Asia Pacific J Clin Nutr (1994) 3, 33-39
Asia Pacific J Clin Nutr (1994) 3, 33-39
Body composition in the pathogenesis
and management of diabetes: a Malaysian perspective
Ali Osman* MD, MPH, PhD and B.A.K. Khalid**
MBBS, PhD, FRACP
*Department of Community Health, **Dean,
Faculty of Medicine, 53000, Kuala Lumpur, Malaysia.
There is an increasing prevalence of diabetes mellitus
around the world associated with rapid sociocultural development
and changing lifestyles. Increased prevalence of obesity, with a
higher consumption of animal products and lower consumption of fruits
and vegetables, increases the risk of diabetes mellitus and other
chronic degenerative diseases. Insulin-dependent diabetes (IDD)
is caused by insulin deficiency, whereas the main feature of non-insulin-dependent
diabetes (NIDD) which accounts for more than 90% of diabetics, is
hyperinsulinemia and insulin resistance, which may eventually lead
to actual insulin deficiency. Hyperinsulinemia is undesirable because
it increases the risk of developing vascular disease. In Malaysia,
the prevalence of NIDD in some communities now exceeds 5%, and of
impaired glucose tolerance 10%. Along with these increases in prevalence
of hyperglycemia are increases in prevalence of overweight (BMI>25)
and almost certainly abdominal fatness. In terms of management,
nutrition is given priority. Insulin and hypoglycemic drugs (sulphonylureas
or biguanides), where required, may adversely affect body composition
if overused. Newer therapeutic strategies require greater attention
to the underlying problem in NIDD of abdominal fatness by attention
to the relevant nutritional factors, physical activity and other
lifestyle factors like cigarette smoking and alcohol. The greater
impact of obesity and diabetes on Malaysian women as opposed to
men also needs to be addressed.
Diabetes mellitus was described as early as 1600 BC
as a disease with polyuria and insatiable thirst but the detailed
description of the disease and its pathogenesis did not exist until
the nineteenth century. This disease occurs in almost all populations;
however, the prevalence varies depending on the population, its age
structure, genetic background and lifestyle. High prevalences are
found among the Pima Indians in North America, Nauruans, Indians and
Australian Aborigines1 and low prevalence among the Melanesians
in Solomon Islands. Part of the heterogeneity between populations
is probably accounted for by body composition, in turn dependent on
diet, physical activity and substance abuse, over and above genetic
background2. The present report draws on recent observations
of increasing prevalences among Malaysians.
Community-based studies from Malaysia show that the
prevalence of diabetes is highest among urban Malays and is lower
whe 1000 re the socio-economic development is less (Table 1). However,
urban Malays have lower prevalences of impaired glucose tolerance
(IGT) compared to their rural counterparts. On the other hand, the
prevalence of diabetes mellitus and IGT among Malaysian aborigines
(Orang Asli) is very low in all locations. Certain genetic factors
for the moment probably protect the Orang Asli from the disease, whereas
environmental influences have already increased the prevalence among
genetically susceptible Malays. Community comparisons of fasting,
2 hour post-glucose load and Hb A1 values support an environmental
influence on diabetes occurrence (Table 2).
Table 1. Crude and adjusted prevalence rates
of diabetes mellitus and IGT (per cent)3.
|Stages of development
|Lanai (n=110) (ABO)
|Ulu Sungai (n=136) (MAL)
|Betau (n=136) (ABO)
|Koyan (n=132) (MAL)
|Lanjan (n=75) (ABO)
|Kg. Kerinci (n=92)
ABO = Orang Asli. MAL = Malays. * Five-year age-specific
rates (30-64 years) were calculated and standardization was performed
using the direct method against the standard population of Segi. **
95% confidence interval based on Poisson distribution.
Table 2. Blood glucose and HbA1 by social development3.
|Stages of development
||Fasting blood glucose (mM)
||2 hours post glucose load (mM)
|Lanai Aborigines settlement
|Ulu Sungai Malay village
|Betau Aborigines settlement
|Sungai Koyan Malays
||5.1 ± 0.8
|Lanjan Abongines village
|Kerinci Malays village
Values are means± sd. *P<0.05 vs remote rural Malays. **P<0.05
vs rural Malays. ***P<0.05 vs urban Malays.
and diabetes mellitus
Various epidemiological studies have shown that a
high consumption of refined carbohydrates and fats, low intake of
dietary fibre, together with obesity and on inactive lifestyle contribute
to the development of non-insulin-dependent diabetes (NIDD)4-6.
