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Diabetes and impaired glucose tolerance in an Asian community in Tanzania
Diabetes Research and Clinical Practice, 8 (1990)
221-234
227
Elsevier DIABET 00359
Diabetes and impaired glucose tolerance in an Asian community in Tanzania ‘A.B.M. Swai, ‘D.G. McLarty, ‘F. Sherrif, 2L.M. Chuwa, ‘E. Maro, 3Z. Lukmanji, ‘W. Kermali, ‘W. Makene and 4K.G.M.M. Alberti ‘Department
of Medicine,
University of Dar-es-Salaam,
Muhimbili Medical Centre, Dar-es-Salaam.
Clinical Biochemistry, Muhimbili Medical Centre, Dar-es-Salaam, Dar-es-Salaam,
Tanzania and 4Department of Medicine,
Tanzania, 2Department of
Tanzania. 3Tanzania Food and Nutrition Centre,
The Medical School, Framlington Place, Newcastle-upon-Tyne,
NE2 4HH,
U.K.
(Received 23 February 1989) (Revision received 10 September 1989) (Accepted 15 September 1989)
Summary The prevalence of diabetes and impaired glucose tolerance has been determined in an Asian Muslim community in Dar-es-Salaam, Tanzania. Two-h oral glucose (75 g) tolerance tests were performed on 1049 subjects over 14 years old, who were fasting, from a random sample of families. The overall age and sex-adjusted prevalence of diabetes was 7.1% (4.4% known, 2.7% previously undiagnosed) with a steady increase from 0.8% at 15-24 years and 3.0% at 25-34 years, to 24.9% for 65 years and over. Impaired glucose tolerance (IGT) rates ranged from 11.4% (15-24 years) to 22.3% (over 64 years). The overall age-adjusted prevalence of IGT was 21.5%. The mean body indices (BMIs) were 24.3 and 26.4 for males and females, respectively, but age-adjusted diabetes rates were similar in the two sexes (7.0% and 7.62, respectively). Diabetes and IGT were commoner in those with BMI > 25 only in the older age groups. Diabetes and IGT were commoner in those with a family history of diabetes. Increasing parity was also associated with a higher diabetes prevalence. Diabetes and IGT are thus common in Asians in Tanzania, in contrast to the indigenous community. Rates are indeed higher than in most other immigrant Asian communities. Key words: Non-insulin-dependent diabetes diabetes; Obesity; Migrant
mellitus;
Address for correspondence: Tyne, NE2 4HH, U.K.
of Medicine, The Medical School, Framlington
0168-8227/90/$03.50
K. Alberti, Department
0 1990 Elsevier Science Publishers
Impaired
B.V. (Biomedical
glucose tolerance
Division)
test; Prevalence
of
Place, Newcastle-upon-
228 Introduction
lations except in Fiji where rates of 10.8 y0 in rural dwellers and 11.2 % in urban dwellers were found in those over the age of 19 years [ 121 and in Trinidad where, in urban subjects aged 39-69years, rates of 10% and 11.6% for men and women, respectively, were found [ 131. The present cross-sectional study was undertaken to establish the prevalence of diabetes and IGT and their relationship to age and obesity in a discrete Muslim Indian community in Dar-esSalaam, Tanzania. The study was also designed to act as the basis of a long-term follow-up and intervention study and also to give comparative data for studies of the indigenous population.
Non-insulin-dependent diabetes mellitus (NIDDM) is a common disorder world-wide. Prevalence rates in adults vary from about 1% to more than 30% in certain selected populations [ 11. Amongst those groups with high prevalence rates are migrants from the Indian sub-continent with rates of more than 4% in nearly all groups studied (reviewed in [2]). It is commonly believed that obesity is a major determining factor and indeed, Kelly West showed a close association between body mass and adult NIDDM rates when combining data from several countries [3]. Others have argued that obesity is only one of several factors involved in the aetiology of NIDDM; race, diet and physical activity being other important determinants [4]. One problem with prior studies of migrants has been that subjects from several backgrounds and subgroups have been considered as one homogenous group. The situation has been further confounded by the use of different diagnostic criteria in the different studies. Relatively few data are available using the standard WHO criteria [5]. WHO also introduced the new category of impaired glucose tolerance (IGT), which implies an increased risk of subsequent development of diabetes and atherosclerosis [5-l 11. Little information is available on IGT rates in Indian popu-
Subject and methods Subjects The Ithnaashiri Indian community was studied. It is a community of strict Muslims and there is little alcohol intake. The married women are housewives, A few single women seek employment. The men tend to be self-employed businessmen with relatively low rates of physical activity. In 1985, a census had been taken of all members of the community. In 1986 a sample of 360 families was drawn at random from this and all subjects aged 15 years and over in these families were invited to the study. One thousand
TABLE 1 Age and gender distribution Age (years)
of the selected population
