Sugarman syndrome

Recent diabetes research is challenging the longstanding emphasis on the primary role genes play in the type 2 diabetes epidemic among Native American and other high prevalence populations. Increasingly, "thrifty genotype" models are being reevaluated and modified in order to accommodate experimental and epidemiological research that highlights the powerful effects of the prenatal environment in the development of the disorder. This body of research suggests that, especially in high-risk populations, diabetes may result initially from prenatal malnutrition followed by calorically adequate diets in adulthood, and then be propagated in subsequent generations via maternal hyperglycemia during pregnancy. The present paper highlights the recent research that is challenging the dominant genetic-predisposition model of diabetes, and then explores the promise of future community-based diabetes intervention strategies informed by this research. It suggests that prevention programs that focus on improved prenatal care have the best chance of significantly reducing the incidence and prevalence of diabetes in high risk Native American communities, and explains why such programs are likely to enjoy improved community support and participation.

Key words: diabetes, Native Americans, thrifty genotype, fetal origins, intervention

The Presumed Native American Genetic Predisposition to Type 2 Diabetes

World-wide, no other racial/ethnic group suffers more with type 2 diabetes than Native Americans. While diabetes was virtually unknown, or extremely rare, prior to WW II (West 1974), beginning in the 1950s incidence and prevalence rates rose dramatically (Knowler et al. 1990; Sugarman et al. 1990; Young et al. 1985) and they continue to increase today. By the 1990s, age-adjusted prevalence among Native Americans was over 2.5 times the overall U.S. prevalence according to Indian Health Service and National Institutes of Health data (Ghodes 1995). Although Native Americans suffer disproportionately from diabetes as an ethnic/racial group, incidence and prevalence rates nevertheless vary widely among the hundreds of Indian tribes and reservation communities in the U.S. and Canada. Young (1994), in his thorough review of the Native American-diabetes literature, identifies three prevalence divisions: a "high prevalence" group, which would include all Indian communities with an adult prevalence of >30% (e.g., Pima, Havasupai, Oji-Cree); a "low prevalence" group, with an adult prevalence

For the last forty years, the disproportionately high prevalence of type 2 diabetes among Native Americans has been explained primarily in terms of a genetic predisposition to the disorder. Originally the "thrifty genotype" was hypothesized as having been "selected for" among past foraging (e.g., nonagricultural Native American) populations enduring common feast or famine cycles. Such cycles were presumed to have favored individuals with a "quick insulin trigger," which resulted in greater fat storage when plasma glucose levels were highest during times of abundance. The fat then served as an energy reserve to be utilized in more difficult times. According to the hypothesis, however, while this special, genetically-based capacity promoted survival under aboriginal feast or famine conditions, when coupled with stable, adequate diets and sedentary lifestyles (common in Native American reservation communities beginning after WWII) it promotes obesity, insulin resistance, and ultimately, type 2 diabetes (Neel 1962; 1982; 1999). While other investigators have refined or reformulated Neel's original hypothesis in various ways (e.g., Brand Miller and Colagiuri 1994; Reaven 1998; Ritenbaugh and Goodby 1989; Szathmary 1987; Weiss, Ferrell and Hanis 1984; Wendorf and Goldfine 1991), the essential elements of the thrifty genotype hypothesis endure today (Diamond 2003), and remains an often-cited evolutionary explanation of the disproportionately high rates of type 2 diabetes among the world's highest prevalence populations. (see Benyshek, Martin and Johnston 2001 for an in-depth discussion and review of these genetically-mediated etiological models and research findings.)

An Alternative Etiological Model: 'Fetal Origin' Hypotheses

Recent experimental and epidemiological studies challenge the thrifty-genotype etiological model of type 2 diabetes, and suggest that the disorder may be a disease with primarily fetal, developmental origins. This body of research shows that type 2 diabetes may result initially from metabolic adaptations of the fetus in response to maternal malnutrition during gestation, and be propagated to subsequent generations via hyperglycemic pregnancies.

In a series of papers published during the early 1990s, Barker and colleagues introduced what would become the general principles of the "fetal origins" etiological model of chronic disease (see Barker 1998). One of those papers proposed the "thrifty phenotype hypothesis" in an effort to accommodate recent epidemiological findings and experimental animal research data implicating fetal undernutrition rather than genetics in the development of type 2 diabetes (Hales and Barker 1992). Hales and Barker argued that certain physiological responses of the undernourished fetus are adaptive in utero, but that such "fetal programming" of pancreatic and liver function persists throughout life, increasing the risk of developing type 2 diabetes in adulthood.

