The Impact of Obesity on Gynecologic Cancer Screening: An Integrative Literature Review

The Impact of Obesity on Gynecologic Cancer Screening: An Integrative Literature Review Tess Aldrich, MSc, APRN, and Barbara Hackley, CNM, MS Introduction: Evidence indicates lower rates of breast and cervical cancer screening among obese compared to nonobese women. This integrative review examines the association between gynecologic cancer screening and body weight, as well as potential barriers to screening. Methods: A literature search of standard computerized databases was conducted for peer-reviewed articles published between 1950 and January 2009. Results: Twenty-three studies met the criteria for review. Of the 17 studies that evaluated rates of cervical cancer screening, 13 found obese women significantly less likely than their nonobese counterparts to have had a recent Papanicolaou test, a trend that was stronger in white women when compared to African American women. Eight of the 15 studies examining routine mammography found an inverse association between increasing body weight and recent screening, although findings generally pertained only to women who were white and/or severely obese. Possible barriers to care included embarrassment and perceived weight stigma in the clinical setting, lack of appropriately sized examination equipment, and poor patient–provider communication. Discussion: Further research is needed to clarify the challenges that obese women face in accessing care and to evaluate strategies such as ensuring the availability of appropriate equipment and supplies, the use of alternative screening methodologies, and more culturally sensitive counseling approaches that may improve screening rates in obese women. J Midwifery Womens Health 2010;55:344–356 Ó 2010 by the American College of Nurse-Midwives. keywords: body mass index, mammogram, obesity, Papanicolaou test, screening

INTRODUCTION The prevalence of obesity, defined as body mass index (BMI) >30 kg/m2, has increased markedly among adults in the United States in the last decade, from an estimated 23% between 1988 and 1994 to 32% in 2004.1,2 The highest rate of obesity is among African American women, of whom 49.7% were obese in 1999 and 2000, compared to 39.7% of Mexican American women and 30% of white women.1 Obesity is associated with many well-documented health risks, including an increased incidence of endometrial and postmenopausal breast cancer3–5 and later-stage breast cancer diagnosis.6,7 Importantly, mortality from both cervical and breast cancer is also higher among obese compared to nonobese women.4,8 Several reasons exist for these trends. The hormonal milieu associated with obesity—namely, high levels of unopposed estrogen resulting from increased aromatization of androgen precursors in adipocytes and decreased levels of sex hormone–binding globulin—may favor the development of hormone-dependent tumors.4 While this hormonal phenomenon is less consistently associated with cervical cancer, a number of large, population-based studies have found increasing cervical cancer mortality risk with higher BMI values, particularly with adenocarcinomas of the cervix.4,8–10

Address correspondence to Tess Aldrich, MSc, APRN, 101 S. Oxford St., Brooklyn, NY 11217. E-mail: [email protected]

344 Ó 2010 by the American College of Nurse-Midwives Issued by Elsevier Inc.

Despite their heightened risk for certain gynecologic cancers, a growing body of literature is documenting decreased rates of routine breast and cervical cancer screening among obese compared with nonobese women.11–28 Obesity in the United States has historically been overrepresented among minority and lower socioeconomic groups and is perhaps associated with lower rates of health insurance29,30—factors that can negatively affect women’s access to and use of preventive care services. However, body weight is increasingly recognized as an independent predictor of gynecologic cancer screening, with a number of large, retrospective studies finding significantly lower Papanicolau (Pap) test and mammography rates among obese women, after controlling for factors such as age, race, health insurance, socioeconomic group, and comorbidity. These findings raise questions about the implications obesity itself has on women’s receipt of gynecologic care. Primary care clinicians are uniquely positioned to increase cancer screening rates, reduce disparities in access to health care, and improve quality of care for all women. Accomplishing these goals will require better insight into high-risk groups and the specific challenges they face in the health care system. This article examines the impact of obesity on breast and cervical cancer screening, first comparing screening rates among obese and nonobese women as presented in the published literature, and secondly reviewing the articles obtained and other relevant research to identify barriers faced by overweight and obese women in obtaining recommended cancer screening tests. Volume 55, No. 4, July/August 2010 1526-9523/$36.00  doi:10.1016/j.jmwh.2009.10.001

METHODS A literature search was conducted of English language peer-reviewed journal articles published between 1950 and January 2009 using the standard computerized databases Medline, PubMed, and the Cumulative Index to Nursing and Allied Health Literature (CINAHL). The following terms and/or combinations of terms were used: ‘‘obesity,’’ ‘‘body mass index,’’ ‘‘breast neoplasms,’’ ‘‘uterine cervical neoplasms,’’ ‘‘screening,’’ ‘‘mammography,’’ ‘‘Pap smear,’’ ‘‘barriers,’’ ‘‘weight stigma,’’ ‘‘weight bias,’’ ‘‘comorbidity,’’ and ‘‘minority health.’’ The search included quantitative studies examining predictors of gynecologic cancer screening and research on attitudes and practices of obese women and providers who manage this population, regarding both Pap tests and mammography. Citations from the reference lists of reviewed articles were also searched for relevant papers. RESULTS Gynecologic Cancer Screening in Obese and Nonobese Women Twenty-six studies were identified that explored differences in breast and/or cervical cancer screening based on obesity status. Of these, 23 studies met the criteria for review.11–28,31–35 Seven of the 23 studies pertain to Pap tests, six to mammography, and 10 to both cervical and breast cancer screening. The majority of the studies are cross-sectional, retrospective analyses of populationbased surveys, such as the National Health Interview Survey (NHIS) and the Behavioral Risk Factor Surveillance System (BRFSS), or chart reviews. Two studies used a prospective design,11,13 which allowed for more detailed questions about women’s and providers’ perspectives. In general, studies examining cervical cancer screening included women 18 years of age and older, while those specific to mammography limited analyses to women $40 years of age to correspond to mammography screening guidelines. The majority of studies determined the proportion of women having obtained a Pap test and/or mammogram within the previous 1 to 3 years. Most authors calculated BMI from participants’ self-reported weight and height and used the following World Health Organization (WHO) categories: normal weight (BMI 19–24.9 kg/ m2), overweight (BMI 25–29.9 kg/m2), class I obesity (BMI 30–34.9 kg/m2), class II obesity (BMI 35–39.9 kg/ m2), and class III obesity (BMI $40 kg/m2). Five studies12,14,16,17,25 examined overall predictors of gynecologic Tess Aldrich, MSc, APRN, is as a nurse practitioner at Housing Works– Women’s Health Center in Brooklyn, NY. Barbara Hackley, CNM, MS, is an associate professor at the Yale University School of Nursing, New Haven, CT, and provides clinical care at the South Bronx Health Center for Children and Families, Bronx, NY.

