Adverse Childhood Experiences and Cervical Cancer Screening

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Background: Adverse childhood experiences (ACEs) have been associated with an increased risk of a variety of diseases, including cancer. However, research ...
Original Article

JOURNAL OF WOMEN’S HEALTH Volume 00, Number 00, 2016 ª Mary Ann Liebert, Inc. DOI: 10.1089/jwh.2016.5823

Adverse Childhood Experiences and Cervical Cancer Screening He´ctor E. Alcala´, PhD, MPH,1 Emma Mitchell, PhD, RN,2 and Jessica Keim-Malpass, PhD, RN2

Abstract

Background: Adverse childhood experiences (ACEs) have been associated with an increased risk of a variety of diseases, including cancer. However, research has largely ignored how ACEs impact cancer screening, a potential intermediate outcome. As such, the present study examined the association between ACEs and ever and recent use of Papanicolaou (Pap) test, among women aged 21 and older. Materials and Methods: Analyses used the 2009 Tennessee Behavioral Risk Factor Surveillance System (n = 1527) to model odds of ever and recently (within the last 3 years) engaging in Pap tests screening from nine different adversities. Bivariate and multivariate logistic regression models were run to accomplish this. Results: In bivariate and multivariate models, living in a household in which adults treated each other violently increased odds of ever receiving a Pap test. In bivariate models, physical and sexual abuse was associated with decreased odds of receiving a recent Pap test. After accounting for confounders, only the latter association remained significant. Conclusions: Results highlight a potential mechanism by which early childhood experiences can impact the development of cervical cancer. Providers of care should consider modifications to their screening practices, including screening for child abuse, to better serve all women.

This same research showed that experiencing acts of terrorism was not associated with cervical cancer screening.5 Qualitatively, women who have experienced sexual abuse identified the mechanism of the examination, gender of provider, negative emotions, power disparities, trust, pain, safety and disclosure, communication barriers, and sexual victimization as potential barriers to screening.6,7 Despite the evidence suggesting sexual abuse is associated with decreased cancer screening, other ACEs remain unexamined. There are several reasons to suspect that ACEs may be associated with cervical cancer screening. First, as evidenced from the findings examining survivors of sexual abuse, exposure to some ACEs may motivate women to eschew screening.5 This is unsurprising considering the relatively invasive nature of the procedure and when considering that sizable proportions of women believe Pap tests to be painful.8 Second, experiencing ACEs has been associated with a wide pattern of risky health behaviors that includes alcohol abuse,9,10 drug use,11,12 tobacco use,13 and risky sexual behaviors.14 In the family context, individuals can adopt these health behaviors as a means of coping with a hostile or cold family environment, or because uninvolved adults are not

Introduction

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nnually, more than 12,000 American women are diagnosed with cervical cancer, with more than 4,000 women dying of the disease.1 Cervical cancer rates have been on the decline for decades,2 thanks, in large part, to early detection provided by Papanicolaou (Pap) tests. Women who adhere to Pap screening recommendations have better cure rates than those who are overdue for screening.3 Given the importance of Pap tests in the early detection of cervical cancer, it is essential to consider what psychosocial factors are associated with the initial uptake and continued compliance to cervical cancer screening. One potential predictor of cervical cancer screening that has not received adequate attention is the potential impact adverse childhood experiences (ACEs) may have on use of Pap tests. These ACEs encompass both child abuse and household dysfunction experienced before the age of 18, such as physical abuse and parental separation.4 Available research, focusing almost exclusively on sexual abuse, has found that women who have experienced childhood sexual abuse are less likely to receive cervical cancer screenings.5

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Department of Public Health, University of Virginia, Charlottesville, Virginia. School of Nursing, University of Virginia, Charlottesville, Virginia.

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available to monitor the uptake of these harmful behaviors.15 Similarly, it is possible that these parents or adults are themselves not receiving screening for cancers, thus modeling negative health behaviors to children around them. Third, in the specific context of healthcare utilization, ACEs have been associated with increased utilization of care, partially because these individuals are more likely to be sick.16 Given that this runs counter to the established findings showing an association between sexual abuse and cervical cancer screening, it is impossible to know if specific ACEs will follow the general pattern seen among health behaviors or if cancer screening will more closely match the pattern observed among utilization of healthcare services. Finally, experiencing ACEs can impact cervical cancer screening indirectly through socioeconomic status as a potential mediator. Specifically, experiencing ACEs has been associated with diminished socioeconomic status in adolescence and adulthood,17–21 which, in turn, is associated with lower rates of cervical cancer screening.22,23 In sum, individual ACE items may positively or negatively impact the utilization of Pap tests. The goal of the current study is to examine if ACEs are associated with uptake and continued use of Pap tests among American women. Specifically, this analysis ascertains whether specific ACEs are associated with odds of women ever receiving a Pap test or having recently received a Pap test. Materials and Methods Data source

