EMPIRICAL ARTICLE
The Effects of Ovarian Hormones and Emotional Eating on Changes in Weight Preoccupation across the Menstrual Cycle Britny A. Hildebrandt, MA1* Sarah E. Racine, PhD2 Pamela K. Keel, PhD3 S. Alexandra Burt, PhD1 Michael Neale, PhD4 Steven Boker, PhD5 Cheryl L. Sisk, PhD1,6 Kelly L. Klump, PhD1
ABSTRACT Objective: Previous research has shown that fluctuations in ovarian hormones (i.e., estradiol and progesterone) predict the changes in binge eating and emotional eating across the menstrual cycle. However, the extent to which other eating disorder symptoms fluctuate across the menstrual cycle and are influenced by ovarian hormones remains largely unknown. This study sought to examine whether the levels of weight preoccupation vary across the menstrual cycle and whether the changes in ovarian hormones and/or other factors (i.e., emotional eating and negative affect) account for menstrual cycle fluctuations in this eating disorder phenotype. Method: For 45 consecutive days, 352 women (age, 15–25 years) provided daily ratings of weight preoccupation, negative affect, and emotional eating. Saliva samples were also collected on a daily basis and assayed for levels of estradiol and progesterone using enzyme immunoassay techniques. Results: Weight preoccupation varied significantly across the menstrual cycle, with the highest levels in the premenstrual and menstrual phases. However, ovarian hormones did not account for
within-person changes in weight preoccupation across the menstrual cycle. Instead, the most significant predictor of menstrual cycle changes in weight preoccupation was the change in emotional eating. Discussion: Fluctuations in weight preoccupation across the menstrual cycle appear to be influenced primarily by emotional eating rather than ovarian hormones. Future research should continue to examine the relationships among ovarian hormones, weight preoccupation, emotional eating, and other core eating disorder symptoms (e.g., body dissatisfaction, compensatory behaviors) in an effort to more fully understand the role of these biological and behavioral factors for the full specC 2014 Wiley trum of eating pathology. V Periodicals, Inc. Keywords: weight preoccupation; menstrual cycle; ovarian hormones; estradiol; progesterone; binge eating; emotional eating; eating disorders; bulimia nervosa (Int J Eat Disord 2015; 48:477–486)
Introduction Accepted 14 June 2014 Supported by RO1 MH082054, T32 MH018269, T32 MH070343 from The National Institute of Mental Health. *Correspondence to: Britny A. Hildebrandt, MA, Department of Psychology, Michigan State University, 316 Physics Road-Room 43, East Lansing, MI. E-mail: [email protected] 1 Department of Psychology, Michigan State University, East Lansing, Michigan 2 Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 3 Department of Psychology, Florida State University, Tallahassee, Florida 4 Departments of Psychiatry, Human Genetics, and Psychology, Virginia Commonwealth University, Richmond, Virginia 5 Department of Psychology, University of Virginia, Charlottesville, Virginia 6 Neuroscience Program, Michigan State University, East Lansing, Michigan Published online 26 June 2014 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/eat.22326 C 2014 Wiley Periodicals, Inc. V
International Journal of Eating Disorders 48:5 477–486 2015
Ovarian hormones (i.e., estradiol and progesterone) have recently been implicated in the etiology of eating disorders in women.1–4 Most of the research, to date, has focused on the role of ovarian hormones in risk for binge eating. This is not surprising, given the findings from animal studies, demonstrating that ovarian hormones have direct, causal effects on food intake.5,6 Specifically, the removal of the source of ovarian hormones through bilateral ovariectomy in rats causes increased food intake, and adminstration of estradiol reverses this effect. In contrast, progesterone causes increased food intake, in part, by antagonizing the inhibitory effects of estradiol.6–8 In humans, food intake, binge eating, and emotional eating (i.e., the tendency to eat when 477
HILDEBRANDT ET AL.