Increased per capita energy consumption per day, especially of oils
and fats, animal products and sugar, with a concomitant decline in
the dietary energy from complex carbohydrates such as cereals and
other plant products (pulses, nuts and oilseeds, fruits and vegetables)
are associated with a high risk of developing NIDD. Ingestion of carbohydrates
has not been shown to increase the risk of diabetes except by virtue
of contributing to excessive weight gain7, although there
is interest in partial substitution of carbohydrate with monounsaturated
oils, as in the Mediterranean diet, as a way of minimizing hyperglycemial9a.
of obesity and diabetes mellitus
Overweight and obesity are important determinants
of NIDD whether in the city or in the village. Data available from
epidemiologic studies and surveys in the USA indicates that 24% of
American women and 22% of men are obese, by criteria of relative body
weight (>120%) or BMI >27.5 kg.m-2. In general, obesity
is common among women from lower socio-economic groups8
and with lower education. The prevalence of overweight and obesity
(BMI ³ 25) in developing countries such as Malaysia
is on an upward trend (Table 3), for urban subjects about 25-30% and
rural subjects 5-15%. The prevalence of diabetes among overweight
Malaysian subjects BMI ³ 25 was 7.3% (9/123) compared to
1.6% (9/560) with BMI <253. Malay females have a six-fold
risk of developing diabetes compared to males, and they also have
a greater prevalence of overweight and obesity.
Table 3. Prevalence of overweight among Malaysians
as indicated by BMI4.
|Age groups (years)
||Criteria of overweight (BMI) (kg/m2)
||Prevalence of overweight
of diabetes mellitus
There is a complex interaction between genetic predisposition
and environmental factors in the pathogenesis of diabetes. Diabetes
is not a single disorder but a heterogenous syndrome with varying
pathogenesis. There are broadly two different forms of the disease
type I (insulin-dependent, IDD) and type II (non-insulin-dependent,
NIDD)9. Approximately 90% of diabetics are type II. The
differences in characteristics are shown in Table 4. The development
of type I (IDD) diabetes is based on a chronic, progressive inflammation
of the islet cells (insulinitis) due to the presence of antibodies
against the cells. Hyperglycemia develops because of insulin deficiency
of the B-cells. Environmental factors, possibly including diet are
increasingly regarded as important in the pathogenesis. Type II diabetes
(NIDD) is related to insulin resistance and defective or insufficient
Table 4. Comparison between IDD and NIDD.
|IDDM (type I)
||NIDDM (type II)
|Prevalence approx 0.2%
Rapid onset of the disease*
Mostly in young age of <40
No frequency difference by sex
Nutritional status - thin
Environmental factors play important roles (viruses or chemicals)
Presence of islet-cell antibodies
Poor insulin production or total deficiency
Absolute insulin deficiency
Good insulin sensitivity
No response to sulphonylureas
Generally onset after age of 40
More frequent in female
Normal or obese
Genetic factors plays important roles
ICA not present
Reduced insulin production or hyperinsulinemia
Insulin resistance or relative insulin deficiency
Poor insulin sensitivity
Ketosis resistant except during infection or stress
Good response to sulphonylureas
*Although the onset symptoms in IDD is abrupt, its
revolution may involve an antecedent period of slowly developing autoimmune
to the pancreatic B ceils.
The prevalence of overweight among people with NIDD
is more than 80%; that of abdominal obesity may even be higher. Individuals
who are 40% overweight have almost a seven times greater chance of
having diabetes mellitus as individuals of normal weight (Figure 1).
Diabetic morbidity also rises as body weight increases7.
The predominant and most characteristic anatomic changes among obese
individuals is the excessive accumulation of adipose tissue or increased
body fat content in certain parts of the body. Determination of overfatness
by skin fold thickness (SFT) and by BMI for total body fatness have
become the most widely used means of assessing body fatness10.
With SFT and truncal circumferences, distribution in body fatness
can also be ascertained.
Fig 1. Incidence of diabetes and body weight
(from Diabetes Source Book, 1969).
Many studies have shown that obesity as indicated
by body mass index (BMI) is significantly associated with incidence
or prevalence of diabetes11-13. Other nutritional indices
such as mid-arm circumference (MAC) and triceps skin fold thickness
(TSFT) subscapular and supralic skin folds (SSSF and SSISFT) also
support the importance of obesity (in particular upper body obesity)
in the development of diabetes. Upper body obesity not only predicts
the prevalence of diabetes mellitus but also IGT (P<0.0001)3.
