Abstract
Objective
To examine the association between (GWG) and epithelial ovarian cancer (EOC).
Methods
We compared GWG between 670 incident EOC cases and 1,551 community controls from a population-based, case–control study conducted in Pennsylvania, Ohio, and New York from 2003 to 2008. Multivariable unconditional logistic regression was used to calculate odds ratios (ORs) and 95% confidence intervals (CIs) associated with GWG adjusting for potential confounders. To explore the potential effect of maternal long-term weight retention after childbearing, we restricted analyses to women who began their childbearing years as normal/underweight and examined differences in EOC risk between those who were normal/underweight versus those who were overweight/obese at study baseline reference date.
Results
Average GWG per full-term pregnancy did not differ between cases and controls. Among women who were normal/underweight at study baseline, greater average GWG was not associated with EOC (OR = 0.9, 0.8, 0.7 for quartiles 2, 3 and 4 of GWG gain, respectively, compared to quartile 1). In contrast, among women who were overweight/obese at study baseline, greater average GWG was positively associated with EOC (OR = 1.4, 1.8, 1.2, for quartiles 2, 3, and 4 compared to quartile 1; interaction p = 0.04).
Conclusion
We posit that maternal post-partum weight retention and not gestational weight gain itself among normal/underweight women may impact subsequent risk of EOC. If our hypothesis is supported in other studies designed to assess this question directly, then counseling women on the importance of healthy weight management after a pregnancy could provide another means to help women reduce their risk of this often-fatal malignancy.
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Introduction
Gestational weight gain (GWG), defined as the weight a woman gains during pregnancy, impacts both maternal and fetal health [1, 2]. The Institute of Medicine (IOM) has developed guidelines based on a woman’s pre-pregnancy body mass index (BMI) in order to promote optimal health in both the mother and child [3]. GWG outside IOM guidelines, especially too much weight gain, has negative maternal consequences, including maternal weight retention and future maternal obesity [4,5,6,7,8,9,10,11,12]. Excessive GWG may thus give rise to future obesity-related health conditions in women.
Epithelial ovarian cancer (EOC) is the sixth most common cancer worldwide and the most lethal of all gynecologic malignancies [13]. This high fatality rate coupled with the lack of well-established prevention strategies (beyond oral contraceptive use and bilateral salpingo oophorectomy) makes it critical to identify modifiable risk factors for the disease [14]. Body mass index (BMI) may be one such factor, as studies suggest that increasing BMI may be associated with increasing EOC risk [15,16,17,18,19,20], and several cancer groups, including the World Cancer Research Fund (WCRF) [21], the US National Cancer Institute (NCI) [22], and International Agency for Research on Cancer (IARC) [23], consider being overweight or obese an ovarian cancer risk factor. It is possible, then, that GWG, which has the possibility of leading to long-term maternal weight retention [4,5,6,7,8,9,10,11,12] and subsequent increased BMI, may impact EOC risk.
To determine whether GWG is associated with risk of EOC, we used data from the Hormone and Ovarian cancer PrEdiction (HOPE) Study, a large, population-based, case–control study of EOC designed to assess the relationship between hormone-related factors (such as pregnancy) and EOC risk. Because excessive GWG is associated with subsequent maternal weight retention [4,5,6,7,8,9,10,11,12] and because increasing BMI may be associated with increased EOC risk [15,16,17,18,19,20], we hypothesized that greater GWG would be associated with increasing EOC risk. Although there have been studies examining the association between non-pregnancy weight-gain and EOC [15,16,17,18,19,20] to our knowledge there have been no previous studies examining the GWG–EOC association. In addition, the paucity of ovarian cancer studies that collected information on GWG provided the HOPE Study a unique opportunity to explore the GWG–EOC association.
Material and methods
Subjects
Details of the HOPE Study have been described elsewhere [24, 25]. Briefly, cases were women age 18 and over diagnosed within 9 months of study enrollment with incident epithelial ovarian, peritoneal, or fallopian tube cancer (EOC) from 2003 to 2008 in the contiguous regions of western Pennsylvania, eastern Ohio and southwestern New York. Controls were identified through random-digit dialing and were frequency matched to cases by 5-year age groups and 3-digit telephone exchanges. Women without at least one intact ovary were excluded from the study. A total of 902 cases and 1,802 controls participated in the study. Institutional Review Board approval was obtained from all hospitals from which cases were identified and from the University of Pittsburgh.