experiencing negative emotions9) have been found to be significantly higher during the midluteal and premenstrual phases of the menstrual cycle as compared to the follicular/ovulatory phases.1,3,10–13 The studies that have directly examined the levels of estradiol and progesterone confirm that withinperson changes in ovarian hormones account for these menstrual cycle fluctuations.1,3,13 Specifically, although initial pilot data suggested that lower estradiol and higher progesterone levels were associated with increases in binge eating and emotional eating,1,3 a recent study indicated that the interactions between estradiol and progesterone (i.e., high levels of both) contribute to midluteal increases in emotional eating as well.14 In addition, ovarian hormone/dysregulated eating associations have been shown to be stronger in women with clinically significant levels of binge eating compared to women without binge episodes.13 Importantly, in all previous studies, hormone effects on binge eating and emotional eating were independent of important covariates that also change across the menstrual cycle, including negative affect and body mass index (BMI).1,3,13,14 Far fewer studies, however, have examined menstrual cycle changes in other disordered eating variables. Broadening the phenotypes examined is important for developing more complete models of the role of ovarian hormones in the full spectrum of eating pathology. One particularly important set of variables to investigate are those related to weight concerns/preoccupation (i.e., intense preoccupation with weight, dieting, and the pursuit of thinness15). Weight concerns have been identified as one of the most robust prospective risk factors for the development of clinically significant eating disorders,16 and weight concerns are directly related to core symptoms (e.g., undue influence of body weight/shape on self-evaluation) of anorexia nervosa and bulimia nervosa.17 In the only previous report of its kind, Racine et al.4 examined the association between menstrual cycle fluctuations in ovarian hormones and changes in weight concerns in two independent samples of women. In the first sample, robust fluctuations in weight preoccupation were observed across the menstrual cycle, where the levels of weight preoccupation were highest in the midluteal phase. Menstrual cycle changes in weight preoccupation were primarily accounted for by within-person increases in progesterone and, to a lesser extent, decreases in estradiol. However, in a second sample, more modest, nonsignificant changes in weight preoccupation were observed across the menstrual cycle, and weight preoccupation was highest during 478
the premenstrual phase. Reasons for the discrepant results across samples are unclear although the very small sample sizes of these studies (N 5 8 and 10, respectively) may have contributed to instability in effects. Clearly, additional research using larger samples of women is needed to clarify the presence/absence of within-person menstrual-cycle fluctuations in weight preoccupation. In addition, it will be important for these studies to determine whether menstrual-cycle changes in weight preoccupation are due to changes in ovarian hormones, changes in psychological factors (e.g., increased negative affect), and/or the changes in emotional eating that have been shown to fluctuate across the menstrual cycle in past research.1,3,13,14,18,19 For example, emotional eating has been previously linked to ovarian hormones,1,3,13,14 and we might expect weight concerns to increase during certain menstrual cycle phases as a result of emotional eating. Specifically, increased emotional eating during the midluteal phase could cause women to be more concerned and/or conscious about their body shape/weight; in this case, weight concerns may be owing to eating in the presence of negative emotions rather than to changes in ovarian hormones. Thus, it is important to determine the factors that might account for menstrual cycle changes in weight preoccupation: emotional eating, psychological factors (e.g., negative affect), and/or ovarian hormones. Given the above, the aim of the current study was to investigate within-person changes in weight preoccupation across the menstrual cycle utilizing a large, community-based sample of women. First, we were interested in examining whether the levels of weight preoccupation significantly vary across the menstrual cycle. Second, we wanted to investigate whether within-person fluctuations in weight preoccupation across the menstrual cycle are best accounted for by within-person changes in ovarian hormones, negative affect, emotional eating, or a combination of these factors.
Method Participants Participants included 352 same-sex female twins (194 monozygotic twins; 158 dizygotic twins) between the ages of 15 and 25 years drawn from the Twin Study of Hormones and Behavior Across the Menstrual Cycle14 within the Michigan State University Twin Registry (MSUTR20,21). All participants completed written informed consent before enrolling in the study. Importantly, a subset of these participants (N 5 174; 49% of the International Journal of Eating Disorders 48:5 477–486 2014
WEIGHT PREOCCUPATION ACROSS THE MENSTRUAL CYCLE TABLE 1.
