Prevalence of Type 2 diabetes and central adiposity in La Réunion Island, the REDIA Study

Diabetes Research and Clinical Practice 67 (2005) 234–242 www.elsevier.com/locate/diabres

Prevalence of Type 2 diabetes and central adiposity in La Re´union Island, the REDIA Study Franc¸ois Faviera,b,*, Isabelle Jaussenta, Nathalie Le Moullecb, Xavier Debusschec, Marie-Claude Boyerc, Jean-Claude Schwagerb, Laure Papoza The REDIA Study Group1 a

INSERM U500, 39, Av. Charles Flahault, 34093 Montpellier Cedex 5, France Department of Diabetology, South Reunion Hospital Group, St. Pierre, La Re´union Island, France c Department of Diabetology, District Hospital Center, St. Denis, La Re´union Island, France

b

Received 10 March 2004; received in revised form 30 June 2004; accepted 7 July 2004

Abstract La Re´union Island, a French overseas department in the Indian Ocean provides an example of rapid urbanisation and drastic changes in the way of life—from traditional to ‘‘westernised’’ lifestyle—over a few decades. To study the impact of this epidemiologic transition, a diabetes prevalence study was performed in 1999–2001. Fasting capillary blood glucose (cBG) and glycated hemoglobin (HbA1c) were systematically measured in a random sample of 3600 subjects aged 30–69 years. Weight, height, waist and hip circumferences were also measured to assess body mass index and waist-hip ratio. Diagnosis was assessed using an oral glucose tolerance test according to the World Health Organization recommendations in 363 subjects who had a cBG value
6.1 mmol/l, and/or a HbA1c value
6%. The overall diabetes prevalence rate was 17.7% for men and 17.3% for women, and the standardized diabetes prevalence rate was 20.1% (95% confidence interval: 18.7–21.4%). The most important morphological factor linked to Type 2 diabetes mellitus was waist-hip ratio, a marker of central adiposity, especially in women. This study confirms that Type 2 diabetes is increasing dramatically in societies in epidemiologic transition and is strongly linked to nutritional status. # 2004 Elsevier Ireland Ltd. All rights reserved. Keywords: Diabetes mellitus; Obesity; La Re´union Island

* Corresponding author. Present address: CIC-EC INSERM, Groupe Hospitalier Sud-Re´union, BP 350, 97448 St. Pierre, La Re´union, France. E-mail address: [email protected] (F. Favier). 1 REDIA Study Group—Coordination, INSERM Montpellier: Dr. L. Papoz (Principal Coordinator), A. Sanchez, B. Lecointre, I. Jaussent, Field survey, La Re´union Island; Dr. Favier (Local Coordinator), Dr. F. Martinet, Dr. A. Brissot, T. Dijoux, M. Damour, M.J. Andrieu, S. Rivie`re, J. Mani, N. Naty; South Reunion Hospital Group, St. Pierre, La Re´union Island: Dr. J.C. Schwager, Dr. N. Le Moullec, Dr. J. Guiserix, Dr. A. Clabe´; District Hospital Center, St. Denis, La Re´union Island: Dr. M.C. Boyer, Dr. X. Debussche, Dr. B. Bourgeon, Dr. H. Caillens. 0168-8227/$ – see front matter # 2004 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.diabres.2004.07.013