Selected population Men n
sample
n
tested for diabetes Sub-sample
Women (%)
sample and the sub-sample
Men
Total (%)
n
tested
(%)
n
Women (%I
n
(%I
15-24 25-34 35-44 45-55 55-65 65 +
321 389 263 229 163 80
22.2 26.9 18.2 15.8 11.3 5.5
368 410 301 250 149 92
23.4 26.1 19.2 15.9 9.5 5.9
689 799 564 479 312 172
22.9 26.5 18.7 15.9 10.3 5.7
44 97 119 112 15 38
9.1 20.1 24.6 23.2 15.5 7.7
70 122 133 148 69 23
12.4 21.6 23.5 26.0 12.2 4.1
Total
1445
100.0
1570
100.0
3015
100.0
483
100.0
566
100.0
229
two hundred and fifty-three (87%) of the expected 1440 subjects responded. Of the 1253 responders 1049 were tested for diabetes using an oral glucose tolerance test. There were no significant differences in age and sex structure between this sub-sample and the whole sample (Table l), although the tested sample tended to be older, and there were more men than women. It was not possible to find out details of the non-responders but most were students at school. To minimize bias, the rates calculated for the total group have been sex- and age-adjusted to the population structure of the whole community. Methods Subjects were requested to report to their mosque after an overnight fast. Venous blood samples were obtained after fasting and, except for known diabetics, 2 h after a 75-g oral glucose (monohydrate) load (2-HBG). Subjects were encouraged to remain seated and abstain from smoking until the end of the study. During the interval, weight and height were measured, without shoes or coats. A beam balance was used. Body mass index (BMI) was calculated as weight (kg) divided by the square of height (m’). Age, sex, occupation, duration of stay in the city, previous residence and duration thereof, the year the subject was diagnosed by a doctor as having diabetes, drinking habits, obstetric history and family history of diabetes were recorded. Portions of the fasting and 2-HBG blood were drawn into fluoride tubes and analysed immediately in the mosque for glucose using a Yellow Spring Instruments (YSI) glucose analyser (Yellow Spring Instruments, OH, U.S.A.). Every fifth sample was measured in duplicate and the remainder of the blood sample was kept cool (4’ C) and reanalysed later the same morning in the hospital laboratory using another YSI glucose analyser. A further aliquot was frozen, stored at - 2O”C, and analysed by a hexokinase fluorimetric method, using a Cobas Bio centrifugal analyser in Newcastle, U.K. The coefficient of correlation between the duplicate readings at the survey site was 0.998. The correlation between the survey
values and the laboratory YSI values was 0.99 and that between the survey values and Newcastle laboratory was 0.92. None of the slopes differed significantly from unity. The coefficient of variation for measurements on site was 1.8 %. Data analysis The data were analysed using the SPSSjPC + for the I.B.M. microcomputer [ 14,151. Diabetes was defined according to the 1985 World Health Organisation criteria [ 11, i.e., 2-h venous whole blood glucose concentrations equal to or greater than 10.0 mmol/l. Impaired glucose tolerance (IGT) was diagnosed when fasting venous whole blood glucose was less than 6.7 mmol/l and 2-h venous whole blood glucose concentration was equal to or greater than 6.7 mmol/l but less than 10.0 mmol/l. For clinical purposes two abnormal blood glucose values are required to diagnose diabetes in an asymptomatic person [5]. For epidemiological studies, a single diagnostic value is acceptable [ 1,161 and will correctly diagnose 97% of individuals [ 171. Fifty-five subjects, who at the time of the study had already been diagnosed diabetic (known diabetics) were included as diabetic irrespective of their current therapy or their fasting blood glucose concentration. All bar six had fasting blood glucose levels of at least 6.7 mmol/l. Three of the six were taking oral hypoglycaemic agents and three were on diet alone. The SPSS/PC + procedure Anova and procedure Oneway were used for analysis of variance. Results Eighty per cent of the study group had lived in Dar-es-Salaam for at least ten years. Only 4% had been in the city for one year or less. Ninty-two per cent had not lived outside Africa and 85 y0 not outside Tanzania. Only 3 y0 of the men and none of the women admitted to drinking. The data was, therefore, not further analysed with respect to drinking habits.
230 TABLE 2 Diabetes
and IGT prevalence
by gender and 10 year age group
Male
Age (years)
n
IGT (%)
15-24 25-34 35-44 45-55 55-65 65;
44 96 118 112 75 38
Total”
483
a Total percentage
Female
5 11 26 28 22 9
(11.4) (11.5) (22.0) (25.0) (29.3) (23.7)
101 (18.1)
DM (%)
n
0 (0) 5 (5.2) 11 (9.3) 11 (9.8) 10 (13.3) 6 (15.8)
70 122 134 148 69 23
43
566
(7.0)
Total” (%) DM (%)
IGT
DM
(11.4) (24.6) (32.1) (33.8) (27.5) (30.4)
1 1 5 18 15 9
(1.4) (0.8) (3.7) (12.2) (21.7) (39.1)
11.4 18.2 27.4 29.6 28.5 22.3
0.8 3.0 6.3 11.0 17.3 24.9
157 (25.1)
49
(7.6)
21.5
1.1
IGT (%) 8 30 43 50 19 7
figures adjusted for gender and age as appropriate.
