NUTRITION RESEARCH, Vol. 5, pp. 1035-1045, 1985 0271-5317/85 $3.00 + .00 Printed in the USA. Copyright (c)1985 Pergamon Press Ltd. All rights reserved. SELECTED RISK FACTORS FOR DIABETES IN NATIVE AMERICANS
Mary E. Mohs, M.S., R.D., Tina K. Leonard, B.S., and Ronald R. Watson, Ph.D. 1 Department of Family and Community Medicine The University of Arizona Tucson, Arizona 85724
ABSTRACT Since the early 1940s, type II diabetes mellitus has become a widespread health problem among the Native American peoples of North America. This paper focuses on some etiologic risk factors directly related to diet. Some interrelationships of these factors with genetic predisposition are discussed. The geographic focus is on Native American populations residing in Arizona because of the extensive studies on the epidemiology and biochemistry of diabetes among the Fima and other Arizona tribes. Obesity and alcohol abuse both directly produce adverse biochemical/physlolgoical effects on glucose metabolism. In addition, alcohol abuse is indirectly diabetogenic by producing organ damage. The Western dietary and lifestyle acculturation in affected Native American populations is thought to be connected to their increasing obesity and diabetes incidence and prevalence. Acceptability and efficacy of treatment may be increased by greater participation of Native American health professionals in planning and implementation of research and treatment programs, and administration and staffing of health care facilities both on the reservation and in urban settings. The use of traditional foods among tribal groups, and the adoption of multidisciplinary, local approaches to health programs should be encouraged. Key words: diabetes, obesity, alcohol, genetics, Native Americans INTRODUCTION Many Native American tribal populations surveyed for diabetes mellitus have sho~m a prevalence of adult-onset, non-insulin dependent or Type II diabetes much greater than that of the general U.S. population (i). The range of diabetes prevalence is great, however, with the highest, well-documented rate occurring among the Pima Indians of Arizona. In addition, many non-tribal people throughout North America with some Native American ancestry may have increased risk of diabetes, for genetic predisposition, as well as diet and lifestyle changes, is thought to be an etiologic factor in diabetes among Native Americans (2-7). There are dlabetogenic aspects of obesity (4,8-10) and of alcohol abuse (11-18) which may produce potentially major dietary/nutrltional impacts on diabetes incidence, prevalence, and severity. Therefore, we will take a limited look at the epldemlology of diabetes in Native Americans, including some ways in which genetics, obesity and alcohol abuse may relate to diabetes and its development. However, these factors are only three of several, including exercise patterns, stress, seasonal changes, 1 Author responsible for correspondence and to whom requests for reprints should be addressed: Ronald R. Watson, Ph.D., Department of Family and Community Medicine, the University of Arizona, Tucson, Arizona 85724
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and seasonal viruses, which may affect Type II diabetes and its outcome in human populations (19). EPIDEMIOLOGY OF TYPE II DIABETES The epidemic of diabetes is a relatively recent phenomenon, dating to the mid-40's in onset, and continuing to increase proportionate to the Native American population to date (i). The rising diabetes rate is seen in almost all groups of the U.S. Native American population (i) with the notable exceptions being the Alaskan Athabascan Indians and the Eskimos of Alaska (20,21). These two groups, although ethnically distinct from each other, share an active outdoor llfe style. Their diets are also similar, with high protein, low carbohydrate, and moderate fat content (20). Although the incidence of clinical diabetes mellitus continued to be rare among Eskimos of Western Alaska through 1972, between 1962 and 1972, they