Data collection and exposure assessment
Both cases and controls underwent a standardized, 2-h in-person interview by trained interviewers. During the in-person interviews, detailed information on reproductive, medical, and demographic data from birth until a study baseline reference date was obtained. The study baseline reference date was calculated as 9 months prior to diagnosis for cases and 9 months prior to interview for controls to ensure that exposures occurred before ovarian cancer diagnosis in cases and within a similar time frame for controls. A woman’s height and weight at ages 18, 30, and at study baseline were collected during the in-person interview and used to calculate body mass index (BMI) at various times throughout the life course.
To aid recall, a life events calendar with milestones, such as marriages, births, and deaths, was used throughout the in-person interview [26]. Each pregnancy was denoted on the calendar by coloring the month of pregnancy initiation until pregnancy end. For each pregnancy, a woman was asked the outcome (live birth, still birth, miscarriage, abortion). For each live or still (i.e., full-term) birth, she was asked detailed information, including “How much weight did you gain with this pregnancy?”
Average GWG was calculated by summing the reported weight gain for each full-term pregnancy and dividing by the number of full-term pregnancies. Cases and controls were classified by quartiles of average GWG using cut points from quartiles in the control population. We explored the impact of weight gain within the current IOM BMI-based recommended range [3] by classifying average GWG using BMI at the age closest to but preceding the first full-term pregnancy (i.e., age 18 or 30). Current IOM BMI-based weight gain guidelines are 27.5–39.6 lb for underweight women; 25.3–35.2 lb for normal weight women; 15.4–25.3 lb for overweight women; and 11–19.8 lb for obese women [3].
Statistical analyses
Analyses were limited to cases and controls who reported having at least one full-term birth (live or still birth) and who reported the amount of weight gained for all full-term pregnancies. Among the 1,802 controls, 167 were never pregnant, 62 reported no full-term pregnancy, and 22 were missing GWG for at least 1 pregnancy, leaving 1,551 controls included in the current analyses. Among the 902 cases, 167 were never pregnant, 46 reported no full-term pregnancy, and 19 were missing GWG for at least 1 pregnancy, leaving 670 cases for the current analyses.
Differences in demographic, medical and anthropometric factors between cases and controls were initially assessed using χ2 tests. Multivariable unconditional logistic regression was used to calculate odds ratios (ORs) and 95% confidence intervals (CIs) for the association between GWG metrics and EOC adjusting for potential confounders. Age at study baseline (continuous), race (white, blank and others), education level [less than high school, high school, post high school (not college) or some college, college graduate or postgraduate], and OC duration (continuous), were chosen a priori as potential confounders and included in final models. Sensitivity analyses for other potential confounders, including BMI at study baseline (continuous), BMI prior to first full-term birth (continuous), parity (1, 2, 3+), age at first birth (continuous), age at last birth (continuous), ever breastfed (yes/no), smoking status (never/former/current), alcohol use (ever/never), tubal ligation (yes/no), hysterectomy (yes/no), menopausal status (yes/no/unknown), use of hormone replacement therapy (yes/no/unknown), and family history of ovarian cancer (yes/no) did not alter results and were omitted from final models.
To explore potential effects of long-term maternal weight retention after childbearing on EOC risk, analyses were repeated limiting subjects to the 1997 women who reported being normal or underweight prior to their first full term pregnancy and then stratified by whether the woman was obese/overweight at interview study baseline. BMI prior to first full-term pregnancy was calculated using the self-reported height and weight closest to but preceding the first full-term pregnancy. Specifically, for women who reported the first full-term before or at age 30, we used self-reported height and weight at age 18. For women whose first full-term pregnancy was after age 30, we used self-reported height and weight at age 30. A woman was considered normal/underweight prior to her first full-term pregnancy if her BMI prior to her first full-term pregnancy was less than or equal to 24.99 kg/m2. A woman was considered obese/overweight at study baseline if her BMI using reported height and weight at study baseline was greater than 24.99 kg/m2, otherwise she was considered normal/underweight at study baseline. Interactions and linear trends were assessed with Wald tests. To assess whether any observed relationship between GWG and EOC was a result of GWG’s correlation with other weight-related metrics, we calculated Pearson’s correlation coefficients. All p-values were two-sided and considered significant at the p < 0.05 level. All analyses were conducted using Stata/SE version 15.1 (StataCorp).
