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ORIGINAL RESEARCH |
From the Department of Medicine, Division of Preventive Medicine, and Endocrine-Hypertension Division, Brigham and Women’s Hospital; Department of Medicine and Renal Unit, Massachusetts General Hospital; Departments of Nutrition and Epidemiology, Harvard School of Public Health and Harvard Medical School, Boston, Massachusetts.
Address reprint requests to: Ravi Thadhani, MD, MPH 55 Fruit Street, Founders 036 Boston, MA 02114 E-mail: thadhani.ravi{at}mgh.harvard.edu
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Abstract |
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Methods: We studied 15,262 women who gave birth between 1991 and 1995. Pregravid exposures including BMI and self-reported history of elevated cholesterol were ascertained by biennial mailed questionnaires. Gestational hypertension or preeclampsia was confirmed by medical record review according to standard criteria. Proportional hazards analysis was used to adjust for potential confounding variables.
Results: We confirmed 216 cases of gestational hypertension and 86 cases of preeclampsia. The risk of gestational hypertension increased as pregravid BMI increased (P < .01). Compared with women with a pregravid BMI of 21–22.9 kg/m2, the relative risk (RR) of gestational hypertension was 1.6 (95% confidence interval [CI] 1.0, 2.3) for women with BMI of 23–24.9 kg/m2, 2.0 (95% CI 1.3, 3.0) for BMI 25–29.9 kg/m2, and 2.6 (95% CI 1.6, 4.4) for BMI over 30 kg/m2. Leaner women (BMI less than 21 kg/m2) had a reduced risk (RR 0.7, 95% CI 0.4, 1.0). For preeclampsia, the RR of women with pregravid BMI over 30 kg/m2 was 2.1 (95% CI 1.0, 4.6) (P for trend 0.09). A history of elevated cholesterol was not associated with the risk of gestational hypertension (RR 0.9, 95% CI, 0.6, 1.4). In contrast, the RR of preeclampsia in women with a history of elevated cholesterol was 2.0 (95% CI 1.2, 3.3).
Conclusion: Pregravid BMI and hypercholesterolemia could identify women at higher risk for hypertensive disorders during pregnancy.
Hypertensive disorders of pregnancy affect 5–10% of all pregnancies worldwide and cause substantial maternal and perinatal morbidity and mortality.1–3 Women with preeclampsia are two to three times more likely to have a cesarean delivery compared with normotensive women and have longer hospital stays even after accounting for the type of delivery.4 Interventions including use of antihypertensive treatment early in pregnancy have not convincingly demonstrated a benefit,5–9 thus focus has shifted to risk factors present before pregnancy with the goal of prevention.
Previous studies examining pregravid risk factors suggest that obese women have a two-fold to three-fold higher risk of developing hypertensive disorders of pregnancy.10–13 Investigators have postulated that hypertension during pregnancy occurs because of an increase in cardiac output11 and higher sympathetic tone (
Gans RO, Dekker GA. Preeclampsia—a state of sympathetic overactivity. N Engl J Med 1997;336: 1326–7. Letter.
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Materials and Methods |
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Women who reported either pregnancy-related high blood pressure (BP) or toxemia-preeclampsia of pregnancy on the biennial questionnaires in 1993 or 1995 were sent a supplementary questionnaire to confirm their self-report and to request permission to obtain medical records. Prenatal records were used to determine whether specific criteria for gestational hypertension or preeclampsia were fulfilled.19 The criteria for gestational hypertension after the 20th week of pregnancy are (1) a baseline systolic BP less than 140 mmHg and a systolic increase of more than 30 mmHg on two occasions; (2) a baseline diastolic BP less than 90 mmHg and a diastolic increase of more than 15 mmHg on two occasions; and (3) urinalysis data demonstrating less than or equal to 1 + proteinuria. The criteria for preeclampsia are an increase in BP as defined for gestational hypertension and new-onset of at least 2 + protein by urine dipstick or at least 300 mg of urine protein per 24 hours, in the absence of urinary tract infection. In addition to these criteria, we also required all cases to have an absolute systolic BP greater than 140 mmHg or diastolic BP greater than 90 mmHg, as in previous studies.6,7,12 Furthermore, like other investigators6,20 we chose at least 2 + protein by dipstick test to diagnose preeclampsia because of the high false-positive rate when 1 + is used as the cut-point.21
During normal pregnancy, BP decreases and reaches a nadir by the end of the second trimester.19 Therefore, a woman with undiagnosed chronic hypertension initially examined in the second trimester might be mistakenly considered normotensive.22,23 Thus, medical records were considered eligible for review only when baseline BP measurements and urinalysis results were documented during the first trimester.3 This protocol excluded women with undiagnosed chronic hypertension or preexisting proteinuria who might have been diagnosed at their first-trimester prenatal visit. Blood pressure and urinalysis during labor or at delivery were not considered.