Epidemiological and experimental evidence supporting fetal origin models of diabetes has grown considerably since the publication of Hales and Barker's seminal paper. It is well established that (full term) low birthweight is often a consequence of compromised nutrition (especially protein-calorie malnutrition) during gestation (Hurley 1980:110), and in human populations, numerous reports have demonstrated a significant relationship between low birthweight and diabetes in later life, independent of other risk factors such as low physical activity levels and obesity (see Byrne and Phillips 2000 for a review). In addition, a large number of animal studies have shown that protein calorie restriction of the mother during pregnancy leads to low birthweight offspring and glucose intolerance in those offspring after they mature (see Ozanne 2001 for a review).

Maternal alcohol consumption during pregnancy may also be implicated in non-genetic,'fetal origin' etiologies of diabetes. Like the experimental-animal maternal food restriction studies, recent animal research has shown that maternal alcohol consumption during pregnancy is also associated with low birthweight offspring who develop insulin resistance and impaired glucose tolerance in adulthood (Chen and Nyomba 2004; Chen and Nyomba 2003; Elton et al. 2002). The possible affects of prenatal exposure to alcohol on diabetes risk may be of particular relevance to Native American and other ethnic and socio-economic groups with high incidence of fetal alcohol syndrome (Abel 1995). While human epidcmiological studies examining the role of prenatal maternal alcohol consumption on the diabetes risk to offspring are severely lacking (Castells et al. 1981), this remains an important area of future research'.

Taken together, this cumulative research indicates that a genetic predisposition is not necessary for maternal diet to induce diabetes. This is significant because most Native American populations with high rates of diabetes all share a common history of deprivation (including periods of severe nutritional stress) due to ecological factors, political-economic oppression, and forced relocation/concentration, and it is the individuals born during these periods who first manifest the syndrome some 40 or 50 years later when lifestyle-related diabetes risk factors (e.g., obesity) first emerge in these communities (Benyshek, Martin and Johnston 2001). What remains to be explained then, is how diabetes would be transmitted to subsequent generations that were no longer experiencing severe food shortages.

The answer to this question may come from a considerable body of experimental and epidemiological research that suggests that gestational hyperglycemia (as opposed to maternal malnutrition) may also lead to abnormal insulin/glucose metabolism among offspring. Experimental animal research has revealed that offspring of females with chemically-induced hyperglycemia and offspring of fetally malnourished, adult female rats develop striking insulin resistance if well-nourished in adulthood (see Fowden and Hill 2001 for a review).

An extensive body of epidemiological research also supports this additional fetal pathway to diabetes. Research has shown that prior to the development of full-blown diabetes, blood sugars rise very slowly with increasing age in prediabetics, and that this rise is exacerbated by pregnancy (Pettitt et al. 1991; Silverman et al. 1995). It is also known that the risk for the offspring of diabetic mothers of developing type 2 diabetes increases four fold when the mother has impaired glucose tolerance during pregnancy, and five to six fold when she is gestationally diabetic (Martin et al. 1985; Pettitt et al. 1988). Indeed, one landmark study demonstrated that even modest (non-diabetic) maternal hyperglycemia during pregnancy significantly increases the risk of developing diabetes among these mothers' offspring (Pettitt et al. 1991 ).

In sum, research on the possible "fetal origins" of diabetes suggests that, in many cases, the etiology of the disorder among the highest prevalence populations may have more to do with multiple fetal physiological responses (phenotypic plasticity) during gestation in modern times than genotypic adaptation in the prehistoric past. This is consistent with epidemiological evidence which shows that it is among those Native American populations that have endured prolonged periods of severe politico-economic oppression and nutritional stress, followed by adequate (or more than adequate) nutrition, that diabetes is likely to be a health problem of epidemic proportions (Benyshek, Martin and Johnston 2001). Thus, at least among the highest prevalence populations, type 2 diabetes may not be a disease with a primarily genetic etiology. This has tremendously important implications for the primary prevention of diabetes in high-risk communities. Indeed, the promise of future diabetes prevention programs in high prevalence Native American communities informed by fetal origin research can hardly be understated.

