Diabetes in Asia

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Diabetes in Asia

Transcript Of Diabetes in Asia

REVIEW

Diabetes in Asia
Epidemiology, Risk Factors, and Pathophysiology

Juliana C. N. Chan, MBChB, MD
Vasanti Malik, MSc
Weiping Jia, MD, PhD
Takashi Kadowaki, MD, PhD
Chittaranjan S. Yajnik, MD, PhD
Kun-Ho Yoon, MD
Frank B. Hu, MD, PhD
ONCE CONSIDERED A DISease of the West, type 2 diabetes is now a global health priority.1 The International Diabetes Federation has predicted that the number of individuals with diabetes will increase from 240 million in 2007 to 380 million in 2025, with 80% of the disease burden in lowand middle-income countries.2 More than 60% of the world’s population with diabetes will come from Asia, because it remains the world’s most populous region. The number of individuals with diabetes and impaired glucose tolerance (IGT) in each Asian country will increase substantially in coming decades (TABLE 1).1 Unlike in the West, where older populations are most affected, the burden of diabetes in Asian countries is disproportionately high in young to middle-aged adults (FIGURE).2
Asia has undergone marked economic and epidemiologic transition in recent decades. Increasing globalization and East-West exchanges have been accompanied by increasing population movements, changes in food supply and dietary patterns, technology transfer, and cultural admixtures. In the recent World Economics Forum Report, the increasing burden of chronic diseases including diabetes was highlighted as a major global risk predicted to cause substantial financial loss resulting from in-

Context With increasing globalization and East-West exchanges, the increasing epidemic of type 2 diabetes in Asia has far-reaching public health and socioeconomic implications.

Objective To review recent data in epidemiologic trends, risk factors, and complications of type 2 diabetes in Asia.

Evidence Acquisition Search of MEDLINE using the term diabetes and other relevant keywords to identify meta-analyses, systematic reviews, large surveys, and cohort studies. Separate searches were performed for specific Asian countries. The review was limited to English-language articles published between January 1980 and March 2009; publications on type 1 diabetes were excluded.

Evidence Synthesis The prevalence of diabetes in Asian populations has increased rapidly in recent decades. In 2007, more than 110 million individuals in Asia were living with diabetes, with a disproportionate burden among the young and middle aged. Similarly, rates of overweight and obesity are increasing sharply, driven by economic development, nutrition transition, and increasingly sedentary lifestyles. The “metabolically obese” phenotype (ie, normal body weight with increased abdominal adiposity) is common in Asian populations. The increased risk of gestational diabetes, combined with exposure to poor nutrition in utero and overnutrition in later life in some populations, may contribute to the increasing diabetes epidemic through “diabetes begetting diabetes” in Asia. While young age of onset and long disease duration place Asian patients with diabetes at high risk for cardiorenal complications, cancer is emerging as an important cause of morbidity and mortality.

Conclusions Type 2 diabetes is an increasing epidemic in Asia, characterized by rapid rates of increase over short periods and onset at a relatively young age and low body mass index. Prevention and control of diabetes should be a top public health priority in Asian populations.

JAMA. 2009;301(20):2129-2140

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creased health care expenditure and lost productivity.3 However, there is considerable heterogeneity in ethnicity, cultures, and stages of socioeconomic development within Asia, all of which affect clinical presentation, management, and prevention of diabetes. In this article, we review epidemiologic trends and com-
Author Affiliations: Hong Kong Institute of Diabetes and Obesity, Department of Medicine, and Li Ka Shing Institute of Health Sciences, The Chinese University of Hong Kong, Hong Kong SAR, China (Dr Chan); Departments of Nutrition and Epidemiology, Harvard School of Public Health, and Channing Laboratory, Department of Medicine, Brigham and Women’s Hospital, and Harvard Medical School, Boston, Massachusetts (Drs Malik and Hu); Department of Endocrinology and Metabolism, Shanghai Jiaotong University Affiliated Sixth People’s Hospital, Shanghai, China (Dr Jia); Department of Metabolic Diseases, Graduate School of Medicine, University of Tokyo,

plications of type 2 diabetes in Asian populations and discuss risk factors implicated in this epidemic.
EVIDENCE ACQUISITION
We searched MEDLINE using the term diabetes and other relevant keywords (diabetes mellitus, metabolic syndrome,
Tokyo, Japan (Dr Kadowaki); Diabetes Unit, KEM Hospital Research Center, Pune, India (Dr Yajnik); and Department of Endocrinology and Metabolism, Seoul St. Mary’s Hospital, The Catholic University of Korea, Seoul, Republic of Korea (Dr Yoon). Corresponding Authors: Juliana C. N. Chan, MBChB, MD, Department of Medicine and Therapeutics, The Chinese University of Hong Kong, The Prince of Wales Hospital, Shatin, Hong Kong SAR, China ([email protected] .edu.hk) and Frank B. Hu, MD, PhD, Departments of Nutrition and Epidemiology, Harvard School of Public Health, 665 Huntington Ave, Boston, MA 02115 ([email protected]).

