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Asia Pacific J Clin Nutr (1995) 4: 351-353

Asia Pacific J Clin Nutr (1995) 4: 351-353

Thrifty genotype concepts and health in modernising Samoans

Stephen T McGarvey, PhD, MPH

Depts of Medicine and Community Health, Brown University, Providence, Rhode Island, USA

Proceedings from a symposium organised by the Australasian Clinical Nutrition Society (New Zealand Division) held at the School of Medicine, University of Aukland on 8-9 December 1994. Presented on pages 337-370.


Thrifty genotype concepts are described and applied to the case of increasing overweight with modernisation. The prevalence of overweight (BMI ³ 30 kg/m2) among American Samoans and Western Samoans is increasing substantially as described in surveys conducted in 1976-82 and in 1990-91. There is a possible role of insulin and the sympathetic nervous system in weight gain and energy balance. The thrifty genotype concept provides important hypotheses which can be applied to concrete studies among modernising Samoans.


Introduction

The role of evolutionary events in structuring genetic influences on disease has received increased theoretical and empirical attention1. One of the most cited ideas has been the thrifty genotype concept of Neel2. Neel speculated that the increase in the prevalence and incidence of diabetes mellitus in Western industrial populations, and those experiencing modernisation, was associated with genetic factors which in the past had favoured storage of calories in the form of adipose tissue in response to natural selection during food shortages. Individuals possessing tendencies towards "thriftiness" or metabolic efficiency might have been healthier, survived longer, and had more offspring3. With lifestyle changes due to economic modernisation there were increases in available food energy and decreases in energetic expenditure from lower physical activity. Thus, the advantage for a "thrifty" genotype in lean times became a disadvantage in times of plenty, leading to overweight, hyperinsulinaemia, and eventually development of glucose intolerance and diabetes mellitus.

This paper describes some of the research we are conducting among modernising Samoans, and illustrates the utility of thrifty genotype ideas for generating concrete studies of health and social change. Results on Samoan overweight, already reported using overweight criteria from US studies will be reported here using another criterion more in favour with other Pacific researchers.

Because of the widespread overweight and obesity characterising modern Pacific peoples, especially Polynesians, thrifty genotype ideas have proved very attractive to researchers working on biological and health studies with Pacific Island populations4-7. Many of these studies were summarised and reported in a recent 1000 paper on evolutionary and adaptive perspectives on adiposity and the "thrifty" genotype among Polynesians3. Briefly, the large body weight and adiposity of contemporary adult Polynesians were not present at the time of European contact, although the tall stature, rugged skeletal frame size and muscularity were described. Survey work across Polynesia from the 1960s and later did show differences in weight, body mass and fatness between rural versus town or traditional versus modernised lifestyles. There is a clear gradient of adiposity with degree of modernisation, as body mass index (BMI) values increase steadily in men and women with degree of modernisation. Also, at each step of the traditional to modern continuum women have larger BMI values than men. Further increases in Polynesian overweight and adiposity were documented in other surveys and longitudinal follow-up of individuals3.

Considerations of the discovery and settlement of Polynesia and their energetic and survival risks has led to a detailed evolutionary scenario in which tendencies to adipose deposition might have been advantageous for the first Pacific Islanders3,5. We and others have also delineated how genetically-influenced "efficient metabolisms" may play a role in the relations among overweight, adiposity, individual and family patterns in insulin secretion, insulin resistance and the development of Type II diabetes8-10.

Brief review of Samoan overweight results

A series of cross-sectional studies have described the striking overweight and adiposity among modern Samoans residing in California, Hawaii, American Samoa and Western Samoa11-13. Repeat representative surveys in American Samoa across 14 years also demonstrated the continued increase in age-specific overweight in young males and severe overweight in females of all ages14. Five-year and fourteen-year longitudinal results in American Samoa also showed continued increases in weight and greater proportions in the overweight and severely overweight categories, especially among younger adults7,15. This occurs despite pre-existing large body weight and significant adiposity.

The cross-sectional data were compiled and summarised in one report using BMI criteria for overweight and severe overweight specific to percentiles from a US national survey7. This approach made for difficult comparisons with other studies, particularly those using ³ 30 kg/m2 as the criterion for obesity. In this paper, I report the data on overweight, using ³ 30 kg/m2 as the criterion, in American Samoa from surveys conducted in 1976-787 and in 199014, and in Western Samoa from surveys conducted in 1979-827 and in 199116,17. The earlier Western Samoa data came from total population surveys of three rural villages on ‘Upolu. The later survey in Western Samoa was a randomly selected sample (>90% participation) from nine villages including four from Savai’i, a very rural and traditional area, three from rural ‘Upolu and two from Apia, the capital and urban center16. Comparisons are made across study period within American Samoa and Western Samoa, and also between American and Western Samoa with similar time periods. Within Western Samoa, overweight is compared also between 1978-82 and 1991 only for the three rural 1000 ‘Upolu villages which are similar to each other in proximity to Apia. In fact one of the three villages was studied both in 1982 and 1991.