Implications of the Fetal Origin Models for Diabetes Prevention in High Prevalence Native American Communities: Background

The "causes" of the diabetes epidemic among Native Americans beyond the etiological factors described above are multiple and complex. Smith-Morris (2004) provides an excellent review of the factors impinging on the diabetes epidemic in "Indian country" and highlights some of the most important lessons learned from diabetes prevention and treatment programs implemented in Native American communities over several decades. The diabetes epidemic among the Pima Indians of Arizona and other high prevalence Indian populations, Smith-Morris suggests, is due not only to physiological factors, including such risk factors as the growing prevalence of obesity, but to "political-economic" ones, including poverty, reduced access to nutritious and affordable foods, the structure of and limited access to health care, and the lack of sustainable community-based diabetes programs, among others. "Cultural factors" too are identified by Smith-Morris as contributing to the Native American diabetes epidemic, and include culturally shaped beliefs, values and norms regarding diet, exercise, and body-image, among others. She concludes that while a number of diabetes prevention and treatment programs in Indian communities have been hailed for their "success" in recent decades, they have often been measured in terms of "the number of participants enrolled and completing programs, rather than by a net reduction of diabetes within the community" (2004:39). To date, no diabetes prevention program in Indian country has resulted in a net reduction of diabetes prevalence/incidence. According to Smith-Morris, this very significant shortcoming is due not only to the enormity and complexity of the epidemic, but the inability of any programs thus far implemented to adequately attend to all three of the "domains" influencing Native American diabetes: political-economic, etiological (genetic/non-genetic), and cultural factors. Attaining the goal of reduced diabetes rates (and diabetes-related complications) through future prevention and treatment programs in Native American communities, Smith-Morris suggests, will depend on their ability to effectively address all of these domains (2004:42-43).

As noted above, anthropologists have been working alongside Native and non-Native public health professionals, clinicians, government officials and concerned community members on diabetes-related issues for several decades. Much of this work has been epidemiological, highlighting known prevalence/incidence rates and risk factors, as well as anthropometric data, diet patterns and activity levels for various Native American populations (see Young 1994; Young et al., 2000). Other anthropological work has concentrated on what Smith-Morris calls the "cultural sensitivity and relevance" of intervention programs (2004:39). These efforts have been geared toward improving participation in, and support for Indian diabetes prevention and management efforts by better understanding local (emic) perspectives about diabetes and then integrating these perspectives into existing community-based intervention programs and clinical encounters (Gittelsohn et al. 1995; Hagey 1984; Hanley et al, 1995; Lang 1985). Whether they are community-health or clinic-based approaches, conventional type 2 diabetes prevention/management standards of care typically include: community screening, diabetes education, diet modification, weight loss, increased physical exercise, regular blood-glucose monitoring, and, where appropriate, close adherence to physician-prescribed medication regimens (ADA 2002). Noncompliance with clinical diabetes prevention/management recommendations in high prevalence Native American communities has often been described as especially problematic, in some cases exceeding 80 percent (Broussard, Bass and Jackson 1982; Hickey and Carter 1994; Lang 1985; Venkat Narayan et al., 1998). Collections of multiple, individual illness narratives about diabetes provide local and non-local health care planners and practitioners with valuable information that can be used to improve prevention/ management programs and clinical protocols. Some of these explanatory narratives have included beliefs about the root cause(s) of diabetes in local Indian communities. Two beliefs that appear repeatedly in the literature deserve special attention here: 1) diabetes has been caused by the deprivations and acculturative changes brought about in the reservation era; and 2) diabetes is inevitable, uncontrollable, and unpreventable in high prevalence communities.

