Early Prevention of Diabetes & Improved Access to Health Care diabetes through community-based planning to enhance physical activity and/or …
Ph ysical Activ ity and the Preven tion of Type II NonInsul in-Depen dent Di abet es
An drea Kri ska
UNI VERS ITY OF PIT TSBU RGH
ORIGINALLY PUBLISHED AS SERIES 2, NUMBER 10, OF THE PCPFS RESEARCH DIGEST
HI GHLI GHT
T h ere is a st ron g li n k be t wee n t y p e II d i a bet es a n d se d en t a ry li vin g Th e bi gges t be n efi t s a p p ea r t o be fo u n d a m on g t h ose wh o in corp ora t e so m e le vel of re gu la r p h ysic a l a c t ivi t y in t o t h eir d a ily li ves Ph ysic a l a c t ivi t y, a s re com m en d e d by t h e Su rgeo n Ge n era l, wo u ld se em t o be a p r u d en t st ra t e gy fo r a l l p e op le , es p eci a lly t h ose wh o a r e a t ri sk fo r t y p e II d i a bet es
A NOTE FRO M TH E ED ITOR S
According to the Surgeon Generals report, as many as 8 million Americans know they have diabetes and at least 8 million more have diabetes but do not know it More than 150,000 deaths each year are attributed to this condition We asked Dr Andrea Kriska, a researcher who studies diabetes, to write about this physical activity association There are two general classes of diabetes As noted in the Surgeon Generals Report, diabetes is a group of disorders
that are associated with high blood sugar levels Insulindependent diabetes mellitus IDDM or type I is characterized by an absolute deficiency of circulating insulinpage 125 Noninsulin-dependent diabetes mellitus N IDDM , or ty pe II is ch arac teri zed by e leva ted in suli n le vels th at ar e in effe ctiv e in no rmal izin g bl ood su gar le vels or by im pair ed in suli n se cret ion p age 12 5 Be caus e mo st ca ses of di abet es ar e of th e se cond ty pe t ype II an d be caus e ph ysic al ac tivi ty ha s be en sh own to be mo re re late d to th is ty pe of di seas e, we ha ve as ked Dr Kr iska to fo cus on ty pe II di abet es In th is pa per, ma ny qu esti ons ab out di abet es ar e an swer ed an d ta bles su mmar ize ke y po ints A li st of ba sic de fini tion s of ke y te rms us ed in th e pa per is pr esen ted in Fi gure 11 1
FI GURE 1 1 1
Ba sic de f in i tion s of k e y te r m s
In s ul i n A hor mone sec rete d by the pan crea s th at r egul ates lev els of s ugar in the bloo d
In s ul i n Re s i s t an c e A con diti on t hat occu rs w hen insu lin beco mes inef fect ive or l ess effe ctiv e th an i s ne cess ary to r egul ate suga r le vels in the bloo d In
s ul i n S e n s i t i v i t y A per son with ins ulin res ista nce see abo ve is s aid to h ave decr ease d in suli n se nsit ivit y T he b ody s ce lls are not sens itiv e to ins ulin so they res ist it a nd s ugar lev els are not regu late d ef fect ivel y Di ab e t e s A gro up o f di sord ers that res ults in too much sug ar i n th e bl ood, eit her beca use the body doe s no t ma ke e noug h in suli n or mak es i nsul in b ut c anno t pr oper ly u se i t Or al G l uc o s e T o l e r an c e Te s t A tes t to det ermi ne i f a pers on i s di abet ic The test mea sure s th e bo dys abi lity to clea r su gar from the blo od i n a reas onab le t ime afte r ha ving tak en a sta ndar dize d or al d ose of glu cose su gar B l o o d Gl uc o s e S ugar lev els in t he b lood
WH AT I S TYPE I I DI ABET ES?