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cancer screening, of which obesity and/or BMI was one; in these cases, obesity was usually examined as a binary variable. Seventeen studies examined the association between cervical cancer screening and obesity,11–13,17–26,32–35 with all but two18,22 finding a significant inverse association between obesity and recent Pap testing and one25 reporting a borderline significant association (Table 1). Where analyses were conducted separately based on race, results are included in Table 1. In general, large, retrospective studies of national survey data found a trend of less cervical cancer screening with increasing BMI, although this finding pertains only to white women in several of the studies.20,24,26,34 A number of studies also found a significant inverse association between high BMI and up-to-date cervical cancer screening only for severely obese women.13,32,17 Datta et al.17 were the only authors to study African American women exclusively in a large, national survey, and these authors found that women who were either underweight (BMI <20) or severely obese (BMI $30) were significantly more likely to have delayed Pap testing than their healthy weight counterparts. Of the two studies that found no association between obesity and cancer screening,18,22 the Lubitz et al.22 study was based on a very low overall cervical cancer screening rate of roughly 20% in a sample of primarily low-income, minority women at an urban teaching hospital. The most common reason cited for not performing a Pap test regardless of patients’ weight was lack of physician time, followed by terminal illness and advanced age. However, physicians were significantly more likely to cite acute illness, vaginitis, or menstruation as reasons for delayed Pap tests among obese compared to nonobese women (odds ratio [OR] = 4.59; 95% confidence interval [CI], 1.67–12.5). Ferrante et al.18 found obese women significantly less likely than healthy weight women to have had a recent Pap test in crude analyses; however, their results were not significant in the adjusted model. Fifteen studies examined routine mammography rates by body weight, with eight reporting significant differences in screening between obese and nonobese women (Table 2).14–16,19,20,24,27,32 In general, the association between BMI and breast cancer screening was not as consistent as that between obesity and cervical cancer screening. Several large, retrospective studies of national data observed a significant association, although it generally pertained only to women in the most extreme category of obesity.19,27,32 Cohen et al.,15 who surveyed a large sample of women in the Southern Community Cohort Study, the majority of whom were African American, also found that only black women with BMI $40 kg/m2 were significantly less likely than their nonobese counterparts to have had a mammogram in the past 2 years, an association that was not significant for obese and nonobese women of other ethnicities. Interestingly, Wee et al.27 analyzed 1998 NHIS data and observed that while white women with class III obesity had 345

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Table 1. Relationship Between Obesity and Cervical Cancer Screening Study, Year 35

Subjects and Methodology

Main Findings

Comments

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Williams et al., 1972

N = 161 women 35–54 y old, race NR; prospective survey: mail-in questionnaires; unadjusted analysis

Correlation between obesity (increasing Ponderal index) and decreased likelihood of Pap test (R2 = –0.24)

Two-part survey to determine the extent to which various preventive health behaviors are interrelated using factor analysis

Adams et al.,11 1993

N = 291 women 40–65 y old, 99% white; N = 1316 physicians; women’s and physician’s mail-in survey; unadjusted analysis

Pap test in last 2 y Average weight Moderately overweight Very overweight

% 68.1 (P < .05) 66.7 (P < .05) 47.5 (P < .05)

Both women’s reluctance to obtain a Pap test and negative opinions of appearance increased as weight increased. A large proportion of physicians was reluctant to perform examinations on obese women and on women who appeared reluctant

Olson et al.,23 1994

N = 310 nursing staff 21–68 y old, race NR; self-administered survey; unadjusted analysis

Delayed care/cancelled appointment BMI 20–24.9 BMI 24–26.9 BMI $27

OR (95% CI) 1.00 2.132 (1.098–5.423) 3.885 (1.509–10.274)

Women with increasing BMI significantly less likely to have had a recent a Pap test (figures NR); most common reason for delaying medical care was ‘‘embarrassment about weight’’

Lubitz et al.,22 1995

N = 970 women, 62% black; secondary analysis from prospective study; unadjusted analysis

Pap test at recommended visit Normal weight Obese Morbidly obese

% 21 (NS) 20 (NS) 20 (NS)

Low (20%) Pap test rate at study clinic. Physicians more likely to cite illness/vaginitis/menses as reason for not performing Pap on obese and morbidly obese women (OR = 4.59; 95% CI, 1.67–12.5)

