary intake. Is it now time

for family doctors and hospital clinics to collect this information routinely, and if so,

how?5 8

This is a major challenge but the dialogue on this subject must start.

In the meantime, progress has certainly been made on the optimal dietary advice for

diabetes, but there are broader issues at play. For instance, increasing vegetable and

fruit intake is generally recommended by most dietary guidelines. However, the cost

of vegetables and fruit remain prohibitively high in many settings: for instance, the

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cost of two servings of fruits and three servings of vegetables per day per individual

accounted for 52%, 18%, 16% and 2% respectively of household income in low-

income, low-to-middle income, upper-to-middle income and high-income countries.9

There is also an expensive market of foods labelled as “suitable for diabetics”, with

products often being no healthier, and sometimes worse than mainstream foods. In

some countries such as the U.K., following new European legislation, food

regulations were updated as recently as July 2016 to ban such misleading labels. This

is not the case elsewhere, however, and even in the U.K. what will happen post-

‘Brexit’ to such regulation, is currently unclear, highlighting the importance of the

political environment.

What do current dietary guidelines for diabetes recommend? An evidence based

approach

In some, primarily developed, countries dietary guidelines for the management of

diabetes have evolved from a previous focus on a low-fat diet to the recognition that

more important considerations are the macronutrient quality (that is the type,

versus the quantity, of macronutrient), avoidance of processed foods (particularly

processed starches and sugars) and overall dietary patterns. Many scientific

systematic reviews and national dietary guidelines have comprehensively appraised

the evidence for optimal dietary advice, and this article will not repeat that evidence

review.10-16

We focus on some important principles where there is broad consensus

in the scientific and clinical community, and highlight areas of uncertainty.

Areas of consensus

(1). Type 2 diabetes is a state most commonly associated with overweight or obesity

and insulin resistance. Therefore, reducing weight and maintaining a healthy weight

is a core part of clinical management. Weight loss is also linked with improvements

in glycaemia, blood pressure and lipids, and hence has benefits for delaying or

preventing complications, particularly cardiovascular events.

(2). Most guidelines recommend promoting weight loss among overweight or obese

individuals by reducing energy intake. Portion control is one strategy, and a healthful

eating pattern and physical activity, with ongoing support are recommended.

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(3). An understanding of ‘healthful eating’ in T2D has largely been derived from long-

term prospective studies and limited RCT evidence among general populations for

the prevention of diabetes, supplemented with more limited evidence among

people with known T2D. Overall, there is a good case for convergence of dietary

advice for both the prevention and management of T2D, rather than treating them

as different entities and making a special case for those with known T2D. An

important consideration, however, is to account for degree of glycaemic control,

type and dose of antidiabetic medication, and to co-ordinate dietary intake

appropriately.12

(4). Taken together, evidence review points to promoting overall patterns of food

intake that are high in vegetables, fruit, whole grains, legumes, nuts, and dairy

products such as yoghurt, but some dietary approaches (such as low-carbohydrate

diets) recommend restricting the intakes of fruits, whole grains and legumes, due to

their sugar or starch content. For fruit intake, in particular among those with existing

diabetes, there is ongoing debate with divided opinion among scientists and

clinicians (see Box in appendix). Many guidelines continue to recommend fruit,

however, on the basis that fructose intake from fruits is preferable to isocaloric

intake of sucrose or starch due to fruits’ micronutrient, phytochemical, and fibre

content.

(5) Taken together, there is evidence-based consensus on reducing or avoiding

habitual intakes of refined grains, processed red meats, and sugar-sweetened

beverages. For unprocessed red meat, the evidence of potential disbenefit is overall

less consistent and of smaller magnitude, but more research is needed on specific

benefits or harms in people with T2D. Cardio-metabolic health considerations, highly

relevant to diabetes, also extend recommendations to reductions in foods high in

sodium and trans- fat.

(6) There is also general consensus on the benefits of certain dietary patterns such as

the ‘Mediterranean diet’ but expert guidelines also support other healthful eating

patterns that take account of local socio-cultural factors and personal preferences

tailored to individuals appropriately.