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DIABETES EPIDEMIC IN ASIA

diabetic complications, clinical studies, registry, prospective cohorts, crosssectional cohorts, case-control, cohorts, epidemiology, prevalence, incidence, causes, causation, diagnosis, prognosis, socioeconomic status, ethnicity, depression, psychosocial stress, smoking, haemoglobinopathy, thalassaemia, visceral fat, hepatitis, C reactive proteins, infections, tobacco, alcohol, dietary factors,

persistent organic pollutants, environmental toxins, pollutants, urbanization, acculturation, iron, iron overload, birthweight, body mass index, waist circumference, central obesity, waist hip ratio, exercise, physical activity, risk score, risk equation, risk prediction, adolescent obesity, gestational diabetes, inflammation, nutritional transition, sleep, television watching).

Table 1. Top 10 Countries in Asia With the Highest Number of Persons With Type 2
Diabetes and Impaired Glucose Tolerance in the Age Group 20 to 79 Years in 2007 and Projected Data in 2025a

Diabetes

Impaired Glucose Tolerance

Country

2007

2025

India

40 850

69 882

China

39 809

59 270

Japan

6978

7171

Bangladesh

3848

7416

Korea

3074

4163

Thailand

3162

4660

Philippines

3055

5572

Indonesia

2887

5129

Malaysia

1530

2743

Vietnam
Subtotal b Western Pacific

1294 66 993

2500 99 401

Southeast Asia

46 543

80 341

Grand total Asiab

113 536

179 742

a Source: International Diabetes Federation.2 All values are in thousands. b Includes numbers from Asian countries not shown here.

2007 35 906 64 323 12 891
6819 3224 1896 4410 14 144 2915 1175
111 898 45 169
157 067

2025 56 228 79 058 12 704 10 647
4240 2399 7582 20 597 4442 1902
142 693 70 525
213 218

Separate searches were performed for specific Asian countries. We limited the searches to English-language articles published between January 1980 and March 2009; non–English-language studies were excluded, because the quality of these studies is difficult to evaluate. Publications on type 1 diabetes were excluded. High-priority articles included meta-analyses, systematic reviews, large surveys, and cohort studies.
EVIDENCE SYNTHESIS
Epidemiologic Trends
of Diabetes in Asia
In this global epidemic of diabetes, Asian countries undergoing economic and nutritional transitions have experienced a particularly notable increase (TABLE 2).4-46 In China, the prevalence of diabetes increased from 1% in 1980 to 5.5% in 2001,7 with much higher rates in urban areas such as Shanghai.51 Nearly 10% of Chinese adults residing in affluent regions such as Hong Kong and Taiwan have diabetes.52 Among individuals with diabetes, two-thirds in Mainland China and one-half in Hong Kong and Taiwan remain undiagnosed.52

Figure. Number of Persons With Diabetes in Different Age Groups and Number of Deaths Attributable to Diabetes in Different Regions of the World in 2007

No. With Diabetes (Millions) No. of Deaths

40 Age group, y

35

20-39

40-59

30

60-79

25

Diabetes

20

15

10

5

0 Africa EMME Europe North SACA
America

SEA Western Pacific

600 000 500 000 400 000 300 000 200 000 100 000
0

Deaths Attributable to Diabetes, Ages 20-79 Years
Men Women

Africa

EMME

Europe

North America

SACA

SEA Western Pacific

Source: International Diabetes Federation.2 EMME indicates Eastern Mediterranean/Middle East; SACA, South America/Central America; SEA, Southeast Asia (comprises Bangladesh, Bhutan, India, Maldives, Mauritius, Nepal, and Sri Lanka [total population, 770 350 000; estimated prevalence of diabetes in the region, 6%]). Western Pacific comprises Australia, Brunei Darussalam, Cambodia, China, Hong Kong, Macau, Cook Islands, Fiji, French Polynesia, Guam, Indonesia, Japan, Kiribati, Korea (Democratic People’s Republic of ), Korea (Republic of ), Lao People’s Democratic Republic, Malaysia, Marshall Islands, Micronesia (Federal States of ), Mongolia, Myanmar, Nauru, New Caledonia, New Zealand, Niue, Palau, Papua New Guinea, Philippines, Samoa, Singapore, Solomon Islands, Taiwan, Thailand, Timor-Leste, Tokelau, Tonga, Tuvalu, Vanuatu, and Vietnam (total population, 1 468 598,000; estimated prevalence of diabetes in the region, 7.6%).

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Table 2. Trend of Prevalence of Type 2 Diabetes in Asia in Comparison With That in the United States During the Last 2 to 3 Decades Diabetes

Country United States4-6
1976-1980 1999-2000 2005-2006 Mainland China7-9 1980 1994-1995 2000/2001
Hong Kong10,11 1993 1995-1996
Taiwan12,13 1987-1988
1996 Japan14-16
1981-1982 1988 1990-1992 Korea17-19 1991
1997 2001
2003
India20-22 1979

Sample
National National National

Age, y
20-74 20-74 20-74

14 provinces 19 provinces 31 provinces

NA 25-64 35-74

Employees b Entire region

30-64 25-74

Pu-Li

Ն30

Tainan city

Ն20

Tokyo

Ն30

Hisayama, suburban
Fungata, rural

40-79 Ն40

Yonchon County, South Korea
Chongup-rural

30-64 Ͼ30

Nationwide

Ͼ20

Chongup-rural Ն30

Multicenter

NA

Women, % 51.9 50.4 51.07
Male/Female 44.8 51.4
39.8 Men/Women
52.1
48.7 21.6 54.2 56.3 56.3 41.4 57
40.8
NA