Eighty-six per cent of the women were housewives. Of the men, 43% worked in an office but standing most of the time and 48% also worked in an office but seated most of the time. There was no association between these occupational groups and diabetes. Fifty-five subjects were known to be diabetic before the survey (5.2% of the sample). Of the known diabetics only five were on insulin: one was 34 years old with a BMI of 23.9 and the other four were over 45 years old with BMI values of 22.4,35.3,31.9, and 34.2. This represented 9% of known diabetics or a prevalence of 0.5 % of tested subjects, only one having clearly identifiable IDDM. A further 15 men and 22 women were detected giving an overall crude prevalence rate of 8.9% in men and 8.7% in women. This yielded
age-adjusted rates of 7.0% and 7.6% in men and women, respectively (Table 2). The prevalence rates of diabetes and IGT by age and sex are shown in Table 2. The agespecific diabetic rates were higher in women over 45 years old than in men, but the overall rates did not differ significantly between sexes. IGT was extremely common, ranging from 11.4% to 38.8% in the different age bands. Rates tended to increase with age, plateauing at the age bands over 35 years. Overall rates were higher in women than men. In sex-adjusted prevalence rates by age and BMI group (< 25 and 2 25) are shown in Table 3. Diabetes rates increased with age for both BMI groups. IGT rates increased significantly with age in those with low BMI (P < 0.001) but were
TABLE 3 Diabetes Age (years)
15-24 25-34 35-44 45-54 55-64 64i
and IGT prevalence
rates by BMI and age group (adjusted
for gender) BMI 2 25
BMI < 25 n
IGT (%)
DM (%)
n
IGT (%)
DM (%)
43 94 117 106 74 38
12.8 14.6 21.9 25.4 29.6 24.9
0 5.2 10.2 9.2 14.1 13.6
70 122 130 148 69 22
10.4 25.3 32.0 31.4 27.8 30.6
0.8 1.2 3.1 10.7 19.9 36.6
231 TABLE 4 Diabetes
and IGT prevalence
Family history of diabetes
rates in subjects over 34 years of age by family history and BMI BMI < 25
BMI 2 25
n
IGT (%)
DM (%)
n
IGT (%)
DM (%)
IGT
DM
160 41
25.5 21.3
5.6 11.5
153 6-l
31.0 32.1
12.5 20.0
28.4 28.9
9.3 17.4
-ve
+ve
already high by age 25-34 years in those with a high BMI. The mean BMI was lower for men than for women (24.2 men, 26.4 women). Overall diabetes rates were similar in those with normal and raised BMI, although rates tended to be higher in the latter in the older age groups. Unlike the fasting blood glucose, the 2-h blood glucose concentrations in subjects with normal glucose tolerance increased significantly with age (Table 4). The BMI increased with age to a maximum in the 45-54-year age group and then decreased. In subjects with normal glucose tolerance both the fasting glucose and 2-HBG showed no increase with BMI. There was a positive association between family history of diabetes and diabetes, with 17.4% of those over 34 years old with a positive history having diabetes compared with 9.3% in those with negative history. This association was even more marked in the overweight (Table 4). By TABLE 5 Fasting and 2-h blood glucose by age group in subjects with normal glucose tolerance Age (years )
Blood glucose (mmol/l)
n
Fasting
2-h”
118 221 252 258 140 61
4.2 4.3 4.3 4.4 4.5 4.4
4.9 5.0 5.1 5.2 5.3 4.9
-_ 15-24 25-34 35-44 45-54 55-64 65 +
Total ___-
(0.66) (0.62) (0.59) (0.65) (0.67) (0.57)
(0.95) (0.94) (0.93) (1.00) (0.88) (0.91)
il Difference between groups significant by analysis of variance (P < 0.001). SD values shown in parentheses.
contrast, there was no association between IGT and a family history of diabetes, suggesting perhaps that in the majority of IGTs there is a different aetiology to the glucose intolerance. The average number of viable pregnancies per woman was 2.7 for the whole study sample. Nineteen per cent of all the women in the sample had had five or more viable pregnancies. The average for those aged 40 years or more was 3.8. For women over 39 years old, there was a positive association between parity and diabetes (P < 0.05), which disappears, however, after adjustment for BMI. Fasting blood glucose levels in those with normal glucose tolerance did not alter significantly with age (Table 5). There was, however, a small increase in the 2-h post-glucose load value.
Discussion The results of studies on the prevalence of diabetes in expatriate Indians were reviewed in 1983 by Taylor and Zimmet [2]. They concluded that expatriate Indians have higher prevalence rates than the population residing in the Indian subcontinent and usually higher than the predominant racial group or other racial groups in the host country. This led to a further conclusion that both genetic and powerful environmental factors are of importance in the aetiology of non-insulindependent diabetes (NIDDM). The high prevalence rates of diabetes found in the community studied here are consistent with the similarly high rates in other migrant Indian communities. A crude overall rate of 3% has been reported for
232
urban Indians in India: in the studies from which this rate was derived [ 18,191, diabetes rates of 10.3 % for those aged 5 l-60 years and 16.4% for those aged over 60 prevailed. Such rates are still lower than those from the present study but firm conclusions about differences between Indians in India and expatriate Indians must be based on groups matched for the other known determinants of diabetes such as age and BMI. It is worth noting that the IGT rates found in our group are higher than in any other study of Indians. This may be related to body weight: the mean BMI was higher than in some previous studies with lower IGT rates e.g., Fiji Indians, where the mean BMI for the urban Indians were 22.8 in men and 23.9 in women [20]. IGT rates were still higher in the overweight group (BMI > 25). It is worth commenting that obesity cannot be the only answer as average BMI values were little in excess of those found in many Caucasian societies which have lower IGT and NIDDM rates and, indeed, were lower than those found in an Asian community studied recently in the U.K. This latter group had similar diabetes rates to our subjects but much lower IGT rates [21]. Lack of physical exercise may be an additional important contributory factor [ 121. Regardless of cause it suggests a high potential pool of diabetes and perhaps atherosclerosis risk in the community [6,7-111. The results confirm the findings of many other studies that glucose intolerance increases with age (reviewed by Davidson [22]). Table 3 shows that IGT and diabetes mellitus (DM) rates increase with age for those with low BMI. For those with high BMI, IGT rates do not increase with age, presumably because rates are already high by the 25-34-year age band. These results are explicable if, for a population, there is a group predisposed to glucose intolerance upon whom advancing age or increasing BMI each, independently, causes a worsening of the glucose tolerance. Being overweight promotes diabetes at an earlier age. In those with normal glucose tolerance there was no increase in fasting or 2-h glucose with age, suggesting that ageing alone does not cause an