Fontaine et al.,21 1998

N = 6314 women $18 y old, 80% white; 1992 NHIS; multivariate analysis

No Pap test in past 3 y BMI 25.1 BMI 35 BMI 40

OR (95% CI) 1.00 1.29 (1.04–1.58) 1.46 (1.07–1.98)

In adjusted model, each 1-unit increase in BMI corresponded to an average 0.063-unit increase in physician visits. However, obese and severely obese women more likely than nonobese women to delay clinical breast examinations and Pap tests

Simoes et al.,25 1999

N = 1690 women $18 y old, 85% white; 1994 BRFSS and Missouri Enhanced Survey; multivariate analysis

No Pap test in past 1 y BMI #27.3 BMI >27.3

OR (95% CI) 1.0 1.2 (0.9–1.5)

Nonadherence to Pap tests higher in white, uninsured, and women with cost barrier. Obese women less likely than nonobese to have routine vs diagnostic Pap (OR = 0.7; 95% CI, 0.4–1.0)

Wee et al.,26 2000

N = 7405 women 18–75 y old, 73% white; 1994 NHIS; multivariate analysis

Pap test in past 3 y: White women BMI 18.5–<25 BMI 25–<30 BMI 30–35 BMI 35–<40 BMI $40 Pap test in last 3 y: Black women BMI 18.5–<25 BMI 25–<30 BMI 30–35 BMI 35–<40 BMI $40

Rate difference (95% CI) 0 3.4 (–6.4 to –0.5) 9.4 (–13.5 to –5.2) 8.3 (–14.2 to –2.3) 8.8 (–16.9 to –0.7) Rate difference (95% CI) 0 2.5 ( 8.0–3.1) 0.2 (–4.5–4.1) 0.5 (–7.8–6.8) 1.7 (–5.0–8.4)

84% of nonobese vs 78% of overweight and 78% of obese women reported Pap test in past 3 years in crude analysis (P < .001). Association between body weight and Pap testing not significant for black women in adjusted model

(Continued)

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Table 1 (Cont’d). Relationship Between Obesity and Cervical Cancer Screening Study, Year 20

Subjects and Methodology

Main Findings

Comments

Fontaine et al., 2001

N = 72,889 women $18 y old, 85% white; 1998 BRFSS: phone survey; multivariate analysis

No Pap test in past 2 y BMI 18.5–<25 BMI 25–<30 BMI 30–<35 BMI 35–<40 BMI $40

OR (95% CI) 1.00 1.13 (1.07–1.08) 1.22 (1.14–1.30) 1.43 (1.30–1.57) 1.69 (1.49–1.92)

Underweight, overweight, and obesity class 1 women more likely than healthy weight women to delay Pap test >2 years, adjusting for age, race, smoking, and insurance. Trend strongest for white compared to black women

Amonkar et al.,12 2002

N = 12,949 women $18 y old, 79% white; 1997 BRFSS data; Appalachian states; multivariate analysis

Pap test in past BMI <30 BMI >30

OR (95% CI) 1.00 0.80 (0.66–0.96)

Predictors of Pap testing also included: better self-reported health, receipt of other preventive services, higher education, having insurance, being married, and black race/ethnicity

Coughlin et al.,32 2004

N = 60,479 women $18 y old, 75% white; 1999 BRFSS data; multivariate analysis

Pap test in past 3 y BMI <18.5 BMI >18.5-24.9 BMI 25-29 BMI >30

% (95% CI) 83.7 (81.8–85.7), NS 86.7 (86.1–87.3), NS 86.5 (85.7–87.2), NS 85.9 (84.9–86.8), P < .05

Study designed to assess association between gynecologic cancer screening and various characteristics. Only women with BMI >30 significantly less likely to have had recent Pap (P < .05). Lack of testing also associated with smoking and lack of cholesterol screening

Datta et al.,17 2005

N = 40,009 women 21–65 y old, 100% black; 1995 Black Women’s Health Study (mail-in); multivariate analysis

No Pap test in past 2 y BMI <20 BMI 20–24.9 BMI 25–29.9 BMI $30

OR (95% CI) 1.3 (1.1–1.6) 1.00 1 (0.9–1.1) 1.6 (1.4–1.7)

Older age, lower education, smoking, parity, neighborhood poverty, and BMI <20 and $30 all significant predictors of recent Pap test in multivariate model. Only study conducted exclusively among black women

Ostbye et al.,24 2005

N = 4434 women (1996 survey) and 4009 women (2000 survey) 50–64 y old, 82% white; Health and Retirement Study (US); multivariate analysis

Pap test in past 2 y: White women BMI 18.5–24.9 BMI 25–29.9 BMI 30–34.9 BMI 35–39.9 BMI $40 Pap test in past 2 y: Black women BMI 18.5–24.9 BMI 25–29.9 BMI 30–34.9 BMI 35–39.9 BMI $40

OR (95% CI) 1.00 0.78 (0.68–0.89) 0.68 (0.57–0.80) 0.59 (0.45–0.78) 0.50 (0.35–0.71) OR (95% CI) 1.00 1.50 (1.07–2.12) 1.22 (0.84–1.77) 1.13 (0.70–1.85) 0.75 (0.45–1.26)

Study designed to evaluate association between BMI and gynecologic cancer screening in middle-aged women. Associations remained significant after controlling for number of physician visits in past year

(Continued)

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Table 1 (Cont’d). Relationship Between Obesity and Cervical Cancer Screening Study, Year 34