Mean BMI in Survey Diagnosis

Population

Method

Criteria a

25.3

FPG

ADA 1997

28.0

FPG

ADA 1997

28.7

FPG/

ADA 1997

OGTT

NA
23.8 (NGT) 25.2 (diabetes) 24.3 (urban) 23.3 (rural) 24.8 (North) 22.8 (South)

FPG/ OGTT
FPG/ OGTT
FPG

Ͼ130/Ͼ200 mg/dL
WHO 1985
ADA 1997

NA
23.5 (NGT) 26.6 (impaired fasting
glucose [ADA criteria])

FPG/ OGTT
FPG/ OGTT

WHO 1985 WHO 1999

23.0 (NGT) 23.7 (diabetes; 23.0 (previous, 24.6 (new)
Not reported

FPG/ OGTT

WHO 1985 (modified)

OGTT

WHO 1985

Not reported
22.9 (men) 23 (women) Not reported

FPG/ OGTT
OGTT

WHO 1980 WHO 1985

OGTT

WHO 1985

Not reported

OGTT

WHO 1985

23.6 (NGT) 25.5 (IGT)
23.3 (NGT men) 24.2 (IGT men) 22.8 (NGT women) 24.4 (IGT women)
22.9 (NGT, men) 24.4 (diabetes, men) 24.3 (NGT, women) 26.2 (diabetes,
women)
NA

OGTT FPG OGTT
NA

ADA 1997 ADA 1997 ADA 1997
NA

1999-2002 Nationwide

Ն25

50.8

Not reported

OGTT

WHO 1999

2003-2005 Nationwide

Pakistan23 1994-1999

Nationwide

15-64

51

Ն25

65.2

23.1 (urban males) 24 (urban females) 20.3 (rural males) 20.8 (rural females)
22.4 (urban men) 24.5 (urban women) 22.6 (rural men) 25 (rural women)

Self-report

NA

OGTT

WHO 1985

Prevalence, % 5.3 8.2
12.6
Ϸ1 2.5 5.5

Age Adjusted
Yes Yes Yes
Yes
Yes
No

7.7

No

9.8

6.9 (previous)

Yes

4.4 (new)

9.2

Yes

3.6

No

10.2

Yes

10.1

No

7.2

Yes

6.9

Yes

7.6

Yes

11.7

Yes

3 (urban)

No

1.3 (rural)

4.3

Yes

5.6 (urban)

2.7 (rural)

4.5

Yes

7.3 (urban)

3.1 (rural)

6 (urban men) 3.5 (urban women) 3.3 (rural men) 2.5 (rural women)

No (continued)

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DIABETES EPIDEMIC IN ASIA

Table 2. Trend of Prevalence of Type 2 Diabetes in Asia in Comparison With That in the United States During the Last 2 to 3 Decades (continued) Diabetes

Country Bangladesh24-26
1997
1999 2004 2005 Nepal27-29 1990
1999-2001 2007 Sri Lanka30,31 1994 c 2005-2006 Indonesia32,33 1981-1982 1995 Malaysia34-36 1982

Sample

Age, y

Women, %

Mean BMI in Survey Diagnosis

Population

Method

Criteria a

Dhaka city-

30-64

35.2

20.17 (NGT, men)

FPG/

WHO 1985

suburban

21.6 (diabetes, men)

OGTT

19.7 (NGT, women)

23 (diabetes,

women)

Chandra region- Ն20

57.2

rural

20.2

FPG/

WHO 1999

OGTT

Chandra region- Ն20

59.8

rural

20.7

FPG/

WHO 1999

OGTT

Dhaka city-

Ն20

52.9

urban

19.4

FPG/

WHO 1999

OGTT

Kathmandu/

Ն20

Kabhre

Urban/rural

Ն20

52

19.5 (suburban

FPG

men)

20 (rural men)

19.6 (suburban

women)

20.4 (rural women)

53.7

Not reported

FPG

ADA 1997 (post hoc)
ADA 1997

Semi-urban

21-94

60

NA

NA

Suburban National

30-64

50.7

Not reported

Ͼ20

60

21.2 (NGT)

23.8 (diabetes)

OGTT
FPG/ OGTT

WHO 1985 ADA 1997

Jakarta-urban Jakarta-urban

Ն15 NA

52.8 Male/Female

NA

OGTT

WHO 1980

NA

NA

NA

National

NA Male/Female

NA

NA

NA

Prevalence, % 4.5

Age Adjusted
Yes

2.3

No

6.8

No

8.1

No

1.4 (suburban)

No

0.3 (rural)

14.6 (urban)

No

2.5 (rural)

9.5

NA

5.0

Yes

10.3

Yes

1.63

No

5.7

NA

2.1

NA

1992-1995 2005-2006 Thailand37-39 1991 2000 2004
Vietnam40,41 1990
2001
Cambodia42 2004
Philippines43 1982-1983 2002

Kelantan-Malay/ rural
National

Ն30 25-64

Men/Women Men/Women

NA

FPG/

WHO 1980

OGTT

NA

FPG

Ն7 mmol/L

National National National

Ն30

56.5

22 (men)

23.5 (women)

FPG

Ն7.8

mmol/L

Ն35 Men/Women 23.8 (NGT) 25.4 (diabetes)