experienced a 4.5% increase in glucose intolerance together with a 6% increase in overweight persons. The positive correlation between obesity and glucose intolerance observed in the Eskimos suggested that changing lifestyle involving diet and exercise was implicated (2!). There is a continental character to the diabetes epidemic among Native American populations (Table i) (5,8,21-32). In 1965, 29% of surveyed Cherokees on the 0ual!a Reservation in North Carolina over 34 years of age were found to have diabetes (Table i). In the diabetic group, 60% were previously confirmed diabetics. Notably, 30% of the new cases were 20% or more overweight. The diet on gross appraisal appeared to be high in carbohydrate and total calories (22). Also by 1965, a 5-year study of diabetes prevalence among 80% of southeastern Oklahoma's Choctaws had shown a diabetes rate of 53.2 per 1,000 in full-blood Indians, which was six times the national average. The Choctaw diet was high in calories, (4,000 Kcal per day) and was low in protein, and high in carbohydrate and fat (23,24). By 1969, nineteen Native American tribes had been studied and fourteen had shown a prevalence of diabetes between 4 and 23%. In addition, the disease produced as much vascular and infectious sequellae in ~ t i v e Americans as in the general U.S. population (33). This realization, which d~spelled the myth that diabetes in Native Americans was benign, was re-emphasized recently by a cross-sectional study of Hopi and Navajo Indians with Type II diabetes (34). The patients were obese and non-ketotic. Researchers found that the frequencies of vascular complications were strongly related to duration of diabetes, for the prevalence rates were duration-specific. When the variables of age, sex, obesity, duration, and method of treatment were individually considered in association with nephropathy, peripheral neuropathy, and infection or amputation of the lower extremities, the only significant association was that of duration (34). Diabetic patients with a problem of 10 years or greater duration showed rates for retinopathy (57%), nephropathy (40%), peripheral vascular disease (28%), and peripheral neuropathy (21%) similar to those seen in many other non-Native American diabetic patients (34). Oklahoma and Arizona have the two largest and highly varied Native American populations in the U.S. By 1974, diabetes was a very common problem in all Oklahoma tribes, which represent seven of the eight Native American linguistic groups of North America (35). Arizona has a more complex diabetic prevalence picture. The Pimas, Papagos, Yumas, Hualapis, Havasupis, Cocopahs, Mohaves and Maricopas have shown high rates, with the Pima having the highest well-documented rate on record (1,8,30-32,36). The Hopi, Navajo, and Apaches have shown lower rates of diabetes prevalence in the past, but they were still higher than general U.S. population rates (i). In addition, some rates may be still rising (i). In 1969, the Cocopah Indians of Arizona, who are a Yuman group living in
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DIABETES IN NATIVE AMERICANS TABLE i DIABETES PREVALENCE IN SELECTED UNITED STATES NATIVE AMERICAN POPULATIONS
Tribe Athabascan Cherokee Choctaw Pawnee Aleuts
Area Alaska N. Carolina Oklahoma Oklahoma Alaska
Year 1969 1965 1965 1966 1969
Seneca Washoe N. Paiute Mandan Arlckara Hidatsa 3 Affil. Zuni
New York Nev.,Callf. Nev.,Calif. N. Dakota N. Dakota N. Dakota N. Dakota New Mexico
1969 1973 1973 1978 1978 1978 1978 1978
Cocopah
Arizona
1969
Mohave Pima
Arizona Arizona
1966 1971
Prevalence (%) 1.3 29.0 5.3 11.7 2.1 13.7 13.4 10.7 11.5 39 22.8 21.1 27.1 6% 23.9% 26.5% 17% 34% 60.0% 50% 21.1%
Age Group (Years) Adult ~34 All ages All Ages ~20 ~39 Adult 215 >15 >35 >35 ~35 ~35 25-45
45-64 >64 ~5 ~35 Adult __>35 ~ 5
Data Showed Correlation With Indian Inheritance yes yes
yes
yes yes yes
Reference 20 22 23,24 25 26 27 28 28 5 5 5 5 29
30 8 31 32