Subjects and Methodology

Main Findings

Comments

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Wee et al., 2005

N = 9993 women 18–75 y old, 71% white; 2000 NHIS; unadjusted analysis

Pap test in past 3 y: White women BMI 18.5–<25 BMI 25–<30 BMI 30–<35 BMI 35–<40 BMI $40 Pap test in past 3 y: Black women BMI 18.5–<25 BMI 25–<30 BMI 30–<35 BMI 35–<40 BMI $40 Pap test in past 3 y: Latina women BMI 18.5–<25 BMI 25–<30 BMI 30–<35 BMI 35–<40 BMI $40

% 87 (NS) 87 (NS) 83 (P < .05) 85 (NS) 78 (P < .05) % 88 (NS) 89 (NS) 89 (NS) 83 (NS) 87 (NS) % 75 (NS) 81 (P < .05) 81 (NS) 83 (NS) 84 (NS)

High overall Pap rate. Severely obese white women less likely to have recent Pap (OR = 0.92; 95% CI, 0.83–0.99); trend not seen for black women in adjusted model. Obese white women more likely than black or Latina counterparts to cite embarrassment or discomfort as reason for delaying Pap

Amy et al.,13 2006

N = 481 women $21 y old, 68% white; N = 129 health care providers; self-administered questionnaire; unadjusted analysis

Pap test in past 2 y BMI 25–35 BMI 35–45 BMI 45–55 BMI >55

% 86.3 (NS) 85.8 (NS) 84.3 (NS) 68.3 (P > .02)

68% of women with BMI >55 cited weight as reason for delaying visit; 83% viewed their weight as a barrier to care. 85% of providers surveyed stated that gynecologic care for obese women was more challenging

Ferrante et al.,18 2006

N = 800 women 40–74 y old, 10% white; medical chart review; multivariate analysis

Pap test in past 3 y BMI 18–29.9 BMI 30–34.9 BMI 35–35.9 BMI $40

OR (95% CI) 1.00 0.74 (0.51–1.09) 1.31 (0.77–2.24) 0.68 (0.42–1.13)

Obese women less likely than nonobese to have had recent Pap test (69% vs 77%; P < .001). However, results NS after adjusting for age, race/ethnicity, insurance, smoking, and number of visits. Association between obesity and screening not mediated by age or race/ethnicity

Ferrante et al.,19 2007

N = 5521 women 40–74 y old, race NR; 2000 NHIS; multivariate analysis

Pap test in past 3 y BMI 18.5–24.9 BMI 25–29.9 BMI 30–34.9 BMI 35–39.9 BMI $40

OR (95% CI) 1.00 0.97 (0.74–1.27) 0.65 (0.44–0.97) 0.73 (0.44–1.22) 0.43 (0.27–0.70)

Women with class I and III obesity significantly less likely than normal weight women to have had recent Pap test in adjusted model. No difference in physician recommendation for Pap test based on women’s BMI

Mitchell et al.,33 2008

N = 37,673 women 20–69 y old, 92% white; 2003 Canadian Community Health Survey; multivariate analysis

Pap test in past 3 y BMI 18.5–24.9 BMI 25–29.9 BMI 30–34.9 BMI 35–39.9 BMI $40

OR (95% CI) 1.00 0.87 (0.81–0.94) 0.79 (0.72–0.88) 0.62 (0.54–0.71) 0.61 (0.53–0.72)

Overweight women significantly more likely to cite ‘‘provider factors’’ as reason for delaying Pap test. Women with class III obesity more than twice as likely as nonobese women to cite ‘‘fear’’ as barrier to examination

BMI = Body mass index; BRFSS = Behavioral Risk Factor Surveillance System; CI = confidence interval; NHIS = National Health Interview Survey; NR = not reported; NS = not significant; OR = odds ratio.

A recent review by Cohen et al.36 examining the association between obesity and breast, cervical, and colorectal cancer screening also found an inverse relationship between increasing BMI and rates of both Pap tests and mammograms, with the latter applying only to white women. This review included many of the same studies as those detailed in this article. However, Cohen et al.36 highlighted many of the methodologic differences among studies. In this article, we include studies published since the Cohen et al.36 article and also explore some reasons for observed differences in screening rates for the purpose of identifying areas for future study and intervention. Given the consistency of these findings in the literature, it is imperative to understand why obese women tend to receive less screening. Despite the number of published reports on the negative impact of obesity on gynecologic cancer screening, limited qualitative data exist to explain the observed trends. However, findings from studies reviewed in this article suggest several possible explanations that are both patient- and provider-driven. These factors may act as barriers to breast and cervical cancer screening for obese women, thereby placing them at greater risk for disease.

sionals, which can manifest in various forms.37–39 In a small study of obese, predominantly white men and women, participants cited friends, spouses, family members, and health care professionals among the most common sources of weight stigma.40 Amy et al.13 conducted one of a small number of studies to explore both women’s and providers’ views regarding the impact of obesity on gynecologic cancer screening. In this study, which employed focus groups and structured interviews to elicit respondents’ views on receiving breast and cervical cancer screening, overweight women reported discourteous treatment by clinic staff, being told they were ‘‘too heavy’’ for a Pap test, and being examined using medical equipment, gowns, and examination tables that were too small, making the visit awkward or even painful.13 Importantly, women also cited a tendency for clinicians to ascribe patients’ diverse health complaints to their obesity alone and to give unwanted counsel on weight loss.13 Such practice implies a trend among providers to overemphasize a patient’s weight in setting the visit’s agenda, which may not correspond to a woman’s own needs. These types of provider attitudes, whether real or perceived, may undermine overall quality of care received by obese women. The available literature also suggests that attitudes of embarrassment, stress, and fear among obese women regarding gynecologic cancer screening play an important role in deterring them from seeking care. In a recent study by Mitchell et al.,33 which found a decreased likelihood of recent Pap testing for overweight and obese women, severely obese women were twice as likely as normal weight controls to cite ‘‘fear’’ as a deterring factor, in reference to the pain of the examination, shame and embarrassment, and concern that the test would detect a malignancy or pathology. A related theme common to several studies on avoidance of preventive health care visits among obese women is reluctance to be weighed at each visit and to receive what is perceived as unhelpful advice about weight loss.13,23,41 Olson et al.23 studied 310 female nursing staff at a Wisconsin community hospital and found that appointment cancellation—including appointments for Pap testing—was significantly associated with higher BMI but was unaffected by participants’ age, education, occupation, or reason for last visit. Among the roughly 13% of women who cancelled visits for weight-related reasons, the most common motives were shame and reluctance to be ‘‘lectured’’ about their weight, as reported by 25% of obese and 55% of extremely obese women (P < .001).23 Similar results were reported by Drury et al.,41 who documented greater avoidance of health care with increasing BMI because of women’s shame at having gained weight since their last visit.