For at least some Native Americans in high-risk communities, diabetes is believed to be the direct result of political and economic oppression, especially with respect to the deprivations suffered at the hands of the U. S. government during the early reservation era. Lang (1989:319) reports that among many Dakota people living near Devil's Lake, North Dakota, diabetes is seen as a "new condition" brought about by the "most recent instance of white man's destruction of Indian society and culture," and the consequence of the loss of "balance" and "tradition" in peoples' lives. For other Native Americans, diabetes is largely due to the destruction of traditional foodways. Based on her work in an Anishanaabe (Ojibway) community in Manitoba, Canada, Garro (1995:41) suggests that one common explanation of diabetes places the disease within the context of imposed foods; from an aboriginal diet that promoted health and longevity, to a modern Western diet that leads to disease and early death. Still other Indian people view diabetes as a direct result of, or worsening due to, the cumulative stresses of modern life-both on and off the reservation/reserve. In her work with Cree and Ojibway Indians in Toronto, Canada, Hagey (1984:269) suggests that, for many, "unemployment, poverty, family breakdown, alcoholism, [and] diabetes" were the result of modern Indian life that, unlike pre-reservation times, is "out of control." Similarly, Garro and Lang (1994:317-318) identify "worry and stress" about "socioeconomic conditions, housing, [and] general social problems in the community" as important factors that may lead to, or exacerbate diabetes among the Dakota and Anishinaabeg research participants they interviewed. It should be emphasized that the three "themes" identified above (deprivation/acculturation; foodways; stress) are not mutually exclusive or community-specific "causal factors." To the contrary, they represent a constellation of widely shared explanations of diabetes in Native American communities hardest hit by the current epidemic (see also: Joe and Young 1994; Joos 1984; Weiner 1999).

For other Native American people, however, diabetes is ultimately linked to "Indian blood." This notion is likely due to the recognition that diabetes tends to run in families and that Indian people in general are more likely to develop the disorder. Based on ethnographic research conducted in Indian communities located in California and southern Arizona, Weiner (1999:164) notes that "inheritance" (or "genetics") was the most often cited lay-etiology of diabetes among the more than 150 persons she interviewed. Similar research conducted in the GiIa River Indian Community (Pima) of Arizona prompted Kozak ( 1996) to identify a social response to type 2 diabetes he calls "surrender." He explains that in a community that has the highest reported prevalence in the world, "surrender" is characterized as a view in which diabetes is seen as "inevitable," "uncontrollable," "inherited," and eventually, "fatal." Kozak reports that nearly 80 percent (34/44) of the participants in his study identified a familial or genetic link as the underlying cause for their reservation's diabetes epidemic. He goes on to say that perhaps the belief in the genetic basis of diabetes is the reason many Pimas can be said to be "waiting for a cure" rather than taking an active role in the community's high profile prevention and treatment programs that emphasize life-long diet and lifestyle modifications (1996:354). Pima diabetics do not appear to be unique in this regard. Given the reported tendency of many Native American diabetics to "give up," "live it up" (Hagey 1984:268), or succumb to feelings of powerlessness and fatalism (Taylor et al. 2004; Judkins 1978) in the face of what appears to be an unavoidable fate of diabetic symptoms and complications, it is possible that what Kozak calls "surrender" is quite common in many diabetes-prone American Indian populations.

Given the steadily increasing diabetes incidence and prevalence over the last thirty-five years, the perceived limited efficacy of clinical recommendations, the difficulties associated with compliance, and the long-standing message delivered by clinicians, NIH researchers and public health officials-that diabetes is "in their genes"-it is of little wonder that some Indian people might feel a sense of resignation with regard to diabetes in their community. Ironically, diabetes prevention and treatment programs aimed at decreasing incidence and prevalence rates in some Indian populations may have inadvertently contributed to feelings of the inevitability of diabetes in their family or community, and a sense of futility in efforts to prevent or treat it.

Focusing on Prenatal Care: The Best Current Strategy for Effective Primary Prevention of Type 2 Diabetes

While nutritional inadequacy was a common problem in many Native American populations in the relocation and early reservation/reserve period in the United States and Canada, in general, contemporary Native American diets are much more likely to include adequate or more than adequate total energy (calories) and protein (Jackson 1994). This means that unlike their parents and grandparents, comparably few Native Americans born today are at increased risk of developing diabetes as a result of maternal malnutrition during pregnancy, although impaired glucose tolerance during pregnancy, gestational diabetes and maternal diabetes (along with the resultant complications) are significant and growing problems among Native peoples in the United States and Canada (Murphy 1994; Sugarman 1989; Young et al. 2000). Yet, even given this alarming trend, prenatal care for Native American women in the United States remains especially poor. Baldwin et al. (2002) report that, based on a cross-sectional study of all recorded singleton births to Native American mothers in the National Center for Health Statistics Database, nearly one-fifth of rural, and approximately 15 percent of urban Native American mothers received inadequate basic prenatal care from 1989 to 1991. Rates for both groups were over twice that for U.S. Whites (6.8%), and reflect the enduring substandard level of overall health care Native Americans have received since the beginning of the reservation era (see Joe 1991).

