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Perspectives on obesity, pregnancy and birth outcomes in the United States: The scope of the problem
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Perspectives on obesity, pregnancy and birth outcomes in the United States: The scope of the problem E. Albert Reece, MD, PhD, MBA
O BESITY AND D ISEASE Overweight (body mass index [BMI] ⬎25-⬍30 kg/m2) and obese individuals (BMI ⱖ30) have a 50-100% increased risk of death from all causes, especially cardiovascular causes, compared with normal-weight individuals (Figure 1).1 Specifically, obesity is a known risk factor for coronary heart disease; stroke; hypertension (32.2% of women with BMI ⬎30 have high blood pressure, compared with 16.5% for those with BMl ⬍252); high cholesterol; gall bladder disease; osteoarthritis (risk increases 9-13% for every kg increase in weight); and some cancers, including colon cancer, breast cancer, endometrial cancer, and gallbladder cancer.1,3,4
The obesity-diabetes link Type 2 diabetes, like many other causes of preventive deaths, can be linked to overweight and obesity,5 and not surprisingly, several studies have shown that the risk of diabetes increases as weight increases.6-9 Diabetes is typically divided into 3 classes: type 1 (insulin dependent), type 2 (non–insulin dependent), and gestational, with type 2 being by far the most common. The development of type 2 diabetes is associated with weight gain after
From the Departments of Obstetrics, Gynecology, and Reproductive Sciences, and Biochemistry and Molecular Biology, University of Maryland School of Medicine, Baltimore, MD. Received Feb. 21, 2007; revised May 24, 2007; accepted June 29, 2007. Reprints: E. Albert Reece, MD, PhD, MBA, Office of the Dean, School of Medicine, University of Maryland, 655 West Baltimore St, Room 14-029, Baltimore, MD 21201. [email protected] 0002-9378/$34.00 © 2008 Mosby, Inc. All rights reserved. doi: 10.1016/j.ajog.2007.06.076
Obesity poses a serious health challenge. In addition to being a serious disease in its own right, obesity has also added fuel to a multitude of other diseases. An increasing body of evidence indicates that obesity does indeed beget obesity: children of obese parents have a strong tendency toward obesity and a multitude of resultant complications. Although preventive measures are, in many cases, relatively straightforward and simple, the vicious cycle of obesity is rapidly spiraling upward as this tendency is passed from parent to child. Judging by the speed of its progression and the toll it is taking, obesity can truly be called America’s newest and fastest-growing epidemic. Key words: complications, obesity, pregnancy and outcomes
age 18 years in both men and women10,11 and with excessive abdominal girth.10,12 Statistics show that among people diagnosed with type 2 diabetes, 67% have a BMI 27 kg/m2 or greater, and 46% have a BMI ⱖ30 kg/m2.13 However, the Nurses’ Health Study recently found that the risk of developing type 2 diabetes increases by approximately 25% for each additional BMI unit over a BMI as low as 22 kg/m2.11 Additionally, it was recently estimated that 27% of new cases of diabetes could be attributed to an adulthood weight gain of 11 pounds or more.14 Current statistics indicate that an estimated 70% of diabetes risk in the United States can be attributed to excess weight.13 In 2005, almost 21 million people in the United States were known to have diabetes, and of those, 1.5 million were newly diagnosed adults older than the age of 20.15 More significantly, about 17 million of those people had type 2 diabetes, accounting for more than 80% of diabetes cases.15 The economic impact of such a widespread illness is profound (Table 1). In 2002, the total annual cost of type 1 and type 2 diabetes was $132 billion, with $92 billion in direct medical expenditures and $40 billion in indirect costs.16 Such expenses include, but are not limited to, hospitalization, physician office visits, emergency room visits, prescription drugs, and loss of productivity.17
Obesity and pregnancy Obesity and its resultant diseases are not a concern only for the adult population. As we witness a growing trend toward overweight and obesity among our children, we also see far too many of them faced with the burden of type 2 diabetes and other complications. There is mounting evidence that these children may be predisposed to obesity and its related complications, even before birth. Studies indicate that the intrauterine environment affects the incidence of obesity, and that as a direct result of maternal obesity, the child faces a life-long risk of obesity17-19 and related health problems. In fact, 29-33% of infants of obese mothers are in the 90th percentile for age, and the child of an overweight mother is 3 times more likely to be overweight by age 7.20 Thus, it is clear that obesity is of special concern for women who are pregnant or who plan to become pregnant. Overweight and obesity have long been known to complicate pregnancy and are associated with increased morbidity for both the mother and the child. Both of these conditions increase the chances for such serious and potentially life-threatening complications of pregnancy as pregnancy-associated hypertension and preeclampsia, as well as anesthesia-related risks, should the woman undergo surgery.17,18,21,22 Nearly half of women of child-bearing age are either over-
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FIGURE 1
TABLE 1
Obesity: a vicious cycle
Total cost of diabetes, 2002
Hypertension High Cholesterol
Cost component
Diabetes Mellitus
Components’ proportion of total cost (%)*
Health care expenditures
91,861
70
Institutional care
54,215
41
Hospital inpatient care
40,337
31
.....................................................................................................................................................................................................................................
Coronary Heart Disease Cancer
Total cost attributable to diabetes (millions of dollars)
..................................................................................................................................................................................................................................... .....................................................................................................................................................................................................................................
OBESITY
Nursing home care
13,878
11
20,130
15
10,033
8
2162
2
.............................................................................................................................................................................................................................................. Stroke
Outpatient care
.....................................................................................................................................................................................................................................
Physician office-based care
Gall Bladder Disease
..................................................................................................................................................................................................................................... Sleep Apnea
Osteoarthritis
Emergency care
.....................................................................................................................................................................................................................................
Ambulance services
146
0
Hospital outpatient care
3315
3
Home health care
3930
3
543
0
.....................................................................................................................................................................................................................................
Reece. Perspectives on obesity, pregnancy, and birth outcomes in the US. Am J Obstet Gynecol 2007.
..................................................................................................................................................................................................................................... .....................................................................................................................................................................................................................................