Abdominal fat distribution in men and women also predicts certain
risk factors of macrovascular disease, such as hypertriglyceridemia
and hypertension. The mechanism by which abdominal fatness increases
the risk for NIDD is not clear. Adipose tissue located in the abdomen
is more sensitive to lipolytic stimuli than adipose tissue elsewhere51.
The lipolytic products, glycerol and free fatty acid (FFA), are directly
delivered to the liver in the splanchnic circulation and enhance gluconeogenesis
and Very Low Density Lipoprotein-Triglyceride (VLDL-synthesis)5l;
FFA also reduce peripheral glucose uptake50; hypertriglyceridemia
Fat distribution rather than total fat is a better
predictor for NIDD. Upper body obesity is associated with high prevalence
of NID 1000 D especially among women14-16. Biceps and subscapular
skin fold thicknesses and waist-hip ratio are strongly associated
with NIDD in many studies17-20.
Many obese patients have frank NIDD. They are not
ketosis-prone and do not require exogenous insulin for blood glucose
control. Many other obese patients have IGT. The prevalence in the
community increases strikingly according to lifestyle changes leading
to obesity. However, while obesity may be a very important risk factor
for NIDD, it is and by itself, insufficient to produce this disease.
A genetic susceptibility for NIDD may be necessary for obesity to
induce clinical disease48-49. These are the processes which
now require more intensive study in Malaysian communities.
and insulin resistance
One of the metabolic features of obesity especially
upper body obesity is the existence of hyperglycemia in the face of
hyperinsulinemia. This means insulin's ability to influence glucose
metabolism is impaired, a condition referred to as insulin resistance.
With abdominal fatness cells become less sensitive to insulin21
and insulin binding for receptors are reduced22.
Hyperinsulinemia in the presence of normal glucose
tolerance is evident in young people in Pacific Ocean communities
who have high susceptibility to NIDD. Subsequently, insulin resistance
occurs which leads to secondary pancreatic b -cell exhaustion23-27.
The exhaustion leading to an abnormality of insulin synthesis or secretion
may be genetically determined. Both population surveys and prospective
studies of prediabetic Pima Indians indicate that insulin resistance
predates the onset of NIDD28,29. The 'thrifty genotype'
in NIDD could contribute to insulin resistance in muscle. A selective
insulin resistance in muscle would have the effect of blunting the
hypoglycemia that occurs during fasting but would allow energy storage
in fat and liver during feeding. Both of these features could allow
hunter-gatherers to have survival advantages during periods of food
shortage. However, in sedentary individuals allowed free access to
food, these individuals become obese with secondary insulin resistance
in fat and liver. Post-prandial hyperglycemia occurs would then lead
to glucose toxicity with decreased insulin secretion from b -cells30.
Insulin resistance is recognized by diminished response
to endogenous insulin (hyperinsulinemia with normal or elevated blood
glucose concentration) or exogenous insulin (diabetes requiring very
large doses of insulin). Such resistance may be due to changes in
insulin receptors, post-receptor events, or both31. In
obese individuals, the insulin resistance could result from impaired
glucose uptake by peripheral tissues such as skeletal muscle and adipose
tissue, impaired glucose uptake by the liver or increased hepatic
glucose production. However, resistance to insulin action also occurs
in lean individuals with NIDD. Thus it is considered that peripheral
tissue insulin resistance is a characteristic of NIDD and obesity
may not require to produce it27, unless subtle increases
in abdominal visceral fat have not been recognized.
The number of receptors appears to be lower in obese
patients7,13. One theory concerning the development of
insulin resistance in obese NIDD postulates that repetitive postprandial
hyperglycemia initially leads to a down regulation of insulin receptors,
which then results in a compensatory increase in insulin secretion
to prevent glucose intolerance. With more prolonged and greater hyperglycemia,
postbinding defects in insu 1000 lin action then emerge. Decreases
in the intracellular and plasma pools of glucose transporter may occur.
Overt diabetes develops only in individuals whose pancreas is unable
to meet the increased and sustained demand for insulin secretion24.