FPG

Ն7 mmol/L

Ն15 Male/Female 22.3 (NGT)

FPG

Ն7 mmol/L

28.3 (diagnosed

diabetes)

Hanoi

30-64

53.5

19.3 (men)

OGTT

WHO 1985

20.1 (women) (subset

of 116 with new

diabetes)

Ho Chi Minh

Ն15

74.4

21.1 (NGT, males)

FPG

ADA

21.8 (NGT, females)

22.7 (diabetes, men)

23.3 (diabetes,

women)

Rural/suburban 30-64

63.6

20.4 (men)

21.3 (women)

OGTT

WHO 1999

Luzon-urban Luzon-urban

Adults Men/Women

NA

20-65

63.5

22.9 (men)

23.3 (women)

OGTT OGTT

Ն11.1 mmol/L
WHO 1999

10.5

NA

11

NA

2.4 (men)

Yes

3.7 (women)

9.6

Yes

6.7

Yes

1.4

Yes

3.8

Yes

9.7 (suburban) 5.6 (rural)
3.3
4.8
5.1

Yes
No Yes No (continued)

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Table 2. Trend of Prevalence of Type 2 Diabetes in Asia in Comparison With That in the United States During the Last 2 to 3 Decades (continued) Diabetes

Country

Sample

Age, y

Women, %

Mean BMI in Survey Diagnosis

Population

Method

Criteria a

Prevalence, %

Age Adjusted

Singapore44-46

1984-1985 National

18-69 Men/Women 25.8 (Chinese)

OGTT

WHO 1985

4.7 e

Yes

27 (Malay) 24.1 (Indian)d

1992

National

18-69

49.5

22.3 (Chinese men) OGTT

WHO 1985

8.4 f

Yes

22.8 (Malay men)

23.6 (Indian men)

21.3 (Chinese

women)

23.8 (Malay women)

23.7 (Indian women)

2004

National

18-69 Men/Women

NA

FPG/

WHO 1985

8.9 (men)

NA

OGTT

7.6 (women)g

Abbreviations: ADA, American Diabetes Association; BMI, body mass index; FPG, fasting plasma glucose; IGT, impaired glucose tolerance; NA, not available; NGT, normal glucose tolerance; OGTT, oral glucose tolerance test; WHO, World Health Organization.
SI conversion factor: To convert glucose values to mg/dL, divide by 0.0555. a ADA 199747: fasting plasma glucose level 7.0 mmol/L or greater; WHO 198048: fasting plasma glucose level 7.8 mmol/L or greater or 2-hour plasma glucose level 11.1 mmol/L or
greater; WHO 198549: fasting plasma glucose level 7.8 mmol/L or greater or 2-hour plasma glucose level 11.1 mmol/L or greater; WHO 199850: fasting plasma glucose level 7.0 mmol/L or greater or 2-hour plasma glucose level 11.1 mmol/L or greater. b Employees from 2 work sites of a major public utility company and regional hospital. c Publication year. d Mean BMI among individuals with diabetes. e Age-standardized prevalence of diabetes was 4.2 in Chinese men, 4 in Chinese women, 9.1 in Malay men, 6.4 in Malay women, 12.3 in Indian men, and 5.5 in Indian women. f Age-standardized prevalence of diabetes was 12.2 in Asian Indians, 10.1 in Malays, and in 7.8 in Chinese. g Prevalence of diabetes was 7.1 in Chinese, 15.3 in Indians, and 11 in Malays (unsure if age-standardized).

In urban Indian adults, diabetes prevalence increased from 3% in the early 1970s to 12% in 2000, with a narrowing rural-urban gradient.20 In 2006, the rate of type 2 diabetes in rural South India was 9.2%, compared with an increase in urban South India from 13.9% in 2000 to 18.6% in 2006.53
In rural Bangladesh, prevalence of diabetes increased from 2.3% to 6.8% between 1999 and 2004.24 In a national survey in 2001, 8% of Korean adults had diabetes, with little difference between urban and rural areas.17 In a nationwide survey in Singapore in 1998, Indians had the highest prevalence of diabetes (12.8%), followed by Malays (11.3%) and Chinese (8.4%).54 Similarly, 11% of Malays living in Malaysia have diabetes.34,35 Other Asian countries including Japan, Sri Lanka, Indonesia, Thailand, and Vietnam also have experienced a marked increase in prevalence of diabetes (Table 2). While some Asian countries like China and India have a very large number of patients with diabetes, the prevalence of diabetes can be as high as 40% in some Pacific Island populations.55

Risk Factors for the Diabetes
Epidemic in Asia
Increasing Overall and Abdominal Obesity. Asians have lower rates of overweight and obesity than their Western counterparts, using conventional definitions (body mass index [BMI] Ն25 for overweight and Ն30 for obesity, calculated as weight in kilograms divided by height in meters squared). Despite lower BMI, some Asian countries have similar or even higher prevalence of diabetes than Western countries.56 These data confirm that the risk of type 2 diabetes starts at a lower BMI for Asians than for Europeans.57
In China, the prevalence of overweight (BMI Ն25) in adults increased from 14.6% to 21.8% between 1992 and 2002.58 In a cross-sectional survey of 15 540 Chinese adults aged 35 to 74 years in 2000-2001, the age-standardized prevalence of overweight was 26.9% in men and 31.1% in women, with higher rates in northern than in southern China as well as higher rates in urban than in rural residents.59 In India, between 2003 and 2005, the prevalence of overweight ranged from 9.4% in rural men to 38.8% in urban women.21 Using the same BMI