Of the 15,827 women who remained eligible for the study, 501 (3.2%) women who self-reported pregnancy-related high BP and 366 (2.3%) who self-reported toxemia-preeclampsia were sent a supplementary questionnaire. There were 246 women who either denied permission to obtain medical records or for whom records were incomplete (despite three requests to their physicians); these women were excluded from the analysis. Of the remaining 621, the diagnosis of gestational hypertension was confirmed in 216 women (63% of eligible women who reported pregnancy-related hypertension with complete medical records) and preeclampsia was confirmed in 86 (40% of the eligible women who reported preeclampsia with complete medical records). Women who reported preeclampsia but who only met the criteria for gestational hypertension were included in the latter group, and women who did not meet the criteria for either disorder (n = 319) were excluded from the analysis. Thus, 15,262 women remained in the study: 14,960 noncases, 216 women with gestational hypertension, and 86 women with preeclampsia.
Self-reported baseline information in 1989 included age, weight, height, serum cholesterol levels, smoking habits, parity, family history of hypertension, history of chronic hypertension, and history of preeclampsia. Information on BMI, parity, preeclampsia, pregnancy and non-pregnancy-related hypertension, elevated cholesterol, diabetes, and other medical conditions was updated every 2 years.
Body mass index was calculated as weight in kilograms divided by the square of height in meters. In Nurses’ Health Study I, self-reported weights were highly correlated with actual measurements (r = 0.96).24 A validation study of recalled weight at age 18 years in Nurses’ Health Study II compared recalled weight with records from physical examinations conducted at college or nursing school entrance. The correlation between recalled and measured past weight was 0.87 (P < .01); the correlation for BMI at age 18 was 0.84 (P < .01).25 Self-reported BMI was shown previously in this cohort to be an important predictor of gestational diabetes.26
In 1989 and at every follow-up mailing, participants were asked to report any history of elevated cholesterol. Of the 15,262 women in this study, in 1989, 9483 (62%) reported their most recent serum cholesterol level if checked within the past 2 years (11 categories). Of these, 1237 (13%) reported a history of elevated cholesterol in 1989. Ninety percent of women who did not report a history of elevated cholesterol reported a serum cholesterol level less than 200 mg/dL, and 97% reported a level less than 220 mg/dL. Of 1237 women who reported a history of elevated cholesterol, 89% reported a serum level over 180 mg/dL, and 77% reported a serum level over 200 mg/dL. Of 5779 women who did not report a serum level in 1989, only 0.5% concomitantly reported a history of elevated cholesterol. Self-reported history of elevated cholesterol was previously shown in Nurses’ Health Study I to be associated with subsequent myocardial infarction.27
Follow-up time was divided into two periods, from January 1991 through June 1993, and July 1993 through December 1995. Women with at least one singleton pregnancy lasting 6 months or more during either time period were included in the analyses for the respective period. Exposures were updated at the start of each time period and analyzed. Because pregnancy can influence certain exposures, women who were already pregnant at the start of a time period were assigned their exposure status from the previous period.