Hospice care
..............................................................................................................................................................................................................................................
weight or obese and must face these concerns.23 Obesity also frequently leads to delivery complications (Table 2). Studies show that both overweight and obese women are admitted earlier (based on cervical dilation assessment) to labor and delivery and have their labor induced and receive oxytocin more often, compared with normal-weight women.23 In addition, these women progress through labor more slowly than do normal-weight women: 7.9 hours for obese women, compared with 6.2 hours for normal-weight women.17 Observational studies show that obese women have up to a 2-fold increased risk for a cesarean delivery, compared with normal-weight women, and that the majority of these deliveries are performed during the first stage of labor and based on an indication of dystocia and fetal distress.23 Finally, macrosomia is common among the offspring of obese mothers, with infants of overweight and obese mothers being 60-100 g heavier than those of normal-weight women, thus increasing the risk of birth trauma.23 Perhaps one of the most significant risks an obese, pregnant woman may face is the likelihood of developing gestational diabetes mellitus (GDM). Pregnancy naturally induces insulin resistance,21 which in about 7% of pregnant women in the United States, leads to GDM17 (Figure 2). However, if the 24
Outpatient medication and supplies
17,516
13
Outpatient medication
5516
4
Insulin and delivery supplies
6991
5
Oral agents
5009
4
39,810
30
..................................................................................................................................................................................................................................... ..................................................................................................................................................................................................................................... .....................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................
Indirect costs because of lost productivity
.....................................................................................................................................................................................................................................
Lost work days
4503
3
.....................................................................................................................................................................................................................................
Restricted activity days
6256
5
21,558
16
7494
6
131,672
100
.....................................................................................................................................................................................................................................
Mortality
.....................................................................................................................................................................................................................................
Permanent disability
..............................................................................................................................................................................................................................................
Total cost
..............................................................................................................................................................................................................................................
* Cost component percentages do not necessarily add up to category totals because of rounding. Copyright © 2003 American Diabetes Association. From Diabetes Care®, vol. 26, 2003; 917-932. Reprinted with permission from The American Diabetes Association.
woman is obese, her risk of developing GDM is significantly increased.24 In a population-based cohort study (n ⫽ 96,801), the risk of GDM was increased 5.2-fold in obese women (BMI ⱖ30.0; odds ratio [OR], 5.2; 95% confidence interval [CI], 4.3-6.2), compared with women categorized as lean (BMI ⬍20.0; OR, 1.0) and normal-weight women (BMI 20.0-24.9; OR, 1.3; CI, 1.1-1.5).24 Whereas GDM generally lasts the duration of pregnancy, 5-10% of women who had GDM will continue to be diabetic (type 2), even after pregnancy. Overall, women with a history of GDM have a 20-50% chance of developing diabetes in the future25 (Table 3). The presence of GDM is associated with pregnancy and perinatal risks, such as spontaneous abor-
American Journal of Obstetrics & Gynecology JANUARY 2008
tion, neonatal hypoglycemia, respiratory distress syndrome, and stillbirth.17-19
The environmental connection The age-adjusted prevalence of obesity was 30.5% in 1999-2000, compared with 22.9% in 1988-1994 (P ⬍ .001).26 The prevalence of overweight also increased from 55.9% to 64.5% (P ⬍ .001) over the same time period (Figure 3).26 Approximately 15.3% of children aged 6-11 years and 15.5% of adolescents aged 12-19 years were overweight in 2000.27 Our environment is a major determinant of overweight and obesity. The current environment in the United States encourages consumption of energy and discourages expenditure of energy.28 A variety of highly palatable, calorie-dense
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TABLE 2
Intrapartum characteristics of term, nulliparous women, according to their prepregnancy body mass index (Pregnancy, Infection, and Nutrition Study, 1995-2002)
Cervical dilation at admission (cm)
Normal (BMI 19.8-26.0 kg/m2) (n ⴝ 297)
Overweight (BMI 26.1-29.0 kg/m2) (n ⴝ 115)
3.0 (1.0, 5.0)
2.5 (1.0, 6.0)
Pa .39
Obese (BMI >29.0 kg/m2) (n ⴝ 200)
Pb
2.0 (0.0, 5.0)
.03
................................................................................................................................................................................................................................................................................................................................................................................
Contractions present at admission
.47
.01
.......................................................................................................................................................................................................................................................................................................................................................................
Yes, regular
181 (60.9)
63 (54.8)
90 (45.0)
Every 1-5 min
165 (55.5)
57 (49.6)
78 (39.0)
Every 6-15 min
16 (5.4)
6 (5.2)
12 (6.0)
Yes but unknown frequency
13 (4.4)
4 (3.5)
10 (5.0)
Yes but irregular
31 (10.4)
9 (7.8)
30 (15.0)
No
67 (22.6)
35 (30.4)
68 (34.0)
5 (1.7)
4 (3.5)
2 (1.0)
....................................................................................................................................................................................................................................................................................................................................................................... ....................................................................................................................................................................................................................................................................................................................................................................... ....................................................................................................................................................................................................................................................................................................................................................................... ....................................................................................................................................................................................................................................................................................................................................................................... ....................................................................................................................................................................................................................................................................................................................................................................... .......................................................................................................................................................................................................................................................................................................................................................................
Unknown
................................................................................................................................................................................................................................................................................................................................................................................
Labor onset
⬍ .001
.22
.......................................................................................................................................................................................................................................................................................................................................................................
Spontaneous
205 (69.0)
69 (60.0)
106 (53.0)
Induction without cervical ripening
45 (15.2)
23 (20.0)
36 (18.0)
Induction with cervical ripening
47 (15.8)
.......................................................................................................................................................................................................................................................................................................................................................................
.......................................................................................................................................................................................................................................................................................................................................................................
23 (20.0)
58 (29.0)
................................................................................................................................................................................................................................................................................................................................................................................
Method of cervical ripening
.21
.11
.......................................................................................................................................................................................................................................................................................................................................................................
Foley bulb
23 (7.7)
15 (13.0)
38 (19.0)
Prostaglandins
24 (8.1)
8 (7.0)
20 (10.0)
Received oxytocin
167 (56.2)
79 (68.7)
.02
150 (75.0)
Cervical dilation at oxytocin administration (cm)
3.0 (1.0, 8.5)
3.0 (1.0, 8.5)
.98
3.0 (1.0, 7.0)
Received epidural analgesia
200 (67.3)
81 (70.4)
.64
142 (71.0)
.43
Cervical dilation at epidural analgesia placement (cm)
5.0 (3.0, 9.0)
5.0 (3.0, 9.0)
.70
5.0 (3.0, 8.0)
.72
....................................................................................................................................................................................................................................................................................................................................................................... ................................................................................................................................................................................................................................................................................................................................................................................