Obese Women’s Attitudes and Perceptions Towards Gynecologic Cancer Screening

Provider Perceptions Regarding Gynecologic Examinations in Obese Women

Several studies have documented pervasive weight bias and stigma—both subtle and overt—among health care profes-

Health care provider attitudes and practices regarding the gynecologic examination and obese women likely play

lower rates of recent mammography than their nonobese counterparts, obesity was associated with increased screening among African American women. Several studies that reported significantly lower rates of cervical cancer screening with increasing BMI failed to observe a similar trend for mammography in multivariate analyses.18,21,26,33 In addition, a recent study of 100,197 New Hampshire women $40 years of age found that while underweight women were less likely than their healthy weight counterparts to have had a mammogram in the previous 2 years (OR = 0.57; 95% CI, 0.48–0.68), women who were in the overweight and obesity class I and II categories were slightly more likely to adhere to regular screening.31 The authors point to major public education campaigns and recent advances to reduce the physical discomfort of mammography as possible reasons for discrepancies between this and earlier studies that observed a reverse trend.14,20 Colbert et al.16 was the only study identified that examined age of initiation of screening mammography based on body weight, and these authors found that obese women began screening 1.6 years later than healthy weight women (P < .001) in a large, predominantly white population. Here, the effect of obesity on age of first mammogram was greater than that of race or ethnicity.16 Understanding Barriers to Care

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a critical role in influencing care-seeking behavior. This concept could apply to subtle negative attitudes providers convey to heavier women during the examination as well as to more overt actions, such as the lack of recommendations or referrals for obese women to be screened. In a survey of 1316 physicians and 291 women, Adams et al.11 found that patients’ likelihood of receiving routine Pap tests decreased as BMI increased; importantly, 17% of providers expressed a disinclination to perform the pelvic examination in obese women and 83% of providers were reluctant to examine women who themselves appeared reluctant. Providers’ specific reasons for reluctance to perform Pap tests in larger women were not reported, though aversion was greater among younger physicians.11 In a more recent prospective study with primary care providers, including nurse practitioners and other nursing professionals, 85% of respondents stated that the gynecologic examination was more challenging in obese women.13 More than half of respondents also stated they had received no specific training on providing gynecologic care to severely obese patients and expressed a desire for such training. In response to an open-ended question on what would aid them the most in caring for large women, providers listed general information on health care for the very obese and more accessible supplies that are sized appropriately for obese patients, including larger speculums, gowns, and blood pressure cuffs.13 Respondents also cited the challenge of providing adequate counseling and health education in the very short visit. Research on provider recommendations for breast and cervical cancer screening in obese women is limited, although in general, studies do not suggest strong disparities in provider referrals based on body weight.19,22,27 Using patient data obtained from a computerized medical record system, Lubitz et al.22 analyzed physician and resident reports of Pap testing—and reasons for not testing—eligible women. The likelihood of performing the test for obese and nonobese women did not differ significantly after controlling for patient age and race. The authors point out, however, that this was a secondary analysis of data, and overall cervical cancer screening rates were very low, at roughly 20%. In a much larger study that included white, African American, and Latina women responding to the 2000 NHIS, Wee et al.27 also found that, among women who had not had a Pap test in the 3 years preceding the survey, both obese and nonobese women were equally likely to have received a physician recommendation to be screened. Ferrante et al.19 reported similar findings. Increased Illness Burden in Obese Women Several authors suggest that overall poor health status among obese women may also deter them from obtaining routine cancer screening and other preventive care, often in spite of seeing multiple providers and spending signif350