The cellular mechanism for insulin resistance in NIDD
is still poorly understood. Early reports indicated the inconsistent
relationship between insulin receptor binding and diabetes. However,
more recent reports have found evidence for a postbinding defect in
NIDD. Increased lipolysis in the glucose-fatty acid cycle is partly
responsible for the post-insulin receptor resistance. Insulin resistance
in NIDD is associated with increase in VLDL-TG and decrease in HDLC.
However, whether insulin resistance causes increased VLDL or, conversely,
whether elevations in VLDL impair insulin action, is yet to be determined33.
Hyperinsulinemia and associated insulin resistance
with normal glucose tolerance and not impaired insulin secretion could
be considered as an early phase in the development of NIDD24,34,35.
Progression from normal to IGT is associated with a reduction in insulin
sensitivity. However, glucose tolerance is mildly impaired with a
further compensatory increase in insulin secretion. Syndrome X is
the name given to the association of obesity, hypertension, hypertriglyceridemia,
hyperuricemia and insulin resistance. It is conceivable that abdominal
visceral obesity underlies most of the syndrome, and, in turn, genetic
predisposition to it along with a fatty refined diet and physical
inactivity. If this be the case, then greater attention to the increasing
problem of NIDD, and underlying visceral obesity in Malaysia may have
a useful impact on the Nation's health.
The defective functioning of b -cells and insulin receptors are
difficult to reverse. Therefore, treatment remains symptomatic correction
of the metabolic defects. Exogenous insulin may not be effective due
to a presence of insulin resistance. However, diet, oral hypoglycemic
agents and exercise may be beneficial in obese NIDD23,36-38.
Even so all treatment should be designed to suit individual patients
in relation to ethnic groups' lifestyle, work schedule and education.
Dietary adjustment to reduce weight is the choice
for obese NIDD patients with insulin resistance. Weight loss results
in an improvement in the metabolic aspects of the diabetic state of
obese individuals with diabetes. In many patients, glucose, lipid,
protein metabolism and insulin secretion and action are restored to
normal. In others, weight loss improves the diabetic state but some
metabolic derangements still persist32. The choice of the
best diet may depend on the degree of obesity and the stage of progression
of b -cell dysfunction39.
A reduced-energy regimen should consist of 50-55%
carbohydrates, 15% protein and 30-35% fats (with a high percentage
of polyunsaturated fats). Obese diabetics will benefit from weight
reduction because reducing body weight actually reduces high glucose
levels to normal (improved glucose tolerance)40. Many obese
NIDD patients, in the earlier stages of diabetes, tolerate weight-maintenance
high-carbohydrate, low-fat diets without deterioration of glucose
tolerance. However, as their insulin reserve declines, high-carbohydrate
diets may further raise glucose levels, so a lower carbohydrate diet
seems preferable. However, in advanced NIDD with deficiency of insulin
secretion, high-carbohydrate diets espe 1000 cially refined carbohydrates
should be avoided39.
Diets which are high in carbohydrate and natural fiber
content produce a lowering of blood glucose as well as a lowering
of low-density lipoprotein cholestrol (LDLC) and triglycerides in
patients with NIDD41. In such patients, glucose homeostasis
improvement is due to increased insulin sensitivity. For obese patients
with diabetes, increased fiber in the diet may also enhance satiety,
thereby aiding in weight reduction. A study carried out in Oxford
found that diets containing a very high proportion of beans (61% carbohydrate,
18% fat, 21% protein and 96.9 g of fibre per day) resulted in the
whole of the glucose profile being lowered41. Delayed absorption
can be achieved by delayed gastric emptying presumably by dietary
fibres or by using 'swelling substances' and slow breakdown of carbohydrates7.
Guar gum and pectin (soluble fibre) was found to delay the absorption
and can be useful in NIDD.
The arteriosclerotic complications found in patients
with diabetes have been attributed partly to elevated plasma lipid
concentrations which are influenced by fat intake. Diets for patients
with diabetes should therefore have reduced fat intake to correct
the unfavourable lipid profile. Achievement of ideal weight, glycemic
control, and when necessary, medical treatment of hyperlipidemias
will retard the process of atherosclerosis. HMG Co-A reductase inhibitor
(pravastatin), and other hypolipidemic agents such as gemfibrozil42,
and bezafibrate reduce cardiovascular risk through the correction
Biguanies act to decrease absorption, inhibit gluconeogenesis,
stimulate glucose conversion in muscle and fatty tissue and lower
plasma lipid levels. Their action, therefore, is linked to the presence
of endogenous or exogenous insulin and so they are particularly suitable
for obese diabetics. The side effect of lactic acidosis is probably
less with metformin than other biguanides7.