upward drift in glucose values. This has also been noted in certain Pacific populations [ 111. The results in Table 4 demonstrate similar interactions of glucose tolerance between obesity and family history of diabetes. In this welleducated closed community family history data, although ‘soft’, is likely to be reasonably reliable. Family history of diabetes has an independent effect on glucose tolerance, enhanced by being overweight. In contrast with diabetes, there was no association of family history with IGT, regardless of BMI. This raises intriguing possibilities with regard to differing aetiologies of IGT and diabetes. Parity has no independent effect on glucose tolerance but increasing parity may be associated with being increasingly overweight [ 221 and, consequently, increasing glucose intolerance. Previous studies have reported on the relation between parity and glucose tolerance but many did not consider the confounding effects of age and being overweight [ 16,24,25]. The results are not inconsistent with the hypothesis advanced by Luft et al. [26] on the pathogenesis of NIDDM. They postulate that NIDDM is an interaction of two factors - insulin response and insulin resistance. NIDDM subjects have a low insulin response as a principal genetic defect. The onset of NIDDM is related to increased insulin resistance, which may occur with being overweight, ageing, physical inactivity, stress, drugs and endocrine disorders. In the present study, as in the U.S.A. population, obesity and a positive family history of diabetes each doubles the prevalence of diabetes and both together quadruple the rates (Table 4). About 25 y0 of the present community are obese. Elimination of obesity may therefore result in a decrease in the present diabetes rates by about 20%. In the non-obese subjects, the diabetes rates in the present study were 1.4 times those of the U.S.A. population, irrespective of family history of diabetes [ 241. This difference may be attributable to genetic factors and factors such as physical inactivity. In conclusion, this study has shown high diabetes and IGT rates in an expatriate Indian
233 community. Obesity and age are important determinants acting on genetically predisposed groups. Finally, the high rates reported place a high burden on local health care services. This is not just for diabetes, but also because of the close association of IGT with cardiovascular morbidity and mortality [ 6-10 J. Measures which may combat and decrease the prevalence of these disorders require development and testing urgently.
Acknowledgements We gratefuly acknowledge the help of the Ithnaashiri community, including nurse A. Meghi and the laboratory staff of the Department of Biochemistry, Muhimbili Medical Clinical particularly Mr. Dar-es-Salaam, Centre, C. Msuya. The assistance of Dr. N. Malentlema, Director of the Tanzania Food and Nutrition Centre, and Mr. V. Assey was greatly appreciated as was the support of members of the Department of Medicine, University of Newcastle-upon-Tyne, U.K. We are indebted to the British Council for major financial support; and to Farmitalia Carlo Erba, Milan, Italy, the Lions Club of Dar-esSalaam (Host), the British Diabetic Association, Novo Industries (Copenhagen) and Boehringer Mannheim (F.R.G.) for further support. Muhimbili Medical Centre provided material support, and we would like to thank the Director General, Professor P.M. Sarungi. We should also like to thank Professor H. Keen, and P. Zimmet and Mr. and encouragement for advice N. Hamilton for instruction on computing. References World Health Organisation Study Group on Diabetes Mellitus (1985) Tech. Rep. Ser. 727. WHO, Geneva. Taylor, R. and Zimmet, P. (1983) Migrant studies in diabetes epidemiology. In: J.I. Mann, K. Pyorala and A. Teuscher (Eds.), Diabetes in Epidemiological Perspective. Churchill Livingstone, Edinburgh, pp. 58-77. West, K.M. (1978) Epidemiology of Diabetes and its Vascular Lesions. Elsevier, New York. Zimmet, P. (1982) Type 2 (non-insulin-dependent)
5
6
7
8
9
10
11
12
13
14 15 16 17
18
19
diabetes mellitus - an epidemiological overview. Diabetologia, 22, 339-411. World Health Organisation Expert Committee on Diabetes Mellitus (1980) WHO Tech. Rep. Ser. 646. WHO, Geneva. Epstein, F.H., Ostrander L.D. Jr., Johnson, B.C. et al. (1965) Epidemiological studies of cardiovascular disease in a total community- Tecumseh, Michigan. Ann. Intern. Med. 62, 1170-1187. Jarrett, R.J., McCartney, P. and Keen, H. (1982) The Bedford survey: ten year mortality rates in newly diagnosed diabetics, borderline diabetics and normoglycaemic controls and risk indices for coronary heart disease in borderline diabetics. Diabetologia 22, 79-84. Fuller, J., Shipley, M.J., Rose, G., Jarrett, R.J. and Keen, H. (1980) Coronary heart disease risk and impaired glucose tolerance. The Whitehall study. Lancet i, 1373-1376. Stamler, R. and Stamler, J. (Eds.). (1980) Asymptomatic hyperglycemia and coronary heart disease. J. Chron. Dis. 32,683-837. Stern, M.P., Rosenthal, M. and Haffner, S.M. (1985) A new concept of impaired glucose tolerance. Relation to cardiovascular risk. Atherosclerosis 5, 31 l-3 14. Zimmet, P. and King, H. (1985) The epidemiology of diabetes mellitus: recent developments, In: K.G.M.M. Alberti and L.P. Krall (Eds.), Diabetes Annual, Vol. 1. Elsevier, Amsterdam, pp. l-15. Taylor, R., Ram, P., Zimmet, P.. Raper, L.R. and Ringrose, H. (1984) Physical activity and prevalence of diabetes in Melanesian and Indian men in Fiji. Diabetologia 27, 578-582. Becles, G.L.A., Miller, G.J., Kirkwood, B.R., Alexis, S.D., Carson, D.C. and Byam, N.T.A. ( 1986) High total and cardiovascular disease mortality in adults of Indian descent in Trinidad, unexplained by major coronary risk factors. Lancet i, 1298-1301. Norusis, M.J. (1986) S.P.S.S./Pc+ : SPSS for the I.B.M. PC/XT/AT. Chicago, S.P.S.S. Inc. Norusis, M.J. (1986) Advanced Statistics. SPSS/Pc + : S.P.S.S.forthe1.B.M. PC/XT/AT. Chicago, S.P.S.S. Inc. Jarrett, R.J. (1986) Diabetes Mellitus. Croom Helm, London. Harris, MI., Hadden, W.C., Knowler, W.C. and Bennett, P.H. (1985) International criteria for the diagnosis of diabetes and impaired glucose tolerance. Diabetes Care 8, 562-567. Gupta, O.P., Joshi, M.H. and Dave, S.K. (1978) Prevalence of diabetes in India. In: M. Miller and P.H. Bennett (Eds.), Advances in Metabolic Disorders, Vol. 9. Academic Press, New York, pp. 147-165. Ahuja, M.M.S. (1979) Epidemiological studies on diabetes mellitus in India. In: M.M.S. Ahuja (Ed.), Epidemiology of Diabetes in Developing Countries. Interprint, New Delhi, pp. 29-38.