Despite the overall inadequacy of basic prenatal care for a large segment of the Native American population, at least two high prevalence communities have initiated prenatal programs focusing on gestational diabetes. One small, short-term program sought to reduce the prevalence of gestational diabetes among Alaskan Native women in the Yukon-Kuskokwim Delta region through a nutritional education program aimed at reducing the consumption of sweetened beverages. Over a five-year period (1988-1993), prevalence of gestational diabetes mellitus (GDM) declined from 6.1% to 1.6% (Schraer et al. 1995). Another program in Quebec, Canada, attempted to reduce weight gain and gestational diabetes in four high prevalence Cree communities through diet and exercise counseling (Gray-Donald et al. 2000). The intervention did not result in significant changes in prenatal diet, rate of weight gain over the second half of pregnancy, plasma glucose levels, or birthweight, however. The authors conclude that this may have been due to the project's insufficient sensitivity to especially salient local cultural and historical factors.

Due to insufficient funding, a shortage of critical health care personnel/resources, and a lack of community-based prenatal diabetes prevention program initiatives, inadequate prenatal care for many Native American women persists even though there is overwhelming evidence that susceptibility to type 2 diabetes is greatly increased by glucose intolerance during pregnancy, and that these abnormalities, at minimum, put the mother and the offspring exposed to such environments at greater risk for diabetes and its associated complications (Freinkel 1980; O'Sullivan 1982; Pettitt etal. 1988; Pettittet al. 1991; Martin et al. 1985). It is also known that by tightly controlling their blood sugar levels, through diet modification, exercise programs and/or insulin/medication therapies, pregnant women can reduce their own risk of developing type 2 diabetes later on, as well as short and long term pathologies in their children (Jovanovic 2000; O'Sullivan and Mahan 1980; Sartor et al. 1980). In a best case scenario, and consistent with the findings discussed above, some researchers have suggested that by working with pregnant women to help them carefully monitor and control their blood-glucose levels, the familial chain of type 2 diabetes might be broken altogether (Godfrey 1998). Well short of this goal, it should be stressed that even if important genetic factors in the development of diabetes are eventually discovered, improved and intensive prenatal care for high risk mothers offers the best means of substantially reducing future incidence and prevalence rates of diabetes in high risk communities at this time, even as the precise etiology(ies) of the disorder continue to be debated.

It should be stressed, however, that an emphasis on prenatal care as a diabetes intervention strategy in the highest prevalence Native American communities carries its own set of political risks. One type of individualizing approach to diabetes may be replaced by another if medical common sense simply shifts responsibility for diabetes from "maladaptive genes" to an unhealthy prenatal environment, and by extension, the "irresponsible" lifestyles of pregnant Native American women. In recent decades, as numerous feminist commentators have noted, biomedical concern with prenatal conditions have tended to abstract the fetus and separate it from the woman who carries it, thus fostering a view of the pregnant woman as a possible threat to the fetus and justifying intensive monitoring and surveillance of pregnant women (Martin 1987). Moral responsibility for prenatal well-being is placed firmly on individual women, whose behaviors while pregnant are construed as personal choices to be evaluated solely in terms of their effects on the fetus. Disadvantaged women tend to bear the brunt of this individualistic approach to prenatal care-an approach that overlooks the social conditions that shape their everyday lives and, instead, emphasizes personal self-control. Future diabetes prevention efforts focusing on prenatal health, therefore, must guard against these sorts of reductionistic and moralizing tendencies by carrying out prenatal care in a way that realistically addresses the constraints within both the families and the communities within which pregnant women live.