⬍ .001
................................................................................................................................................................................................................................................................................................................................................................................
.84
................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................
................................................................................................................................................................................................................................................................................................................................................................................
⬍.01
Method of membrane rupture
.41
.......................................................................................................................................................................................................................................................................................................................................................................
Spontaneous
133 (44.8)
35 (30.7)
83 (41.5)
Artificial
159 (53.5)
80 (69.3)
117 (58.5)
0 (0.0)
0 (0.0)
....................................................................................................................................................................................................................................................................................................................................................................... .......................................................................................................................................................................................................................................................................................................................................................................
Undetermined
5 (1.7)
................................................................................................................................................................................................................................................................................................................................................................................
Data are presented as n (percent) or median (10th, 90th percentiles; test or Wilcoxon rank sum test). 2
a
Comparison between normal weight and overweight women.
b
Comparison between normal weight and obese women.
Reprinted from Vahratian A, Zhang J, Troendle JF, Savitz DA, Siega-Riz AM. Maternal prepregnancy overweight and obesity and the pattern of labor progression in term nulliparous women. Obstet Gynecol 2004;104:943-51. With permission from Lippincott Williams & Wilkins.
food is available nearly everywhere in our country and is promoted by aggressive and sophisticated food marketing in the mass media, supermarkets, and restaurants. This is especially evident in fast food restaurants in which menu items are typically high in energy density. Cross-sectional and longitudinal data on self-reported fast food restaurant use per se and consumption of foods frequently sold at fast food restaurants (eg, ham-
burgers and french fries) have been shown to be positively associated with body weight.29 For many people, even when caloric intake is within recommended levels, physical activity is insufficient to offset consumption. Low levels of physical activity are associated with an increased risk of obesity,30 and our current environment tends to discourage physical activity.31 Mechanization lim-
its the amount of physical activity required to function in society, and for most people, the days are filled with sedentary routines consisting of sitting at work, sitting in traffic, and sitting in front of a television or a computer monitor. In a community-based study examining the relationship between television viewing and 3-year change in BMI, television viewing was positively associated with BMI among women.32
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TABLE 3
Estimated percent of women with gestational diabetes developing NIDDM or IGT after pregnancy BMI before index pregnancy
BMI before index pregnancy
Fasting plasma (mg/dL) during pregnancy
2 y after pregnancy, %
4 y after pregnancy, %
100
1.2
2.5
5.5
2.3
8.1
10.6
120
2.5
5.5
11.4
5.1
10.6
20.0
140
5.5
11.4
22.3
10.8
20.9
37.0
15
25
35
15
25
35
.............................................................................................................................................................................................................................................. .............................................................................................................................................................................................................................................. ..............................................................................................................................................................................................................................................
Risk of subsequent NIDDM or impaired glucose tolerance is calculated from a regression equation based on data from 350 former women with gestational diabetes retested at 0-10 years after their index pregnancy with a 75 g 2 h OGTT using National Diabetes Data Group criteria. IGT, impaired glucose tolerance; NIDDM, non–insulin-dependent diabetes mellitus; OGTT, oral glucose tolerance test. Adapted from Coustan DR, Carpenter MW, O’Sullivan PS, Carr SR. Gestational diabetes mellitus: predictors of subsequent disordered glucose metabolism. Am J. Obstet Gynecol 1993;168:1139-45. Reprinted from Diabetes’ in America. 2nd Ed. National Diabetes Data Group of the National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD.
Television viewing also increases the risk of being overweight to younger, preschool-aged children.33 Less than one-third of US adults get regular leisure time physical activity, and about 10% do no physical activity at all in their leisure time.34 The direct cost of physical inactivity may be as high as $24.3 billion.35 We face a daunting challenge that encompasses the reedu-
FIGURE 2
Cumulative incidence of diabetes in women with normal glucose tolerance or gestational diabetes during their index pregnancy
cation and retraining of an entire society if we are to end the spread of this diabetes epidemic.
A N ATIONAL C OMMITMENT What exactly would such a solution entail? In truth, our options are few, but the simple solutions are often the most effective. We must do the obvious, which is to teach people to improve the quality of their diets by eating more fruits and vegetables and fewer fats and calories. Individuals should be encouraged to increase their level of exercise, ideally to 30 minutes a day, 4-5 times a
week. As primary care practitioners, obstetrician-gynecologists are in an ideal position to emphasize the importance of these lifestyle changes to all our patients, not just those who are overweight or obese. Efforts should not, however, be limited to patient encounters. We must take our efforts farther than the examination room. We must exert our influence as medical professionals where it can be heard the most: among the food industry giants, insurance companies, and public education systems. We should encourage our government to support incentives, such as tax breaks, to the food industry for the promotion of fruits, vegetables, and whole grains, and for the development of low-calorie, low-fat, and low-cholesterol foods. We should encourage health insurance to provide premium breaks to those who exercise regularly and lead a healthy lifestyle Furthermore, we should insist that fitness programs are a required part of all primary, high school, and college education programs. Finally, employers, educators, and public officials must be mobilized to contribute to this effort. In addition, we must encourage and promote research designed to clarify and quantitate the contribution and the role of societal policies, procedures, laws, and other factors to the development of obesity.
FIGURE 3
Age-adjusted prevalence of overweight and obesity
Adapted from O’Sullivan JB. Subsequent morbidity among GDM women. Sutherland HW, Stowers JM eds. In: Carbohydrates Metabolism in Pregnancy and the Newborn. New York: Churchill Livington. 1984;174-180. Reprinted from Diabetes in America. 2nd Ed. National Diabetes Data Group of the National Institute of Diabetes and Digestive and Kidney Disease, National Institutes of Health, Bethesda, MD.
26
Adapted from CDC/NCHS, Health, United States, 2000 (Obtained from the National Institute of Diabetes and Digestive and Kidney Diseases Website [http://win.niddk.nih.gov/statistics/index.htm]) and the 1999-2000 NHANES study, available at http://www.cdc.gov/nchs/about/major/nhanes/nhanes99_00.htm.