Sulphonylureas act by stimulating b -cells to release insulin (it depends
upon the existence of b -cells) and helping glucose sensitize the
cells. They are useful for NIDD which cannot be controlled by diet
alone. In NIDD insulin is secreted after stimulation by glucose, but
its secretion is delayed and at low peak. About 30% reduction of blood
glucose level will be produced by using these drugs. Since sulphonylureas
increase insulin secretion, they may be relatively contraindicated
in obese people with diabetes and hyperinsulinism.
Physical activity improves physical fitness, increases
energy expenditure, helps appetite regulation, favourably influences
serum lipoproteins, lowers blood pressure and, importantly, decreases
the risk of coronary artery disease. Physical training can increase
insulin sensitivity42a. However, the long-term effects
on blood glucose control with exercise alone are not proven. In NIDD,
since the population is often obese and sedentary, exercise would
be expected to have beneficial effects in promoting weight reduction
and thereby improving glucose regulation44. Exercise alone
may have a marked effect on the long-term metabolic abnormalities
of NIDD. But exercise combined with diet that produces greater effects.
Moreover, the weight loss produced by exercising is more easily maintained45,46.
Even through exercise programs may have beneficial
effects for patients with diabet 1000 es in conjunction with diet
or hypoglycemic agents, it is inappropriate to exercise all patients
at the same level of intensity, duration and frequency47.
Weight reduction and sulphonylurea therapy can achieve
a decrease in insulin resistance. Exercise and weight reduction in
obese individuals are accompanied by increased insulin receptor binding
and postbinding insulin actions.
The changing lifestyle, particularly in respect of
fatty, refined diets and decreasing physical activity are likely to
be contributing to visceral obesity, insulin resistance and related
phenomena in Malaysia as elsewhere. Prevention and management of NIDD
require greater research and understanding of these phenomena.
1. King H, Zimmet P. Trends in prevalence and incidence
of diabetes: Non-insulin dependent diabetes mellitus. Rapp Trimes
Statist Mond 1988; 41:190-96.
2. Zimmet PZ, King HM. Developing nations. Diet and
diabetes. In: Tandhanand S, Nitiyanant W, Vichayanrat A, Vannasaeng
S, eds. Diabetes mellitus. Proceeding of the third world congress
on diabetes in tropics and developing countries. Bangkok, 1984.
3. Osman Ali, Khalid BAK, Tan TT, Wu LL, Sakinah O,
Ng ML. Prevalence of NIDDM and impaired glucose tolerance in aborigines
and Malays in Malaysia and their relationship to sociodemographic,
health and nutritional factors. Diabetes Care 1993; 16(1):68-75.
4. Khor GL, Gan CY. Trends and dietary implications
of some chronic non-communicable diseases in peninsular Malaysia.
Asia Pacific J Clin Nutr 1992; 1:159-168.
5. Colditz GA, Manson JE, Stamfer MJ, Rosner B, Willet
WC, Speizer FE. Diet and risk of clinical diabetes in women.Am J Clin
Nutr 1992; 55:1018-1023.
6. Boyce VL, Swinburn BA. The traditional Pima Indian
diet; composition and adaptation for use in a dietary intervention
study. Diabetes Care 1993; 16 (suppl 1): 369-371.
7. Schmitt EW. A new principle in the treatment of
diabetes mellitus. Asten, The Netherlands: Mennen, 1987.
8. Stunkard AJ. Obesity and the social environment:
current status, future prospees In: Bray G, ed. Obesity in America.
US DHEW Publication HNIH, 1979.
9. WHO study groups: Diabetes Mellitus. World Health
Organisation technical report series 727, Geneva, 1985.
10. Durnin JVGA, Womersly J. Body fat assessed from
total body density and its estimation from skinfold thickness: measurements
of 481 men and women aged 17 to 72 years. Br J Nutr 1974: 32-77.
11. Lundgren H, Bengtsson C, Blohme G, Lapidus L,
Sjostrom L. Adiposity and adipose tissue distribution in relation
to incidence of diabetes in women: results from a prospective population
study in Gothenburg, Sweden. Int J Obes 1989; 13(4):413-23.
12. Newell-Morris LL, Treder RP, Shuman WP, Fujimoto
WY. Fatness, fat distribution and glucose tolerance in second-generation
Japanese-American (Nisei) man. Am J Clin Nutr 1989; 50(1):9-18.