Results
Compared to controls, cases were less likely to be better educated or white, and more likely to have a family history of breast or ovarian cancer (Table 1). Controls were more likely to have breastfed, used oral contraceptives, and had a tubal ligation. There were no case–control differences in BMI at study baseline, BMI prior to first full-term pregnancy, age at first full-term pregnancy, first full-term pregnancy after age 30, age at last full-term pregnancy, parity, and smoking status. There was also no case–control difference in the average number of years between age at first pregnancy and age used to calculate BMI prior to first full-term pregnancy. Similarly, among women who were normal/underweight prior to their first full-term pregnancy, there were no case–control differences in the age at first full-term pregnancy, first full-term pregnancy after age 30, age at last full-term pregnancy, difference in the average number of years between age at first pregnancy and age used to calculate BMI prior to first full-term pregnancy (Table 2).
Gestational weight gain correlated only very weakly with measures of weight gain and weight-related factors, including BMI at study baseline, weight at study baseline, and weight gain throughout the childbearing years, implying that GWG could potentially be independently associated with ovarian cancer risk (Table 3).
Average weight gain per full-term pregnancy did not differ between cases and controls (Table 4). When examining average GWG according to IOM recommendations, no case–control differences were found (Table 4). When restricting analyses to the women who were normal/underweight prior to their first full-term pregnancy, no case–control differences were found for average weight gain nor for weight gain outside of IOM recommendations (Table 4). Results were similar when including age at first and last birth in the final models (Table 4). Sensitivity analyses showed that results were also similar when restricting the 1997 women who were normal/underweight prior to their first full-term pregnancy to those who gave birth prior to or at age 30 (i.e., women for whom BMI prior to first full-term pregnancy was calculated using weight at age 18).
To explore the potential effect of long-term weight retention after childbearing, we restricted analyses to the 1997 women who began their childbearing years as normal or underweight and examined differences in EOC risk between those who were overweight/obese and those who were normal/underweight at study baseline (Table 5). Among women who were normal/underweight at study baseline, greater GWG was not associated with EOC (OR = 0.9, 0.8, 0.7 for quartiles 2, 3 and 4, respectively compared to quartile 1). In contrast, among women who were overweight/obese at study baseline, greater GWG was positively associated with EOC (OR = 1.4, 1.8, 1.2, interaction p = 0.04). Sensitivity analyses showed that results were similar when restricting subjects in Table 5 to those who gave birth prior to or at age 30, as well as when using BMI at age 18 for women included in Table 5.
Discussion
In the HOPE study, increasing GWG itself was not associated with increased EOC risk. Results were similar when considering average GWG per pregnancy and weight gain according to IOM guidelines. However, greater GWG was positively associated with EOC among women who were normal/underweight at the start of their childbearing years and who reported being overweight/obese at study baseline (Table 5), as women who reported being normal/underweight prior to their first full-term pregnancy and also reported being normal/underweight at study baseline were not at an increased EOC risk regardless of how much weight they gained in pregnancy.
The finding of no association between GWG and EOC in general is surprising because greater GWG is associated with increased risk of subsequent maternal obesity [4,5,6,7,8,9,10,11,12] a risk factor for EOC [15,16,17,18,19,20]. We therefore anticipated a positive association between increasing GWG and EOC, something we did not find in general. We did, however, find a significant interaction between BMI at study baseline and GWG among women who began their childbearing years lean. Assuming that among those women, the women who were overweight/obese at study baseline retained weight gained during a pregnancy for the long term while the women who were normal/underweight at study baseline did not, our findings suggest that long-term maternal weight retention after pregnancy and not absolute GWG may impact EOC risk among women who are lean at the beginning of their childbearing years. This assertion is consistent with a recent meta-analysis of two prospective studies, which reported a positive association between adult weight gain and ovarian cancer risk [27].
It is also possible that the timing of weight gain may be relevant to EOC risk, thereby explaining our observations. GWG is related to weight change in early and mid-adulthood. Recently, the Nurses’ Health Study reported that early life (pre-adult) weight gain and adiposity are more strongly associated with EOC risk than adiposity during the pre-menopausal years [20]. Thus, the lack of an association between EOC and GWG may relate more to timing of the weight change than the actual change in weight itself. It is also possible that the lack of association may be related to our study population, as in the general HOPE population [28] and among the parous women (Table 1), BMI at study baseline was not associated with EOC risk, although repeated non-pregnancy related weight gain with subsequent weight loss was associated with decreased EOC risk [28]. This latter finding is consistent with our observation that lean women who appeared to lose the weight gained in pregnancy were at no increased risk for EOC. It is possible, then, that the underlying physiology of weight loss (and not weight gain alone) may impact EOC risk.