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www.AJOG.org C ONCLUSION As the nation’s fastest growing epidemic, obesity is having devastating effects on multiple fronts: it exacerbates existing illnesses, increases the risk of developing others, and poses a severe health threat for generations to come. A highly visible case in point is diabetes mellitus. Studies have clearly documented the growing prevalence of this life-threatening disease as our society gains weight. The economic impact of diabetes alone is staggering, but even worse is the havoc it wreaks on patients’ quality of life as well as the very real potential for a diabetic mother to pass a tendency for the disease on to her children. As our future generations face increasing risks for the many major health problems linked to obesity, it becomes clear that we can no longer simply treat the symptoms as these diseases develop. We must diligently uproot the source of these problems: obesity caused by the unhealthy habits of an industrialized and f mechanized society. REFERENCES 1. Clinical Guidelines on the Identification, Evaluation, and Treatment of Overweight and Obesity in Adults—The Evidence Report. National Institutes of Health. Obes Res 1998;6:464. 2. Haffner SM, Mitchell BD, Hazuda HP, Stern MP. Greater influence of central distribution of adipose tissue on incidence of non-insulin-dependent diabetes in women than men. Am J Clin Nutr 1991;53:1312-7. 3. Cicuttini FM, Baker JR, Spector TD. The association of obesity with osteoarthritis of the hand and knee in women: a twin study. J Rheumatol 1996;23:1221-6. 4. Ritter MM, Schraudolph M, Richter WO, Herbert M, Wiebecke B, Schwandt P. [Obesity, heart failure and pulmonary insufficiency in a 26-year-old female]. Med Klin (Munich) 1990;85:371-5. 5. McGinnis JM, Foege WH. Actual causes of death in the United States. JAMA 1993; 270:2207-12.
6. Westlund K, Nicolaysen R. Ten-year mortality and morbidity related to serum cholesterol. A follow-up of 3.751 men aged 40-49. Scand J Clin Lab Invest Suppl 1972;127:1-24. 7. Lew EA, Garfinkel L. Variations in mortality by weight among 750,000 men and women. J Chronic Dis 1979;32:563-76. 8. Larsson B, Bjorntorp P, Tibblin G. The health consequences of moderate obesity. Int J Obes 1981;5:97-116. 9. Medalie JH, Papier C, Herman JB, et al. Diabetes mellitus among 10,000 adult men. I. Five-year incidence and associated variables. Isr J Med Sci 1974;10:681-97. 10. Chan JM, Rimm EB, Colditz GA, Stampfer MJ, Willett WC. Obesity, fat distribution, and weight gain as risk factors for clinical diabetes in men. Diabetes Care 1994;17:961-9. 11. Colditz GA, Willett WC, Rotnitzky A, Manson JE. Weight gain as a risk factor for clinical diabetes mellitus in women. Ann Intern Med 1995;122:481-6. 12. Sparrow D, Borkan GA, Gerzof SG, Wisniewski C, Silbert CK. Relationship of fat distribution to glucose tolerance. Results of computed tomography in male participants of the Normative Aging Study. Diabetes 1986;35: 411-5. 13. Maureen I. Harris. Personal communication to Susan Z. Yanovski, NIDDK/NIH; 1999. 14. Ford ES, Williamson DF, Liu S. Weight change and diabetes incidence: findings from a national cohort of US adults. Am J Epidemiol 1997;146:214-22. 15. Centers for Disease Control and Prevention. National diabetes fact sheet: general information and national estimates on diabetes in the United States, 2000. Atlanta, GA: US Department of Health and Human Services, Centers for Disease Control and Prevention; 2002. 16. American Diabetes Association. Diabetes Care 2003;26:917-32. 17. Diabetes in America, 2nd ed. NIH publication no. 95-1468. Bethesda (MD): National Diabetes Data Group, National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases; 1995. 18. Prentice A, Goldberg G. Maternal obesity increases congenital malformations. Nutr Rev 1996;54:146-50. 19. Cnattingius S, Bergstrom R, Lipworth L, Kramer MS. Prepregnancy weight and the risk of adverse pregnancy outcomes. N Engl J Med 1998;338:147-52. 20. Salsberry PJ, Reagan PB. Dynamics of early childhood overweight. Pediatrics 2005; 116:1329-38.
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21. American Diabetes Association. Gestational diabetes mellitus (position statement). Diabetes Care 2004;27(Suppl 1):S88-90. 22. Johnson SR, Kolberg BH, Varner MW, Railsback LD. Maternal obesity and pregnancy. Surg Gynecol Obstet 1987;164:431-7. 23. Vahratian A, Zhang J, Troendle JF, Savitz DA, Siega-Riz AM. Maternal prepregnancy overweight and obesity and the pattern of labor progression in term nulliparous women. Obstet Gynecol 2004;104:943-51. 24. Baeten JM, Bukusi EA, Lambe M. Pregnancy complications and outcomes among overweight and obese nulliparous women. Am J Public Health 2001;91:436-40. 25. National Institute of Diabetes and Digestive and Kidney Diseases. National diabetes fact sheet: general information and national estimates on diabetes in the United States. Bethesda (MD): National Institute of Diabetes and Digestive and Kidney Diseases; 2005. 26. Flegal KM, Carroll MD, Ogden CL, Johnson CL. Prevalence and trends in obesity among US adults, 1999-2000. JAMA 2002;288:1723-7. 27. National Institute of Diabetes and Digestive and Kidney Diseases. Diabetes Prevention Program Meeting Summary. August 8, 2001. Bethesda, MD: Diabetes Mellitus Interagency Coordinating Committee (DMICC). 28. Hill JO, Wyatt HR, Reed GW, Peters JC. Obesity and the environment: where do we go from here? Science 2003;299:853-5. 29. Jeffery RW, French SA. Epidemic obesity in the United States: are fast foods and television viewing contributing? Am J Public Health 1998;88:277-80. 30. US Department of Health and Human Services. Physical activity and health: a report of the Surgeon General. Atlanta (GA): US Department of Health and Human Services; 1996. 31. Hill JO, Peters JC. Environmental contributions to the obesity epidemic. Science 1998; 280:1371-4. 32. Crawford DA, Jeffery RW, French SA. Television viewing, physical inactivity and obesity. Int J Obes Relat Metab Disord 1999;23:437-40. 33. Dennison BA, Erb TA, Jenkins PL. Television viewing and television in bedroom associated with overweight risk among low-income preschool children. Pediatrics 2002;109:1028-35. 34. Barnes MA, Schoenborn CA. Physical activity among adults: United States, 2000. National Center for Health Statistics. Adv Data 2003;333 Y-6. DHHS Publication No. 20031250, 03-0234 (4/03). 35. Colditz G. Economic costs of obesity and inactivity. Med Sci Sports Exerc 1999;31(11 Suppl):S663-7.