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1. Introduction Type 2 diabetes mellitus, which represents about 85% of all cases of diabetes, had an estimated prevalence of 4% in adults worldwide in 1995 which was predicted to rise to 5.4% by the year 2025 [1]. However, the prevalence rate of Type 2 diabetes varies with population characteristics: age structure, socioeconomic and nutritional status, genetic and environmental factors. It is very high among certain native populations like the Pima Indians [2] or the Nauruans [3]; it is reaching epidemic proportions in populations living in urban areas of developing countries, as well as in minorities and disadvantaged groups from industrialized countries [4,5]. Moreover, migrant populations (such as Indian, Chinese and HispanicAmerican groups, Chinese Mauritians) are at higher risk [6]. Many studies support the role of total obesity and intra-abdominal location of body fat in the etiology of Type 2 diabetes, accounting for the epidemic of diabetes by the life-style and socioeconomic changes mainly characterized by a decrease of physical activity and an increase in high fat intake [7–9]. Genetic susceptibility also plays a major causal role in the etiology of Type 2 diabetes: the concordance for Type 2 diabetes in monozygous twins (60%) is twice the rate observed in dizygous twins [10]. In subjects genetically predisposed to Type 2 diabetes, environmental factors influence the expression of the genotype. The tropical islands are particularly interesting because they present a combination of several risk factors for Type 2 diabetes: lifestyle change characterized by rapid urbanisation, low socioeconomic status and migration, which all add to the genetic susceptibility. In addition to Nauru, which has the highest prevalence in the world, high prevalences have been found in Guadeloupe [11], Mauritius and Rodrigues [12,13], Seychelles [14], New Caledonia [15], Vanuatu [16] and Polynesia [17]. In a French overseas island located in the Indian Ocean, called La Re´ union Island, local clinicians reported a recent increase in cases of diabetes and difficulties in their management. In a local study on a small population sample, the frequency of diabetes in La Re´ union Island had been estimated in 1992 at 7.5% (95% CI: 6–10%) in the adult population. Additional

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data on the characteristics of the various forms of the disease or on its control were not available.

2. Population and methods 2.1. Location and demography La Re´ union is a French ‘‘de´ partement’’ (administrative area, similar to a county) of 703,800 inhabitants. Its surface area is 2504 km2. It is located about 800 km east of Madagascar, and belongs to the Mascareignes archipelago (including Mauritius and Rodrigues) in the Indian Ocean. Discovered in the 17th century, initially named Bourbon Island, it was uninhabited and populated firstly by Malagasy and Europeans. The intensive culture of sugar cane led to the use of slaves from Africa, until the middle of the 19th century. When slavery was abolished, the planters hired workers coming mostly from the Indian Malabar coast, and also from Gudjurat (northern India), East Africa and China. Nowadays, the main ethnic groups are the white Creoles with a Caucasian ascendancy, the Caffres with African ascendancy, the Malbars with southern Indian ascendancy, the Zarabs with northern Indian ascendancy, Asiatic and Metropolitans being in the minority. However, because of the high rate of interbreeding in the island, and French law limiting the use of ethnic items in population censuses and surveys, ethnicity was not included in this report. The island was included in the French Republic as a department in 1946. This political decision induced thorough changes in the local population, essentially rural, and traditionally marked by a low life expectancy, poverty, scarcities or even famines. Over a few decades, it became a consumer society of western type, with a global improvement in conditions, a decline in mortality, an increase in energy consumption, and a decrease in physical activity. However, strong social disparities and economic difficulties still remain for an important part of the population: 40% of the working population is unemployed and more than 60,000 persons live on the minimum guaranteed income. Differences exist in the development of the north and the south of the island. The north, with the county town St. Denis, a city of 120,000 inhabitants, is the

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most active part of the island, while the south, where the main city is St. Pierre, is more rural. The littoral part (the ‘‘lows’’) is highly urbanized, whereas the mountainous part (the ‘‘heights’’) is still rural. 2.2. Population The target population was defined as subjects of both sexes, aged 30–69 years, born in La Re´ union Island, or if not so, living for at least 10 years in the island, free of life threatening chronic disease or disability preventing moving. Three areas were selected for their demographic and geographic representativeness (urban/rural, heights/lows): two in the south, the city of St. Pierre (in the lows, mainly urban) and the town of Le Tampon (in the heights, mainly rural), and a site in the northeast area, the town of St. Andre´ , mixed urban and rural. The ethnic distribution shows a population mainly Caffre and half-caste in St. Pierre, white Creole in Le Tampon and Malbar in St. Andre´ . In each area, a number of islets of population (28 in St. Pierre, 39 in Le Tampon, 31 in St. Andre´ ), as defined by the National Institute of Statistics and Economic Studies, were selected at random. Every household of the selected islet was visited by a technician in charge of recruitment. All subjects aged 30–69 years who fulfilled the inclusion criteria, were systematically asked to participate in the survey. Overall, 3600 subjects (1576 men and 2024 women) entered the study, representing a response rate of 80.6%. Among them, 363 subjects who had a cBG value or a HbA1c value defined as positive (see below), have had an oral glucose tolerance test to assess the diagnosis of diabetes. 2.3. Data collection Subjects were screened at home. Diabetes screening was performed through a two-step procedure. At the first visit, capillary blood glucose (cBG) was measured with glucose strips and interpreted immediately on a reflectance meter (One Touch II, LifeScan, Ortho Diagnostics, Milpitas, CA). In parallel, HbA1c was also systematically measured (DCA 2000, Ames, Bayer Diagnostics, Basingstoke, England). Each subject was asked whether he (she) had diabetes. All known diabetic subjects (whatever their capillary