In American Samoa, females had a higher proportion of overweight than males at the earlier time but that difference narrowed by 1990 (Table 1). American Samoan males had a significantly greater proportion of overweight at all ages in 1990 than 12-14 years earlier, whereas this was true only among the youngest and oldest females (Table 1).

In Western Samoa the comparisons of all villages studied in 1991 with the three rural ‘Upolu villages seen in 1979-82 showed significant increases in overweight over time in young males and middle aged females only (Table 2). The better comparison of temporal changes in overweight in Western Samoa is based on the three rural ‘Upolu villages (Table 3). In males, there was a non-significant trend for more overweight in 1991 in those 25-34 and 45-54 years, and a significant difference in those 35-44 years. In females, there was a similar temporal difference in those 45-54 years. There were absolute differences in overweight at other ages, although small sample sizes affected the ability to detect significant differences (Table 3).

Table 1. Proportion of overweight (BMI ³ 30 kg/m2) by age and sex in the 1976-78 and 1990 American Samoa samples.
Age

25-34

35-44

45-54

55-64

Males        
1976-78 %

50.3

49.6

53.7

37.4

N

157

133

175

1000

147

1990 %

66.7

72.7

77.8

78.3

N

93

117

90

23

p value

<0.01

<0.001

<0.001

<0.001

Females        
1976-78 %

63.0

78.0

78.7

64.1

N

227

254

249

153

1990 %

73.9

83.3

82.8

84.8

N

142

150

87

46

p value

<0.03

n.s.

n.s.

<0.01

p value - probability of Chi-square test testing the difference in overweight between the two time periods.

Table 2. Proportion of overweight (BMI ³ 30 kg/m2) by age and sex in the 1979-82 and total 1991 Western Samoa samples.
Age

25-34

35-44

45-54

55-64

Males        
1979-82 %

6.5

22.2

25.0

35.7

N

46

36

44

28

1991 %

19.2

45.6

33.3

50.0

N

146

103

90

8

p value

<0.04

<0.02

n.s.

n.s.

Females        
1979-82 %

31.3

42.2

50.0

56.3

N

67

45

1000

48

32

1991 %

39.7

60.8

67.7

100.0

N

156

120

99

4

p value

n.s.

<0.03

<0.04

n.s.

p value - probability of Chi-square test testing the difference in overweight between the two time periods.

Table 3. Proportion of overweight (BMI ³ 30 kg/m2) by age and sex, 1979-82 and 1991 rural ‘Upolu villages, Western Samoa
Age 25-34

35-44

45-54 55-64
Males        
1979-82 %

6.5

22.2

25.0

35.7

N

46

36

44

28

1991 %

17.3

43.2

42.9

50.0

N

52

37 28 2
p value

<0.10

<0.05 <0.10 n.s.
Females        
1979-82 %

31.3

42.2 50.0 56.3
N

67

45 48 32
1991 %

41.4

55.6 73.0 0
N

42

45 37 0
p value

n.s.

n.s. <0.03 --

p value - probability of Chi-square test testing the difference in overweight between the two time periods.

Overall, overweight was more prevalent in American Samoans than in Western Samoans for almost all age-sex groups at both times, especially in the earlier time.

These results for American Samoa are obviously similar to those using the same data but a different criterion for overweight14. The 1991 Western Samoan results here for the three rural ‘Upolu villages are similar to results from a recent study which included rural ‘Upolu villages, except in the youngest age group18.

It is reasonable to conclude from our and other’s Samoan results that a high prevalence of overweight and increasing overweight over time is causally associated with societal modernisation and the individual level behaviours related to energy balance. The question remains, however, is the increase in overweight with the temporal processes of modernisation also due to an interaction with a population level genetic susceptibility?

Thrifty genotype, insulin and cardiovascular health

Some of the mechanisms proposed for the thrifty genotype involve insulin levels, hyperinsulinaemia and insulin resistance. This has led to 1000 a fuller examination of insulin’s role in many cardiovascular risks factors and disease processes19-25. Landsberg offered a comprehensive review demonstrating the associations among insulin levels, energy balance, weight gain, sympathetic nervous system stimulation and blood pressure regulation19. However, many questions remain about the exact mechanisms linking insulin levels to these and other cardiovascular risk factors. Populations experiencing modernisation with sharp changes in diet, physical activity, weight and insulin levels provide many opportunities to study the longitudinal relations among insulin and health and their biological and behavioural contexts3,5,8.

Conclusion

The thrifty genotype concept and its refinements can provide ideas for further research on insulin’s influence in several

aspects of cardiovascular health status, especially in modernising groups. If such ideas allow us to hypothesise operational relations about insulin, adiposity and cardiovascular disease with concrete variables, then the thrifty genotype concept still holds value as a source of research questions.