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Perspectives on obesity, pregnancy and birth outcomes in the United States: The scope of the problem E. Albert Reece, MD, PhD, MBA
O BESITY AND D ISEASE Overweight (body mass index [BMI] ⬎25-⬍30 kg/m2) and obese individuals (BMI ⱖ30) have a 50-100% increased risk of death from all causes, especially cardiovascular causes, compared with normal-weight individuals (Figure 1).1 Specifically, obesity is a known risk factor for coronary heart disease; stroke; hypertension (32.2% of women with BMI ⬎30 have high blood pressure, compared with 16.5% for those with BMl ⬍252); high cholesterol; gall bladder disease; osteoarthritis (risk increases 9-13% for every kg increase in weight); and some cancers, including colon cancer, breast cancer, endometrial cancer, and gallbladder cancer.1,3,4
The obesity-diabetes link Type 2 diabetes, like many other causes of preventive deaths, can be linked to overweight and obesity,5 and not surprisingly, several studies have shown that the risk of diabetes increases as weight increases.6-9 Diabetes is typically divided into 3 classes: type 1 (insulin dependent), type 2 (non–insulin dependent), and gestational, with type 2 being by far the most common. The development of type 2 diabetes is associated with weight gain after
From the Departments of Obstetrics, Gynecology, and Reproductive Sciences, and Biochemistry and Molecular Biology, University of Maryland School of Medicine, Baltimore, MD. Received Feb. 21, 2007; revised May 24, 2007; accepted June 29, 2007. Reprints: E. Albert Reece, MD, PhD, MBA, Office of the Dean, School of Medicine, University of Maryland, 655 West Baltimore St, Room 14-029, Baltimore, MD 21201. [email protected] 0002-9378/$34.00 © 2008 Mosby, Inc. All rights reserved. doi: 10.1016/j.ajog.2007.06.076
Obesity poses a serious health challenge. In addition to being a serious disease in its own right, obesity has also added fuel to a multitude of other diseases. An increasing body of evidence indicates that obesity does indeed beget obesity: children of obese parents have a strong tendency toward obesity and a multitude of resultant complications. Although preventive measures are, in many cases, relatively straightforward and simple, the vicious cycle of obesity is rapidly spiraling upward as this tendency is passed from parent to child. Judging by the speed of its progression and the toll it is taking, obesity can truly be called America’s newest and fastest-growing epidemic. Key words: complications, obesity, pregnancy and outcomes
age 18 years in both men and women10,11 and with excessive abdominal girth.10,12 Statistics show that among people diagnosed with type 2 diabetes, 67% have a BMI 27 kg/m2 or greater, and 46% have a BMI ⱖ30 kg/m2.13 However, the Nurses’ Health Study recently found that the risk of developing type 2 diabetes increases by approximately 25% for each additional BMI unit over a BMI as low as 22 kg/m2.11 Additionally, it was recently estimated that 27% of new cases of diabetes could be attributed to an adulthood weight gain of 11 pounds or more.14 Current statistics indicate that an estimated 70% of diabetes risk in the United States can be attributed to excess weight.13 In 2005, almost 21 million people in the United States were known to have diabetes, and of those, 1.5 million were newly diagnosed adults older than the age of 20.15 More significantly, about 17 million of those people had type 2 diabetes, accounting for more than 80% of diabetes cases.15 The economic impact of such a widespread illness is profound (Table 1). In 2002, the total annual cost of type 1 and type 2 diabetes was $132 billion, with $92 billion in direct medical expenditures and $40 billion in indirect costs.16 Such expenses include, but are not limited to, hospitalization, physician office visits, emergency room visits, prescription drugs, and loss of productivity.17
Obesity and pregnancy Obesity and its resultant diseases are not a concern only for the adult population. As we witness a growing trend toward overweight and obesity among our children, we also see far too many of them faced with the burden of type 2 diabetes and other complications. There is mounting evidence that these children may be predisposed to obesity and its related complications, even before birth. Studies indicate that the intrauterine environment affects the incidence of obesity, and that as a direct result of maternal obesity, the child faces a life-long risk of obesity17-19 and related health problems. In fact, 29-33% of infants of obese mothers are in the 90th percentile for age, and the child of an overweight mother is 3 times more likely to be overweight by age 7.20 Thus, it is clear that obesity is of special concern for women who are pregnant or who plan to become pregnant. Overweight and obesity have long been known to complicate pregnancy and are associated with increased morbidity for both the mother and the child. Both of these conditions increase the chances for such serious and potentially life-threatening complications of pregnancy as pregnancy-associated hypertension and preeclampsia, as well as anesthesia-related risks, should the woman undergo surgery.17,18,21,22 Nearly half of women of child-bearing age are either over-
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FIGURE 1
TABLE 1
Obesity: a vicious cycle
Total cost of diabetes, 2002
Hypertension High Cholesterol
Cost component
Diabetes Mellitus
Components’ proportion of total cost (%)*
Health care expenditures
91,861
70
Institutional care
54,215
41
Hospital inpatient care
40,337
31
.....................................................................................................................................................................................................................................
Coronary Heart Disease Cancer
Total cost attributable to diabetes (millions of dollars)
..................................................................................................................................................................................................................................... .....................................................................................................................................................................................................................................
OBESITY
Nursing home care
13,878
11
20,130
15
10,033
8
2162
2
.............................................................................................................................................................................................................................................. Stroke
Outpatient care
.....................................................................................................................................................................................................................................
Physician office-based care
Gall Bladder Disease
..................................................................................................................................................................................................................................... Sleep Apnea
Osteoarthritis
Emergency care
.....................................................................................................................................................................................................................................
Ambulance services
146
0
Hospital outpatient care
3315
3
Home health care
3930
3
543
0
.....................................................................................................................................................................................................................................
Reece. Perspectives on obesity, pregnancy, and birth outcomes in the US. Am J Obstet Gynecol 2007.
..................................................................................................................................................................................................................................... .....................................................................................................................................................................................................................................