blood glucose value) were invited to come to the health center for further investigation. As far as possible, their physician was contacted to document the history of diabetes. All other subjects having a fasting capillary blood glucose value
6.1 mmol/l or HbA1c value
6% were invited to come to the health center for a more detailed examination. In non-fasting subjects, a capillary blood glucose value of 7.8 mmol/l was chosen as the cut-off point for further examination. The second step was performed at the health center early in the morning. It included a 2 h oral glucose tolerance test with a 75 g glucose load according to the WHO recommendations [18]. Blood samples were taken at fasting and 2 h after the glucose load. For ethical reasons, the glucose load was replaced by a standard meal (bread, ham, dairy products, resulting in 67 g carbohydrates, 18 g proteins and 20 g fat) in previously known diabetic subjects and newly detected subjects with a fasting capillary blood glucose value higher than 11.1 mmol/l or 16.7 mmol/l nonfasting. Blood samples were frozen, and sent to the local laboratory in St. Pierre or St. Denis. Plasma glucose values fasting and 2 h post-load were measured by the glucose oxidase method. Obesity was assessed on the basis of the body mass index (BMI) calculated as weight/height2 (kg/m2). Subjects were classified as lean, normal, overweight or obese according to body mass index <19, 20–25, 25– 29,
30 kg/m2, respectively. Waist circumference (WC) and hip circumference were measured in the standing position with a special tape to the nearest centimeter, the first at the umbilicus, the second at the iliac spines. The waist to hip ratio (WHR) was calculated as an index of fat distribution (classified as high if
1.0 in men or
0.9 in women). This two-step protocol was proposed in 1991 [19], applied in New Caledonia in 1992–1994 [15], and approved for this study by the Ethical Committee of the Hospital St. Eloi, Montpellier. Each subject recruited for this study gave written informed consent. 2.4. Criteria for diabetes The three measurements of blood glucose levels were used for diagnosis: at the first test, capillary blood glucose (cBG), at the second test, fasting plasma glucose (FPG) and 2 h plasma glucose (2h-PG).

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Subjects not previously known to have diabetes were classified as newly detected cases if: - cBG or 2h-PG was
11.1 mmol/l, or - 2h-PG was <11.1 mmol/l but FPG
7.0 mmol/l and fasting cBG
7.0 mmol/l. These criteria correspond to WHOs recommendations revised after the publication of a report of the American Diabetes Association [18,20,21]. The crude prevalence rates were corrected according to the results observed in a sample of 275 negative screenees who also underwent a 2 h oral glucose tolerance test. Five new cases of diabetes were found in this group, leading to an estimate of 1.8% of cases missed in the age-group 30–69 years with our methodology. 2.5. Statistical methods The corrected prevalence rate was calculated considering separately the subsample of subjects not known as diabetic and the subsample of previously known diabetic subjects: - among subjects not known as diabetic, the prevalence rate is: p ¼ p1 þ p2 where p1 represents the prevalence in positive screenees and p2 the prevalence in negative ones. Each contribution should be weighted by its probability. Thus, p1 = % diabetes among positive screenees  probability to be positive and p2 =% diabetes among negative screenees  probability to be negative. - Finally, the total prevalence p ¼ p þ p0 ¼ p1 þ p2 þ p0

(1)

p0

where is the prevalence rate of previously known diabetic subjects. The 95% confidence intervals were calculated using as variance the sum of the variances of the three independent terms of expression 1. For direct application to the population of La Re´ union, the total age-specific prevalence rates obtained after correction were used to estimate the

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age-adjusted prevalence rate. For between countries comparisons, the prevalence rates and their confidence intervals were age-adjusted by direct standardization using the World Standard Population. The Statistical Analysis System was used for all analyses (SAS Institute, Cary, NC, USA).