In the 2009 IOM report [3], excessive GWG was found to be common in US women. Approximately 35% of normal weight women and 60% of overweight and obese women gain more than the recommended weight during pregnancy [29,30,31,32,33]. Failure to lose weight post-partum is a strong predictor of subsequent maternal obesity [4,5,6,7,8,9,10,11,12] and is associated with metabolic diseases later in life [11], which may increase the risk of obesity-associated outcomes. Our data raises the possibility that EOC may be one such outcome.
To our knowledge, we are the first to report on the GWG–EOC relationship in general and among lean women. Therefore, replication in other studies is important to confirm our finding that long-term weight retention after childbearing and not absolute GWG is associated with increased EOC risk in lean women. Specifically, this finding warrants more careful consideration in a prospective study wherein gestational weight gain and postpartum weight retention are carefully detailed by clinical or study staff in order to more accurately assess any true association.
Some methodologic issues must be noted. First, our analyses assume that among women who began their childbearing years lean, being overweight/obesity at study baseline resulted from long-term maternal weight retention due to GWG. Since women tend to increase in weight over the life course and especially in young adulthood [34,35,36,37], it is possible that other factors and not GWG played a role in the resulting high BMI at study baseline. Second, all weight information was self-reported, so we cannot eliminate the possibility of recall bias. If recall bias were non-differential with respect to case/control status or if cases underestimated their reported weights, results would be bias towards the null. Overestimate of reported weights by cases but not the controls could bias results away from null. Notably, women with higher BMI tend to underestimate their weight whereas women with lower BMI tend to overestimate their weight [38, 39], which suggests that recall bias in our study would likely attenuate any true associations. To reduce recall bias in HOPE, all participants were asked the same set of questions in the same way by trained study staff, and neither study staff nor participants were aware of any hypotheses involving GWG and EOC. Together, these factors would reduce recall bias, although as with all case–control studies, it cannot be eliminated. Third, a woman’s weight immediately prior to a pregnancy was not included in the demographic assessment. We therefore used weight at 18 or 30 (whichever age was closest to but preceded the first full-term pregnancy) as a surrogate for pre-pregnancy weight when categorizing weight gain by IOM guidelines and when calculating BMI to identify subjects for the subset analyses restricted to women who were normal/underweight prior to their first full-term pregnancy. Since age-related weight gain is most pronounced in early adulthood, especially in one’s 20′s [34,35,36,37], differences in the unknown actual pre-pregnancy weight versus assigned weight could lead to misclassification and bias. The use of weight closest to but preceding first full-term pregnancy was an attempt to reduce the difference in actual versus assigned weight for women who reported a first full-term pregnancy after age 30, as any weight gained during in the 20′s would be accounted for in weight at age 30. Notably, only 13% of subjects reported a first full-term pregnancy after age 30 with no significant difference in the percent of cases versus controls (Table 1). Thus, there was no case–control difference in use of weight at 18 versus weight at 30 as a surrogate for pre-pregnancy weight/BMI. There was also no significant case–control difference in the number of years between age at first full-term pregnancy and age used to assign pre-pregnancy weight/BMI in general (Table 1) and among women who began their childbearing years normal/underweight (Table 2). Together, these data suggest that any misclassification of pre-pregnancy weight/BMI would be non-differential with respect to case–control status, thereby obscuring a potential association. Finally, as this is a retrospective study, the data can only suggest a potential association and not causation.
Despite these limitations, this study has several strengths including its unique data set that included GWG for each pregnancy, as well as its large, population-based design, the use of life calendars to increase recall, and the use of standardized, structured, in-person interviews administered by a small number of highly trained interviewers, all of which increase data quality and help reduce bias.
In conclusion, based on the findings reported herein, we posit that for women who are normal/underweight, long-term weight retention after pregnancy, and not absolute GWG, may increase risk of ovarian cancer. If our hypothesis is supported in other studies designed to assess this question directly, then counseling women on the importance of healthy weight management after a pregnancy could provide another means to help women reduce their risk of this often-fatal malignancy.
Data availability
Data are available upon request from the senior author.
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Funding
This work supported by National Cancer Institute (K07-CA80668, R01CA095023); the Department of Defense (DAMD17-02-1-0669); and the University of Pittsburgh School of Medicine Dean’s Faculty Advancement Fund.
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Institutional Review Board approval was obtained from all hospitals from which cases were identified and from the University of Pittsburgh.
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Fu, Z., Kelley, J.L., Odunsi, K. et al. Gestational weight gain and risk of epithelial ovarian cancer. Cancer Causes Control 32, 537–545 (2021). https://doi.org/10.1007/s10552-021-01405-5
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DOI: https://doi.org/10.1007/s10552-021-01405-5