13. Young TK, Sevenhuyen GP, Ling N, Moffatt ME. Determinants
of plasma glucose level and diabetic status in northern Canadian Indian
population. Can Med Assoc J 1990; 142(8):821-30.
14. Mueller WH, Joos SK, Hanis CL, Zavalete AN, Eichner
J, Schull WJ. The diabetes alert study: growth, fatness and fat patterning,
adolescence through adulthood in Mexican Americans. Am J Phys Anthropol
15. Haffner SM, Stern MP, Hazuda MD, Rosenthal M,
Kno 1000 pp JA, Malina RM. Role of obesity and fat distribution in
non-insulin dependent diabetes in Mexicans Americans and non-Hispanic
whites. Diabetes Care 1986; 9: 153-61.
16. Rimm AA, Hartz AJ, Fischer ME. A weight shape
index for assessing risk of disease in 44,820 women. J Clin Epidemiol
17. Albrink MJ, Meigs JW. Interrelationship between
skinfold thickness, serum lipids and blood sugar in normal men. Am
J Clin Nutr 1964; 15:255-73.
18. Feldman R, Sender AJ, Siegelaub AB, Oakland MS.
Difference in diabetic and non-diabetic fat distribution patterns
by skinfold measurements. Diabetes 1969; 18:478-86.
19. Feskens EJM, Daan K. Effects of body fat and its
development over a ten-year period on glucose tolerance in euglycaemic
man. The Zutphen study. Int J Epidemiol 1989; 18(2):36S373.
19a. Gorg A, Bonaname A, Grundy SM, Zhang ZJ, Unger
RH. Comparison of a high-carbohydrate diet with highmonounsaturated-fat
diet in patients with non-insulindependent diabetes mellitus. New
Eng J Med 1988, 319(13):829-34.
20. Harlan LC, Harlan WR, Landis R, Goldstein NG.
Factors associated with glucose tolerance in adults in the United
States. Am J Epidemiol 1987; 126(4):674-683.
21. Salans LB, Knittle JL, Hirsh J. The role of adipose
cell size and adipose tissue insulin sensitivity in the carbohydrate
intolerance of human obesity. J Clin Invest 1968; 47:153-165.
22. Harrison LC, Martin FIR, Milick RA. Correlation
between insulin receptor binding in isolated fat cells and insulin
sensitivity in obese human subjects. J Clin Invest 1976; 58:1435-41.
23. Zimmet PZ, Collins VR, Dowse GK, Knight LT. Hyperinsulinemia
in youth is a predictor of type II diabetes mellitus. Diabetologia
24. DeFronzo RA. Pathogenesis of type 2 diabetes mellitus:
a balanced overview. Diabetologia 1992; 35:389-397.
25. Elbein SC, Maxwell TM, Schumacher MC. Insulin
and glucose levels and prevalence of glucose intolerance in pedigrees
with multiple diabetic siblings. Diabetes 1991; 40: 1024-1032.
26. Porte D. B-cells in type II diabetes mellitus.
Diabetes 1991; 40:166-180.
27. Kolterman OG, Gray RS, Griffin J, Burstein P,
Instel J, Scarlett JA, Olefsky JM. Receptor and post-receptor defects
contribute to the insulin resistance in non-insulin dependent diabetes
mellitus. J Clin Invest 1981; 68:957-969.
28. Bogardus C, Lilioja S, Howard BV, Mott DM, Bennet
PH. Cross-sectional and longitudinal studies of carbohydrate metabolism
in Pima Indian In: Grill W, ed. Pathogenesis of insulin dependent
diabetes mellitus. New York: Raven, 1989: 285-301.
29. Knowler WC, Saad Mohammed, Pettitt DJ, Nelson
RG, Bennet PH. Determinants of diabetes mellitus in the Pima Indians.
Diabetes Care 1993; 16 (suppl 1):216-226.
30. Wendorff M, Goldfine ID. Archaeology of NIDDM;
Excavation of the 'thrifty' genotype. Diabetes 1991; 40:161-165.
31. Shafrir E, Bergman M, Felig P. The endocrine pancreas:
Diabetes mellitus In: Felig P, Baxter JD, Broadus AE, Frohman LA,
eds. Endocrinology and metabolism. New York: McGraw Hill Book Company,
32. Salans LB. The Obesities In: Felig P, Baxter JD,
Broadus AE, Frohman LA, eds. Endocrinology and metabolism. New York:
McGraw Hill Book Company, 1991; 1203-1224.