Relative risk (RR) (cumulative incidence among women in a category of exposure divided by the corresponding incidence in the comparison category) was used as the primary measure of association. Age-adjusted risks were calculated after stratification according to 5-year age categories. The Mantel extension test was used to evaluate linear trends across categories of BMI.28 In this test, the smaller the P value, the more likely the null hypothesis (that the association is horizontal and not a linear trend) is false. Proportional-hazards analyses were performed to adjust simultaneously for multiple potential confounding variables. Variables included in the models were age (three categories), BMI (less than 21 kg/m2, 21 to 22.9 kg/m2, 23 to 24.9 kg/m2, 25 to 29.9 kg/m2, over 30 kg/m2, and missing), parity (nulliparous, multiparous, missing), smoking (never, past, current, missing), diabetes (non-gestational, gestational), family history of hypertension (maternal, paternal), and history of elevated cholesterol. For all RR, we calculated 95% confidence intervals (CI). All P values were two tailed.
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. The mean ages of the groups were similar. The mean pregravid BMI was higher in women who had gestational hypertension, compared with women who did not (24.7 ± 4.7 kg/m2 compared with 23.2 ± 4.0 kg/m2, respectively, P < .01). In contrast, the mean pregravid BMI did not differ significantly between women who had preeclampsia and those who did not (23.8 ± 4.2 kg/m2 compared with 23.2 ± 4.0 kg/m2, respectively, P = .16). The frequency of reported elevated cholesterol was much higher in women who had preeclampsia compared with noncases (P < .01). Women with either hypertensive disorder of pregnancy were more likely to be nulliparous compared with noncases (67% compared with 19%, respectively, P < .01). Finally, the pregravid smoking status of women did not differ between groups.
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. The RR of developing gestational hypertension increased as pregravid BMI increased (P for trend < .01). Compared with women who had a BMI of 21–22.9 kg/m2, the RR for gestational hypertension among women in the highest category of BMI (over 30 kg/m2) was 2.6 (95% CI 1.6, 4.4). After adjusting for parity, the magnitude of the association between BMI and gestational hypertension was higher, with the RR increasing from 2.2 to 2.6. Further adjustment did not change the RR.
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Discussion |
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Women with chronic hypertension are at increased risk of developing superimposed preeclampsia.2,19 Because chronic hypertension is associated with obesity, previous studies linking obesity with preeclampsia might have been confounded by inclusion of women with chronic hypertension.2,29 Previous studies excluding women with chronic hypertension infrequently examined first-trimester prenatal records.30,31 Blood pressure during pregnancy naturally decreases, reaching a nadir by the end of the second trimester; thus a woman with undiagnosed chronic hypertension initially examined in the second trimester could mistakenly be labeled as normotensive.22,23 We excluded all women who reported a history of chronic hypertension, and all potential cases for whom we did not have normal baseline BP measurements documented in the first trimester. Furthermore, all the women in our analysis had a screening physical examination before their pregnancy.
Misclassification cannot be excluded in previous studies that defined outcomes by International Classification of Disease codes or birth certificate data.1,4,30 When studies were unable to distinguish women with gestational hypertension from women with preeclampsia,30,32 mixing the two groups might have prevented identification of distinct risk factors. It remains controversial whether gestational hypertension and preeclampsia are different diseases.2,3 Our results and those of other studies17,18,33,34 support the notion that the pathogenesis of preeclampsia differs from that of isolated gestational hypertension.
Given the difficulty of characterizing a large group of women before pregnancy and prospectively following them during pregnancy, it is not surprising that most studies examining pregravid exposures collected this information retrospectively.11,13 In a case-control study, Eskenazi et al13 abstracted pregravid exposures from medical charts of 139 women who developed preeclampsia and a comparable number of controls. Risk factors associated with preeclampsia included high BMI (over 25.8 kg/m2) and nulliparity. These investigators acknowledged that a cohort study was needed to determine whether the risk factors they identified would prospectively predict preeclampsia.
Previous prospective studies of preeclampsia examined risk factors in women initially enrolled in prevention trials.10,12,20 Women in most studies had a mean age of 20 to 21 years, were enrolled at a mean gestational age of 17 to 20 weeks, and were nulliparous.10,20 The results for obesity were consistent. Sibai et al10 found a higher risk of preeclampsia in women with a substantially elevated BMI (26 to 34.9 kg/m2, and over 35 kg/m2) measured at the time of randomization. Our study extends the results of these previous studies by including narrower BMI categories than used in previous studies,14,35 women in a broader age group, and gestational hypertension and preeclampsia as distinct outcomes.