234 20 Zimmet, P., Taylor, R., Ram, P. et al. (1983) Prevalence of diabetes and impaired glucose tolerance in the biracial (Melanesian and Indian) population of Fiji: a rural urban comparison. Am. J. Epidemiol., 118, 673-688. 21 Simmons, D., Williams, D.R.R. and Powell, M.J. (1988) Prevalence of diabetes in a predominantly Asian community: preliminary findings of the Coventry diabetes study. Br. Med. J. 298, 18-21. 22 Davidson, M.B. (1979) The effect of ageing on glucose metabolism: a review of the English literature and a practical approach to the diagnosis of diabetes in the elderly. Metabolism 28, 688-705. 23 Heliovaara, M. and Aromaa, A. (198 1) Parity and obesity. J. Epidemiol. Commun. Health 35, 197-199.
24 Bennett, P.H., Burch, T.A. and Miller, M. (1971) Diabetes mellitus in Pima (American) Indians. Lancet ii, 125-128. 25 West, K.M. and Kalbfleisch, J.M. (1970) Diabetes in Central America. Diabetes 19, 656-663. 26 Efendic, S., Luft, R. and Wajngot, A. (1984) Aspects of pathogenesis of type 2 diabetes. Endocrine Rev. 5, 395-410. 27 Harris, M., Hadden, W.C., Knowler, W.C. and Bennett, P.H. (1987) Prevalence of diabetes and impaired glucose tolerance and plasma glucose levels in U.S. population aged 20-74 years. Diabetes 36, 523-534.
221-234
227
Elsevier DIABET 00359
Diabetes and impaired glucose tolerance in an Asian community in Tanzania ‘A.B.M. Swai, ‘D.G. McLarty, ‘F. Sherrif, 2L.M. Chuwa, ‘E. Maro, 3Z. Lukmanji, ‘W. Kermali, ‘W. Makene and 4K.G.M.M. Alberti ‘Department
of Medicine,
University of Dar-es-Salaam,
Muhimbili Medical Centre, Dar-es-Salaam.
Clinical Biochemistry, Muhimbili Medical Centre, Dar-es-Salaam, Dar-es-Salaam,
Tanzania and 4Department of Medicine,
Tanzania, 2Department of
Tanzania. 3Tanzania Food and Nutrition Centre,
The Medical School, Framlington Place, Newcastle-upon-Tyne,
NE2 4HH,
U.K.
(Received 23 February 1989) (Revision received 10 September 1989) (Accepted 15 September 1989)
Summary The prevalence of diabetes and impaired glucose tolerance has been determined in an Asian Muslim community in Dar-es-Salaam, Tanzania. Two-h oral glucose (75 g) tolerance tests were performed on 1049 subjects over 14 years old, who were fasting, from a random sample of families. The overall age and sex-adjusted prevalence of diabetes was 7.1% (4.4% known, 2.7% previously undiagnosed) with a steady increase from 0.8% at 15-24 years and 3.0% at 25-34 years, to 24.9% for 65 years and over. Impaired glucose tolerance (IGT) rates ranged from 11.4% (15-24 years) to 22.3% (over 64 years). The overall age-adjusted prevalence of IGT was 21.5%. The mean body indices (BMIs) were 24.3 and 26.4 for males and females, respectively, but age-adjusted diabetes rates were similar in the two sexes (7.0% and 7.62, respectively). Diabetes and IGT were commoner in those with BMI > 25 only in the older age groups. Diabetes and IGT were commoner in those with a family history of diabetes. Increasing parity was also associated with a higher diabetes prevalence. Diabetes and IGT are thus common in Asians in Tanzania, in contrast to the indigenous community. Rates are indeed higher than in most other immigrant Asian communities. Key words: Non-insulin-dependent diabetes diabetes; Obesity; Migrant
mellitus;
Address for correspondence: Tyne, NE2 4HH, U.K.
of Medicine, The Medical School, Framlington
0168-8227/90/$03.50
K. Alberti, Department
0 1990 Elsevier Science Publishers
Impaired
B.V. (Biomedical
glucose tolerance
Division)
test; Prevalence
of
Place, Newcastle-upon-
228 Introduction
lations except in Fiji where rates of 10.8 y0 in rural dwellers and 11.2 % in urban dwellers were found in those over the age of 19 years [ 121 and in Trinidad where, in urban subjects aged 39-69years, rates of 10% and 11.6% for men and women, respectively, were found [ 131. The present cross-sectional study was undertaken to establish the prevalence of diabetes and IGT and their relationship to age and obesity in a discrete Muslim Indian community in Dar-esSalaam, Tanzania. The study was also designed to act as the basis of a long-term follow-up and intervention study and also to give comparative data for studies of the indigenous population.