Diabetes can be defined simply and succinctly as too much glucose in the blood West, 1978 It is a devastating disease that can often lead to complications such as blindness, kidney failure, coronary heart disease, circulatory problems that may result in amputation, nerve problems, and premature death Among those with diabetes, type II is the most common type, accounting for
9095 of all diabetic cases and affecting about 7 of the US population DIA; Harris, 1987 Among those with type II diabetes, most 6090 but not all are obese when the disease is diagnosed National Diabetes Data Group, 1979 Symptoms that are usually associated with the onset of type II diabetes are the direct result of the high blood glucose, although in many milder cases of diabetes, there may not be any symptoms West, 1978 In fact, it has been estimated that the number of individuals in the general population who are not aware that they have type II diabetes is equal to the number of individuals who have been diagnosed with the disease Harris, 1995 Just as hypertension is diagnosed at the upper end of a blood pressure distribution, the diagnosis of diabetes is usually made at the upper end of a continuum of blood glucose values Typically, the diagnosis of type II diabetes is determined based upon a specific test administered in a fasting state an oral glucose tolerance test in which the blood glucose values are measured two hours after drinking a specific glucose solution WHO, 1980 An individual is considered to have diabetes if the blood glucose values two hours after drinking the
mixture are 111 mmol/l or greater Just as someone with borderline blood pressure values are at high risk for hypertension, an individual is considered to be at risk for diabetes if his/her blood glucose values two hours after drinking the solution are 78110 mmol/l, which is called impaired glucose tolerance WHO, 1980
Despite the fact that type II diabetes is a complex condition caused by both genetic and behavioral factors, the basic metabolic abnormalities responsible for the high blood glucose values are resistance of the bodys cells to the action of insulin termed insulin resistance or decreased insulin sensitivity and the inability of the pancreas to secrete enough insulin to meet the glucose demand termed insulin deficiency During the early stages of the disease development in a genetically prone individual, insulin resistance of the insulin-sensitive tissues of the body muscles and liver can usually be found DeFronzo, 1992 Being insulin resistant means that the glucose cannot readily enter the cells, resulting in a rise of blood glucose concentrations This increase in blood glucose causes the pancreas to secrete more insulin in an attempt to normalize the blood glucose
levels If allowed to continue, this cycle of resistance and secretion proceeds until the amount of insulin that is secreted is no longer sufficient to compensate for an extreme amount of tissue insulin resistance, resulting in elevated blood glucose values and eventually diabetes Saad, 1988; Knowler, 1995
WH AT I S TH E PH YSIO LOGI CAL BASI S BEHIND A PO TENT IAL RELA TION SHIP BET WEEN PHYSICA L AC TIVI TY A ND T HE P REVENTIO N OF TYP E II DI ABET ES?
Various reviews of the effects of physical activity on insulin resistance and glucose tolerance have identified the physiological reasons why a relationship between physical activity and type II diabetes is possible Vranic, 1979; Björntorp, 1985; Koivisto, 1986; Lampman, 1991; Horton, 1991; Wallberg-Henriksson, 1992; Zierath, 1992 In general, active individuals have better insulin and glucose profiles than their inactive counterparts Stevenson, 1995; Lohmann, 1978 with detraining and bed rest shown to deteriorate these metabolic parameters Lipmann, 1972; Heath, 1983 Equally as convincing, exercise training studies have found physical activity to improve insulin action or, in other words, decrease insulin resistance Saltin, 1979;
Lindgärde, 1983; Krotkiewski, 1983; Trovati, 1984; Schneider, 1984; Seals, 1984; Rönnemaa, 1986 Less consistently, some exercise training studies have also found activity to improve glucose metabolism in both normal individuals and those with mild type II diabetes Minuk, 1981; Holloszy, 1986 Based upon the findings of these training studies, it appears that physical activity would most likely impact on insulin action in individuals at high risk for diabetes with hyperinsulinemia, that is, those individuals whose capacity to secrete insulin is still intact and insulin resistance is the major cause of the abnormal glucose tolerance Holloszy, 1986 Obesity and fat distribution specifically, the distribution of body fat in the central as compared to the peripheral regions are major contributors to insulin resistance and are therefore, strongly involved in the pathogenesis of type II diabetes Björntorp, 1988; Björntorp, 1991; Dowse, 1991; Haffner, 1986; Hartz, 1983; Kissebah, 1989; Knowler, 1991; Modan, 1986; Ohlson, 1985; Stern, 1991 Physical activity has also been shown to be inversely associated with obesity and central fat distribution, with studies demonstrating that physical
training can reduce both of these parameters Björntorp, 1979; Brownell, 1980; Despres, 1988; Krotkiewski, 1988 In other words, it is feasible that physical activity may also prevent or delay type II diabetes through decreasing overall fat and/or intra-abdominal fat
In summary, it appears that physical activity may not only be related to type II diabetes directly but also indirectly through obesity Since most individuals with type II diabetes are obese, and change in activity is often associated with small but important changes in fat and body composition, complete separation of the effects of activity from the effects of body composition on type II diabetes is often difficult Schwartz, 1997 However, clinical studies examining the effects of physical training on patients with type II diabetes have suggested a direct relationship between the two, independent of obesity
FI GURE 1 1 2
Possible mechanisms through which the development of type II diabetes
s s s s s
physical
activity may prevent
or d e l a y
De crea se i nsul in r esis tanc e/im prov e in suli n se nsit ivit y Im prov e bl ood gluc ose leve ls gluc ose tole ranc e De crea se o vera ll a dipo sity Re duce cen tral
adi posi ty De sira ble chan ges in m uscl e ti ssue
DO EPI DEMI OLOG Y ST UDIES SUPPORT A RELATI ONSH IP BETWEEN P HYSI CAL ACTI VITY AND TYPE I I DI ABET ES?