Elevated BMI might contribute to hypertensive disorders of pregnancy through various mechanisms. Nonpregnant obese women have an expanded blood volume and cardiac output,36 which could increase even more during pregnancy.11 Obesity might also act through insulin resistance or increased sympathetic activity, both of which have been associated with hypertensive disorders of pregnancy ( Ganz RO. N Engl J Med 1997;336:1326–7).36,37 Investigators have also postulated that abnormal lipid metabolism and hyperlipidemia, which are often associated with obesity, are responsible for the physiologic alterations of vasoactive mediators leading to hypertension during pregnancy.11,14,38
In our study, higher BMI was significantly associated with gestational hypertension even after adjusting for elevated cholesterol. Compared with the age-adjusted analysis, multivariate analysis demonstrated further increases in the RR in women in the two highest BMI categories. This change was due to negative confounding by parity, which is consistent with previous reports that found that multiparous women have a lower risk of hypertensive disorders of pregnancy13 but have a higher BMI compared with nulliparous women.39 Our data support the latter observation, with the mean BMI of multiparous women of 23.3 ± 4.0 kg/m2 compared with 22.6 ± 3.7 kg/m2 among nulliparous women (P < .01). Furthermore, the increased risk of preeclampsia in women with a history of elevated cholesterol was independent of BMI. Therefore, the previously held belief that obesity is associated with either gestational hypertension or preeclampsia through its association with elevated lipids is not supported by these data. The finding that elevated cholesterol is associated with preeclampsia but not gestational hypertension is consistent with previous data demonstrating abnormal lipid metabolism in women with preeclampsia but not women with isolated gestational hypertension.16,17,40
Several lines of evidence support the association between abnormal lipid metabolism and the systemic manifestations of preeclampsia. First, women with preeclampsia have higher serum lipid levels compared with pregnant controls.17,40–43 In one recent study, first-trimester serum total cholesterol levels were significantly elevated in the 11 women who subsequently developed preeclampsia but not in the 26 women who developed isolated pregnancy-induced hypertension.16 Second, placental vessels of affected women had atherosclerotic-like changes, including deposition of fibrinoid material and foam cells.18,44 Third, byproducts of lipid peroxidation are elevated in women with preeclampsia,45,46 and these byproducts might be associated with endothelial cell damage and vasoconstriction.45,47 Levels of endothelin, a potent vasoconstrictor, are also higher in these women,48 and elevated serum cholesterol is associated with elevated endothelin activity in animals.49 Finally, elevated lipid level is a component of insulin resistance syndrome,50 and insulin resistance is associated with preeclampsia.51,52 Therefore, elevated cholesterol level before pregnancy could render a woman susceptible to the deleterious systemic manifestations of preeclampsia during pregnancy.
Although normal pregnancy is a state of hyperlipidemia,41 measurements obtained during pregnancy suggest women with preeclampsia have an increase in lipids that is 1.5 to 2 times the normal elevation.17,38,41,45 Our study extends this observation to a time period before pregnancy. We adjusted for parity, which might otherwise confound the association, as other studies have noted higher serum lipids in multiparous women compared with nulliparous women.16,39 In certain studies, the relevant lipid component was the triglycerides,17,41,45 and in other studies it was the total serum cholesterol.16,53 We did not have information about specific subfractions of serum lipids.