the desert area of the southwest tip of Arizona on the Mexican border, showed a 17% prevalence of diabetes in those with at least 25% Cocopah genetic inheritance who were 5 years old or older. This rate increased to 34% in those 35 years old or older. Those 15 years and older also showed a high frequency of obesity. However, it is noteworthy that although the Cocopah obesity frequency was higher than the Pima, their diabetes prevalence was lower (30). Thus, hereditary factors may have been working differentially in the two tribes. Alternatively, a different environmental/ nutritional milieu may have existed between them. In 1966, the Mohave Indians of the Colorado River Reservation were studied via clinical observation, chart review, and statistical survey (8). This data indicated that at least 60% of the people had adult diabetes mellltus with 90% of the people being classed as obese. The diet consisted of 75% fried carbohydrate. For years, various aspects of diabetes have been intensively studied among the Pima in south-central Arizona due to the very high diabetes prevalence rate (31,32,36-39). In 1971, this prevalence was conservatively estimated at 50% among Pimas aged 35 years and older (31). The rate from 5 years and older was 21.1%, which was cited as 12.7 times higher than that experienced by a predominantly white population in Rochester, Minnesota, at 1.66% (32). Pima diabetes patients are usually obese. Type II diabetes is the type seen, and low-calorle, low carbohydrate diets can restore beta-cell responsiveness to glucose (37). This indicates that a loss of beta-eell sensitivity to glucose is involved, rather than inability to produce insulin. The prevalence rate of known diabetes is also high in young Pimas at almost 9.1 per 1,000 between the ages of 15 and 24 years. Glucose intoleranee in this age range was also greater than in other populations, and was associated with obesity (38). The
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overall diabetes incidence was 26.5 cases per 1,000 person-years, which increased through adulthood to a peak at age 40 in males, 50 in females, and then declined. This incidence was 18.7 times higher than that of the Rochester, Minnesota population (32). In a study of nondlabetic Pima Indians and Caucasians, measurement of resistance to exogenous insulin by the steady-state plasma glucose (SSPG) technique showed that SSPG concentrations were significantly correlated with fasting insulin concentrations and with obesity in both Pimas and Caucasians (39). Hyperlnsullnemia was significantly higher in Pimas even after adjustment for obesity, age, and sex. Researchers suggested that the Pimas' hyperlnsulinemla reflected resistance to insulin action, and that a greater resistance to insulin action in obese Pimas than in comparably obese Caucasians was also indicated (39). The closely-related Papago tribe (36) of Arizona also has a high prevalence at 42.3% in those 35 years and older (Table 2). However, genetic predisposing factors, although of importance in development of differential prevalence rates for diabetes, cannot explain why two closely-related Apache tribes of eastern Arizona show a 2-fold difference in glucose intolerance (36). The Whlteriver Apaches of White Mountain and the San Carlos Apaches have 11.0% and 24.8% glucose intolerance prevalences, respectively, in those 35 years old and older (Table 2). It is possible that the small population numbers involved in this comparison may explain the difference in observed rates. TABLE 2 DIABETES PREVALENCE IN SOUTHWESTERN NATIVE AMERICANS AGED 35 YEARS AND OVEN.a
Tribe
Number examined
Diabetesb, c
(z) Apache, Whlteriver Apache, San Carlos Navajo Washoe Palute Upland Yumans Zuni Cocopah Papago Pima
268 317 55 66 54 313 292 79 365 898
ii.0 24.8 12.8 16.9 25.9 29.9 31.3 d 33.3 42.3 49.6
aModified from Bennett PH, et al (36). bMeans of male and female rates. Cplasma glucose concentration of 160 mg/dL 2 hours after a 75-gm carbohydrate load. dplasma glucose concentration of 180 mg/dL 1 hour following a 75-gm carbohydrate load.