icant amounts of money on health care.18,19,21,33,42–44 Obesity increases the risk for cardiovascular disease, osteoarthritis, obstructive sleep apnea, pregnancy complications, and menstrual irregularities, and is associated with other endocrine pathologies, such as polycystic ovarian syndrome.45,46 In a retrospective study with women 50 to 75 years of age, Beckman et al.47 observed that women with diabetes had significantly lower rates of screening mammography than matched controls, adjusting for race and insurance status, despite averaging a higher number of office visits. Similar findings were reported by Fontana et al.,48 who observed that having diabetes reduced women’s odds of recent mammography by roughly onehalf (OR = 0.53; 95% CI, 0.29–0.97); women with heart disease were also less likely than those without to have had a recent Pap test (OR = 0.32; 95% CI, 0.19–0.54). An inverse association between increasing comorbidity and the likelihood of recent cervical cancer screening49 and mammography acceptance50 has also been shown. In addition to the impact of competing health care priorities on routine cancer screening, obese women may tend to see multiple providers/specialists but lack a primary ‘‘gatekeeper’’ who ensures that they receive routine screenings. No studies were identified that specifically support this concept, which deserves further exploration. DISCUSSION In general, the studies reviewed here suggest that the negative impact of obesity on routine screening is most relevant to cervical cancer rather than breast cancer screening and to white, as opposed to African American, women. It should be noted that a small number of studies used the same databases for their analyses; for example, both Ferrante et al.19 and Wee et al.34 based their data on the 2000 NHIS and both reported similar findings. The present review may therefore overemphasize these results. However, even when factoring in the redundancy of these studies, there remains compelling evidence that obese women, particularly white women, tend to have lower rates of cervical cancer screening. It has been suggested that the mammogram referral (handled by phone or fax), rather than a scheduled office visit for a Pap test (in which the women is typically weighed and required to disrobe) may lessen the impact of obesity on breast cancer screening.21 With respect to the impact of race, teasing out racial distinctions in the literature is challenging given the variations in sample populations, methodology, covariates, and the historically low numbers of minority women included in this research. The majority of data are based on regression analyses that control for a number of variables, and factors that might account for racial differences in screening rates as a function of BMI are not readily apparent. In addition, where studies analyzed data separately by race, authors generally report results only for white and African American Volume 55, No. 4, July/August 2010

Table 2. Relationship Between Obesity and Breast Cancer Screening Author, Year Fontaine et al., 1998

21

Study Description N = 3105 women $18 y old, 80% white; 1992 NHIS; multivariate analysis

Fontaine et al.,20 N = 38,682 women $18 y old, 2001 85% white; 1998 BRFSS (phone survey); multivariate analysis

Wee et al.,26 2000

N = 3502 women 50–75 y old, 81% white; 1994 NHIS; multivariate analysis

Carney et al.,14 2002

N = 539 women $50 y old, race NR; New Hampshire Mammography Network (mail-in survey); unadjusted analysis N = 49,564 women $40 y old; 1999 BRFSS; multivariate analysis

Coughlin et al.,32 2004

Colbert et al.,16 2004

N = 786 women receiving first screening mammogram, 90% white; MA General Hospital Avon Comprehensive Breast Cancer database; multivariate analysis

Wee et al.,27 2004

N = 5004 women 50–75 y old, 74% white; 1998 NHIS; multivariate analysis

Main Findings Mammogram in past 3 y BMI 25.1 BMI 35 BMI 40

OR (95% CI) 1.00 0.81 (0.59–1.12) 0.73 (0.45–1.19)

No mammogram in past 2 y BMI 18.5–<25 BMI 25–<30 BMI 30–<35 BMI 35–<40 BMI $40 Mammogram in past 3 y: White BMI 18.5–<25 BMI 25–<30 BMI 30–35 BMI 35–<40 BMI $40 Mammogram in past 3 y: Black BMI 18.5–<25 BMI 25–<30 BMI 30–35 BMI 35–<40 BMI $40 Mammogram in past 1 y, mean  SD BMI 26.1  0.3 BMI 27.6  0.4

OR (95% CI) 1.00 1.00 (1.94–1.07) 1.12 (1.02–1.23) 1.13 (1.98–1.30) 1.32 (1.09–1.59) Rate difference (95% CI) 0 1.4 ( –5.6–2.9) 4.4 ( –10.5–1.6) 9.2 (–18.7–0.4) 10.9 (–28.0–6.2) Rate difference (95% CI) 0 8.4 (–19.0–2.2) 7.0 (–20.4–6.5) 10.6 (–5.1–26.3) 0.9 (–24.8–22.9)

Yes No

Comments Adjusted model controlled for age, race, income, education, smoking, and health insurance. No significant differences seen when obesity analyzed as dichotomous variable (BMI #27.3 vs BMI >27.3) Underweight, obesity class 1, and obesity class III women more likely than healthy weight women to delay mammography >2 yrs, adjusting for age, race, smoking, and insurance In crude analysis, 68% of nonobese vs 64% of overweight and 62% of obese women reported mammogram in past 3 y (P < .002); NS in adjusted model. No statistically significant differences observed by race/ethnicity

Women adhering to annual mammography more likely to have lower BMI (P < .003).

Mammogram in past 2 y BMI <18.5 BMI 18.5–<25 BMI 25-29 BMI >30

% (95% CI) Study designed to assess 83.7 (81.8–85.7), NS association between 86.7 (86.1–87.3), NS gynecologic cancer screening 86.5 (85.7–87.2), NS and various health 85.9 (84.9–86.8), P < .05 characteristics. Only women with BMI >30 significantly less likely to have had a recent mammogram (P < .05) Mean age at first mammogram, by Age (95% CI) Obese women began screening 1.6 self-rated body type y later than nonobese women Thin 40.5 (39.5–41.6) (P < .001); body weight had Medium 41.7 (41.0–42.4) larger effect on age of initiation Obese 44.7 (42.5–46.9) than did race. Other factors in delaying first screening: no insurance, no primary care provider, non-English speaking, minority race Mammogram in past 2 y: White OR (95% CI) Class III obese white women are less likely than their nonobese BMI 18.5–24.9 1.00 counterparts to have had BMI 25–29.9 0.98 (0.92–1.04) a recent mammogram. Race– BMI 30–34.9 0.94 (0.86–1.01) BMI interaction term P < .001. BMI 35–39.9 0.83 (0.68–0.96) Obese white women more likely BMI $40 0.90 (0.76–1.07) than nonobese women to have Mammogram in past 2 y: Black OR (95% CI) usual source of care; reverse BMI 18.5–24.9 1.00 trend for black women BMI 25–29.9 1.19 (1.01–1.32) BMI 30–34.9 1.22 (0.98–1.39) BMI 35–39.9 1.37 (1.13–1.50) BMI $40 0.95 (0.60–1.25) (Continued)