cutpoint, 28.6% of adults living in urban Pakistan were overweight.23 In developing countries, obesity in adults is not necessarily a disease of the socioeconomic elite, as is commonly believed.60 In fact, the burden of obesity and diabetes tends to shift toward lower socioeconomic status groups as a country’s gross national product increases.61
The increasing trend of childhood obesity in Asia places many young individuals at high risk for type 2 diabetes in early adulthood. In China, based on the 2000 reference values from the US Centers for Disease Control and Prevention, 22.9% of boys and 10.4% of girls attending urban schools were overweight.62 Among schoolchildren in urban South India, 17.8% of boys and 15.8% of girls were overweight.20 Similar rates have been reported in Malaysia,36 Korea,63,64 and Thailand.65 In Hong Kong, 2.3% of adolescents have the metabolic syndrome, with family history of diabetes, BMI, and low academic performance as independent predictors.66
Asian populations, especially those of South Asian descent, are more prone to abdominal obesity and low muscle mass with increased insulin resistance

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DIABETES EPIDEMIC IN ASIA

compared with their Western counterparts.20,67-73 Thus, waist circumference reflecting central obesity is a useful measure of obesity-related risk of type 2 diabetes, especially in individuals with normal BMI values.67,74 In Singapore, for the same age, sex, and BMI, Indians had the highest body fat percentage, followed by Malays and Chinese. All 3 groups had a higher body fat percentage than whites.70
Using imaging technology (such as computed tomography scan) to measure total body fat and specific depots of fat, healthy Chinese and South Asian individuals were found to have a greater amount of visceral adipose tissue than Europeans with the same BMI or waist circumference.75 These data suggest that the increased risk of type 2 diabetes in Asian populations may be attributed to increased abdominal and visceral adiposity for a given BMI. Despite having a lower body weight, Indian infants have higher subcutaneous fat, leptin, and insulin levels than white infants.76 This “metabolically obese” phenotype (eg, normal weight by conventional BMI standards but increased abdominal adiposity) has been associated with increased risk of insulin resistance and diabetes.77 In Asian populations, the amount of visceral fat (including mesenteric fat) and fatty liver was significantly associated with subclinical atherosclerosis.78 In addition, increased waist circumference has been associated with substantially increased risk of developing diabetes67,79,80 as well as increased risk of cardiovascular and allcause mortality, independent of BMI.81-84
Nutrition Transition and Changes in Diet and Lifestyle. In many Asian countries, rapid socioeconomic development has led to a concurrent shift in infrastructure, technology, and food supply that promotes overnutrition and sedentary lifestyles. Traditional dietary patterns are disappearing as Asians adapt to increasingly industrial and urban conditions resulting from globalization. Rapid nutrition transition has left many countries facing coexisting problems of overnutrition and undernutrition.60,85

In China between 1992 and 2002, the proportion of energy intake from animal foods increased from 9.3% to 13.7% and that from fats from 22% to 29.8%.58 In India the change was more pronounced among urban residents, who consumed 32% of energy from fat compared with 17% in rural residents.86 Substantial increases in animal fat intake also have been reported in Vietnam,40 Japan,87 Korea,64,88 and Thailand.89 Vegetable ghee, such as Dalda—a clarified butter commonly used in cooking in India and other southeastern Asian countries—contains trans fatty acid levels as high as 50%.90 Higher intake of trans fatty acids has been associated with weight gain, increased cardiometabolic risk, and insulin resistance.91-93
Polished rice and refined wheat form the basis of most Asian diets with high glycemic index and glycemic load values.94 The glycemic index of Vietnamese rice ranges from 86 to 109.72 In a prospective cohort study of middleaged Chinese women, a high intake of foods with a high glycemic index or glycemic load, especially rice, is associated with a 2-fold increased risk of type 2 diabetes,95 especially in overweight and obese individuals. Similar findings have been reported in Japan.96 Consumption of sugar-sweetened beverages, an important contributor of dietary glycemic load and excess calories, has increased rapidly worldwide, particularly in Asia.97
Increased urbanization and universal use of automobiles has caused many Asians to shift from a physically active, agrarian lifestyle marked by energy scarcity to a sedentary lifestyle marked by energy surplus. In developing countries, a rapid uptake of technologies has been accompanied by increasing shifts from agriculture and increasing employment in manufacturing and services.90 In Asia, automobiles are rapidly replacing bicycles as the primary mode of transportation. In China, an average of 1 in 10 Beijing permanent residents owns a car.58 In the past decade, the annual rate of increase in motor vehicle ownership in India was approximately 11%.85