3. Results The representativeness of the study sample is described in Table 1. In the general population study centers, the distribution of age was quite similar in St. Pierre and Le Tampon, but the population of St. Andre´ was slightly younger, with more subjects in the agegroup 30–39 years (about 42% in St. Andre´ versus 39– 40% in St. Pierre and Le Tampon). This was observed in both sexes. Overall, although the population of the study areas were fully representative of the populations of the whole Island, the age-group 30–39 years was slightly under-represented in the study sample, whereas the age-group 60–69 years was slightly over-represented in both sexes. The response rate was slightly higher in females than in males (82.5% versus 78.3%).

Table 1 Age distribution by sex in La Re´ union Island population (census of 1999), in the three areas of the study, and in the study sample, La Re´ union Island REDIA Study, 1999–2001 Age-group 30–39

40–49

50–59

60–69

Men (%) La Re´ union Island Three areas of the study St. Pierre Le Tampon St. Andre´ Study sample n

40.09 40.18 40.14 38.89 42.19 36.1 569

29.50 29.30 29.45 29.32 29.01 28.7 452

18.65 18.70 18.80 19.41 17.48 21.6 341

11.76 11.82 11.61 12.38 11.33 13.6 214

Women (%) La Re´ union Island Three areas of the study St. Pierre Le Tampon St. Andre´ Study sample n

40.13 40.49 40.19 39.46 42.51 36.8 745

28.93 28.67 29.30 28.36 28.96 30.1 609

18.04 18.07 18.70 18.42 16.75 19.0 385

12.90 12.77 11.82 13.76 11.78 14.1 285

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Table 2 Description of the study sample by sex and age, La Re´ union Island REDIA Study, 1999–2001 Pa

Age-group 30–39

40–49

50–59

60–69

Men n BMI (kg/m2) Range WHR Range WC (cm) Range

569 24.8 (0.2)b 12.4–44.8 0.90 (0.003) 0.72–1.14 87.3 (0.5) 51–134

452 25.1 (0.2) 16.1–44.3 0.93 (0.003) 0.78–1.13 89.7 (0.5) 66–139

341 24.9 (0.2) 13.4–39.3 0.97 (0.004) 0.71–1.19 91.6 (0.6) 55–127

214 24.9 (0.3) 14.1–43.3 0.99 (0.005) 0.78–1.24 93.0 (0.8) 61–134

Women n BMI (kg/m2) Range WHR Range WC (cm) Range

745 25.0 (0.2) 15.8–54.7 0.84 (0.003) 0.60–1.14 82.0 (0.4) 53–134

609 26.2 (0.2) 15.8–48.9 0.87 (0.003) 0.67–1.25 86.5 (0.5) 58–132

385 27.1 (0.3) 12.7–45.4 0.92 (0.004) 0.69–1.19 91.8 (0.7) 60–139

285 26.6 (0.3) 13.6–47.3 0.96 (0.005) 0.71–1.24 93.5 (0.7) 65–127

a b

NS <0.001 <0.001

<0.001 <0.001 <0.001

Test of regression by ANOVA, NS: not significant. Geometric mean (S.E.) after logarithmic transformation.

Therefore, the subsequent results are presented by age and sex, and overall estimates also adjusted for age and sex when appropriate in the present analysis. This population displays quite particular characteristics regarding obesity and adiposity (Table 2). First of all, in all age-groups, the range (maximum– minimum) of BMI is about 30 kg/m2; secondly, there is little variation of BMI according to age, but highly significant variations of WHR in both sexes (P < 0.001). Low values for the morphological parameters in all age-groups (e.g. the lowest value for BMI was 12.4 kg/m2 among men in the age-group 30–39 years) were unexpected. Indeed, 5.8% of men and 4.8% of women had a BMI lower than 19 kg/m2, the definition of underweight. The analysis by areas of the characteristics of the study samples is presented in Table 3. Again, the average age in St. Andre´ appeared slightly younger. The morphological parameters were similar in the three samples, except for WHR, which was higher in the urban St. Pierre than in the rural Le Tampon (0.89 in St. Pierre versus 0.87 in Le Tampon, and 0.88 in the mixed rural urban St. Andre´ ). This finding confirms the well-known effect of the urban environment on the development of central obesity. Mean fasting cBG value was the highest in Le Tampon, while mean non-fasting cBG was the highest