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Table 2 (Cont’d). Relationship Between Obesity and Breast Cancer Screening Author, Year Ostbye et al., 2005

24

Amy et al.,13 2006

Study Description N = 4439 women (1996 survey) and 4010 (2000 survey) 50–61 y old, 82% white; Health and Retirement Study (US); multivariate analysis

N = 338 women 40–80 y old, 68% white; self-administered questionnaire; unadjusted analysis

Ferrante et al.,18 N = 939 women 40–74 y old, 2006 14% white, 50% Latina, 36% black; medical chart review; multivariate analysis

Zhu et al.,28 2006

N = 8501 women 40–80 y old, 84% white; 2000 NHIS; multivariate analysis

Ferrante et al.,19 N = 7455 women 40–74 y old, 2007 race NR; 2000 NHIS; multivariate analysis

Cohen et al.,15 2007

N = 25,060 women 40–70 y old, 25% white, 75% black; Southern Community Cohort Study (participant interviews); multivariate analysis

Main Findings Mammogram in past 2 y: White BMI 18.5–24.9 BMI 25–29.9 BMI 30–34.9 BMI 35–39.9 BMI $40 Mammogram in past 2 y: Black BMI 18.5–24.9 BMI 25–29.9 BMI 30–34.9 BMI 35–39.9 BMI $40 Mammogram in past 2 y BMI 25–35 BMI 35–45 BMI 45–55 BMI >55 Mammogram in past 2 y BMI 18–29.9 BMI 30–34.9 BMI 35–35.9 BMI $40

OR (95% CI) 1.00 0.90 (0.78–1.05) 0.73 (0.60–0.88) 0.69 (0.51–0.93) 0.59 (0.40–0.88) OR (95% CI) 1.00 1.13 (0.79–1.62) 0.97 (0.65–1.45) 1.03 (0.61–1.76) 1.07 (0.60–1.92) % 86 (NS) 81.2 (NS) 80.3 (NS) 67.7 (NS) OR (95% CI) 1.00 0.99 (0.71–1.39) 1.40 (0.90–2.18) 1.13 (0.72–1.78)

No mammogram in past 2 y: White BMI 18.5–24.9 BMI 25–29.9 BMI 30–34.9 BMI 35–39.9 BMI $40 No mammogram in past 2 y: Black BMI 18.5–24.9 BMI 25–29.9 BMI 30–34.9 BMI 35–39.9 BMI $40 Mammogram in past 2 y BMI 18.5–24.9 BMI 25–29.9 BMI 30–34.9 BMI 35–39.9 BMI $40

OR (95% CI) 1.00 0.90 (0.80–1.10) 1.00 (0.80–1.20) 1.10 (0.80–1.40) 1.40 (1.00–1.90) OR (95% CI) 1.00 1.80 (0.60–1.20) 1.60 (0.40–1.00) 1.90 (0.50–1.70) 1.30 (0.70–2.40) OR (95% CI) 1.00 0.95 (0.81–1.10) 1.01 (0.83–1.23) 0.79 (0.60–1.05) 0.50 (0.37–0.68)

Mammogram in past 2 y: Black BMI 18.5–24.9 BMI 25–29.9 BMI 30–34.9 BMI 35–39.9 BMI $40 Mammogram in past 2 y: White BMI 18.5–24.9 BMI 25–29.9 BMI 30–34.9 BMI 35–39.9 BMI $40

OR (95% CI) 1.00 1.12 (1.00–1.25) 1.25 (1.12–1.40) 1.22 (1.07–1.38) 1.06 (0.93–1.21) OR (95% CI) 1.00 0.89 (0.76–1.05) 0.99 (0.83–1.18) 0.96 (0.78–1.18) 0.70 (0.56–0.87)

Comments Study designed to evaluate association between BMI and gynecologic cancer screening in middle-aged women. Nonsignificant results for black women in multivariate model

68% of women with BMI >55 cited weight as reason for delaying visit; 83% viewed their weight as a barrier to care adjusting for education and insurance Overall mammography rate of 69%; no significant difference based on obesity status. Independent risk factors for insufficient screening included age 40–49 y, smoking, and comorbidity Underweight and extremely obese white women more likely to have no recent mammogram

Controlled for age, race, education, marital status, income, region of country, insurance status, contact with primary care provider, number of visits, alcohol, and vitamin use. No difference in physician recommendation for mammogram based on BMI 58% of black women were obese vs 49% of white women. Among women who had not had a mammogram in past 5 y, no significant difference in physician recommendation based on obesity status. Percent of white women reporting ‘‘embarrassment’’ increased with BMI; pattern not seen for black women

(Continued)

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Table 2 (Cont’d). Relationship Between Obesity and Breast Cancer Screening Author, Year Berz et al., 2008

31

Mitchell et al.,33 2008

Study Description N = 100,197 women $40 y old, 75% white; 2004 BRFSS (New Hampshire); multivariate analysis

N = 13,129 women 50–69 y old, 95% white; Canadian Community Health Survey

Main Findings Mammogram in past 2 y BMI 18.5–24.9 BMI 25–29.9 BMI 30–34.9 BMI 35–39.9 BMI $40 Mammogram in past 2 y

OR (95% CI) 1.00 1.08 (1.01–1.15) 1.08 (0.99–1.18) 1.10 (0.98–1.25) 0.97 (0.84–1.13)

Comments Controlled for age, race, smoking, general health rating, education, and income