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Areas of uncertainty

(1). One of the most contentious issues has been on the optimal macronutrient

composition of the diet. Some guidelines continue to advise macronutrient quantity

goals, such as the European or Canadian recommendation of 45–60% of total energy

as carbohydrate, 10–20% protein, ≤35% fat,13 17

or Indian guidelines recommending

50-60% energy as carbohydrate, 10-15% from protein, and <30% from fat.18

In

contrast, the most recent nutritional guideline from the American Diabetes

Association concluded that there is no one ideal mix of macronutrients for all people

with diabetes, recommending individually tailored goals.12

Alternatively, use of low-

carbohydrate nutrition as a preferred approach for weight and glycaemic control has

gained popularity among some experts, clinicians, and the public. Others conclude

that a low-carbohydrate diet combined with low-saturated fat is optimal.19

For

weight loss, two points are especially noteworthy. First, trial evidence points to

potential greater benefits of low-carbohydrate versus low-fat approach, but the

magnitude of overall weight loss as well as difference in magnitude between diets

can be modest.20

Second, a comparison of named diet programmes with different

macronutrient components highlighted that the critical factor in effectiveness for

weight loss is sustainability of the diet, such that the optimal diet is the one that one

can adhere to.21

A complicating factor in research-to-date for weight or metabolic

outcomes in diabetes is the use of varied definitions for the different macronutrient

approaches. For instance, the definition of low-carbohydrate diet ranged from 4% of

daily energy intake from carbohydrates (promoting nutritional ketosis) to 40% of

daily energy intake.15

Similarly, low-fat diets in studies vary with fat as <30% of daily

energy intake or substantially lower. Given these limitations, the best current

approach may be an emphasis on use of individualised assessment for dietary

advice, and focusing on the pattern of eating that most readily allows the individual

to limit calorie intake together with attention to macronutrient quality (such as

avoiding refined, but not all, carbohydrates).

(2). Regular fish intake of at least two servings a week, including one serving of oily

fish (e.g. salmon, mackerel, trout, etc) is recommended for cardiovascular risk

prevention, but fish intake has diverse associations with risk of developing T2D,

ranging between inverse, null and positive across world regions.22

It is thought that

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types of fish consumed, preparation/cooking practices and possible contaminants

(e.g. methyl mercury, polychlorinated biphenyls) vary by geographical location,

contributing to this heterogeneity. More research is needed to resolve whether fish

intake should be recommended for the prevention of diabetes, but the current

evidence supports an increase in oily fish for individuals with existing diabetes

because of their beneficial effects on lipoproteins and prevention of coronary heart

disease. Regarding omega-3 polyunsaturated fatty acid (fish-oil) supplementation,

there is broad consensus among guidelines for currently not recommending

supplements for cardiovascular prevention among people with diabetes, but more

research is needed and the awaited results from the ASCEND (A Study of

Cardiovascular Events in Diabetes) trial should help to clarify this.23

(3). Dairy foods are encouraged for the prevention of T2D, with more consistent

evidence for benefits of fermented dairy products such as yoghurt, but less so for

other dairy foods. Similar to population-level recommendations for limiting foods

high in saturated fats, current advice for diabetes also favours low-fat dairy

products, but there is ongoing debate and more research with improved methods of

dietary assessment is warranted to resolve this issue. Among edible oils, there is also

ongoing uncertainty around certain vegetable oils and tropical oils such as coconut

oil or palm oil as prospective or RCT evidence of clinical events is sparse or non-

existent. However, olive oil, particularly extra-virgin olive oil, has been studied in

greater detail with evidence for potential benefits for the prevention and

management of T2D24

in addition to the evidence for cardiovascular disease

prevention within the context of a Mediterranean diet25

(see accompanying article

on dietary fats in this series).

There are some global challenges. When dietary guidelines exist (for in many settings

there are none or are adapted from those in developed countries, hence local

applicability is an issue), they vary substantially in whether they are evidence-based

or opinion pieces, and time-appropriate or outdated. Their accessibility, both in

terms of physical availability (e.g. through a website, clinic, etc.) and

comprehensibility for patients and healthcare professionals is heterogeneous. They

vary also in their scope, content, detail, and in highlighting the importance of

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individualised dietary advice and of areas of controversy and further research needs.