Non-insulin-dependent diabetes mellitus (NIDDM) is a common disorder world-wide. Prevalence rates in adults vary from about 1% to more than 30% in certain selected populations [ 11. Amongst those groups with high prevalence rates are migrants from the Indian sub-continent with rates of more than 4% in nearly all groups studied (reviewed in [2]). It is commonly believed that obesity is a major determining factor and indeed, Kelly West showed a close association between body mass and adult NIDDM rates when combining data from several countries [3]. Others have argued that obesity is only one of several factors involved in the aetiology of NIDDM; race, diet and physical activity being other important determinants [4]. One problem with prior studies of migrants has been that subjects from several backgrounds and subgroups have been considered as one homogenous group. The situation has been further confounded by the use of different diagnostic criteria in the different studies. Relatively few data are available using the standard WHO criteria [5]. WHO also introduced the new category of impaired glucose tolerance (IGT), which implies an increased risk of subsequent development of diabetes and atherosclerosis [5-l 11. Little information is available on IGT rates in Indian popu-
Subject and methods Subjects The Ithnaashiri Indian community was studied. It is a community of strict Muslims and there is little alcohol intake. The married women are housewives, A few single women seek employment. The men tend to be self-employed businessmen with relatively low rates of physical activity. In 1985, a census had been taken of all members of the community. In 1986 a sample of 360 families was drawn at random from this and all subjects aged 15 years and over in these families were invited to the study. One thousand
TABLE 1 Age and gender distribution Age (years)
of the selected population
Selected population Men n
sample
n
tested for diabetes Sub-sample
Women (%)
sample and the sub-sample
Men
Total (%)
n
tested
(%)
n
Women (%I
n
(%I
15-24 25-34 35-44 45-55 55-65 65 +
321 389 263 229 163 80
22.2 26.9 18.2 15.8 11.3 5.5
368 410 301 250 149 92
23.4 26.1 19.2 15.9 9.5 5.9
689 799 564 479 312 172
22.9 26.5 18.7 15.9 10.3 5.7
44 97 119 112 15 38
9.1 20.1 24.6 23.2 15.5 7.7
70 122 133 148 69 23
12.4 21.6 23.5 26.0 12.2 4.1
Total
1445
100.0
1570
100.0
3015
100.0
483
100.0
566
100.0
229
two hundred and fifty-three (87%) of the expected 1440 subjects responded. Of the 1253 responders 1049 were tested for diabetes using an oral glucose tolerance test. There were no significant differences in age and sex structure between this sub-sample and the whole sample (Table l), although the tested sample tended to be older, and there were more men than women. It was not possible to find out details of the non-responders but most were students at school. To minimize bias, the rates calculated for the total group have been sex- and age-adjusted to the population structure of the whole community. Methods Subjects were requested to report to their mosque after an overnight fast. Venous blood samples were obtained after fasting and, except for known diabetics, 2 h after a 75-g oral glucose (monohydrate) load (2-HBG). Subjects were encouraged to remain seated and abstain from smoking until the end of the study. During the interval, weight and height were measured, without shoes or coats. A beam balance was used. Body mass index (BMI) was calculated as weight (kg) divided by the square of height (m’). Age, sex, occupation, duration of stay in the city, previous residence and duration thereof, the year the subject was diagnosed by a doctor as having diabetes, drinking habits, obstetric history and family history of diabetes were recorded. Portions of the fasting and 2-HBG blood were drawn into fluoride tubes and analysed immediately in the mosque for glucose using a Yellow Spring Instruments (YSI) glucose analyser (Yellow Spring Instruments, OH, U.S.A.). Every fifth sample was measured in duplicate and the remainder of the blood sample was kept cool (4’ C) and reanalysed later the same morning in the hospital laboratory using another YSI glucose analyser. A further aliquot was frozen, stored at - 2O”C, and analysed by a hexokinase fluorimetric method, using a Cobas Bio centrifugal analyser in Newcastle, U.K. The coefficient of correlation between the duplicate readings at the survey site was 0.998. The correlation between the survey
values and the laboratory YSI values was 0.99 and that between the survey values and Newcastle laboratory was 0.92. None of the slopes differed significantly from unity. The coefficient of variation for measurements on site was 1.8 %. Data analysis The data were analysed using the SPSSjPC + for the I.B.M. microcomputer [ 14,151. Diabetes was defined according to the 1985 World Health Organisation criteria [ 11, i.e., 2-h venous whole blood glucose concentrations equal to or greater than 10.0 mmol/l. Impaired glucose tolerance (IGT) was diagnosed when fasting venous whole blood glucose was less than 6.7 mmol/l and 2-h venous whole blood glucose concentration was equal to or greater than 6.7 mmol/l but less than 10.0 mmol/l. For clinical purposes two abnormal blood glucose values are required to diagnose diabetes in an asymptomatic person [5]. For epidemiological studies, a single diagnostic value is acceptable [ 1,161 and will correctly diagnose 97% of individuals [ 171. Fifty-five subjects, who at the time of the study had already been diagnosed diabetic (known diabetics) were included as diabetic irrespective of their current therapy or their fasting blood glucose concentration. All bar six had fasting blood glucose levels of at least 6.7 mmol/l. Three of the six were taking oral hypoglycaemic agents and three were on diet alone. The SPSS/PC + procedure Anova and procedure Oneway were used for analysis of variance. Results Eighty per cent of the study group had lived in Dar-es-Salaam for at least ten years. Only 4% had been in the city for one year or less. Ninty-two per cent had not lived outside Africa and 85 y0 not outside Tanzania. Only 3 y0 of the men and none of the women admitted to drinking. The data was, therefore, not further analysed with respect to drinking habits.