Authors cite referral-dependent nature of mammography as opposed to Pap testing as possible reason for nonsignificant association between breast cancer screening and obesity, despite significant association with Pap testing

BMI = Body mass index; BRFSS = Behavioral Risk Factor Surveillance System; CI = confidence interval; MA = Massachusetts; NHIS = National Health Interview Survey; NR = not reported; NS = not significant; OR = odds ratio; SE = standard error.

women.15,24,26–28 Wee et al.34 studied the impact of BMI on cervical cancer screening among white, African American, and Latina women, finding that obesity negatively influenced screening only for severely obese white women. Interestingly, a higher percentage of both white and Latina women cited discomfort and embarrassment as the primary reason for not obtaining Pap tests, while African American women were more likely to cite lack of physician recommendation.34 Among Latinas, overweight and obese women were more likely than their healthy weight counterparts to cite the cost of screening as a deterring factor.34 Significant differences may exist between white and African American women with respect to weight consciousness and the avoidance of gynecologic examinations. Several authors have speculated that racial differences in body image and a tendency for African American women to define a larger ideal body size compared to white women account for the trends observed in studies to date.20,36,51,52 More specifically, while African American women have the highest obesity rates in the United States, they may not experience the degree of body dissatisfaction and stigma that appears to deter white women from obtaining pelvic examinations. Wee et al.27 examined the impact of obesity on mammography use among a racially diverse sample of women and found that low self-esteem (defined in this study as feelings of worthlessness, sadness, or hopelessness in the preceding 30 days) did not affect the relationship between BMI and breast cancer screening in the multivariate model. However, obese white women were more likely than their African American counterparts to report feelings of ‘‘worthlessness’’ in the last 30 days. 27 This finding appears to support the concept of racial differences in body satisfaction, which has been reported previously.51 Psychosocial factors related to weight stigma in health care, which may be especially relevant to the gynecologic examination, clearly warrant further study. Simply put, Journal of Midwifery & Women’s Health  www.jmwh.org

overweight and obese women often face disdainful and disrespectful treatment by health care providers.13 Studies reviewed in this article suggest that while obesity does not significantly affect clinicians’ likelihood of recommending routine screening, the nature of the visit and patient/ provider attitudes may be discouraging obese women from obtaining routine gynecologic cancer screening and other types of preventive care. Given the current prevalence of obesity in the United States, increasing provider education on caring for obese patients in a sensitive and effective manner and reducing weight bias in the clinical setting is greatly needed. A number of concrete measures may improve obese women’s comfort during clinical visits, including having armless chairs in waiting rooms, larger blood pressure cuffs, and appropriately sized examination tables, gowns, and speculums; offering women the option to refuse being weighed at each visit, and ensuring that weights are taken in a private setting, may also increase patients’ comfort.13 Research on whether such measures do in fact increase obese women’s likelihood of obtaining breast and cervical cancer screening is needed. Importantly, a number of authors cited the perceived potential for decreased accuracy of gynecologic cancer screening among severely obese women.13,53,54 Studies suggest an association between obesity and decreased breast mass palpability53,55 as well as decreased mammogram specificity.56,57 However, it is unlikely that obesity directly influences the accuracy of the Pap test—although extra adipose tissue may make the speculum examination more challenging and/or decrease the palpability of ovarian and adnexal masses. Whether current large (Graves) speculums are adequate for visualization and endocervical sample collection in severely obese women may require further evaluation. In addition, self-sampling for human papillomavirus (HPV) DNA has been shown to have high accuracy when compared with conventional Pap testing,58,59 and this may be a future option for cervical cancer 353

screening among populations that face barriers to care. De Alba et al.,58 who reported 90% sensitivity and 88% specificity of unsupervised self-collection, also found high satisfaction for this method among Latinas. HPV selfsampling may be one important strategy for obese and other women with documented low rates of cervical cancer screening. Finally, the available literature suggests a critical need to improve patient–provider communication related to body weight during routine visits, such as the well-woman examination. Obesity can increase women’s risk for irregular menses, dysfunctional uterine bleeding, and other gynecologic problems, making the annual examination an opportune time to discuss healthy weight strategies for women across the lifespan. One challenge is effectively offering and integrating weight loss counseling into the visit while recognizing that women may be deterred by an overemphasis on weight during a routine Pap test. Simply being told to ‘‘lose weight’’ is clearly ineffective and even counterproductive for many women. Not wanting to receive this type of unhelpful and perhaps condescending advice was cited by nearly one-third of participants (n = 22) in a study by Drury et al.,41 in which BMI >27.5 kg/m2 directly correlated with delays or avoidance of health care in the past year (r = 0.33; P < .01). The need for a more holistic approach to combating obesity, focusing on overall health rather than simply weight loss, and the development of concrete weight loss strategies and goals together with the patient have been proposed.41,60 Importantly, studies have shown that minority women are less likely than their white counterparts to receive information about the health consequences of obesity60—highlighting once again the need to integrate weight loss counseling into routine gynecologic care for all patients regardless of race. Obesity is now one of the most important public health challenges in the United States and worldwide.61 There is compelling evidence of lower rates of breast and cervical cancer screening for obese compared to healthy weight women, particularly among white women. This trend is concerning given both the epidemic proportions of obesity in the United States and the heightened risk for certain gynecologic cancers associated with obesity. Despite the large number of studies examining barriers and facilitators among women relating to gynecologic examinations and mammography, studies seldom ask specifically about body weight as a factor that may discourage women from seeking care. Research on this topic is greatly needed to inform interventions aimed at improving access to and quality of care for obese women.

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