Sample characteristics
Variable Age Weight preoccupation Estradiol (pg/mL) Progesterone (pg/mL) Negative affect Emotional eating BMI
Mean (SD)
Range
18.10 (1.76) 2.19 (1.98) 2.87 (1.39) 124.76 (67.08) 15.21 (3.78) 0.34 (.41) 24.07 (5.67)
16–22 0.02–7.98 0.70–12.43 18.73–397.04 10–29 0–3 15.81–47.59
Note: The values for weight preoccupation, estradiol, progesterone, negative affect, and emotional eating are average values across the 45-day data collection period. The values for BMI are average values across the three study visits.
current sample) was examined in the study by Klump et al.14 in which significant hormone effects for emotional eating were detected. Our analyses extend these initial results by investigating whether similar hormone effects are present for weight preoccupation scores, after controlling for emotional eating and other important covariates. Twins from the MSUTR are recruited using birth record methods described previously.20,21 Twins included in this study were demographically representative of the recruitment region (81.7% Caucasian, 16.2% African American, 1.0% Asian/Pacific Islander, and 1.0% Native American; http://www.michigan.gov/mdch). To ensure that we captured natural hormonal variations across the menstrual cycle, we developed a variety of participant inclusion/exclusion criteria: (1) regular menstrual cycles (i.e., every 22–32 days) for last 6 months; (2) no hormonal contraceptive use for last 3 months; (3) no psychotropic or steroid medication use for last 4 weeks; (4) no pregnancy or lactation in last 6 months; and (5) no history of genetic or medical conditions that may influence hormones or appetite/weight. Despite these exclusion criteria, participants from this study and those from the previous MSUTR studies without such criteria did not meaningfully differ on the levels of disordered eating (average Cohen’s d 5 .12, range 5 0.01–0.20).
Procedures All study procedures, methods, and materials were reviewed and approved by the Michigan State University Institutional Review Board. Behavioral and hormone data were provided on a daily basis across the 45 days of the study. Salivary samples were collected within the first 30 min of waking using the previously established methods.3 Questionnaires were completed each evening (after 5:00 PM) using an online data system or preprinted scantrons. This pattern of morning saliva samples and evening behavioral data collection was to ensure that hormone measurements preceded behavioral ratings each day. In addition to daily data collection, all participants completed three in-person visits occurring at the start of International Journal of Eating Disorders 48:5 477–486 2014
the study, halfway through the study (day 23), and at the end of data collection (day 45). During these inperson assessments, eligibility was reassessed, height and weight were measured, and completed materials were collected from participants. Between visits, staff contacted the participants 13/week to answer questions and confirm continued protocol adherence. These procedures were effective at identifying the individuals who were no longer eligible to participate due to missed periods, medication use, and/or pregnancy during the study (
The Effects of Ovarian Hormones and Emotional Eating on Changes in Weight Preoccupation across the Menstrual Cycle Britny A. Hildebrandt, MA1* Sarah E. Racine, PhD2 Pamela K. Keel, PhD3 S. Alexandra Burt, PhD1 Michael Neale, PhD4 Steven Boker, PhD5 Cheryl L. Sisk, PhD1,6 Kelly L. Klump, PhD1
ABSTRACT Objective: Previous research has shown that fluctuations in ovarian hormones (i.e., estradiol and progesterone) predict the changes in binge eating and emotional eating across the menstrual cycle. However, the extent to which other eating disorder symptoms fluctuate across the menstrual cycle and are influenced by ovarian hormones remains largely unknown. This study sought to examine whether the levels of weight preoccupation vary across the menstrual cycle and whether the changes in ovarian hormones and/or other factors (i.e., emotional eating and negative affect) account for menstrual cycle fluctuations in this eating disorder phenotype. Method: For 45 consecutive days, 352 women (age, 15–25 years) provided daily ratings of weight preoccupation, negative affect, and emotional eating. Saliva samples were also collected on a daily basis and assayed for levels of estradiol and progesterone using enzyme immunoassay techniques. Results: Weight preoccupation varied significantly across the menstrual cycle, with the highest levels in the premenstrual and menstrual phases. However, ovarian hormones did not account for
within-person changes in weight preoccupation across the menstrual cycle. Instead, the most significant predictor of menstrual cycle changes in weight preoccupation was the change in emotional eating. Discussion: Fluctuations in weight preoccupation across the menstrual cycle appear to be influenced primarily by emotional eating rather than ovarian hormones. Future research should continue to examine the relationships among ovarian hormones, weight preoccupation, emotional eating, and other core eating disorder symptoms (e.g., body dissatisfaction, compensatory behaviors) in an effort to more fully understand the role of these biological and behavioral factors for the full specC 2014 Wiley trum of eating pathology. V Periodicals, Inc. Keywords: weight preoccupation; menstrual cycle; ovarian hormones; estradiol; progesterone; binge eating; emotional eating; eating disorders; bulimia nervosa (Int J Eat Disord 2015; 48:477–486)