GENETICS The etiopathology of various types of diabetes differs with respect to the relatlve contribution by genetic and environmental factors, for diabetes mellltus is thought to be a group of diseases in which different pathogenesls processes result in impaired glucose metabolism (40). Genetic factors in Caucasians are known to play roles in certain insulln-dependent (Type I) diabetes types (2). The higher diabetes prevalence rates in the Native American tribes also point to a strong genetic component in their Type II diabetes. This has been clearly delineated in a recent study which showed a significant positive correlation between percent Native American genes in
DIABETES IN NATIVE AMERICANS
1039
admixtures, and age-adjusted Type II diabetes prevalence rates (3). Prevalences of 14.5%, 10%, and 5% were seen in San Antonio, Texas neighborhoods having 46%, 27%, and 18% Native American genes in their admixture, respectively. By contrast, the San Antonio Anglo population rate was 3.0%, and the predominantly Anglo HANES rate was 3.1% in the U.S. Health and Nutrition Examination Survey (3). Type II diabetes also displays a strongly familial nature in the Pimas, and the HLA-A2 antigen has been found in the Pimas associated with increased risk of Type II diabetes. OBESITY Obesity is also a strong risk factor for diabetes. Obesity is thought to be diabetogenic and to exacerbate the severity of the diabetic state. In the general population, diabetes is ten times more frequent in the obese and twenty times more frequent in the grossly obese (41). The marked effect of obesity is shown by Pima age-sex adjusted incidence rates as a function of body mass index. The thinnest people had a rate near zero, while the most obese persons had a rate of 72 new cases per 1,000 person-years (4). The thrifty gene hypothesis of Neel describes the propensity of Native Americans to become obese as having been an evolutionary advantage which developed through millenia of feast-famine cycles (42,43). With the advent of a steady food supply, this "thrifty gene" advantage is thought to have turned into a detrimental trait, for the resulting obesity helps precipitate non-insulin dependent diabetes (Type II)by progressive impairment of insulin action (4). The fact that weight loss can improve tolerance and significantly increase the pancreas' insulin-secreting ability suggests that the initial obesity-related defect lies in the sensing mechanism of the beta-cells which tells them to produce insulin as needed (i0). Recent studies in Australia, Mexico and Canada support the "thrifty gene" theory (44-46). Obese, diabetic Australian aborigines who began consuming a traditional diet experienced a marked improvement in glucose tolerance and a steady loss in weight (44). The Tarahumara Indians of the Sierra Madre Occidental Mountains of Mexico, an unacculturated group of Native Americans who maintain a physically active life and eat a traditional diet, show a complete lack of obesity (45). Their diet is relatively high in fiber (19 mg/day), low in fat (12% of calories), adequate in protein (13% of calories), and high in carbohydrates (75% of calories) (46). They appear well-adapted to their physical and nutritional environment, which is largely unchanged from ancient times. Insofar as the environment of Native Americans is altered physically and nutritionally, the advantage of maintaining and/or gaining weight in times of scarcity may have turned into a disadvantage in times of a constant, high caloric-density food supply. The Dogrib Indians are an Athapascan-speaking tribe of the Canadian Northwest Territories who live, in varying degrees from village to village, a predominantly traditional lifestyle. Dogribs are not obese by Caucasian skinfold standards, and adult-onset diabetes was unknown among them as recently as 1979. In that year, a study of hyperglycemia in adult Dogrihs of 3 villages showed a significant age-adjusted association of trunkal deposition of body fat with elevated glucose level as well as with iocallty/season. The fat-patterning was of central importance, for increased centripetality of fat, as opposed to long term obesity per se, was thought to be the more important risk factor for hyperglycemia in the Dogrib (46). The continuing and tremendously fast increase in prevalence of diabetes in many other Native American peoples also supports the "thrifty gene" hypothesis. For instance, between 1967 and 1977, the Pima Indians experienced an overall rate increase in diabetes in adults of 42% (58% for males and 38% for females). Over the same time period, the Pima Indians also became more obese. The greatest increases in weight and obesity were among those below 35 years of age, gaining 5.6 to 9.2 kg. The older Pimas also gained about 5 kg. (47). Thus, the genetic component in
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M.E. MOHS et al.