The Promise of Native American Diabetes Prevention Programs Focusing on Prenatal Health

The findings and clinical recommendations above not only have important implications for the structure and content of future diabetes prevention programs, but the community support and participation they are likely to enjoy as well. First, beyond attacking the developmental conditions that increasingly appear to play a major role in the development of the disease, intervention programs which focus on helping women maintain the most healthful blood glucose levels during pregnancy require lifestyle adjustments only for a relatively short period of time, and during a time in which participants are most likely to be highly motivated to make these changes (Johnson, McCarter and Ferenz 1987). This is extremely important, since recent diabetes intervention studies have shown that it is maintaining (for the long-term) the beneficial behaviors associated with diet and lifestyle modifications that is invariably problematic for persons suffering with diabetes (Swinburn, Metcalf and Ley 2001 ; Wing et al. 2001), and that greatly limits the efficacy of diabetes interventions based on such lifestyle changes (Zimmet, Shaw and Alberti 2003). As a result, in high risk Native American communities, primary prevention programs guided by the fetal-origin models of diabetes would be less likely to inspire impractical calls for a wholesale return to "pre-reservation" foodways, or to be perceived as requiring uncompromising, life-long adherence to treatment and prevention behaviors that may run counter to some current Native American food preference/consumption, and body image norms. To the contrary, future primary diabetes-prevention projects based on fetal-origin etiological models of diabetes may be quite effective even if some community members are only able to participate briefly but intensively in the program (i.e., only during pregnancy). These programs may also enjoy considerable continuity with elements of traditional culture-including those practices which have largely fallen out of use, but which, among some people, remain important markers of ethnic and tribal identity and a shared history. For example, intensive prenatal diabetes prevention projects based in part on diet modification for pregnant women may resonate quite well with the observance of traditional food restrictions during pregnancy common in many Native American cultures (Driver 1969).

Second, the fetal-origin models of diabetes may articulate better with the views of those Native people that emphasize the historical, socio-cultural and political cause(s) of diabetes. Interestingly, the fetal-origin models of diabetes provide scientific validation of the arguments made by some Indian people that the roots of diabetes are historical and political. This might provide even more common ideological ground on which Native and non-Native health professionals (along with the larger Indian communities they serve) can together develop effective, community-specific diabetes intervention strategies based on improved prenatal care.

Third, intervention programs that recognize these discoveries and exploit the impact of fetal life on the risk of developing diabetes, shift the emphasis away from the ideas that Indians are existentially flawed, with deleterious genes and bad lifeways. These notions, which have been subtly transmitted to Indian people for forty years, must contribute to the "surrender" syndrome identified among the Pima by Kozak, and the feelings of powerlessness and fatalism expressed in other high prevalence Indian communities. Instead, the latest research implicating the fetal origins of diabetes provides Indian communities with powerful new information, research which suggests that diabetes is not necessarily "inevitable," "uncontrollable," "inherited," or a "death sentence" for future generations.

Finally, all of this is not meant to suggest that current, well designed and implemented, conventional secondary and tertiary diabetes prevention programs, including those which focus on nutrition, exercise, and weight loss (see Ritenbaugh et al. 2003) should be abandoned, but rather that, in terms of primary prevention, priority should be given to programs which focus on prenatal health. This is not only because from a public health perspective even modest improvements in diabetes-oriented prenatal care has the greatest potential to significantly reduce the incidence and prevalence of diabetes among the world's highest risk communities, but that among high risk Native American populations such programs are likely to enjoy greater community support, participation, and adherence than standard clinical and community-based diabetes prevention efforts.

Notes

1 Other studies have attempted to determine whether or not individual alcohol consumption (as opposed to prenatal alcohol exposure) affects diabetes risk. Results have been mixed. While some studies with human populations have shown a positive association between alcohol intake and diabetes risk (Holbrook, Barrett-Connor, and Wingard 1990; Kao et al. 2001), other studies have found either no association, or a negative association (Saremi et al. 2004; Hodge et al. 1993; Ajani et al. 2000). As a result, currently the role of individual alcohol consumption on diabetes risk remains unclear.

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Daniel C. Benyshek is Assistant Professor in the Department of Anthropology, University of Nevada Las Vegas (email: benyshek@unlv.nevada. edu). A version of this paper was originally presented at the 2002 annual meeting of the American Anthropological Association in New Orleans, LA, in a session entitled, "Health Lifestyles and Communities: Future Scenarios to Reduce the Diabetes Epidemic, " organized by Dennis Wiedman. The author would like to thank Elizabeth Harmon and the anonymous HO reviewers for their helpful comments and suggestions on earlier drafts of this paper.

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