in St. Andre´ . These differences between centers are small and probably due to different factors, including the season, the degree of severity of the diabetic subjects, and their number. In contrast, HbA1c did not differ between centers. At the second step, 363 positive screenees (41% were positive from cBG alone, 22% from HbA1c alone, and 37% from both) were submitted to a 2 h glucose tolerance test: Overall, 93.6% of the diabetic subjects detected in the study had HbA1c
6%, including 25% with cBG <6.1 mmol/l. In the whole population studied, the prevalence rate of diabetes mellitus was 17.7% for men and 17.3% for women, after correction for undetected cases at screening, and adjustment for age (Table 4). Two thirds of these patients were already diagnosed and one third were new cases diagnosed in the study. Between the age-groups 30–39 and 60–69, the prevalence increases by 5 in men and about by 7 in women. This increase is mainly due to known cases of diabetes. Glycemic control was not achieved in most of the known diabetic patients (181 men and 249 women), whatever the sex (mean cBG: 9.3 mmol/l; mean HbA1c: 8.5%). Very similar results were found in both sexes for age at entry to the study (54 years, S.D.: 9.5) and age at diagnosis (45 years, S.D.: 11.5). In contrast, we observed a large difference in the frequency of

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Table 3 Results of the screening steps by study areas, La Re´ union Island REDIA Study, 1999–2001 Study area

St. Pierre

Le Tampon

St. Andre´

P

n Sex (% of men) Age (years)a

1117 44.0 46.2  0.3

1006 44.2 46.5  0.3

1477 43.3 45.3  0.3

NS <0.02

Men BMI (kg/m2) WHR WC (cm)

24.8  0.2a 0.94  0.01 89.2  0.5

25.2  0.2 0.93  0.01 90.2  0.5

24.8  0.2 0.94  0.01 89.7  0.4

NS NS NS

Women BMI (kg/m2) WHR WC (cm)

26.2  0.2 0.89  0.01 87.8  0.05

26.0  0.2 0.87  0.5 86.6  0.5

25.9  0.2 0.88  0.01 86.3  0.5

NS <0.01 NS

Both sexes cBG (mmol/l)b Fasting (n = 3335) Non-fasting (n = 265)

5.3 (0.1) 5.6 (0.2)

5.8 (0.1) 5.9 (0.2)

5.5 (0.1) 6.2 (0.2)

<0.001 <0.05

HbA1c (%)b

5.5 (0.1)

5.8 (0.1)

5.5 (0.1)

NS

a b

Mean  S.E. Geometric mean (S.E.) after logarithmic transformation.

Table 4 Prevalence of diabetes by sex and age in adults, La Re´ union Island REDIA Study, 1999–2001

Table 5 Relationships between Type 2 diabetes and body mass index (BMI) waist circumference (WC), and waist-hip ratio (WHR), La Re´ union Island, REDIA Study, 1999–2001

Age-group a

30–39 40–49 50–59 60–69 30–69 Men (%) n Known diabetes New casesb Total

569 2.5 4.6 7.1

452 10.0 8.1 18.1

341 20.2 8.9 29.1

214 24.8 9.6 34.4

1576 10.7% 7.0% 17.7%

Women (%) n Known diabetes New casesb Total

745 2.7 3.2 5.9

609 10.7 5.6 16.3

385 21.0 7.2 28.2

285 29.1 10.9 40.0

2024 11.7 5.6 17.3

Both sexes (%) Overall adjusted ratea Standardized ratec a

17.5 20.1

95% IC: 16.2–18.7 95% IC: 18.7–21.4

Overall prevalence rate adjusted for the age and sex distributions in the population of La Re´ union Island. b After correction for the lack of sensitivity of the screening method (see text). c Standardized according to the theoretical World Standard Population age distribution between 30 and 69 years (30–39: 30%; 40–49: 30%; 50–59: 22.5%; 60–69: 17.5%).