The underlying quality of research that informs dietary guidelines also needs greater

investment from the scientific community and funders. Moreover, wider issues

regarding lack of transparency in the guideline development process and regarding

biases in the primary nutritional studies can undermine the development of reliable

dietary guidelines; recommendations for their improvement must be heeded.26

Can type 2 diabetes be reversed by diet?

Once thought to be irreversible and progressive after diagnosis, there has been

much interest in the potential for the remission, or even reversal, of T2D. Consensus

on definitions is a sign of progress: partial remission, defined as hyperglycaemia

below the diagnostic level for diabetes in the absence of anti-hyperglycaemic

medications; and complete remission as a return to normal glucose levels in the

absence of anti-hyperglycemic therapy for at least one year.27

There is, however,

ongoing controversy on the predominant role of energy deficit versus macronutrient

composition of the diet in achieving remission. We appraise this evidence next.

Remission of type 2 diabetes through a low-calorie energy deficit diet

Although the clinical observation of the lifelong, steadily progressive nature of T2D

was confirmed by the UK Prospective Diabetes Study (UKPDS),28

rapid normalisation

of fasting plasma glucose after bariatric surgery suggested that deterioration was not

inevitable.29

As the major change involved was one of sudden calorie restriction, a

low-calorie diet was used as a tool to study the mechanisms involved. In one study,

fasting plasma glucose normalised within seven days in the context of decreased

hepatic fat levels and restoration of hepatic insulin sensitivity.30

This normalisation

achieved by diet occurred despite simultaneous withdrawal of metformin therapy.

Gradually over eight weeks, glucose-stimulated insulin secretion returned to

normal.30

Was this a consequence of calorie restriction or composition of the diet?

To achieve the degree of weight loss obtained (15kg), ~610 kcal per day was

provided; 510kcal as a liquid formula diet plus approximately 100kcal as non-starchy

vegetables. The formula diet consisted of 59g of carbohydrate (30g as sugars), 11.4g

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fat and 41g protein, including required vitamins and minerals. This high ‘sugar’

approach to controlling blood glucose may surprise, but the critical aspect here is

not what is eaten, but the gap between energy required and taken in. Because of

this deficit, the body must call upon previously stored energy. Intrahepatic fat is

mobilised first, and the 30% decrease in hepatic fat in the first 7 days appears

sufficient to normalise the insulin sensitivity of the liver.30

Secondarily, pancreatic fat

content fell over 8 weeks and beta cell function improved. This is now recognized to

relate to regain of insulin secretory function by re-differentiation after fat removal.31

The durability of these changes was tested by devising a nutritional and behavioural

approach to achieving long term isocaloric eating after the acute weight loss phase.32

This was guided by individual preference, focusing upon weight stability guided

initially by estimated calorie requirements and then by monthly weighing. It was

successful in maintaining weight steady over the subsequent six-month study period.

Overall, calorie restriction was associated with both hepatic and pancreatic fat

content remaining at the achieved low levels. The initial remission of T2D was closely

related to duration of diabetes, and the individuals with T2D of shorter duration who

achieved normal levels of blood glucose maintained normal physiology during the six

months follow-up period.

A common criticism of the energy deficit research has been that very low-calorie

diets may not be achievable or sustainable. Indeed, adherence to most diets over

the longer term is a key challenge.21

Yet, ‘Look-AHEAD’, the largest randomized

study of lifestyle intervention in T2D (n=5145), randomized individuals to intensive

lifestyle management including the goal to reduce total caloric intake to 1200 to

1800 kcal/d through a low-fat diet assisted with liquid meal replacements, and this

approach was effective in achieving greater weight loss and partial remission of

diabetes at year 1 and year 4 than in the control group.33

Using a goal-directed

method for weight loss and subsequent weight stability can be effective,32

and

results on diabetes remission from a structured low-calorie weight loss programme

in the DiRECT trial in a UK-primary care setting are eagerly awaited.34

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There is considerable interest in whether low-calorie diets associated with diabetes

remission can also help to prevent diabetic complications. Evidence is sparse due to

lack of long-term follow-up studies, but the existing research is promising. A return

to the non-diabetic state brings an improvement in cardiovascular risk (Qrisk

decreasing from 19.8% to 5.4%);32

case reports of individuals facing impending foot

amputation record a return to low-risk state over 2-4y with resolution of painful

neuropathy;35 36

and retinal complications are unlikely to occur or advance.37

But, as

other evidence highlights risk of worsening of treatable maculopathy or proliferative

retinopathy following a sudden fall in plasma glucose levels,38 39

retinal imaging

within 4-6 months is required for individuals with more than minimal retinopathy if

undergoing low-calorie remission diet. Annual review is recommended for all in the

post-diabetic state, with a ‘diabetes in remission’ code (C10P) incorporated in the