Acknowledgements

I thank Boyd Swinburn, MD of the Department of Community Health, University of Auckland for the invitation to participate in the symposium on The Thrifty Genotype in Auckland, December 8-9, 1994. The research described here was supported by the US National Institutes of Health Grant AG09375. Many of the ideas discussed here derive from fun conversations and spirited debates among my colleagues, especially Paul T Baker, James R Bindon, Lawrence P Greksa, Daniel J Galanis, and Alexandra Brewis.


References

  1. Weiss KM. Genetic Variation and Human Disease. Cambridge, Cambridge University Press. 1993.
  2. Neel JV. Diabetes mellitus: a "thrifty" genotype rendered detrimental by "progress"? Am J Hum Gen 1962; 14: 353-62.
  3. McGarvey ST. The thrifty gene concept and adiposity studies in biological anthropology. J Polynesian Soc 1994; 103: 29-42.
  4. Prior IAM. Nutritional Problems in Pacific Islanders. Proceedings of Nutrition Society of New Zealand. 1977.
  5. Zimmet P. Epidemiology of diabetes and its macrovascular manifestations in Pacific populations: The medical effects of social progress. Diabetes Care 1979; 2: 144-53.
  6. Baker PT. Migrations, genetics and the degenerative diseases of South Pacific islanders. In: Boyce A, ed. Migration and Mobility. London: Taylor and Francis Ltd. 1984: 209-239.
  7. McGarvey ST. Obesity in Samoans and a perspective on its etiology in Polynesians. Am J Clin Nutr 1991; 53: 1586S-1594S.
  8. McGarvey ST, Bindon JR, Crews DE, Schendel DE. Modernization and Adiposity: Causes and Consequences. In: Little MA, Haas JD eds. Human Population Biology. New York: Oxford Press. 1989: 263-279.
  9. Reaven GM, Bernstein R, Davis B, Olefsky JM. Nonketotic diabetes mellitus: insulin deficiency or insulin resistance. Am J Med 1976; 60: 80-8.
  10. Stern MP, Haffner SM. Body fat distribution and hyperinsulinemia as risk factors for diabetes and cardiovascular disease, Arteriosclerosis 1986; 6: 123-30.
  11. McGarvey ST, Baker PT. The effects of modernization and migration on Samoan blood pressure. eb0 Human Biology. 1979; 51: 461-75.
  12. Pawson IG, Janes CG. Massive obesity in a migrant Samoan population. Am J Pub Health 1981; 71: 508-513.
  13. Bindon JR. Baker PT. Modernization, migration and obesity among Samoan adults. Annals Human Biol 1985; 12: 67-76.
  14. McGarvey ST, Levinson PD, Bausserman L, Galanis DJ, Hornick C. Population change in adult obesity and blood lipids in American Samoa from 1976-1978 to 1990. Am J Hum Biol 1993; 5: 17-30.
  15. Gershater E, McGarvey ST. Fourteen-year changes in adiposity and blood pressure in American Samoan adults. Am J Human Biology 1995; 7: 597-606.
  16. Chin-Hong PV, McGarvey ST. Lifestyle incongruity and adult blood pressure in Western Samoan. Psychosomatic Med 1996; 58: 146-154.
  17. Galanis DJ, McGarvey ST, Sobal J, Bausserman L, Levinson PD. Relations of body fat and fat distribution to the serum lipid, lipoprotein and insullin concentrations of Samoan men and women. Int J Obesity 1995; 19: 731-738.
  18. Hodge AM, Dowse GK, Toelupe P, Collins VR, Imo T, Zimmet PZ. Dramatic increase in the prevalence of obesity in Western Samoa over the 13 year period 1978-1991. Int J Obesity 1994; 18: 419-28.
  19. Landsberg L, Diet, obesity and hypertension: An hypothesis involving insulin, the sympathetic nervous system, and adaptive thermogenesis. Quarterly J Med 1986; 61: 1081-90.
  20. McGarvey ST. Modernization, lifestyle and cardiovascular health. In: Panter-Brick C, Worthman C, eds. Hormones, health and behavior: a developmental and ecological perspective. London: Cambridge Universirty Press; (in press).
  21. Swinburn BA, Nyomba BL, Saad MF et al. Insulin resistance associated with lower rates of weight gain in Pima Indians. J Clin Invest 1991; 88: 168-173.
  22. Valdez R, Mitchell BD, Haffner SM, Hazuda HP, Morales PA, Monterrosa A, Stern MP. Predictor of weight change in a bi-ethnic population. The San Antonio Heart Study. Int J Obes 1994; 18: 85-91.
  23. James G, Baker PT, Jenner DA, Harrison GA. Variation in lifestyle characteristics and catecholamine excretion rates among young Western Samoan men. Soc Sci Med 1987; 25: 981-986.
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  25. Donahue RP, Skyler JS, Schneiderman N, Prineas R. Hyperinsulinemia and elevated blood pressure: cause, confounder or coincidence? Am J Epidemiol 1990; 132: 827-836.


Copyright © 1995 [Asia Pacific Journal of Clinical Nutrition]. All rights reserved.
Revised: January 19, 1999 .

 

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