Men BMI (kg/m2) <25 25–29
30 WC (cm) <90
90 WHR <1.0
1.0 Women BMI (kg/m2) <25 25–29
30 WC (cm) <85
85 WHR <0.9
0.9

Type 2 diabetes (%)

OR

95% CI

9.7 19.1 24.2

1 2.3 3.2

1.7–3.2 2.0–5.0

8.0 21.5

1 2.6

1.9–3.6

9.3 37.1

1 3.7

2.7–5.1

8.3 20.1 26.2

1 2.4 3.2

1.7–3.2 2.3–4.5

5.5 24.5

1 3.8

2.8–5.3

4.5 31.7

1 6.2

4.5–8.6

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Fig. 1. Age-specific prevalence rate of Type 2 diabetes according to WHR, in men and women, La Re´ union Island REDIA Study, 1999–2001.

overweight, which was more severe and frequent in diabetic women than in diabetic men: 32.7% of overt obesity in women versus 13.4% in men. Body fat distribution was strikingly more often of android type in women than in men: 81.9% in women (WHR
0.9) versus 50.9% in men (WHR
1.0) (P < 0.0001). The relationships of Type 2 diabetes mellitus (known and newly detected cases) with BMI, or WHR or WC were studied using logistic models (Table 5). The strongest age-adjusted relative risk of diabetes was found with WHR, especially in women: 6.2 versus 3.7 in men, both highly significant (P < 0.001). This result is illustrated in Fig. 1. Regarding BMI, it should be underlined that among underweight subjects (BMI < 19 kg/m2), we found a diabetes prevalence of 4.3% in men, and 7.1% in women. In this particular subgroup, mean height was also lower than in the other

subjects (1.55 m versus 1.62 m, P < 0.05), but only one of these patients was insulin dependent.

4. Discussion One limitation of this study was the difficulty in analyzing the role of ethnicity in the occurrence of Type 2 diabetes. First of all, French law limits the use of ethnic information (it is prohibited in population censuses) and therefore no data were available for the comparison of our sample with the general population. Secondly, there is a very high rate of interbreeding in La Re´ union Island between people from Europe, Africa, Madagascar, and India. Very few people are strictly of one origin, and many have several origins through several generations. Such a full history

F. Favier et al. / Diabetes Research and Clinical Practice 67 (2005) 234–242

requires full cooperation of the subjects, and may be sensitive. Another limitation is the non-participation of about 20% of the subjects selected for this study, linked to age and sex. To correct this bias, the prevalence rates were calculated by age-groups, and the overall rates adjusted for age and sex; in addition, age was introduced in all multivariate analyses. Regarding the objective of assessing the prevalence of diabetes, our methodology was appropriate in several aspects. In addition to the random selection of the subjects, the choice of the study areas in different contexts has contributed to the representativeness of the sample. We tried to avoid the biases due to false positive screenees and to false negative screenees by our two-step design. The validity of the diagnosis of diabetes relies on the two-hour glucose tolerance test, so that false positive screenees were not confirmed at the second step. The percentage of false negative screenees was estimated on a subsample of negative subjects. An interesting finding is the important contribution of the HbA1c measurement to screening efficiency: the majority of the diabetic subjects detected in the study had HbA1c
6%, including one-fourth with normal cBG. Clearly, this study confirms that Type 2 diabetes is increasing rapidly in societies in transition. As in several reports [15,16,22] we found an excess of diabetes in the urban area (St. Pierre) in comparison with the very close rural one (Le Tampon). In the population of La Re´ union Island, it appears that diabetes prevalence is now at least twice that observed less than 10 years ago. Similarly, in Papua New Guinea, Dowse et al. found an impressive increase of diabetes prevalence, which doubled over a 14-year period in an urban area, in parallel with rapid modernization [22]. However, this phenomenon is not specific to tropical regions: the same trend was observed in the northern regions of the world where diabetes mellitus was previously almost unknown. For example, in less than 10 years, from 1990 to 1997, diabetes prevalence has increased by 76% in Alaskan Eskimos, according to the statistics of the US National Health Services [23]. Regarding our data, the prevalence rate of known diabetes found in La Re´ union in the age-group 30–69 years is more than three-fold that issued from the