UK.40

Management or remission of type 2 diabetes through a low-carbohydrate diet

Before insulin was developed as a therapy, reducing carbohydrate intake was the

mainstay treatment for diabetes.41 42

Indeed, carbohydrate restriction for the

treatment of T2D has been an area of intensive interest given that, of the

macronutrients, carbohydrate intake is the chief influence on serum glucose and

insulin levels.43

In a review convened by the American Diabetes Association (ADA), interventions of

low-carbohydrate (<40% of calories) diets published over 2001-2010 were

identified.15

Of 11 trials, 8 were randomized and approximately half the studies

reported greater improvement in HbA1c on the low-carbohydrate diet intervention

versus the comparison diet (typically a low-fat diet), as well as greater reduction in

glucose-lowering medications. Notably, calorie reduction coincided with

carbohydrate restriction in many of the studies, even though it was not often

specified in the dietary counseling. One of the more highly controlled studies in the

review was an inpatient feeding study,44

reporting a decline in mean HbA1c from

7.3% to 6.8% (p=0.006) over just 14 days on a low-carbohydrate diet. Across the low-

carbohydrate studies, cardiovascular benefits on lipid markers included overall

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higher HDL-cholesterol and lower triglyceride levels while the effects on raising the

adverse lipids (total and LDL cholesterol) were modest and non-significant. A number

of other systematic reviews of randomized trials in T2D patients have given varying

conclusions ranging from a superiority of low-carbohydrate versus other diets for

glycaemic control, or even a dose response relationship, with stricter low-

carbohydrate restriction resulting in greater reductions in glycaemia, to caution

about short-term effects not being sustained in the longer term, to no overall

benefit. 45-49

Narrative reviews have been more emphatic on the benefits of low-

carbohydrate diets, including, but not limited to, increased satiety, advantages for

weight loss and metabolic parameters.50 51

Among limitations, which are common to

almost all dietary research and not exclusive to low-carbohydrate nutrition, were

issues of small sample size, short duration (with some trials of between 1 to 16

weeks duration, but some being longer duration), lack of blinding, low dietary

adherence and high dropout rates. The contribution of associated calorie restriction

or weight loss to the results was also unclear, and some trials included any intake

with up to 45% of energy as carbohydrates while others were much more stringent,

but the sustainability at one year for very low-carbohydrate intake (<50g/d) was

particularly challenging.

Concerns about potential detrimental effects on cardiovascular health have been

raised as low-carbohydrate diets are typically high in dietary fat, including saturated

fat. For lipid markers as indicators future cardiovascular events, several studies

found greater improvements in HDL-cholesterol and triglycerides with no relative

worsening of LDL cholesterol in T2D patients following carbohydrate restriction,15

with similar conclusions in non-diabetic populations.50 52-54

LDL cholesterol tends to

decline more with a low-fat comparison diet53 55

and though LDL-c may not clearly

worsen on average with a low-carbohydrate diet55

in the short-term, the longer term

effects are unclear. There exists evidence, however, that low-carbohydrate intake

can lower the more atherogenic small, dense LDL particles.50

56

Because some

individuals may experience an increase in serum LDL-cholesterol when following a

low-carbohydrate approach that is high in saturated fat, monitoring is important.

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Another concern regards the effect of accompanying potential higher protein

content of lower carbohydrate diets on renal function, but evidence in T2D patients

with normal baseline renal function or among individuals without diabetes and with

normal or mildly compromised renal function have not shown worsening of renal

function at one or up-to two years of follow-up, respectively.19

57 58

59

Other potential

side effects of a very low carbohydrate diet include headache, fatigue and muscle

cramping, but these side effects can typically be avoided by adequate fluid and

sodium intake, particularly in the first week or two after initiation when diuresis is

greatest. Concern about urinary calcium loss and potential contribution to increased

future risk for kidney stones or osteoporosis60

have not been verified61

but evidence

is sparse and warrants further investigation. Long-term effects on cardiovascular

disease and chronic kidney disease in patients with diabetes deserve further

evaluation.