Through the years, from early observations to current epidemiological studies, support for the existence of a relationship between physical activity and type II diabetes has been increasing Suggestions of a relationship between physical activity and type II diabetes were supported early on by the fact that societies that had abandoned traditional lifestyles which typically had included large amounts of habitual physical activity had experienced major increases in type II diabetes West, 1978 Indirect evidence of this phenomenon was also provided by the observation that groups of subjects who migrated to a more modern environment had more diabetes than their ethnic counterparts who remained in their native land Hara, 1983; Kawate, 1979; Ravussin, 1994 or that rural dwellers had a lower prevalence of diabetes than their urban counterparts Cruz-vidal, 1979; Zimmet, 1981; Zimmet, 1983; King, 1984 In these studies, differences in physical activity were suggested as partial explanations for the differences in diabetes prevalence
Results of epidemiology studies are described in the following sections and summarized in Figure 113
FI GURE 1 1 3
Ep ide m iolo g ic a l st u die s su p p or tin g a c tiv i ty a n d ty p e I I di a b e t e s th e r e la ti on sh ip b e tw e e n p h y sic a l
Cr o s s - s e c t i o n a l S t udy : B oth diab etes sta tus and glu cose /ins ulin lev els and phy sica l ac tivi ty l evel s ar e de term ined at the same poi nt i n ti me i n th e sa me i ndiv idua ls
s
In divi dual s wi th t ype II d iabe tes are less act ive than tho se w itho ut d iabe tes
s
Am ong thos e wi thou t ty pe I I di abet es, more act ive indi vidu als have low er g luco se a nd i nsul in v alue s th an t heir ina ctiv e co unte rpar ts
Ca s e - C o n t r o l o r R e t ro s p e c t i v e S t udy : I ndiv idua ls w ith and with out type II diab etes are ask ed qu esti ons abou t th eir past , in thi s ca se, thei r ph ysic al a ctiv ity leve ls
s
In divi dual s wi th t ype II d iabe tes repo rted les s ph ysic al a ctiv ity over the ir l ifet ime than ind ivid uals wi thou t di abet es
Pr o s p e c t i v e o r Lo n g i t u di n a l S t udy : I nact ive and acti ve i ndiv idua ls w itho ut t ype II d
iabe tes are fo llow ed o ver time to dete rmin e if phy sica l ac tivi ty l evel s pl ay a rol e in det ermi ning who wil l an d wi ll n ot de velo p th e di seas e
s s
Wo men alum nae who were for mer coll ege athl etes had a l ower pre vale nce of d iabe tes than tho se w ho we re n onat hlet es Fo r me n an d wo men alik e, i ndiv idua ls w ho a re r elat ivel y mo re p hysi call y ac tive are les s li kely to de velo p ty pe I I di abet es i n th e fu ture tha n th ose who are sede ntar y
Ex p e ri me n t al S t udy o r Cl i n i c al Tri al : I ndiv idua ls f ree of t ype II d iabe tes are rand omly ass igne d to a grou p th at i nclu des a ph ysic al a ctiv ity prog ram or d oes not incl ude it Foll ow-u p of the se g roup s ov er ti me w ill exam ine whic h gr oup deve lops mor e di abet es i n th e fu ture
s
In divi dual s as sign ed t o th e gr oup that inc lude s a phys ical act ivit y pr ogra m de velo ped less dia bete s ov er t ime than tho se w ho w ere not assi gned to the acti vity gro up
Cross-sectional studies collect information about the health outcome glucose intolerance or type II diabetes and the potential risk factor physical inactivity at the same time
within the same group This type of epidemiological design is limited because it is not possible to establish causality; ie, did inactivity cause the glucose intolerance or did the condition cause the inactivity Cross-sectional epidemiological studies have shown that physical inactivity was associated with type II diabetes and glucose intolerance within populations Groups of subjects with type II diabetes were found to be less active currently Taylor, 1983; Taylor, 1984; King, 1984; Dowse, 1990; Ramaiya, 1991; Kriska, 1993 than nondiabetic persons In addition, crosssectional studies that have examined the relationship between physical activity and glucose intolerance in individuals without type II diabetes generally showed that blood glucose values after an oral glucose tolerance test Lindgärde, 1981; Cederholm, 1985; Wang, 1989; Schranz, 1991; Dowse, 1991; Kriska, 1993; Periera, 1995 as well as insulin values Lindgärde, 1981; Wang, 1989; Dowse, 1991; McKeigue, 1992; Feskens, 1994; Regensteiner, 1995 were significantly higher in the less active compared to the more active individuals In case-control or retrospective study designs, individuals with and without diabetes are asked