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central data base of the Social Security for mainland France (11.2% versus 2.9%) over the same period [24]. These figures suggest that the level of the risk factors is far above that of mainland France, in spite of the same system of care for 50 years. As to the characteristics of the known diabetic patients, they were, at diagnosis, about 5 years younger in La Re´ union Island than in mainland France (45 versus 50 years on average) [25]. This is consistent with other studies conducted in tropical regions, indicating that Type 2 diabetes has an earlier onset in this context [6]. But the most striking result is that non-insulin dependent diabetes mellitus occurred in about 5% in the subgroup who are very lean. This figure of 5% is above the overall prevalence rate in the adult population (obese or not) of mainland France (2.9%) [24], where non-insulin dependent diabetes is extremely rare in very lean subjects [25]. In contrast, this type of diabetes was observed in a study conducted in West Africa, where 59% of the patients classified as having Type 2 diabetes had a BMI <19 kg/m2 [26]. In the present study, the lower mean height in these subjects may support the hypothesis of chronic malnutrition in a proportion of the adult population. This may be considered as a marker of socioeconomic transition: while some subgroups of the population are still in a situation of under-development, and still exposed to under-nutrition, others lead a modern way of life, and have access to food of western type, being thus exposed to obesity and its consequences In conclusion, diabetes is an extremely common disease among La Re´ union Island inhabitants. Almost 40% of them over the age of 50 have been diagnosed as diabetic, average age of diagnosis 45 years. A strong link was found between WHR and diabetes, indicating the role of both high energy intake and decreased physical activity in societies in epidemiologic transition. In contrast, we also observed Type 2 diabetic subjects characterized by their leanness and short height, markers of undernutrition in a context of low socioeconomic level. Health care systems should consider the two aspects of the development of chronic diseases such as Type 2 diabetes, which obviously have interacting medical and social roots. This holds for the emerging countries, but also for the suburbs of large cities of industrialized countries, where poverty is increasing rapidly. Dramatic figures have arisen from the few

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studies which addressed this issue, showing that people with low income are at high risk for Type 2 diabetes, whatever their ethnic origin [5,27].

Acknowledgements We thank LifeScan who provided the reflectance meters and glucose strips for the whole study, and Mrs. Annie Lacroux for helpful technical assistance. This work was supported by grant DGS 980511 from Direction des Hoˆ pitaux, and grants from INSERM, the Conseil Ge´ ne´ ral de La Re´ union, and the Agence Re´ gionale de l’Hospitalisation de La Re´ union.

References [1] H. King, R.E. Aubert, W.H. Herman, et al. Global burden of diabetes, 1995–2025: prevalence, numerical estimates, and projections, Diabet. Care 21 (1998) 1414–1431. [2] W.C. Knowler, P.H. Bennett, R.F. Hamman, et al. Diabetes incidence and prevalence in Pima Indians: a 19-fold greater incidence than in Rochester, Minnesota, Am. J. Epidemiol. 108 (1978) 497–505. [3] P. Zimmet, H. King, R. Taylor, et al. The high prevalence of diabetes mellitus, impaired glucose tolerance and diabetic retinopathy in Nauru—the 1982 survey, Diabet. Res. 1 (1984) 13–18. [4] A.F. Amos, D.J. McCarty, P. Zimmet, et al. The rising global burden of diabetes and its complications: estimates and projections to the year, Diabet. Med. 14 (1997) S70–S85. [5] V. Connolly, N. Unwin, P. Sheriff, et al. Diabetes prevalence and socioeconomic status: a population based study showing increased prevalence of Type 2 diabetes mellitus in deprived areas, J. Epidemiol. Commun. Health 54 (2000) 173–177. [6] H. King, M. Rewers, Diabetes in adults is now a Third World problem, The WHO Ad Hoc Diabetes Reporting Group, Bull. World Health Organ. 69 (1991) 643–648. [7] A.M. Kriska, R.E. Laporte, D.J. Pettitt, et al. The association of physical activity with obesity, fat distribution and glucose intolerance in Pima Indians, Diabetologia 36 (1993) 863– 869. [8] G.K. Dowse, P.Z. Zimmet, H. Gareeboo, et al. Abdominal obesity and physical inactivity as risk factors for NIDDM and impaired glucose tolerance in Indian, Creole, and Chinese Mauritians, Diabet. Care 14 (1991) 271–282. [9] V.L. Boyce, B.A. Swinburn, The traditional Pima Indian diet. Composition and adaptation for use in a dietary intervention study, Diabetes Care 16 (1993) 369–371. [10] M.I. Harris, Epidemiologic studies on the pathogenesis of noninsulin-dependent diabetes mellitus (NIDDM), Clin. Invest. Med. 18 (1995) 231–239.