Hospice care
..............................................................................................................................................................................................................................................
weight or obese and must face these concerns.23 Obesity also frequently leads to delivery complications (Table 2). Studies show that both overweight and obese women are admitted earlier (based on cervical dilation assessment) to labor and delivery and have their labor induced and receive oxytocin more often, compared with normal-weight women.23 In addition, these women progress through labor more slowly than do normal-weight women: 7.9 hours for obese women, compared with 6.2 hours for normal-weight women.17 Observational studies show that obese women have up to a 2-fold increased risk for a cesarean delivery, compared with normal-weight women, and that the majority of these deliveries are performed during the first stage of labor and based on an indication of dystocia and fetal distress.23 Finally, macrosomia is common among the offspring of obese mothers, with infants of overweight and obese mothers being 60-100 g heavier than those of normal-weight women, thus increasing the risk of birth trauma.23 Perhaps one of the most significant risks an obese, pregnant woman may face is the likelihood of developing gestational diabetes mellitus (GDM). Pregnancy naturally induces insulin resistance,21 which in about 7% of pregnant women in the United States, leads to GDM17 (Figure 2). However, if the 24
Outpatient medication and supplies
17,516
13
Outpatient medication
5516
4
Insulin and delivery supplies
6991
5
Oral agents
5009
4
39,810
30
..................................................................................................................................................................................................................................... ..................................................................................................................................................................................................................................... .....................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................
Indirect costs because of lost productivity
.....................................................................................................................................................................................................................................
Lost work days
4503
3
.....................................................................................................................................................................................................................................
Restricted activity days
6256
5
21,558
16
7494
6
131,672
100
.....................................................................................................................................................................................................................................
Mortality
.....................................................................................................................................................................................................................................
Permanent disability
..............................................................................................................................................................................................................................................
Total cost
..............................................................................................................................................................................................................................................
* Cost component percentages do not necessarily add up to category totals because of rounding. Copyright © 2003 American Diabetes Association. From Diabetes Care®, vol. 26, 2003; 917-932. Reprinted with permission from The American Diabetes Association.
woman is obese, her risk of developing GDM is significantly increased.24 In a population-based cohort study (n ⫽ 96,801), the risk of GDM was increased 5.2-fold in obese women (BMI ⱖ30.0; odds ratio [OR], 5.2; 95% confidence interval [CI], 4.3-6.2), compared with women categorized as lean (BMI ⬍20.0; OR, 1.0) and normal-weight women (BMI 20.0-24.9; OR, 1.3; CI, 1.1-1.5).24 Whereas GDM generally lasts the duration of pregnancy, 5-10% of women who had GDM will continue to be diabetic (type 2), even after pregnancy. Overall, women with a history of GDM have a 20-50% chance of developing diabetes in the future25 (Table 3). The presence of GDM is associated with pregnancy and perinatal risks, such as spontaneous abor-
American Journal of Obstetrics & Gynecology JANUARY 2008
tion, neonatal hypoglycemia, respiratory distress syndrome, and stillbirth.17-19
The environmental connection The age-adjusted prevalence of obesity was 30.5% in 1999-2000, compared with 22.9% in 1988-1994 (P ⬍ .001).26 The prevalence of overweight also increased from 55.9% to 64.5% (P ⬍ .001) over the same time period (Figure 3).26 Approximately 15.3% of children aged 6-11 years and 15.5% of adolescents aged 12-19 years were overweight in 2000.27 Our environment is a major determinant of overweight and obesity. The current environment in the United States encourages consumption of energy and discourages expenditure of energy.28 A variety of highly palatable, calorie-dense
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TABLE 2
Intrapartum characteristics of term, nulliparous women, according to their prepregnancy body mass index (Pregnancy, Infection, and Nutrition Study, 1995-2002)
Cervical dilation at admission (cm)
Normal (BMI 19.8-26.0 kg/m2) (n ⴝ 297)
Overweight (BMI 26.1-29.0 kg/m2) (n ⴝ 115)
3.0 (1.0, 5.0)
2.5 (1.0, 6.0)
Pa .39
Obese (BMI >29.0 kg/m2) (n ⴝ 200)
Pb
2.0 (0.0, 5.0)
.03
................................................................................................................................................................................................................................................................................................................................................................................
Contractions present at admission
.47
.01
.......................................................................................................................................................................................................................................................................................................................................................................
Yes, regular
181 (60.9)
63 (54.8)
90 (45.0)
Every 1-5 min
165 (55.5)
57 (49.6)
78 (39.0)
Every 6-15 min
16 (5.4)
6 (5.2)
12 (6.0)
Yes but unknown frequency
13 (4.4)
4 (3.5)
10 (5.0)
Yes but irregular
31 (10.4)
9 (7.8)
30 (15.0)
No
67 (22.6)
35 (30.4)
68 (34.0)
5 (1.7)
4 (3.5)
2 (1.0)
....................................................................................................................................................................................................................................................................................................................................................................... ....................................................................................................................................................................................................................................................................................................................................................................... ....................................................................................................................................................................................................................................................................................................................................................................... ....................................................................................................................................................................................................................................................................................................................................................................... ....................................................................................................................................................................................................................................................................................................................................................................... .......................................................................................................................................................................................................................................................................................................................................................................
Unknown
................................................................................................................................................................................................................................................................................................................................................................................
Labor onset
⬍ .001
.22
.......................................................................................................................................................................................................................................................................................................................................................................
Spontaneous
205 (69.0)
69 (60.0)
106 (53.0)
Induction without cervical ripening
45 (15.2)
23 (20.0)
36 (18.0)
Induction with cervical ripening
47 (15.8)
.......................................................................................................................................................................................................................................................................................................................................................................
.......................................................................................................................................................................................................................................................................................................................................................................
23 (20.0)
58 (29.0)
................................................................................................................................................................................................................................................................................................................................................................................
Method of cervical ripening
.21
.11
.......................................................................................................................................................................................................................................................................................................................................................................
Foley bulb
23 (7.7)
15 (13.0)
38 (19.0)
Prostaglandins
24 (8.1)
8 (7.0)
20 (10.0)
Received oxytocin
167 (56.2)
79 (68.7)
.02
150 (75.0)
Cervical dilation at oxytocin administration (cm)
3.0 (1.0, 8.5)
3.0 (1.0, 8.5)
.98
3.0 (1.0, 7.0)
Received epidural analgesia
200 (67.3)
81 (70.4)
.64
142 (71.0)
.43
Cervical dilation at epidural analgesia placement (cm)
5.0 (3.0, 9.0)
5.0 (3.0, 9.0)
.70
5.0 (3.0, 8.0)
.72
....................................................................................................................................................................................................................................................................................................................................................................... ................................................................................................................................................................................................................................................................................................................................................................................