questions about their past, particularly their exposure to the specific risk factor in question ie, physical activity level Although this type of study design is valuable in cases where the disease outcome is rare, it does suffer from potential recall bias, in which the diseased or high-risk individual may remember or recall past events differently An example of this type of study design was demonstrated in the Pima Indian Study in which those individuals from the Gila River Indian Community with diabetes reported less physical activity over their lifetime than individuals without diabetes Kriska, 1993 The most powerful observational study design is the prospective or longitudinal study design This particular design identifies and follows individuals initially free of the health outcome of interest diabetes and seeks to establish if initial or subsequent physical activity levels differentiate those who do and do not develop the disease
The fact that a sedentary lifestyle may play a role in the development of type II diabetes has been demonstrated in prospective studies of college alumni, registered nurses, physicians, and middle-aged British men Helmrich, 1991; Manson, 1991, 1992;
Perry, 1995 Women alumnae who were former college athletes had a lower prevalence of diabetes than those who were nonathletes Frisch, 1986 A study of male alumni from the University of Pennsylvania Helmrich, 1991 demonstrated that physical activity was inversely related to the incidence of type II diabetes, a relationship that was particularly evident in men at high risk for developing diabetes defined as those with a high body mass index, a history of hypertension, or a parental history of diabetes In a study of female registered nurses aged 3459 years, women who reported engaging in vigorous exercise at least once a week had a lower incidence of self-reported type II diabetes during the eight years of follow-up than women who did not exercise weekly Manson, 1991 Similar findings were observed between exercise and incidence of type II diabetes in a five-year prospective study of 4084-year-old male physicians Manson, 1992 Finally, the risk of developing diabetes over a 13-year period was reduced by 50 in men engaged in moderate to vigorous levels of physical activity compared to the less active men Perry, 1995 Although the results of all of these prospective epidemiological studies
suggest a causal relationship between physical inactivity and type II diabetes, the strength of their findings is weakened due to the determination of diabetes based upon self-report rather than an oral glucose tolerance test since an estimated 50 of the general population are not aware that they have type II diabetes Similar to measures of physical activity, physical fitness as determined by maximal oxygen uptake or as estimated by vital capacity also appears to play a role in the development of type II diabetes Eriksson, 1996, 1991 In addition, support that physical fitness may provide some protection against mortality in men at all levels of glucose intolerance from those with normal blood glucose to those with type II diabetes was demonstrated in middleaged men Kohl, 1992 Physical activity was a major part of the intervention strategy of a feasibility trial of diabetes prevention in 4749-year-old men from Malmo, Sweden Of those with impaired glucose intolerance at baseline, at least twice as many of those who did not take part in the treatment program had developed diabetes at the five-year follow-up compared with those who participated Eriksson, 1991 However, since the