[11] D. Costagliola, C. Delaunay, J.P. Moutet, et al. The prevalence of diabetes mellitus in the adult population of Guadeloupe as estimated by history or fasting hyperglycemia, Diabet. Res. Clin. Pract. 12 (1991) 209–216. [12] G.K. Dowse, H. Gareeboo, P.Z. Zimmet, et al. High prevalence of NIDDM and impaired glucose tolerance in Indian, Creole, and Chinese Mauritians. Mauritius Noncommunicable Disease Study Group, Diabetes 39 (1990) 390–396. [13] A.M. Hodge, G.K. Dowse, P.Z. Zimmet, et al. Prevalence and secular trends in obesity in Pacific and Indian Ocean Island populations, Obes. Res. 3 (Suppl. 2) (1995) 77–87. [14] L. Tappy, P. Bovet, C. Shamlaye, et al. Prevalence of diabetes and obesity in the adult population of the Seychelles, Diabet. Med. 8 (1991) 448–452. [15] L. Papoz, S. Barny, D. Simon, CALDIA Study Group, Prevalence of diabetes mellitus in New Caledonia: ethnic and urban-rural differences. CALDIA Study Group. CALedonia DIAbetes Mellitus Study, Am. J. Epidemiol. 143 (1996) 1018– 1024. [16] R. Taylor, B. Jalaludin, S. Levy, et al. Prevalence of diabetes, hypertension and obesity at different levels of urbanisation in Vanuatu, Med. J. Aust. 155 (1991) 86–90. [17] D. Simmons, C.F. Thompson, D. Volklander, et al. Polynesians: prone to obesity and Type 2 diabetes mellitus but not hyperinsulinaemia, Diabet. Med. 18 (2001) 193–198. [18] WHO Study Group, Diabetes mellitus, in: Technical Report Series 727, World Health Organization, Geneva, 1985. [19] L. Papoz, Use of fasting blood glucose to estimate diabetes prevalence in epidemiological surveys, Diabet. Med. 8 (1991) 290–291. [20] Report of the expert committee on the diagnosis and classification of diabetes mellitus, Diabet. Care 20 (1997) 1183– 1197. [21] K.G. Alberti, P.Z. Zimmet, Definition, diagnosis and classification of diabetes mellitus and its complications. Part I. Diagnosis and classification of diabetes mellitus, provisional report of a WHO consultation, Diabet. Med. 15 (1998) 539–553. [22] G.K. Dowse, R.A. Spark, B. Mavo, et al. Extraordinary prevalence of non-insulin dependent diabetes mellitus and bimodal plasma glucose distribution in the Wanigela people of Papua New Guinea, Med. J. Aust. 160 (1994) 767–774. [23] N.R. Burrows, L.S. Geiss, M.M. Engelgau, K.J. Acton, Prevalence of diabetes among Native Americans and Alaska Natives, 1990–1997: an increasing burden, Diabet. Care 2 (2000) 1786–1790. [24] P. Ricordeau, A. Weill, N. Vallier, et al. L’e´ pide´ miologie du diabe`te en France me´ tropolitaine, Diabet. Metab. 26 (Suppl. 6) (2000) 11–24. [25] L. Papoz, F. Vauzelle, P. Vexiau, G. Cathelineau, Pattern of treatment among diabetic patients in France, Diabet. Care 11 (1988) 86–91. [26] L. Papoz, C. Delcourt, A. Ponton-Sanchez, et al. Clinical classification of diabetes in tropical West Africa, Diabet. Res. Clin. Pract. 39 (1998) 219–227. [27] L. Riste, F. Khan, K. Cruickshank, High prevalence of Type 2 diabetes in all ethnic groups, including Europeans, in a British inner city, Diabet. Care 24 (2001) 1377–1383