⬍ .001
................................................................................................................................................................................................................................................................................................................................................................................
.84
................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................
................................................................................................................................................................................................................................................................................................................................................................................
⬍.01
Method of membrane rupture
.41
.......................................................................................................................................................................................................................................................................................................................................................................
Spontaneous
133 (44.8)
35 (30.7)
83 (41.5)
Artificial
159 (53.5)
80 (69.3)
117 (58.5)
0 (0.0)
0 (0.0)
....................................................................................................................................................................................................................................................................................................................................................................... .......................................................................................................................................................................................................................................................................................................................................................................
Undetermined
5 (1.7)
................................................................................................................................................................................................................................................................................................................................................................................
Data are presented as n (percent) or median (10th, 90th percentiles; test or Wilcoxon rank sum test). 2
a
Comparison between normal weight and overweight women.
b
Comparison between normal weight and obese women.
Reprinted from Vahratian A, Zhang J, Troendle JF, Savitz DA, Siega-Riz AM. Maternal prepregnancy overweight and obesity and the pattern of labor progression in term nulliparous women. Obstet Gynecol 2004;104:943-51. With permission from Lippincott Williams & Wilkins.
food is available nearly everywhere in our country and is promoted by aggressive and sophisticated food marketing in the mass media, supermarkets, and restaurants. This is especially evident in fast food restaurants in which menu items are typically high in energy density. Cross-sectional and longitudinal data on self-reported fast food restaurant use per se and consumption of foods frequently sold at fast food restaurants (eg, ham-
burgers and french fries) have been shown to be positively associated with body weight.29 For many people, even when caloric intake is within recommended levels, physical activity is insufficient to offset consumption. Low levels of physical activity are associated with an increased risk of obesity,30 and our current environment tends to discourage physical activity.31 Mechanization lim-
its the amount of physical activity required to function in society, and for most people, the days are filled with sedentary routines consisting of sitting at work, sitting in traffic, and sitting in front of a television or a computer monitor. In a community-based study examining the relationship between television viewing and 3-year change in BMI, television viewing was positively associated with BMI among women.32
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TABLE 3
Estimated percent of women with gestational diabetes developing NIDDM or IGT after pregnancy BMI before index pregnancy
BMI before index pregnancy
Fasting plasma (mg/dL) during pregnancy
2 y after pregnancy, %
4 y after pregnancy, %
100
1.2
2.5
5.5
2.3
8.1
10.6
120
2.5
5.5
11.4
5.1
10.6
20.0
140
5.5
11.4
22.3
10.8
20.9
37.0
15
25
35
15
25
35
.............................................................................................................................................................................................................................................. .............................................................................................................................................................................................................................................. ..............................................................................................................................................................................................................................................
Risk of subsequent NIDDM or impaired glucose tolerance is calculated from a regression equation based on data from 350 former women with gestational diabetes retested at 0-10 years after their index pregnancy with a 75 g 2 h OGTT using National Diabetes Data Group criteria. IGT, impaired glucose tolerance; NIDDM, non–insulin-dependent diabetes mellitus; OGTT, oral glucose tolerance test. Adapted from Coustan DR, Carpenter MW, O’Sullivan PS, Carr SR. Gestational diabetes mellitus: predictors of subsequent disordered glucose metabolism. Am J. Obstet Gynecol 1993;168:1139-45. Reprinted from Diabetes’ in America. 2nd Ed. National Diabetes Data Group of the National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD.
Television viewing also increases the risk of being overweight to younger, preschool-aged children.33 Less than one-third of US adults get regular leisure time physical activity, and about 10% do no physical activity at all in their leisure time.34 The direct cost of physical inactivity may be as high as $24.3 billion.35 We face a daunting challenge that encompasses the reedu-
FIGURE 2
Cumulative incidence of diabetes in women with normal glucose tolerance or gestational diabetes during their index pregnancy
cation and retraining of an entire society if we are to end the spread of this diabetes epidemic.
A N ATIONAL C OMMITMENT What exactly would such a solution entail? In truth, our options are few, but the simple solutions are often the most effective. We must do the obvious, which is to teach people to improve the quality of their diets by eating more fruits and vegetables and fewer fats and calories. Individuals should be encouraged to increase their level of exercise, ideally to 30 minutes a day, 4-5 times a
week. As primary care practitioners, obstetrician-gynecologists are in an ideal position to emphasize the importance of these lifestyle changes to all our patients, not just those who are overweight or obese. Efforts should not, however, be limited to patient encounters. We must take our efforts farther than the examination room. We must exert our influence as medical professionals where it can be heard the most: among the food industry giants, insurance companies, and public education systems. We should encourage our government to support incentives, such as tax breaks, to the food industry for the promotion of fruits, vegetables, and whole grains, and for the development of low-calorie, low-fat, and low-cholesterol foods. We should encourage health insurance to provide premium breaks to those who exercise regularly and lead a healthy lifestyle Furthermore, we should insist that fitness programs are a required part of all primary, high school, and college education programs. Finally, employers, educators, and public officials must be mobilized to contribute to this effort. In addition, we must encourage and promote research designed to clarify and quantitate the contribution and the role of societal policies, procedures, laws, and other factors to the development of obesity.
FIGURE 3
Age-adjusted prevalence of overweight and obesity
Adapted from O’Sullivan JB. Subsequent morbidity among GDM women. Sutherland HW, Stowers JM eds. In: Carbohydrates Metabolism in Pregnancy and the Newborn. New York: Churchill Livington. 1984;174-180. Reprinted from Diabetes in America. 2nd Ed. National Diabetes Data Group of the National Institute of Diabetes and Digestive and Kidney Disease, National Institutes of Health, Bethesda, MD.
26
Adapted from CDC/NCHS, Health, United States, 2000 (Obtained from the National Institute of Diabetes and Digestive and Kidney Diseases Website [http://win.niddk.nih.gov/statistics/index.htm]) and the 1999-2000 NHANES study, available at http://www.cdc.gov/nchs/about/major/nhanes/nhanes99_00.htm.