participants were not randomly assigned to the intervention treatment groups, and since the treatment groups differed by medical condition at baseline, the results of this study are not conclusive In other words, the hypothesis that physical activity intervention may prevent type II diabetes was not adequately tested The most powerful and by far the most labor-intensive epidemiological study design is the experimental design or clinical trial in which efforts are made to prevent or delay the onset of the type II diabetes by manipulating the risk factor of interest, in this case, physical activity levels In this design, individuals free of type II diabetes would be randomly assigned to receive either the intervention the physical activity intervention group or no intervention the control group Subsequent follow-up of the two groups over time would determine if the groups differ by the percent who eventually develop the disease outcome
Results of a more recent clinical trial demonstrated that physical activity intervention led to a decrease in the incidence of diabetes over a six-year period among Chinese individuals initially identified with impaired glucose tolerance Pan, 1997 At
the beginning of the study, 577 individuals with impaired glucose tolerance were identified from a citywide health screening in DaQing and randomized by clinic into one of four groups: exercise only, diet only, diet plus exercise and a control group Individuals assigned to the exercise group were encouraged to increase their daily leisure physical activity to that comparable to a 30-minute walk The percent that developed diabetes was significantly lower in each of the three intervention groups compared to the control group exercise 44, diet 47, exercise plus diet 44, control 66 An example of a randomized, multi-center clinical trial of type II diabetes prevention that incorporates physical activity as one of the possible treatments is currently underway in the United States Diabetes Prevention Program, sponsored by the National Institutes of Health; NIH, 1993 In this trial, physical activity is combined with dietary modification to comprise the lifestyle intervention arm of the study Anyone interested in participating in the Diabetes Prevention Program and/or wants to obtain more information about the program should call the following toll-free number 1-888-DDP-JOIN
PH YSIC AL
A CTIVITY RECO MMEN DATI ONS: HOW MUCH I S EN OUGH ?
Recent national physical activity recommendations and summary statements suggest that the majority of overall health benefits from physical activity are gained by performing activities that are not necessarily of high intensity Pate, 1995 In fact, it has been suggested that the sedentary individual who begins to incorporate adequate amounts of moderate levels of physical activity into his/her lifestyle such as walking and gardening may attain substantial health benefits and reduce cardiovascular disease risk Pate, 1995 How can we best incorporate physical activity into our lifestyle to maximize the health benefits specific to type II diabetes?
Ty pe o f Ph y sic al A ct iv it y Reco m m en ded
Most of the exercise training and epidemiology studies done to date have focused on aerobic types of activity that require the use of large muscle mass such as walking, running, and biking Aerobic activities are recommended for the overall public as the primary type of activity because of their potential benefits in regards to improving the type II diabetes and cardiovascular risk profile Surgeon Generals Report, 1996 Recently, the
benefits of incorporating strength training into an overall activity regimen that includes aerobic activity for the prevention and treatment of type II diabetes are being recognized Strength training has been shown to acutely improve glucose tolerance and insulin sensitivity in individuals with both normal and abnormal glucose tolerance Smutok, 1994; Miller, 1994
Fr equ e n cy / Du r a t ion of Ph y s ical Act iv it y Re com m en de d
A substantial part of the improvements in glucose tolerance and insulin resistance due to exercise are believed to be the result of the cumulative effect of a frequent lowering of the blood glucose levels and decreasing insulin resistance with each specific bout of exercise Schneider, 1984 In fact, it appears that a large portion of the effect of exercise in decreasing insulin resistance is short-lived, lasting for a few days, whereas the blood glucose lowering effect of activity may not even last that long Heath, 1983; Koivisto, 1986 Possible additional improvements in glucose tolerance and insulin resistance due to a training effect of regular exercise on these parameters have been suggested as well Young, 1989 In addition, the adaptation caused by