Psychosocial stress, depression, and short sleeping hours, which have become increasingly common in developing countries undergoing rapid economic developments, have been associated with higher risk of the metabolic syndrome and diabetes in Asian populations.98-101 In a meta-analysis, depression was associated with a 60% increased risk of type 2 diabetes, while the latter was associated with a 15% increased risk of depression.102 The coexistence of diabetes and depression was associated with a 50% to 100% increased risk of all-cause mortality.103
Cigarette Smoking. In a recent metaanalysis, current smoking was associated with 44% increased risk of developing diabetes.104 A similar positive association has been reported in Korea,105 Taiwan,106 and China.107 Smoking is known to induce insulin resistance and inadequate compensatory insulin secretion responses. Among individuals with normal BMI, smokers were more likely to have abdominal obesity than nonsmokers.104
In many Asian countries, between 50% and 60% of adult men are regular smokers.105-107 China, followed by India, is the greatest producer and consumer of cigarettes in the world. Almost 1 of 3 cigarettes produced worldwide is consumed in China.108 Most Indians use smokeless tobacco products, such as betel quid, and 40% smoke bidis— small, often flavored, nontaxable cigarettes—the production of which provides employment for many urban poor.109
Pancreatic Beta Cell Function. In the 1980s, Japanese researchers first unraveled that reduced early insulin response was an independent predictor for diabetes.110 Fukushima et al111 found that at all stages of glucose intolerance, Japanese individuals had reduced early and late phases of insulin responses. In Japanese men with normal glucose tolerance, even a small increase in BMI produced a decrease in beta cell function disproportionate to that in insulin sensitivity.112 In a sample of Chinese patients with type 2 diabetes, 50% were of normal weight, with

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low BMI correlating with low levels of fasting plasma C-peptide (a marker of decreased insulin secretion) and high glycated hemoglobin levels.113 In a prospective survey of Japanese Americans, visceral fat area and reduced incremental insulin response were independent predictors for diabetes.114 Taken together, in some Asian populations, inadequate beta cell response to increasing insulin resistance results in loss of glycemic control and increased risk of diabetes, even with relatively little weight gain.
Developmental Origins of Diabetes. Many Asian adults who experienced great hardship during wartime or civil unrest in early life are now experiencing marked changes in lifestyle. In addition, low birth weight and exposure to undernutrition in utero are common in some Asian populations, especially in India, where 30% of infants are underweight.115 Insults or stresses during the intrauterine period can lead to permanent changes in structure, metabolism, and physiology through altered expression of the genome without changes in the DNA codes, a process called epigenetics.116 These early life events may influence later susceptibility to diabetes, the metabolic syndrome, and cardiorenal diseases. Prospective studies from India have shown the impact of fetal undernutrition (often manifested as low birth weight) as well as overnutrition (eg, the infant of a mother with diabetes) on future risk of diabetes.115 In India, thinness in infancy and overweight at age 12 years was associated with increased risk of developing IGT or diabetes in young adulthood.117
A recent meta-analysis of 30 studies found a significant graded association between low birth weight and increased risk of type 2 diabetes.118 Low birth weight has also been found to predict diabetes and the metabolic syndrome in Asian adults and children,119-121 thus lending support to the notion that fetal programming with exposure to poor nutrition in utero or during early childhood can promote a fatpreserving or thrifty phenotype. These

metabolic changes predispose individuals to insulin resistance and reduced beta cell function. Positive energy balance in later life, caused by rapid westernization of diet and lifestyle, may then exaggerate accumulation of adiposity, particularly in the central depots.122
The 2- to 3-fold higher risk of gestational diabetes in Asian women than in their white counterparts also may contribute to the increasing epidemic of young-onset diabetes in Asia.123 Asian women with a history of gestational diabetes have a substantially increased risk of diabetes, while their offspring exhibit early features of the metabolic syndrome, thus setting up a vicious cycle of “diabetes begetting diabetes.” This combination of gestational diabetes, in utero nutritional imbalance, childhood obesity, and overnutrition in adulthood will continue to fuel the epidemic in Asian countries undergoing rapid nutritional transitions.115
Genetic Susceptibility. Among lean, healthy individuals matched for age, BMI, waist circumference, birth weight, and current diet, Asians (especially those of Southeast Asian descent) had higher levels of postprandial glycemia and lower insulin sensitivity than whites in response to a 75-g carbohydrate load.124 These findings raise the possibility that Asians are more genetically susceptible to insulin resistance and diabetes than whites.
Several diabetes genes recently discovered through genome-wide association studies in white populations have been confirmed in Asians as well.125-129 However, there were significant interethnic differences in risk allele frequency and location. Using the transcription factor 7-like 2 gene TCF7L2 (rs7901349) as an example, the minor allele frequency was 0.03 in Asian and 0.27 in European populations.125,126,130 For the potassium voltage-gated channel, subfamily Q, member 1 gene KCNQ1, the minor allele frequency of rs2237892 was 0.28 to 0.41 and 0.05 to 0.07 in East Asian and European populations, respectively.131 Most diabetes genetic variants identified so far, including those in TCF7L2 and KCNQ1,