230 TABLE 2 Diabetes
and IGT prevalence
by gender and 10 year age group
Male
Age (years)
n
IGT (%)
15-24 25-34 35-44 45-55 55-65 65;
44 96 118 112 75 38
Total”
483
a Total percentage
Female
5 11 26 28 22 9
(11.4) (11.5) (22.0) (25.0) (29.3) (23.7)
101 (18.1)
DM (%)
n
0 (0) 5 (5.2) 11 (9.3) 11 (9.8) 10 (13.3) 6 (15.8)
70 122 134 148 69 23
43
566
(7.0)
Total” (%) DM (%)
IGT
DM
(11.4) (24.6) (32.1) (33.8) (27.5) (30.4)
1 1 5 18 15 9
(1.4) (0.8) (3.7) (12.2) (21.7) (39.1)
11.4 18.2 27.4 29.6 28.5 22.3
0.8 3.0 6.3 11.0 17.3 24.9
157 (25.1)
49
(7.6)
21.5
1.1
IGT (%) 8 30 43 50 19 7
figures adjusted for gender and age as appropriate.
Eighty-six per cent of the women were housewives. Of the men, 43% worked in an office but standing most of the time and 48% also worked in an office but seated most of the time. There was no association between these occupational groups and diabetes. Fifty-five subjects were known to be diabetic before the survey (5.2% of the sample). Of the known diabetics only five were on insulin: one was 34 years old with a BMI of 23.9 and the other four were over 45 years old with BMI values of 22.4,35.3,31.9, and 34.2. This represented 9% of known diabetics or a prevalence of 0.5 % of tested subjects, only one having clearly identifiable IDDM. A further 15 men and 22 women were detected giving an overall crude prevalence rate of 8.9% in men and 8.7% in women. This yielded
age-adjusted rates of 7.0% and 7.6% in men and women, respectively (Table 2). The prevalence rates of diabetes and IGT by age and sex are shown in Table 2. The agespecific diabetic rates were higher in women over 45 years old than in men, but the overall rates did not differ significantly between sexes. IGT was extremely common, ranging from 11.4% to 38.8% in the different age bands. Rates tended to increase with age, plateauing at the age bands over 35 years. Overall rates were higher in women than men. In sex-adjusted prevalence rates by age and BMI group (< 25 and 2 25) are shown in Table 3. Diabetes rates increased with age for both BMI groups. IGT rates increased significantly with age in those with low BMI (P < 0.001) but were
TABLE 3 Diabetes Age (years)
15-24 25-34 35-44 45-54 55-64 64i
and IGT prevalence
rates by BMI and age group (adjusted
for gender) BMI 2 25
BMI < 25 n
IGT (%)
DM (%)
n
IGT (%)
DM (%)
43 94 117 106 74 38
12.8 14.6 21.9 25.4 29.6 24.9
0 5.2 10.2 9.2 14.1 13.6
70 122 130 148 69 22
10.4 25.3 32.0 31.4 27.8 30.6
0.8 1.2 3.1 10.7 19.9 36.6
231 TABLE 4 Diabetes
and IGT prevalence
Family history of diabetes
rates in subjects over 34 years of age by family history and BMI BMI < 25
BMI 2 25
n
IGT (%)
DM (%)
n
IGT (%)
DM (%)
IGT
DM
160 41
25.5 21.3
5.6 11.5
153 6-l
31.0 32.1
12.5 20.0
28.4 28.9
9.3 17.4
-ve
+ve
already high by age 25-34 years in those with a high BMI. The mean BMI was lower for men than for women (24.2 men, 26.4 women). Overall diabetes rates were similar in those with normal and raised BMI, although rates tended to be higher in the latter in the older age groups. Unlike the fasting blood glucose, the 2-h blood glucose concentrations in subjects with normal glucose tolerance increased significantly with age (Table 4). The BMI increased with age to a maximum in the 45-54-year age group and then decreased. In subjects with normal glucose tolerance both the fasting glucose and 2-HBG showed no increase with BMI. There was a positive association between family history of diabetes and diabetes, with 17.4% of those over 34 years old with a positive history having diabetes compared with 9.3% in those with negative history. This association was even more marked in the overweight (Table 4). By TABLE 5 Fasting and 2-h blood glucose by age group in subjects with normal glucose tolerance Age (years )
Blood glucose (mmol/l)
n
Fasting
2-h”
118 221 252 258 140 61
4.2 4.3 4.3 4.4 4.5 4.4
4.9 5.0 5.1 5.2 5.3 4.9
-_ 15-24 25-34 35-44 45-54 55-64 65 +
Total ___-
(0.66) (0.62) (0.59) (0.65) (0.67) (0.57)
(0.95) (0.94) (0.93) (1.00) (0.88) (0.91)
il Difference between groups significant by analysis of variance (P < 0.001). SD values shown in parentheses.
contrast, there was no association between IGT and a family history of diabetes, suggesting perhaps that in the majority of IGTs there is a different aetiology to the glucose intolerance. The average number of viable pregnancies per woman was 2.7 for the whole study sample. Nineteen per cent of all the women in the sample had had five or more viable pregnancies. The average for those aged 40 years or more was 3.8. For women over 39 years old, there was a positive association between parity and diabetes (P < 0.05), which disappears, however, after adjustment for BMI. Fasting blood glucose levels in those with normal glucose tolerance did not alter significantly with age (Table 5). There was, however, a small increase in the 2-h post-glucose load value.