33. Howard BV. Diabetes and plasma lipoproteins in
native Americans; studies of the Pima Indians. Diabetes Care 1993;
16 (supp 1): 284-291.
34. Haffner SM, Stern MP, 1000 Hazula HP, Mitchell
BD, Patterson JK. Incidence of type II diabetes in Mexican American
predicted by fasting insulin and glucose levels, obesity, and body-fat
distribution. Diabetes 1990; 39:283-288.
35. Boyko EJ, Keane EM, Marshall JA, Hamman RF. Higher
insulin and C-peptide concentrations in Hispanic population at high
risk for NIDDM, San Luis Valley Diabetes Study. Diabetes 1991; 40:509-515.
36. Zimmet PZ. Primary prevention of diabetes mellitus.
Diabetes Care 1988; 11(3):258-262.
37. King H, Dowd JE. Primary prevention of type 2
(non insulin-dependent) diabetes mellitus. Diabetologia 1990; 33:3-8.
38. Fujimoto WY. Prevention of NIDDM In:P Kuzuya T,
Kanazawa Y/N Tajima N, eds. Dalam: Proc Japan-US diabetes epidemiology
training course. Japan Diabetes Foundation Publication series no.
1. Shinohara Publishers Inc, 1991.
39. Schuman CR. Dietary management of diabetes mellitus
In: Galloway JA, Protvin JH, Shuman CR, eds. Eli Lilly and Company,
40. Perri MG, Sears SF, Clark JE. Strategies for improving
maintenance of weight loss; towards a continuous care model of obesity
management. Diabetes Care 1993; 16(1):200-209.
41. Walker AF. Applied human nutrition for food scientists
and home economists. New York: Ellis Horwood, 1990.
42. Aaron VI, Colwell JA. Effects of gemfibrozil on
triglyceride levels in patients with NIDDM. Diabetes Care 1993; 16(1):37-44.
42a. Despres J-P. Metabolic dysfunction and exercise
In: Hills A, Wahlqvist ML, eds. Exercise and obesity. London: Smith-Gordon,
43. Kazumi T, Yoshino G, Ishida Y, Yoshida M, Baba
S. Lipid metabolism in non-insulin-dependent diabetes mellitus and
treatment. Proc 6th ACN 1991: 345-347.
44. Kerstein MD. Diabetes and vascular disease. Philadelphia:
Lippincot Company, 1990.
45. Wing RR, Epstein LH, Paternostro Bayles M, Kriska
A, Nowalk MP, Gooding W. Exercise in a behavioral weight control programme
for obese patients with type II diabetes. Diabetologia 1988; 31:902-909.
46. Wing RR. Behaviour treatment of obesity; its application
to type II diabetes. Diabetes Care 1993; 16(1):193-199.
47. Ohoshi T, Bessho H, Kadoya Y, Umazumi Y, Nomura
Y, Iinuma J, Nishimura S, Nanjo K, Iwo K, Miyamura K In: Mimura G,
Zhisheng C, eds. Recent trends of diabetes mellitus in East Asia.
Elsevier Science Publisher (Biomedical division), 1990.
48. Zimmet PZ. Kelly West lecture 1991; challenge
in diabetes epidemiology - from the West to the rest. Diabetes Care
49. Zimmet PZ. The prevention and control of diabetes
- an epidemiological perspective. In: Vannasaeng S, Nitiyanant W,
Chandraprasert S, eds. Epidemiology of diabetes mellitus. Proceedings
of the International Symposium on epidemiology of diabetes mellitus.
50. Lasser BW, Wahlqvist MNL, Kaijser L, Carlson LA.
Relationship in man between plasma free fatty acids and myocardial
metabolism of carbohydrate substrates. Lancet 1971; II: 448-450.
51. Boberg J, Carlson LA, Freyschuss U, Lassers BW,
Wahlqvist ML. Splanchnic secretion rate of plasma triglycerides and
plasma free fatty acid total and splanchnic turnover in men with normo
and hyper-triglyceridaemia. Eur J Clin Invest 1972; 2: 454-466.
Copyright © 1994 [Asia Pacific Journal of Clinical
Nutrition]. All rights reserved.
Please note: this article has been scanned and reformatted.
Please contact firstname.lastname@example.org if any errors are suspected.
February 24, 1999