Clinicians and patients with diabetes who adopt low-carbohydrate diets must

understand how to avoid hypoglycaemia by appropriately reducing relevant glucose-

lowering medications, given the hypoglycaemic effect of carbohydrate restriction.

Finally, low-carbohydrate diets potentially restrict whole grain intake, and though

some low-carbohydrate foods can provide the fibre and micronutrients contained in

grains, this may require greater efforts to seek such foods. This has led some experts

to emphasize restriction of refined starches and sugars, but retain whole grains.

Nutrition transition and population specific issues for diet and diabetes

Several countries in Sub-Saharan Africa, South America, and Asia (e.g. India and

China) have undergone rapid nutrition transition during the last two decades. These

changes have paralleled economic growth, foreign direct investment in ‘fast food’

industry, urbanisation, direct-to-consumer marketing of calorie-dense foods, sale of

ultra-processed foods, and as a result, lesser consumption of traditional diets. These

factors link nutrition with obesity and diabetes on the one hand, co-existing with

undernutrition and micronutrient deficiencies on the other.

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Dietary shifts within low-middle income countries have been stark: in India these

include substantial increase in fat intake in the setting of already high carbohydrate

intake, with slight increase in total energy and protein62

and a decreasing intake of

coarse cereals, pulses, fruits and vegetables;63

in China, animal protein and fat as a

percentage of energy also increased, while cereal intake decreased.64

There has

been an almost universal increase in caloric beverage intake, with sugar sweetened

soda drinks being the top beverage contributor to energy intake, such as among

adults and children in Mexico,65

or the substantial rise in China in sales of sugar

sweetened beverages from 10.2 liters per capita in 1998 to 55.0 liters per capita in

2012.66

Movement of populations from rural to urban areas within a country may

also be linked with shifts in diets to more adverse patterns, such as higher intake of

fat and sugar,67

while acculturation of immigrant populations into their host

countries also results in dietary shifts.68

Some populations, such as South Asians, consume rice and wheat-flour bread as

staple foods, with a related high carbohydrate intake (60-70% of calories).69

Though

time trends show that intake of carbohydrate has decreased among South Asian

Indians, the quality of carbohydrates has shifted adversely towards use of refined

carbohydrates.63

The use of oils and traditional cooking practices also have

population-specific patterning. For instance, in India, import and consumption of

palm oil often incorporated in popular oil vanaspati (partially hydrogenated

vegetable oil, high in trans- fats) is high.70

Moreover, traditional Indian cooking

practice of frying at high temperatures and re-heating increases trans- fatty acids in

oils.71

Such oils are low cost, readily available, and have long shelf life, thus are more

attractive to middle and low socio-economic strata, but their long-term effects on

diabetes warrant further research.

Despite nutrition transition being linked with escalating prevalence of T2D, obesity

and other non-communicable diseases, firm efforts to curb harmful foods are not in

place in many countries. Regulatory framework including fiscal policies such as

taxation for sugar sweetened beverages, if effective, need to be strengthened,

alongside effective implementation of other preventive interventions. Efforts to

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control trans- fatty acids in foods have gained momentum, but are largely confined

to developed countries. To reduce such consumption in low- and middle-income

countries will require not only stringent regulations but also availability and

development of alternative choices of healthy and low-cost oils, ready-made food

products, and consumer education.72

The need for nutritional labelling is important;

however, correct comprehension of nutrition labels is a problem in populations with

low literacy or nutrition awareness, highlighting the need for educational activities

and simpler forms of labelling. The role of government in such initiatives is discussed

in a related article in this series.

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Box: FUTURE DIRECTIONS

• High quality research is needed comparing calorie restriction or carbohydrate restriction

to assess efficacy and feasibility longer term. Consensus is needed on definitions of low-

carbohydrate nutrition. The roll out of findings must take account of individual

preferences, and of whole diets and eating patterns.