increased levels of physical activity that can have an impact on insulin resistance over the long term especially in the older adult is the change in body composition This is in light of the fact that a very critical individual goal in regards to glucose intolerance is to attain and maintain an appropriate weight Physical activity, in conjunction with diet, appears to be the best combination for decreasing weight preferentially decreasing centrally distributed fat and to improving glucose tolerance and insulin sensitivity Yamanouchi, 1995 Furthermore, physical activity has been shown to play an important role in long-term weight maintenance Wing, 1988; Pavlou, 1989 Based upon the information provided above, at what frequency should one attempt exercise throughout the week? Since one of the goals for incorporating physical activity into ones lifestyle is to burn more calories, and since a substantial portion of the improvement in insulin and glucose appears to be short-lived, it seems reasonable to recommend a frequency of exercise of several times per week In other words, the weekend exerciser should strongly consider adding a few extra bouts of physical activity throughout the
week to maximize his/her benefits in regards to glucose tolerance and insulin sensitivity not to mention the fact that it is safer from a cardiovascular risk point of view
In t en s it y of P h y si cal Act i v it y Rec om m e n ded
In regards to insulin sensitivity and glucose tolerance, physical training studies suggest that higher intensity exercises are more likely to bring about the desired metabolic changes than lower intensity activities Holloszy, 1986; Seals, 1984 Lower intensity activities appear to follow in the same general direction, although the onset of the effects are much slower and less dramatic Björntorp, 1995 In regards to caloric expenditure, intensity of activity is not an issue The important thing is that activity is being done In general, lower intensity activities are usually easier to adopt in ones lifestyle and are relatively less likely to result in injury Pollock, 1991 It is recommended that beginners start any physical activity slowly and gradually speed up the pace and build up the duration over time Finally, it appears that the largest and most consistent difference in risk of type II diabetes occurs between those individuals who report relatively no
activity and those who report doing something see the review by Kriska, 1994 This would suggest that the individuals who would benefit the most from any public health effort to prevent type II diabetes would be the sedentary individuals If you are currently sedentary, or know people who do not incorporate activity into their lifestyle with any regularity, now is the time, and here is the reason, to begin to incorporate moderate levels of physical activity such as walking and gardening If you have diabetes or coronary heart disease, it is suggested that you talk with your physician before increasing your activity level ADA Council on Exercise, 1990; Schwartz, 1997 If you are already active, keep up the good work
R EF ER EN CE S
Björntorp, P, Sjostrom, L, Sullivan, L 1979 The role of physical exercise in the management of obesity In JF Munro Ed, The treatment of obesity, Lancaster, England: MTP Press Björntorp, P, Krotkiewski, M 1985 Exercise treatment in diabetes mellitus Acta Med Scan, 21, 1737 Björntorp, P 1988 Abdominal obesity and the development of noninsulin-dependent diabetes mellitus Diab Metab Rev, 4, 615622 Björntorp, P 1991 Metabolic implications of body fat