appear to be associated with decreased insulin secretion in whites as well as Asians. In addition, among Asian adults diagnosed with diabetes before age 40 years, approximately 40% had a lean, nonautoimmune phenotype with rapid oral drug failure.132-135 Approximately 10% of these patients carried genetic variants encoding pancreatic beta cell pathways, including transcription factors and amylin, or mitochondrial polymorphisms. These findings provide further evidence that beta cell dysfunction plays a critical role in the development of diabetes in Asians.
Other Risk Factors. Emerging evidence suggests that exposure to environmental irritants, such as persistent organic pollutants, is associated with increased insulin resistance, the metabolic syndrome, and diabetes.136,137 Studies from Taiwan and Bangladesh have found a strong association between chronic arsenic exposure and risk of diabetes.138
Consistent with studies in whites,139 Sun et al140 found that moderate iron overload predicted diabetes in Chinese individuals. Hemoglobinopathies, such as ␣ and ␤ thalassemia traits and hemoglobin H disease, which are associated with increased iron turnover, are present in 8% to 10% of Chinese individuals.141,142 Asian individuals with thalassemia traits were reported to have a several-fold increased risk of gestational diabetes,143 insulin resistance,144 and glucose intolerance.145
Approximately 8% to 10% of Asian populations, including Chinese individuals, are chronic hepatitis B viral carriers.146 Compared with noncarriers, Chinese women who were hepatitis B carriers had a 30% increased risk of gestational diabetes, independent of other well-known diabetes risk factors.147 Chronic hepatitis B carriers affected by type 2 diabetes also had an earlier age of diagnosis and 4-fold higher risk of end stage renal disease (ESRD) than noncarriers.148 Similar risk associations with diabetes and diabetic kidney disease have been reported in chronic hepatitis C carriers.149 Other infections endemic in Asia, such as tu-

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berculosis,150 have also been associated with increased risk of diabetes and severe clinical course of the disease.
Complications and Comorbid
Conditions of Diabetes in Asia
In the World Health Organization Multinational Study of Vascular Diseases in Diabetes, conducted in the early 1970s, stroke and kidney failure were leading causes of death in Chinese, Japanese, and Pima Indian patients with diabetes, compared with coronary heart disease (CHD) in white patients.151
In the Asia-Pacific Collaborative Study, among patients with diabetes, the leading cardiovascular cause of death was stroke (42%) in Asia and CHD (59%) in Australia and New Zealand. However, within Asia, there were marked differences in these complications, with China and Japan having higher rates of stroke than CHD, while in Hong Kong and Singapore, the rate of stroke was similar to or even lower than that of CHD.152
Asian patients with diabetes continue to exhibit high risk for renal complications, even after accounting for socioeconomic status.153 In an international survey, 55% of Asian and 40% of white patients with type 2 diabetes had increased albuminuria.154 Chinese individuals with IGT were found to have a high prevalence of albuminuria, with 2-hour plasma glucose level as an independent predictor.155 In observational studies as well as clinical trials, Asian patients with diabetes were more likely to develop ESRD than their white counterparts. However, only a small fraction of these patients can afford renal replacement therapy in developing countries such as China.156 Importantly, albuminuria and renal function are powerful predictors of CHD in Asian as well as white populations, with or without diabetes.157,158
In a 25-year prospective survey, 60% of young Japanese patients with type 2 diabetes diagnosed before age 35 years became blind or had developed ESRD at a mean age of 50 years.159 In a multiethnic study in Singapore, Indians had the highest risk of diabetes. Among the

individuals with diabetes, Indians had the highest risk for CHD,160 while Malays had the highest risk for ESRD56 and mortality due to heart failure.161 In a Malaysian dialysis registry, diabetic nephropathy contributed 55% of all new cases of dialysis, with a mean age of 50 years and a preponderance of women.162 In this multiethnic registry, Malays had the highest incidence of ESRD, followed by Indians and Chinese.
In Chinese patients with diabetes, risk factors for chronic kidney disease included smoking; long disease duration; high calcium phosphate product; albuminuria; increased blood pressure, waist circumference, and levels of triglycerides, low-density lipoprotein cholesterol, and glycated hemoglobin; and decreased glomerular filtration rate and levels of high-density lipoprotein cholesterol.163 Genetic factors, including aldose reductase and angiotensinconverting enzyme deletion/insertion polymorphisms, were associated with risk of chronic kidney disease in patients with diabetes. In addition, low hematocrit values were found to be an independent predictor of ESRD and cardiovascular complications in Chinese individuals.164 Furthermore, low blood hemoglobin level was associated with decreased levels of insulin growth factor 1 and testosterone in Asian and white men with diabetes, the metabolic syndrome, or diabetic kidney disease.165-169 Given the possible epigenetic regulation of the hypothalamicpituitary-adrenal axis and the growth hormone–insulin growth factor 1 axis, neurohormonal dysregulation is likely to be implicated in diabetic kidney disease.116,170
Several meta-analyses have shown that except for prostate cancer,171 diabetes was associated with a 30% to 40% increased risk of breast,172 endometrial,173 pancreatic,174 liver,175 and colorectal cancers.176 Patients with cancer as well as diabetes also had a 40% to 80% higher risk of death than those without diabetes.177 Communitybased prospective surveys, including those conducted in Asia, reported independent associations of fasting178,179