• In the context of recent widespread recommendations (such as from the World Health

Organization) to reduce free sugars to under 10% or even 5% of total energy intake in

the general population and to avoid sugar sweetened beverages, we need targeted

research on the impact of non-nutritive sweeteners on health outcomes in people with

diabetes and in the whole population.

• In the global context, most dietary guidelines are derived from an evidence-base

generated in Western countries. There is an urgent need to better understand the

specific aetiological factors that link diet/nutrition and diabetes and its complications in

regional context. This will mean investment in developing prospective cohorts and

building capacity for undertaking research in low and middle-income settings. We need

to develop evidence-based and up-to-date dietary guidelines that are locally relevant

and readily accessible to healthcare professionals, patients and the public in different

world regions.

• We need investment in medical education by upskilling medical students and physicians

in lifestyle interventions, including incorporation of nutrition education in medical

training curriculum.

• Individual, collective and upstream factors are important. Issuing dietary guidance does

not ensure its adoption or implementation. To bridge the gap, investment is warranted

in understanding the individual and societal drivers and barriers for healthful eating.

Educating and empowering individuals to make better dietary choices is an important

strategy; in particular, attention is required to the social aspects of eating as most

people eat in family or social groups, and advice needs to take this into account. Equally

important is tackling the wider determinants of individual behaviour - the ‘foodscape’,

socio-cultural and political factors, globalization and nutrition transition.

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KEY MESSAGES

• A considerable body of evidence supports a wide variety of dietary

approaches that apply both to the general population and also for the

prevention and management of T2D.

• Weight management is a cornerstone for metabolic health.

• A key area of controversy is on the role of low-carbohydrate nutrition as the

diet of choice in T2D. Some current guidelines state that there is no single

ideal percentage distribution of calories from different macronutrients

(carbohydrates, fat or protein), but there are calls for a re-review in light of

emerging evidence on the potential benefits of low-carbohydrate diets and

more high quality research is needed. Quality aspects of carbohydrates such

as refined vs. whole grain sources are important, and should not get lost in

the debate on quantity.

• Evidence review indicates consensus regarding a focus beyond nutrients on

foods and healthy eating patterns. In individuals with T2D, emphasis should

be on promoting vegetables, healthy protein foods, nuts and yoghurt and on

avoiding processed foods, refined grains, processed meats and sugar-

sweetened beverages. No single diet applies universally, and dietary advice

should be individually tailored, taking into account personal, cultural and

social factors.

• An exciting recent development is the understanding that T2D does not have

to be a progressive condition on a downward spiral to adverse metabolic,

macrovascular and microvascular outcomes, but that there is potential of

remission, or even reversal, with dietary intervention. This is particularly

feasible in obese patients with shorter duration of T2D.

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This article does not cover the topic of type 1 diabetes or insulin-requiring type 2

diabetes. Though general principles are similar as in diet/nutrition for type 2

diabetes, a key difference is using carbohydrate counting or another meal planning

approach to quantify carbohydrate intake to enable estimation of mealtime insulin

alongside planned carbohydrate consumption.

Funding: NGF acknowledges MRC Epidemiology Unit core support

(MC_UU_12015/5)

Acknowledgements: We thank Sue Brown as a patient representative of Diabetes

UK for her helpful comments and insight into this article.

Contributors and sources: The authors have experience and research interests in the

prevention and management of type 2 diabetes (NGF, AM, VM, RT, WY), in guideline

development (NGF, AM, VM, WY) and in nutritional epidemiology (NGF). Sources of

information for this article included published dietary guidelines or medical nutrition

therapy guidelines for diabetes, and systematic reviews and primary research

articles based on randomized clinical trials or prospective observational study

designs. NGF took the lead role in drafting this manuscript and all authors

contributed parts of the text for manuscript sub-sections. All authors gave

intellectual input to improve the manuscript and have read and approved the final

version. NGF is the guarantor for the manuscript.

Competing interests: We have read and understood BMJ policy on declaration of

interests and declare that AM received honorarium and research funding from

Herbalife and Almond Board of California; VM has received funding from Abbott

Health Care Pvt. Ltd for meal replacement studies and the Cashew Export Promotion

Council of India and Almond Board of California for studies on nuts; RT has received

funding from Diabetes UK for the Diabetes Remission Clinical Trial; WY has received

funding from the Veterans Affairs for research projects examining a low-

carbohydrate diet in patients with diabetes.