Introduction Accepted 14 June 2014 Supported by RO1 MH082054, T32 MH018269, T32 MH070343 from The National Institute of Mental Health. *Correspondence to: Britny A. Hildebrandt, MA, Department of Psychology, Michigan State University, 316 Physics Road-Room 43, East Lansing, MI. E-mail: [email protected] 1 Department of Psychology, Michigan State University, East Lansing, Michigan 2 Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 3 Department of Psychology, Florida State University, Tallahassee, Florida 4 Departments of Psychiatry, Human Genetics, and Psychology, Virginia Commonwealth University, Richmond, Virginia 5 Department of Psychology, University of Virginia, Charlottesville, Virginia 6 Neuroscience Program, Michigan State University, East Lansing, Michigan Published online 26 June 2014 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/eat.22326 C 2014 Wiley Periodicals, Inc. V
International Journal of Eating Disorders 48:5 477–486 2015
Ovarian hormones (i.e., estradiol and progesterone) have recently been implicated in the etiology of eating disorders in women.1–4 Most of the research, to date, has focused on the role of ovarian hormones in risk for binge eating. This is not surprising, given the findings from animal studies, demonstrating that ovarian hormones have direct, causal effects on food intake.5,6 Specifically, the removal of the source of ovarian hormones through bilateral ovariectomy in rats causes increased food intake, and adminstration of estradiol reverses this effect. In contrast, progesterone causes increased food intake, in part, by antagonizing the inhibitory effects of estradiol.6–8 In humans, food intake, binge eating, and emotional eating (i.e., the tendency to eat when 477
HILDEBRANDT ET AL.
experiencing negative emotions9) have been found to be significantly higher during the midluteal and premenstrual phases of the menstrual cycle as compared to the follicular/ovulatory phases.1,3,10–13 The studies that have directly examined the levels of estradiol and progesterone confirm that withinperson changes in ovarian hormones account for these menstrual cycle fluctuations.1,3,13 Specifically, although initial pilot data suggested that lower estradiol and higher progesterone levels were associated with increases in binge eating and emotional eating,1,3 a recent study indicated that the interactions between estradiol and progesterone (i.e., high levels of both) contribute to midluteal increases in emotional eating as well.14 In addition, ovarian hormone/dysregulated eating associations have been shown to be stronger in women with clinically significant levels of binge eating compared to women without binge episodes.13 Importantly, in all previous studies, hormone effects on binge eating and emotional eating were independent of important covariates that also change across the menstrual cycle, including negative affect and body mass index (BMI).1,3,13,14 Far fewer studies, however, have examined menstrual cycle changes in other disordered eating variables. Broadening the phenotypes examined is important for developing more complete models of the role of ovarian hormones in the full spectrum of eating pathology. One particularly important set of variables to investigate are those related to weight concerns/preoccupation (i.e., intense preoccupation with weight, dieting, and the pursuit of thinness15). Weight concerns have been identified as one of the most robust prospective risk factors for the development of clinically significant eating disorders,16 and weight concerns are directly related to core symptoms (e.g., undue influence of body weight/shape on self-evaluation) of anorexia nervosa and bulimia nervosa.17 In the only previous report of its kind, Racine et al.4 examined the association between menstrual cycle fluctuations in ovarian hormones and changes in weight concerns in two independent samples of women. In the first sample, robust fluctuations in weight preoccupation were observed across the menstrual cycle, where the levels of weight preoccupation were highest in the midluteal phase. Menstrual cycle changes in weight preoccupation were primarily accounted for by within-person increases in progesterone and, to a lesser extent, decreases in estradiol. However, in a second sample, more modest, nonsignificant changes in weight preoccupation were observed across the menstrual cycle, and weight preoccupation was highest during 478
the premenstrual phase. Reasons for the discrepant results across samples are unclear although the very small sample sizes of these studies (N 5 8 and 10, respectively) may have contributed to instability in effects. Clearly, additional research using larger samples of women is needed to clarify the presence/absence of within-person menstrual-cycle fluctuations in weight preoccupation. In addition, it will be important for these studies to determine whether menstrual-cycle changes in weight preoccupation are due to changes in ovarian hormones, changes in psychological factors (e.g., increased negative affect), and/or the changes in emotional eating that have been shown to fluctuate across the menstrual cycle in past research.1,3,13,14,18,19 For example, emotional eating has been previously linked to ovarian hormones,1,3,13,14 and we might expect weight concerns to increase during certain menstrual cycle phases as a result of emotional eating. Specifically, increased emotional eating during the midluteal phase could cause women to be more concerned and/or conscious about their body shape/weight; in this case, weight concerns may be owing to eating in the presence of negative emotions rather than to changes in ovarian hormones. Thus, it is important to determine the factors that might account for menstrual cycle changes in weight preoccupation: emotional eating, psychological factors (e.g., negative affect), and/or ovarian hormones. Given the above, the aim of the current study was to investigate within-person changes in weight preoccupation across the menstrual cycle utilizing a large, community-based sample of women. First, we were interested in examining whether the levels of weight preoccupation significantly vary across the menstrual cycle. Second, we wanted to investigate whether within-person fluctuations in weight preoccupation across the menstrual cycle are best accounted for by within-person changes in ovarian hormones, negative affect, emotional eating, or a combination of these factors.