distribution Diabetes Care, 14, 11321143 Björntorp, P 1995 Evolution of the understanding of the role of exercise in obesity and its complications International Journal of Obesity, 19, S1S4 Brownell, KD, Stunkard, AJ 1980 Physical activity in the development and control of obesity In AJ Stunkard Ed, Obesity, pp 300324 Philadelphia: WB Saunders Cederholm, J, Wibell, L 1985 Glucose tolerance and physical activity in a health survey of middle-aged subjects Acta Med Scand, 217, 373378 Cruz-vidal, M, Costas, R, Garcia-Palmieri, M, Sorlie, P, Hertzmark, E 1979 Factors related to diabetes mellitus in Puerto Rican men Diabetes, 28, 300307 Despres, JP, Tremblay, A, Nadeau, A, Bouchard, C 1988 Physical training and changes in regional adipose tissue distribution Acta Med Scand Suppl, 723, 205212 Dowse, GK, Gareeboo, H, Zimmet, PZ, Alberti, KGMM, Tuomilehto, J, Fareed, D, Brissonnette, LG, Finch, CF 1990 High prevalence of NIDDM and impaired glucose tolerance in Indian, Creole and Chinese Mauritians Diabetes, 39, 390396 Dowse, GK, Zimmet, PZ, Gareeboo, H, Alberti, KGMM, Tuomilehto, J, Finch, CF, Chitson, P, Tulsidas, H 1991 Abdominal obesity and physical inactivity are risk factors for
NIDDM and impaired glucose tolerance in Indian, Creole, and Chinese Mauritians Diabetes Care, 14, 271282 Eriksson, KF, Lindgarde, F 1991 Prevention of type II noninsulin-dependent diabetes mellitus by diet and physical exercise Diabetologia, 34, 891898 Eriksson, K, Lindgarde, F 1996 Poor physical fitness, and impaired early insulin response but late hyperinsulinaemia, as predictors of NIDDM in middle-aged Swedish men Diabetologia, 39, 573579 Feskens, EJ, Loeber, JG, Kromhout, D 1994 Diet and physical activity as determinants of hyperinsulinemia: the Zutphen elderly study American Journal of Epidemiology, 140, 350360 Frisch, RE, Wyshak, G, Albright, TE, Albright, NL, Schiff, I 1986 Lower prevalence of diabetes i n female former college athletes compared with nonathletes Diabetes, 35, 11011105 Haffner, SM, Stern, MP, Hazuda, HP, Rosenthal, M, Knapp, JA, Malina, RM 1986 Role of obesity and fat distribution in noninsulin-dependent diabetes mellitus in Mexican Americans and non-Hispanic whites Diabetes Care, 9, 153161 Hara, H, Kawate, T, Yamakido, M, Nishimoto, Y 1983 Comparative observation of micro- and macroangiopathies in Japanese diabetics in Japan and USA In H Abe M Hoshi
Eds, Diabetic Microangiopathy University of Tokyo Press Harris, MI, Hadden, WC, Knowler, WC, Bennett, PH 1987 Prevalence of diabetes and impaired glucose tolerance and plasma glucose levels in US population aged 2074 Diabetes, 36, 523534 Hartz, AJ, Rupley, DC, Kalkhoff, RD, Rimm, AA 1983 Relationship of obesity to diabetes Influence of obesity and body fat distribution Preventive Medicine, 12, 351357 Heath, G, Gavin, J, Hinderlites, J, Hagberg, J, Bloomfield, S, Holloszy, J 1983 Effects of exercise and lack of exercise on glucose tolerance and insulin sensitivity Journal of Applied Physiology, 55, 512517 Helmrich, SP, Ragland, DR, Leung, RW, Paffenbarger, RS 1991 Physical activity and reduced occurrence of noninsulin-dependent diabetes mellitus New England Journal of Medicine, 325, 147152 Holloszy, JO, Schultz, J, Kusnierkiewicz, J, Hagberg, JM, Ehsani, AA 1986 Effects of exercise o n glucose tolerance and insulin resistance Acta Med Scand Suppl, 711, 5565 Horton, ES 1991 Exercise and decreased risk of NIDDM New England Journal of Medicine, 325, 196198 Kawate, R, Yamakido, M, Nishimoto, Y, Bennett, PH, Hamman, RF, Knowler, WC 1979 Diabetes mellitus and its vascular
complications in Japanese migrants on the island of Hawaii Diabetes Care, 2, 161 170 King, H, Zimmet, P, Raper, L, Balkau, B 1984 Risk factors for diabetes in three Pacific populations American Journal of Epidemiology, 119, 396409
Kissebah, AH, Peiris, AN 1989 Biology of regional body fat distribution: Relationship to noninsulindependent diabetes mellitus Diab Metab Rev, 5, 83109 Knowler, WC, Pettitt, DJ, Saad, MF, Charles, MA, Nelson, RG, Howard, BV, Bogardus, C, Bennett, PH 1991 Obesity in the Pima Indians: Its magnitude and relationship with diabetes American Journal o f Clinical Nutrition, 53, S1543S1551 Knowler, W, Narayan, V, Hanson, R et al 1995 Perspectives in diabetes: Preventing noninsulin-dependent diabetes Diabetes, 44, 483488 Kohl, HW, Gordon, NF, Villegas, JA, Blair, SN 1992 Cardiorespiratory fitness, glycemic status, and mortality risk in men Diabetes Care, 15, 184192 Koivisto, VA, Yki-Jarvinen, H, DeFronzo, RA 1986 Physical training and insulin sensitivity Diab Metab Rev, 1, 445481 Kriska, A, LaPorte, R, Pettitt, D, Charles, M, Nelson, R, Kuller, L, Bennett, P, Knowler, W 1993 The association of physical activity with obesity, fat distribution and glucose
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