Discussion The results of studies on the prevalence of diabetes in expatriate Indians were reviewed in 1983 by Taylor and Zimmet [2]. They concluded that expatriate Indians have higher prevalence rates than the population residing in the Indian subcontinent and usually higher than the predominant racial group or other racial groups in the host country. This led to a further conclusion that both genetic and powerful environmental factors are of importance in the aetiology of non-insulindependent diabetes (NIDDM). The high prevalence rates of diabetes found in the community studied here are consistent with the similarly high rates in other migrant Indian communities. A crude overall rate of 3% has been reported for
232
urban Indians in India: in the studies from which this rate was derived [ 18,191, diabetes rates of 10.3 % for those aged 5 l-60 years and 16.4% for those aged over 60 prevailed. Such rates are still lower than those from the present study but firm conclusions about differences between Indians in India and expatriate Indians must be based on groups matched for the other known determinants of diabetes such as age and BMI. It is worth noting that the IGT rates found in our group are higher than in any other study of Indians. This may be related to body weight: the mean BMI was higher than in some previous studies with lower IGT rates e.g., Fiji Indians, where the mean BMI for the urban Indians were 22.8 in men and 23.9 in women [20]. IGT rates were still higher in the overweight group (BMI > 25). It is worth commenting that obesity cannot be the only answer as average BMI values were little in excess of those found in many Caucasian societies which have lower IGT and NIDDM rates and, indeed, were lower than those found in an Asian community studied recently in the U.K. This latter group had similar diabetes rates to our subjects but much lower IGT rates [21]. Lack of physical exercise may be an additional important contributory factor [ 121. Regardless of cause it suggests a high potential pool of diabetes and perhaps atherosclerosis risk in the community [6,7-111. The results confirm the findings of many other studies that glucose intolerance increases with age (reviewed by Davidson [22]). Table 3 shows that IGT and diabetes mellitus (DM) rates increase with age for those with low BMI. For those with high BMI, IGT rates do not increase with age, presumably because rates are already high by the 25-34-year age band. These results are explicable if, for a population, there is a group predisposed to glucose intolerance upon whom advancing age or increasing BMI each, independently, causes a worsening of the glucose tolerance. Being overweight promotes diabetes at an earlier age. In those with normal glucose tolerance there was no increase in fasting or 2-h glucose with age, suggesting that ageing alone does not cause an
upward drift in glucose values. This has also been noted in certain Pacific populations [ 111. The results in Table 4 demonstrate similar interactions of glucose tolerance between obesity and family history of diabetes. In this welleducated closed community family history data, although ‘soft’, is likely to be reasonably reliable. Family history of diabetes has an independent effect on glucose tolerance, enhanced by being overweight. In contrast with diabetes, there was no association of family history with IGT, regardless of BMI. This raises intriguing possibilities with regard to differing aetiologies of IGT and diabetes. Parity has no independent effect on glucose tolerance but increasing parity may be associated with being increasingly overweight [ 221 and, consequently, increasing glucose intolerance. Previous studies have reported on the relation between parity and glucose tolerance but many did not consider the confounding effects of age and being overweight [ 16,24,25]. The results are not inconsistent with the hypothesis advanced by Luft et al. [26] on the pathogenesis of NIDDM. They postulate that NIDDM is an interaction of two factors - insulin response and insulin resistance. NIDDM subjects have a low insulin response as a principal genetic defect. The onset of NIDDM is related to increased insulin resistance, which may occur with being overweight, ageing, physical inactivity, stress, drugs and endocrine disorders. In the present study, as in the U.S.A. population, obesity and a positive family history of diabetes each doubles the prevalence of diabetes and both together quadruple the rates (Table 4). About 25 y0 of the present community are obese. Elimination of obesity may therefore result in a decrease in the present diabetes rates by about 20%. In the non-obese subjects, the diabetes rates in the present study were 1.4 times those of the U.S.A. population, irrespective of family history of diabetes [ 241. This difference may be attributable to genetic factors and factors such as physical inactivity. In conclusion, this study has shown high diabetes and IGT rates in an expatriate Indian
233 community. Obesity and age are important determinants acting on genetically predisposed groups. Finally, the high rates reported place a high burden on local health care services. This is not just for diabetes, but also because of the close association of IGT with cardiovascular morbidity and mortality [ 6-10 J. Measures which may combat and decrease the prevalence of these disorders require development and testing urgently.
Acknowledgements We gratefuly acknowledge the help of the Ithnaashiri community, including nurse A. Meghi and the laboratory staff of the Department of Biochemistry, Muhimbili Medical Clinical particularly Mr. Dar-es-Salaam, Centre, C. Msuya. The assistance of Dr. N. Malentlema, Director of the Tanzania Food and Nutrition Centre, and Mr. V. Assey was greatly appreciated as was the support of members of the Department of Medicine, University of Newcastle-upon-Tyne, U.K. We are indebted to the British Council for major financial support; and to Farmitalia Carlo Erba, Milan, Italy, the Lions Club of Dar-esSalaam (Host), the British Diabetic Association, Novo Industries (Copenhagen) and Boehringer Mannheim (F.R.G.) for further support. Muhimbili Medical Centre provided material support, and we would like to thank the Director General, Professor P.M. Sarungi. We should also like to thank Professor H. Keen, and P. Zimmet and Mr. and encouragement for advice N. Hamilton for instruction on computing. References World Health Organisation Study Group on Diabetes Mellitus (1985) Tech. Rep. Ser. 727. WHO, Geneva. Taylor, R. and Zimmet, P. (1983) Migrant studies in diabetes epidemiology. In: J.I. Mann, K. Pyorala and A. Teuscher (Eds.), Diabetes in Epidemiological Perspective. Churchill Livingstone, Edinburgh, pp. 58-77. West, K.M. (1978) Epidemiology of Diabetes and its Vascular Lesions. Elsevier, New York. Zimmet, P. (1982) Type 2 (non-insulin-dependent)
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