Method Participants Participants included 352 same-sex female twins (194 monozygotic twins; 158 dizygotic twins) between the ages of 15 and 25 years drawn from the Twin Study of Hormones and Behavior Across the Menstrual Cycle14 within the Michigan State University Twin Registry (MSUTR20,21). All participants completed written informed consent before enrolling in the study. Importantly, a subset of these participants (N 5 174; 49% of the International Journal of Eating Disorders 48:5 477–486 2014
WEIGHT PREOCCUPATION ACROSS THE MENSTRUAL CYCLE TABLE 1.
Sample characteristics
Variable Age Weight preoccupation Estradiol (pg/mL) Progesterone (pg/mL) Negative affect Emotional eating BMI
Mean (SD)
Range
18.10 (1.76) 2.19 (1.98) 2.87 (1.39) 124.76 (67.08) 15.21 (3.78) 0.34 (.41) 24.07 (5.67)
16–22 0.02–7.98 0.70–12.43 18.73–397.04 10–29 0–3 15.81–47.59
Note: The values for weight preoccupation, estradiol, progesterone, negative affect, and emotional eating are average values across the 45-day data collection period. The values for BMI are average values across the three study visits.
current sample) was examined in the study by Klump et al.14 in which significant hormone effects for emotional eating were detected. Our analyses extend these initial results by investigating whether similar hormone effects are present for weight preoccupation scores, after controlling for emotional eating and other important covariates. Twins from the MSUTR are recruited using birth record methods described previously.20,21 Twins included in this study were demographically representative of the recruitment region (81.7% Caucasian, 16.2% African American, 1.0% Asian/Pacific Islander, and 1.0% Native American; http://www.michigan.gov/mdch). To ensure that we captured natural hormonal variations across the menstrual cycle, we developed a variety of participant inclusion/exclusion criteria: (1) regular menstrual cycles (i.e., every 22–32 days) for last 6 months; (2) no hormonal contraceptive use for last 3 months; (3) no psychotropic or steroid medication use for last 4 weeks; (4) no pregnancy or lactation in last 6 months; and (5) no history of genetic or medical conditions that may influence hormones or appetite/weight. Despite these exclusion criteria, participants from this study and those from the previous MSUTR studies without such criteria did not meaningfully differ on the levels of disordered eating (average Cohen’s d 5 .12, range 5 0.01–0.20).
Procedures All study procedures, methods, and materials were reviewed and approved by the Michigan State University Institutional Review Board. Behavioral and hormone data were provided on a daily basis across the 45 days of the study. Salivary samples were collected within the first 30 min of waking using the previously established methods.3 Questionnaires were completed each evening (after 5:00 PM) using an online data system or preprinted scantrons. This pattern of morning saliva samples and evening behavioral data collection was to ensure that hormone measurements preceded behavioral ratings each day. In addition to daily data collection, all participants completed three in-person visits occurring at the start of International Journal of Eating Disorders 48:5 477–486 2014
the study, halfway through the study (day 23), and at the end of data collection (day 45). During these inperson assessments, eligibility was reassessed, height and weight were measured, and completed materials were collected from participants. Between visits, staff contacted the participants 13/week to answer questions and confirm continued protocol adherence. These procedures were effective at identifying the individuals who were no longer eligible to participate due to missed periods, medication use, and/or pregnancy during the study (