The potential limitations of these data deserve mention. We did not have information on postulated risk factors during pregnancy, such as working conditions and job stress, but these factors are unlikely to be related directly to pregravid BMI and serum cholesterol. Physiologic changes of preeclampsia are evident early in gestation,18,34,54 thus any effect of etiologic factors would likely have to occur before or early in pregnancy. Therefore, we chose to examine pregravid risk factors. We could not assess the effect of race because 94% of participants in Nurses’ Health Study II are white. In addition, we could not assess the effect of diabetes because few women had this disorder. A history of elevated cholesterol was not reported by all women who developed preeclampsia. Elevated cholesterol might be one of several components involved in the pathogenesis of preeclampsia, and its presence might predispose only those women who are otherwise susceptible. We did not have information on which women had their blood cholesterol checked before the start of the study. Therefore, some women not answering "yes" to the question of "history of elevated blood cholesterol" could have had an elevated blood cholesterol. However, this number is likely to be low given that only 18% of women who knew their serum level reported a level over 200 mg/dL. Furthermore, substantial differential misclassification in answering the question of a history of elevated cholesterol was unlikely; restricting the analyses to women who reported a serum cholesterol value in 1989 (n = 9483) revealed similar RR for all exposures. Finally, we could not examine the effect of prenatal care on the outcomes. We excluded women with a history of chronic hypertension and hypertensive disorder of pregnancy before 1991 to reduce potential surveillance bias during prenatal care. Medical records were not available for all self-reported cases, thus we could not determine absolute incidence rates of either gestational hypertension or preeclampsia. Using self-reported cases (and not just those confirmed by medical record review) and restricting the analysis to nulliparous women, the incidence of gestational hypertension and preeclampsia in our cohort was 6.0% and 5.9%, respectively, which is within the range of reported incidence among nulliparous women enrolled in recent clinical trials.2,6,7
To determine whether bias was introduced by excluding self-reported cases that were not confirmed, we analyzed the data using all self-reported cases (gestational hypertension, n = 501; preeclampsia, n = 366). For women with a BMI over 30, the RR for self-reported gestational hypertension was 4.0 (95% CI 2.8, 5.6) compared with 2.6 (95% CI 1.6, 4.4) when only the confirmed cases were included. The RR of developing preeclampsia was 2.4 (95% CI 1.6, 3.5) compared with 2.1 (95% CI 1.0, 4.6) for confirmed cases. One explanation for the somewhat higher risks when all self-reported cases were used could result from the strict criteria we used to confirm cases. We required not only an absolute threshold for BP (over 140 mmHg systolic or over 90 mmHg diastolic), but also a change from baseline of over 30 mmHg systolic or over 15 mmHg diastolic on two occasions. Because a high BMI is associated with high BP, a woman with a high BMI would require a smaller increase in BP to cross the threshold of 140/90 mmHg and thus would be more likely to be diagnosed with hypertension. However, such a woman would have met our definition only if the increase in her BP also met our change in BP criterion. Another possible explanation is related to the size of the BP cuff: women with a high BMI would be more likely to have a higher measured BP if a small cuff size were used. Among women with elevated cholesterol, the relative risk for self-reported preeclampsia was 1.5 (95% CI 1.1, 1.9) compared with 2.0 (95% CI 1.2, 3.3) for confirmed cases. The attenuation of the RR with self-reported cases was likely due to the inclusion of women who did not have preeclampsia.
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Footnotes |
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Supported by the American Kidney Fund-Amgen Inc. Clinical Scientist in Nephrology Award (RT), and research grants K08HL03804-01 and CA50385 from the National Institutes of Health, Bethesda, Maryland.
Received December 14, 1998. Received in revised form March 22, 1999. Accepted March 25, 1999.