non-insulin dependent diabetes as experienced among some Native Americans may be the propensity to gain weight, thereby precipitating the diabetogenic process (47). Knowler and associates have suggested that this weight-gainlng propensity may be due to differences in sensitivity to insulin in metabolic paths. This difference is thought to occur when the insulin resistance for glucose utilization as seen in Pima diabetics is not matched by a resistance to insulin action in fat metabolism (4). Two other hypothetical mechanisms focus on an over-responsive beta cell, and a down-regulation of insulin receptor response to given insulin levels (43). Knowledge of the predisposition of Native Americans and, to a lesser extent, of those with varying Native American genetic backgrounds to diabetes can be used to direct prevention~treatment programs that are culturally appropriate. ALCOHOL ABUSE Alcoholism can produce pancreatitis, cirrhosis of the liver, and the development of glucose intolerance. Each has been implicated in diabetogenlc processes. Therefore, study and prevention of diabetes problems should consider the possible effects of alcohol. Alcohol-related health problems also extend beyond organic damage. Alcoholics show hi~her caseloads for several diseases, including metabolic and nutritional disorders, and digestive tract diseases (48). Similarly, elevated levels of these disease conditions occur in diabetics (49). The National Indian Board on Alcoholism and Drug Abuse (NIBADA) has called alcohol abuse the number one health problem among the Native American/Alaskan Native populations. There is a pronounced familial tendency towards alcoholism. The proportion that is due to social and cultural environments and/or due to genetic predisposition needs definition. Although Native Americans overall show two to seven times as many alcohol-related health problems as the general American population, there are large differences between groups and generalizations are inaccurate and unfair if made from one tribe to the next (50-52). Pancreatitis due to alcoholism can affect the liver's gluconeogenesis and other glucose metabolic pathways, may decrease the functional islet cell mass, and may lead to atrophy and fibrosis of pancreatic tissue which in turn may decrease insul~n production and result in diabetes (11,12). Hepatic cirrhosis is associated with glucose intolerance characterized by insulin resistance, hyperinsulinemia, decreased hepatic clearance, peripheral underutilization of glucose, hepatic overproduction of glucose, and a decreased number of insulin receptors on monocytes. This abnormal glucose metabolism is due to an altered pancreatic-hepatic peripheral interrelationship (13,14). Alcohol is a concentrated source of energy and it has low nutrient density. Chronic alcohol ingestion can greatly increase the total caloric intake. Alcohol therefore can contribute to obesity prior to progression to severe alcoholism, though not on a par with carbohydrates. Obesity may be a connecting factor between alcohol abuse and diabetes in some cases. Chronic alcoholism is diabetogenic in some genetically predisposed individuals, inducing hyperglycemia and decreased insulin reserves, with resultant decreased insulin release. Over time this may result in the onset of diabetes mellitus. Factors predisposing alcoholic individuals to developing diabetes may include genetic predisposition, existing mild diabetes, and the frequency and length of intermittent abstinence from alcohol allowing periodic recovery time of pancreatic function and existing mild diabetes (15,16). Excessive alcohol intake can induce symptomatic hyperglycemia. This type of alcohol induced diabetes can be reversed in some insulin-dependent diabetics by abstaining from alcohol. Abstention results in the normalization of fasting glucose levels and no future clinical symptoms (15,17). Alcohol can also cause hypoglycemia under a number of conditions. The hypoglycemic
DIABETES IN NATIVE AMERICANS
1041
effect of alcohol ingestion in the fasted state has particularly important ramifications for diabetics who take insulin or other hypoglycemic drugs. Alcohol interferes with hepatic gluconeogenesis. It can enhance the blood glucose clearing action of insulin which potentiates the hypoglycemic effects of these drugs and results in a profoundly hypoglycemic state (53). The symptoms of hypoglycemia and intoxication are very similar. The diabetic who suffers from alcohol induced hypoglycemia may be unable to differentiate between the symptoms and therefore he/she may not seek needed treatment. Others observing the sufferer may similarly misinterpret the hypoglycemia for intoxication. Untreated alcohol-induced hypoglycemia can cause minor brain damage, with repeated episodes it can result in permanent brain damage, and in some cases it can lead to death (18). Diabetes clinics and alcoholism treatment centers on many reservations have collected separate sets of data on their patient populations. However, the extent of concurrency and synergism between diabetes and alcohol abuse has not been investigated for these populations. Retrospective records can be used as a first step in answering these basic questions of concurrency and interactional effects of diabetes and alcohol abuse on a tribe-by-trlbe basis. SUGGESTED APPROACHES Avenues of approach to the problems of diabetes, obesity, and alcohol abuse should be tailored to the culture of each population sub-group so that they are appropriate in orientation and method for the people served. Involvement of both traditional Native American healers and western health care practitioners and encouragement of the use of traditlonal foods and treatments should be broadened. There has been a recent positive trend toward increased involvement of Native American physicians in planning and providing health care for their people. The Association of American Indian Physicians (AAIP) is working to increase the low number of Native American physicians by building support systems which provide counseling, preparatory education, and financial aid for Indian students (54). The Indians Into Medicine (INMED) program serves Indian students from junior high to premed levels. The Indian Health Services (IHS) has been paid for through treaties with the federal government and with tribal bonds. IHS administrations and physicians are federal employees and have for the most part not been Native Americans and not been part of the communities they have served (55). This is beginning to change. In 1974 the Indian Self Determination Act passed allowing tribes to take responsibility for local services previously federally run (55). In addition, community Indian health centers under the direction of Native Americans have sprung up in Midwest cities such as Chicago, Milwaukee, and Minneapolis, providing urban Indians with excellent health services for dealing with problems prevalent in urban Indian communities. These programs are progressive and yet responsive to the traditional needs of the Native American people (54). Any one method is unlikely to help all affected groups, as each may be expected to respond according to its particular genetic and social inheritances and environmental milieu. Neither the cultural nor the genetic inheritances of Native American peoples are homogenous. There also have been large infusions of European genes and Western culture in the past few centuries which have added diversity. Basic information on concurrency of such problems as diabetes and alcohol abuse needs t o b e gathered in tribal groups and urban Native American communities of varying backgrounds and circumstances. This will enable health providers to better assess the possible interactional situation in each group and to better plan future research directions as well as locally effective and appropriate treatment programs.