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Licence: The Corresponding Author has the right to grant on behalf of all authors and

does grant on behalf of all authors, an exclusive licence (or non exclusive for

government employees) on a worldwide basis to the BMJ Publishing Group Ltd

("BMJ"), and its Licensees to permit this article (if accepted) to be published in The

BMJ's editions and any other BMJ products and to exploit all subsidiary rights, as set

out by the BMJ.

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Confidential: For Review Only A case in point: Fruit intake and diabetes – an area of ongoing debate

The author group was divided about whether fruit intake should be promoted for the prevention

and management of T2D, reflecting a wider ongoing debate among scientists and clinicians.

Two sides of the debate

• For fruit: fruits should be promoted as they have low energy density, are high in vitamins,

minerals, phytochemicals and dietary fibre, and are included in the 5-a-day health message.

• Against fruit: fruits should be limited as their higher carbohydrate content raises blood

glucose levels requiring higher doses of antidiabetic medication, and many of their benefits

can be obtained from other sources such as vegetables. Fruit juices and smoothies, widely

believed to count as healthy, increase energy intake and are inimical to overall weight

control

What do current evidence-based guidelines recommend, and what is the evidence?

General population guidelines

• There are widespread public health messages to consume at least 5 portions of vegetables

and fruit a day (more specifically, 3 of vegetables, and 2 of fruit within which fruit juice with

no added sugar is allowed as one portion). In some countries this message promotes at least

7 portions a day (4 vegetable and 3 fruit portions). Variety of intake is promoted.

• Named dietary patterns that are generally considered healthful, include emphasising fruit

and vegetables intake – such as in the Mediterranean diet, DASH diet, and others.

Guidelines for the management of diabetes

• Many national guidelines include consuming fruits as part of general healthy eating pattern,

reasoning that fructose from fruit may result in better glycaemic control compared with

isocaloric intake of sucrose or starch. Some do not mention fruit specifically, focusing

instead on green leafy vegetables.

• Some guidelines recommend consuming fruit with lower glycaemic index, including apples,

pears, oranges, peaches, plums, apricots, and berries while avoiding fruit with higher

glycaemic index (such as some tropical fruits like mango, cantaloupe, watermelon,

pineapple).

Prospective evidence for the prevention of T2D

There is mixed evidence. Some meta-analyses did not find an association of total fruit intake with

new-onset T2D.1 Some large prospective studies suggest that greater variety, not quantity, of fruit

intake is associated with lower incidence of new-onset T2D, while others suggest that inverse, null or

positive associations with new-onset T2D exist with different individual types of fruits, but that the

reasons and mechanisms for this were not yet fully clear.2 3

A critical review of the evidence across

different health endpoints provided support for national programmes that promote vegetable and

fruit intake, but highlighted that specifically for the prevention of T2D the evidence was more mixed,

though potential beneficial effects on T2D prevention through a favourable influence on weight

cannot be ruled out.4

Conclusion

For people with existing T2D, there is some evidence for potential benefits of fruits with lower

glycaemic index, and fructose from fruit is likely to be better than isocaloric intake of sucrose or

starch, particularly as refined carbohydrates, but there is need for further research. Currently, the

consumption of fruits should be guided within the overall dietary pattern of an individual, their taste

and other preferences and by their glycaemic control and need for antidiabetic medication,

supported by healthcare professionals.

References: (1) Carter P, et al. Fruit and vegetable intake and incidence of type 2 diabetes mellitus: systematic review and meta-

analysis. BMJ 2010;341:c4229. (2) Cooper AJ, et al. A prospective study of the association between quantity and variety of

fruit and vegetable intake and incident type 2 diabetes. Diabetes care 2012;35(6):1293-300. (3) Muraki I, et al. Fruit

consumption and risk of type 2 diabetes: results from three prospective longitudinal cohort studies. BMJ 2013;347:f5001.

(4) Boeing H, et al. Critical review: vegetables and fruit in the prevention of chronic diseases. European journal of nutrition

2012;51(6):637-63.

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