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J. M. Roberts and H. Gammill Insulin Resistance in Preeclampsia Hypertension, March 1, 2006; 47(3): 341 - 342. [Full Text] [PDF]
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 L. M. Bodnar, R. B. Ness, G. F. Harger, and J. M. Roberts Inflammation and Triglycerides Partially Mediate the Effect of Prepregnancy Body Mass Index on the Risk of Preeclampsia Am. J. Epidemiol., December 15, 2005; 162(12): 1198 - 1206. [Abstract] [Full Text] [PDF]
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J. M. Roberts and H. S. Gammill Preeclampsia: Recent Insights Hypertension, December 1, 2005; 46(6): 1243 - 1249. [Abstract] [Full Text] [PDF]
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K. Duckitt and D. Harrington Risk factors for pre-eclampsia at antenatal booking: systematic review of controlled studies BMJ, March 12, 2005; 330(7491): 565. [Abstract] [Full Text] [PDF]
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 M. Wolf, A. Shah, R. Jimenez-Kimble, J. Sauk, J. L. Ecker, and R. Thadhani Differential Risk of Hypertensive Disorders of Pregnancy among Hispanic Women J. Am. Soc. Nephrol., May 1, 2004; 15(5): 1330 - 1338. [Abstract] [Full Text] [PDF]
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R. Thadhani, J. L. Ecker, W. P. Mutter, M. Wolf, K. V. Smirnakis, V. P. Sukhatme, R. J. Levine, and S. A. Karumanchi Insulin Resistance and Alterations in Angiogenesis: Additive Insults That May Lead to Preeclampsia Hypertension, May 1, 2004; 43(5): 988 - 992. [Abstract] [Full Text] [PDF]
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 R. Thadhani, W. P. Mutter, M. Wolf, R. J. Levine, R. N. Taylor, V. P. Sukhatme, J. Ecker, and S. A. Karumanchi First Trimester Placental Growth Factor and Soluble Fms-Like Tyrosine Kinase 1 and Risk for Preeclampsia J. Clin. Endocrinol. Metab., February 1, 2004; 89(2): 770 - 775. [Abstract] [Full Text] [PDF]
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 R. B. Ness, N. Markovic, D. Bass, G. Harger, and J. M. Roberts Family History of Hypertension, Heart Disease, and Stroke Among Women Who Develop Hypertension in Pregnancy Obstet. Gynecol., December 1, 2003; 102(6): 1366 - 1371. [Abstract] [Full Text] [PDF]
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E. W. Seely and C. G. Solomon Insulin Resistance and Its Potential Role in Pregnancy-Induced Hypertension J. Clin. Endocrinol. Metab., June 1, 2003; 88(6): 2393 - 2398. [Abstract] [Full Text] [PDF]
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O. Basso, C. R. Weinberg, D. D. Baird, A. J. Wilcox, and J. Olsen Subfecundity as a Correlate of Preeclampsia: A Study within the Danish National Birth Cohort Am. J. Epidemiol., February 1, 2003; 157(3): 195 - 202. [Abstract] [Full Text] [PDF]
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M. Wolf, L. Sandler, R. Jimenez-Kimble, A. Shah, J. L. Ecker, and R. Thadhani Insulin Resistance But Not Inflammation Is Associated With Gestational Hypertension Hypertension, December 1, 2002; 40(6): 886 - 891. [Abstract] [Full Text] [PDF]
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I. Thorsdottir, J. E. Torfadottir, B. E. Birgisdottir, and R. T. Geirsson Weight Gain in Women of Normal Weight Before Pregnancy: Complications in Pregnancy or Delivery and Birth Outcome Obstet. Gynecol., May 1, 2002; 99(5): 799 - 806. [Abstract] [Full Text] [PDF]
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M. Wolf, L. Sandler, K. Munoz, K. Hsu, J. L. Ecker, and R. Thadhani First Trimester Insulin Resistance and Subsequent Preeclampsia: A Prospective Study J. Clin. Endocrinol. Metab., April 1, 2002; 87(4): 1563 - 1568. [Abstract] [Full Text] [PDF]
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M. Wolf, E. Kettyle, L. Sandler, J. L. Ecker, J. Roberts, and R. Thadhani Obesity and Preeclampsia: The Potential Role of Inflammation Obstet. Gynecol., November 1, 2001; 98(5): 757 - 762. [Abstract] [Full Text] [PDF]
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R. THADHANI, J. L. ECKER, E. KETTYLE, L. SANDLER, and F. D. FRIGOLETTO Jr Pulse Pressure and Risk of Preeclampsia: A Prospective Study Obstet. Gynecol., April 1, 2001; 97(4): 515 - 520. [Abstract] [Full Text] [PDF]
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N. SATTAR, P. CLARK, A. HOLMES, M. E. J. LEAN, I. WALKER, and I. A. GREER Antenatal Waist Circumference and Hypertension Risk Obstet. Gynecol., February 1, 2001; 97(2): 268 - 271. [Abstract] [Full Text] [PDF]
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C. G. Solomon and E. W. Seely Brief Review: Hypertension in Pregnancy : A Manifestation of the Insulin Resistance Syndrome? Hypertension, February 1, 2001; 37(2): 232 - 239. [Abstract] [Full Text] [PDF]
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