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M.E. MOHSet al.
Programs for weight control, including those which encourage diets lower in calories and fat and higher in fruits and vegetables, improved availability of fresh fruits and vegetables at reasonable cost, programs for identification and control of alcohol abuse, regularly scheduled clinical evaluations, and health education programs are als0 important. Health education targeting diabetes and related problems and beginning at a young age may result in a trend toward a decrease in these health problems (56). Treatment and educational programs need to be designed for each tribe's traditional cultural beliefs and practices as well as the current psychological and social forces which affect their lives. Some traditional dietary intake patterns which were socioculturally well-adapted to hunting and gathering and feast/famine cycles are now maladaptive with constant food availability and increased food variety. For instance, inconstant food availability evoked a behavioral response of high food intake when available. Similarly, a traditional diet with few food choices resulted in the consumption of whatever was available. The modern U.S. concepts of self-limltatlon of total food intake and of balanced food choice per meal are new and will require time to spread and become internalized. Socioeconomic factors also are important; relatively inexpensive, high fat and carbohydrate diets may be associated with poverty in some groups. Programs must also consider the similarities and differences between reservation and city-dwelling Native Americans. For instance, there may be opportunities among reservation dwellers to increase the use of native plants and the use of traditional foods and practices which have been largely lost due to changes in lifestyle. To this end, some people have demonstrated recipes to incorporate native foods such as amaranth into commodity foods. Similarly, the ~ r i p o s a Foundation for conservation was recently set up for the purpose of studying, propagating, and developing use of the low fat plants, Mariposa (Sego) and Camas lilies, which were historically used as major foods by some North American Indians (57). These are just two examples of relatively novel approaches which may be shown to have some local effect on diabetes prevalence in future. Clearly, a major effort with a wide variety of approaches needs to be applied to deal with these health problems among Native Americans. This can best be achieved through Native American involvement in the planning, implementation and follow up of new programs, and the adaptation of existing programs to the various Native American cultures in order for them to be acceptable to the populations they wish to reach and benefit.
ACKNOWLEDGMENTS Preparation supported by grants from University of Arizona Center for Native American Research and Training and the Mariposa Foundation, to R.R.W, and U.S. Navy Contract NOO244-84-D-1509. The authors express appreciation for the review of this paper by Dr. E. Sekaquaptewa, Dr. C. Ritenbaugh, and Dr. G. Harrison, and for encouragement and support by Dr. P. Skinner.
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Alcoholism
Fed. Proc., 1985; 44:134-138.
54. Anonymous. Serving their own. New disease patterns and boosting physician numbers concern today's Indian MDS. American Medical News 1984 September; 3-14. 55. Thomas P. Choctaws control 40-bed hospital and treat ills of poverty, isolation. Medical Tribune 1984 November; 18. 56. Estes NJ, Heinemann ME. Alcoholism development, consequences and interventions. Missouri:The CV Mosby Company, 1982:239-248. 57. Personal communication to Dr. Ronald R. Watson from Dr. RD Watson of the Mariposa Foundation, 415 Residence St., Moscow, Idaho, 1985.
Accepted for publication July 11,1985.