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www.AJOG.org C ONCLUSION As the nation’s fastest growing epidemic, obesity is having devastating effects on multiple fronts: it exacerbates existing illnesses, increases the risk of developing others, and poses a severe health threat for generations to come. A highly visible case in point is diabetes mellitus. Studies have clearly documented the growing prevalence of this life-threatening disease as our society gains weight. The economic impact of diabetes alone is staggering, but even worse is the havoc it wreaks on patients’ quality of life as well as the very real potential for a diabetic mother to pass a tendency for the disease on to her children. As our future generations face increasing risks for the many major health problems linked to obesity, it becomes clear that we can no longer simply treat the symptoms as these diseases develop. We must diligently uproot the source of these problems: obesity caused by the unhealthy habits of an industrialized and f mechanized society. REFERENCES 1. Clinical Guidelines on the Identification, Evaluation, and Treatment of Overweight and Obesity in Adults—The Evidence Report. National Institutes of Health. Obes Res 1998;6:464. 2. Haffner SM, Mitchell BD, Hazuda HP, Stern MP. Greater influence of central distribution of adipose tissue on incidence of non-insulin-dependent diabetes in women than men. Am J Clin Nutr 1991;53:1312-7. 3. Cicuttini FM, Baker JR, Spector TD. The association of obesity with osteoarthritis of the hand and knee in women: a twin study. J Rheumatol 1996;23:1221-6. 4. Ritter MM, Schraudolph M, Richter WO, Herbert M, Wiebecke B, Schwandt P. [Obesity, heart failure and pulmonary insufficiency in a 26-year-old female]. Med Klin (Munich) 1990;85:371-5. 5. McGinnis JM, Foege WH. Actual causes of death in the United States. JAMA 1993; 270:2207-12.
6. Westlund K, Nicolaysen R. Ten-year mortality and morbidity related to serum cholesterol. A follow-up of 3.751 men aged 40-49. Scand J Clin Lab Invest Suppl 1972;127:1-24. 7. Lew EA, Garfinkel L. Variations in mortality by weight among 750,000 men and women. J Chronic Dis 1979;32:563-76. 8. Larsson B, Bjorntorp P, Tibblin G. The health consequences of moderate obesity. Int J Obes 1981;5:97-116. 9. Medalie JH, Papier C, Herman JB, et al. Diabetes mellitus among 10,000 adult men. I. Five-year incidence and associated variables. Isr J Med Sci 1974;10:681-97. 10. Chan JM, Rimm EB, Colditz GA, Stampfer MJ, Willett WC. Obesity, fat distribution, and weight gain as risk factors for clinical diabetes in men. Diabetes Care 1994;17:961-9. 11. Colditz GA, Willett WC, Rotnitzky A, Manson JE. Weight gain as a risk factor for clinical diabetes mellitus in women. Ann Intern Med 1995;122:481-6. 12. Sparrow D, Borkan GA, Gerzof SG, Wisniewski C, Silbert CK. Relationship of fat distribution to glucose tolerance. Results of computed tomography in male participants of the Normative Aging Study. Diabetes 1986;35: 411-5. 13. Maureen I. Harris. Personal communication to Susan Z. Yanovski, NIDDK/NIH; 1999. 14. Ford ES, Williamson DF, Liu S. Weight change and diabetes incidence: findings from a national cohort of US adults. Am J Epidemiol 1997;146:214-22. 15. Centers for Disease Control and Prevention. National diabetes fact sheet: general information and national estimates on diabetes in the United States, 2000. Atlanta, GA: US Department of Health and Human Services, Centers for Disease Control and Prevention; 2002. 16. American Diabetes Association. Diabetes Care 2003;26:917-32. 17. Diabetes in America, 2nd ed. NIH publication no. 95-1468. Bethesda (MD): National Diabetes Data Group, National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases; 1995. 18. Prentice A, Goldberg G. Maternal obesity increases congenital malformations. Nutr Rev 1996;54:146-50. 19. Cnattingius S, Bergstrom R, Lipworth L, Kramer MS. Prepregnancy weight and the risk of adverse pregnancy outcomes. N Engl J Med 1998;338:147-52. 20. Salsberry PJ, Reagan PB. Dynamics of early childhood overweight. Pediatrics 2005; 116:1329-38.
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21. American Diabetes Association. Gestational diabetes mellitus (position statement). Diabetes Care 2004;27(Suppl 1):S88-90. 22. Johnson SR, Kolberg BH, Varner MW, Railsback LD. Maternal obesity and pregnancy. Surg Gynecol Obstet 1987;164:431-7. 23. Vahratian A, Zhang J, Troendle JF, Savitz DA, Siega-Riz AM. Maternal prepregnancy overweight and obesity and the pattern of labor progression in term nulliparous women. Obstet Gynecol 2004;104:943-51. 24. Baeten JM, Bukusi EA, Lambe M. Pregnancy complications and outcomes among overweight and obese nulliparous women. Am J Public Health 2001;91:436-40. 25. National Institute of Diabetes and Digestive and Kidney Diseases. National diabetes fact sheet: general information and national estimates on diabetes in the United States. Bethesda (MD): National Institute of Diabetes and Digestive and Kidney Diseases; 2005. 26. Flegal KM, Carroll MD, Ogden CL, Johnson CL. Prevalence and trends in obesity among US adults, 1999-2000. JAMA 2002;288:1723-7. 27. National Institute of Diabetes and Digestive and Kidney Diseases. Diabetes Prevention Program Meeting Summary. August 8, 2001. Bethesda, MD: Diabetes Mellitus Interagency Coordinating Committee (DMICC). 28. Hill JO, Wyatt HR, Reed GW, Peters JC. Obesity and the environment: where do we go from here? Science 2003;299:853-5. 29. Jeffery RW, French SA. Epidemic obesity in the United States: are fast foods and television viewing contributing? Am J Public Health 1998;88:277-80. 30. US Department of Health and Human Services. Physical activity and health: a report of the Surgeon General. Atlanta (GA): US Department of Health and Human Services; 1996. 31. Hill JO, Peters JC. Environmental contributions to the obesity epidemic. Science 1998; 280:1371-4. 32. Crawford DA, Jeffery RW, French SA. Television viewing, physical inactivity and obesity. Int J Obes Relat Metab Disord 1999;23:437-40. 33. Dennison BA, Erb TA, Jenkins PL. Television viewing and television in bedroom associated with overweight risk among low-income preschool children. Pediatrics 2002;109:1028-35. 34. Barnes MA, Schoenborn CA. Physical activity among adults: United States, 2000. National Center for Health Statistics. Adv Data 2003;333 Y-6. DHHS Publication No. 20031250, 03-0234 (4/03). 35. Colditz G. Economic costs of obesity and inactivity. Med Sci Sports Exerc 1999;31(11 Suppl):S663-7.
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