and 2-hour plasma glucose levels180,181 with cancer risk. Given the high rates of IGT, which predicts all-cause mortality in Asian populations,182 there is a need to understand the potential role of glucose metabolism and insulin resistance in carcinogenesis.183,184
Changing patterns of disease and medical care are accompanied by secular changes in causes of death in Asian patients with diabetes. In Hong Kong, for example, the majority of Chinese patients with type 2 diabetes died from stroke and ESRD until the early 1990s.185 In the mid-1990s, heart disease emerged as the leading cause of death.186 In 1995, a prospective diabetes registry was established in Hong Kong. It recruited 7000 patients with type 2 diabetes, half of whom were middle-aged at diagnosis. Ten years after diagnosis, 30% had died or had sustained a major clinical event, with cancer (20%), CHD (20%), ESRD (10%), and stroke (10%) as major causes of death.187
COMMENT
The diabetes epidemic in Asia is characterized by rapid rates of increase over short periods and onset at a relatively young age and low BMI. The epidemic is heterogeneous, varying according to different ethnic and cultural subgroups, degree of urbanization, and socioeconomic conditions in different Asian populations. In parallel with economic development and nutrition transition, the rates of overweight and obesity have been increasing rapidly in Asian countries. Abdominal or central adiposity, particularly detrimental to type 2 diabetes and other metabolic diseases, is highly prevalent in Asians. The high rates of gestational diabetes, in combination with in utero exposure to poor nutrition, childhood obesity, and overnutrition in later life, may contribute substantially to the increasing diabetes epidemic in Asia.
While further research is needed to systematically monitor secular trends of diabetes in Asian populations, characterize risk factors, and understand interactions between genetic and envi-

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DIABETES EPIDEMIC IN ASIA

ronmental risk factors, ample evidence
from Asia has shown that diabetes and
its complications is preventable and
highly treatable. In the early 1990s, a
randomized trial in China demon-
strated that dietary and exercise inter-
vention reduced diabetes risk by 31% to 46% in individuals with IGT.188 These
results have since been confirmed in Europe,189 the United States,190 India,191 and Japan.192 In observational
studies and randomized trials con-
ducted in Asia and Europe, control of
multiple risk factors reduced cardiore-
nal complications and all-cause death
by 50% to 70% in individuals with type 2 diabetes.193-195
Type 2 diabetes mellitus has be-
come an epidemic in Asia. To curb this
epidemic, an integrated strategy com-
bining population-wide preventive
policies (eg, changing food and the
built environment), early detection, and
multidisciplinary care programs may re-
duce the risk of diabetes and associ-
ated complications in the general popu-
lation and in high-risk individuals.
Author Contributions: Drs Chan and Hu had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: Chan, Malik, Hu. Acquisition of data: Chan, Malik, Hu. Analysis and interpretation of data: Jia, Kadowaki, Yajnik, Yoon Drafting of the manuscript: Chan, Malik, Hu. Critical revision of the manuscript for important intellectual content: Chan, Malik, Jia, Kadowaki, Yajnik, Yoon, Hu. Administrative, technical, or material support: Chan, Hu. Study supervision: Chan, Hu. Financial Disclosures: Dr Chan reported receiving research funding or speakers’ honoraria from AstraZeneca, Bayer, Bristol-Myers Squibb, Daiichi-Sankyo, GlaxoSmithKline, Lilly, Merck Serono, Merck Sharp & Dohme, Novo Nordisk, Pfizer, Roche, and sanofiaventis; serving as a member of the advisory boards, and/or speaker forums, and/or steering committees of international projects sponsored by AstraZeneca, Bayer, Lilly, and Merck Sharp & Dohme; with her group and on behalf of the Chinese University of Hong Kong, filing a patent application to use genetic markers to predict risk of diabetes and diabetic kidney disease in Chinese populations; and, in a technology transfer project, establishing a university-affiliated diabetes center (Qualigenics) to deliver a multidisciplinary chronic care program in the community (all related revenues and proceeds go to the Chinese University of Hong Kong to support ongoing research and development in diabetes). Dr Kadowaki reported receiving research funding or speakers’ honoraria from Takeda, Daiichi-Sankyo, Astellas, Ono, Dainippon Sumitomo, sanofi-aventis, Novo Nordisk, Novartis, and Lilly and serving as a member of the advisory board of Daiichi-Sankyo, Ono, Merck, Lilly, sanofi-aventis, Novo

Nordisk, and Novartis (all funds go to the University of Tokyo to support ongoing research and development in diabetes). Dr Yoon reported serving as a member of the steering committees, and/or advisory boards, and/or speaker forums of Merck Sharp & Dohme, GlaxoSmithKline, Lilly, Merck Serono, Novartis, and Choongwae Korea on diabetes-related subjects; serving as an investigator on clinical trials supported by AstraZeneca, Bristol-Myers Squibb, Boehringer Ingelheim, Merck Sharp & Dohme, Lilly, sanofi-aventis, GlaxoSmithKline, Roche, CJ Pharmaceutical, and CW Korea; with his team and on behalf of the Catholic University of Korea, filing a patent application to use various Web-based diabetes management programs and intracellular miRNA targets to improve beta cell function in patients with diabetes; and, in a technology project, working with his team to establish a university-affiliated institute for ubiquitous health care and a joint venture company called C & I Healthcare to use protocol-driven care delivered through Internet and mobile communications to improve diabetes care in the community. Dr Hu reported receiving research funding from Merck, Unilever, and the California Walnut Commission and receiving payment or honoraria for presentations at academic conferences supported by Novartis and Novo Nordisk. Mr Malik, Dr Jia, and Dr Yajnik reported no financial disclosures. Additional Contributions: We thank Louisa Lam, MLib, MAIS, librarian, Li Ping Medical Library, Faculty of Medicine, The Chinese University of Hong Kong, The Prince of Wales Hospital, for her assistance and advice on search strategy. Ms Lam received no extra compensation for her contributions. We regret that limited space allows us to cite only a fraction of the work conducted in Asian countries.
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