Data come from the 2009 Behavioral Risk Factor Surveillance System (BRFSS). This random digit dial telephone survey is conducted annually and was designed to be representative of the household-dwelling U.S. states and territories.24 All states and territories administer a core set of questions. Optional modules can be administered by states and territories, to all or some of their respondents. In the 2009 BRFSS, only one state, Tennessee, elected to administer questions on both ACEs and cervical cancer screening.25 In Tennessee, a total of 1971 people received the modules containing both ACEs and cervical cancer screening. Of these, 1967 were women older than the age of 21, which is the age at which Pap tests are recommended.26 Respondents missing data (i.e., missing or responses of ‘‘don’t know’’ or ‘‘refused’’) on any study variable were excluded, yielding an analytic sample of 1527. Measures

The 2009 BRFSS included an 11-item version of the ACE scale, which was used to measure the independent variables for this study. The items measured if several experiences had occurred before age 18.4,27 These items are listed in Table 1. All items were dichotomized to reflect whether or not the respondent had experienced the item, consistent with previous research.28 Three items capturing sexual abuse were combined to create a single measure of sexual abuse. This resulted in nine ACE measures. The main outcome of interest was the utilization of Pap smears. The BRFSS asked two questions related to cervical cancer screening: ‘‘A Pap test is a test for cancer of the cervix.

Table 1. ACE Items and Coding Scheme Question How often did a parent or adult in your home ever hit, beat, kick, or physically hurt you in any way? Do not include spanking. How often did anyone at least 5 years older than you or an adult ever touch you sexually? How often did anyone at least 5 years older than you or an adult try to make you touch them sexually? How often did anyone at least 5 years older than you or an adult force you to have sex? How often did a parent or adult in your home ever swear at you, insult you, or put you down? Did you live with anyone who was depressed, mentally ill, or suicidal? Did you live with anyone who was a problem drinker or alcoholic? Did you live with anyone who used illegal street drugs or who abused prescription medications? Did you live with anyone who served time or was sentenced to serve time in a prison, jail, or other correctional facility? Were your parents separated or divorced? How often did your parents or adults in your home ever slap, hit, kick, punch, or beat each other up?

Coding Ever/never Ever/never Ever/never Ever/never Ever/never Yes/no Yes/no Yes/no Yes/no Yes/no Ever/never

ACE, adverse childhood experiences.

Have you ever had a Pap test?’’ and ‘‘How long has it been since you had your last Pap test?’’ These were used to create the following two variables: (1) ever received a Pap test (yes vs. no) and (2) received a Pap test in the past 3 years (yes vs. no), which would imply currently up-to-date with screening. These variables were based on the 2003 US Preventative Task Force’s recommendations for cervical cancer screening, which recommend that women between the ages of 21 and 65 receive Pap tests at least every 3 years.29 The US Preventative Task Force updated their recommendations in 2012 to include cotesting of Pap and HPV testing every 5 years for women 30–54.26 Because this analysis utilized data from 2009, the former guidelines were considered in analysis. Several variables were included in analyses as potential confounders. Age was included as a continuous variable. Gender was measured as a dichotomous variable. Race and ethnicity were measured using a dichotomous variable (nonLatino white vs. other). Educational attainment was recoded from its original categories (i.e., kindergarten or less, 1st through 8th grade, 9th through 11th grade, high school graduate, 1–3 years of college, and 4 or more years of college) to continuous values that represented the midpoint of the category in terms of years of education, except for the last category coded as 16 years. This coding system has been previously used with analyses using the ACE module in the BRFSS13 and was adopted here because conclusions remained largely unchanged when compared to using the original variable categories.

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Table 2. Sample Characteristics, Women Aged 21+, BRFSS 2009 (N = 1527) Variable Cervical cancer screening (ever) Never screened Cervical cancer screening (last 3 years) Screened in last 3 years Not screened in last 3 years ACEs Physical abuse Sexual abuse Emotional abuse Lived with someone who was mentally ill Lived with problem drinker Lived with drug user Lived with someone who was jailed Parents divorced or separated Adults in household treated each other violently Age Race White Other Educational attainment (years) Hysterectomy No Yes

% or Mean

SE

6.45%

0.79%

85.44% 14.56%

1.44% 1.44%

14.13% 18.62% 27.93% 17.96%

1.23% 1.44% 1.69% 1.41%

25.99% 9.43% 6.92% 26.47% 17.58%

1.61% 1.13% 0.95% 1.65% 0.47%

49.32

0.52

81.88% 18.12% 13.8

1.47% 1.47% 0.08

69.16% 30.84%

1.59% 1.59%

BRFSS, Behavioral Risk Factor Surveillance System; SE, standard error.

Current insurance status was measured using a dichotomous variable, indicating whether or not the respondent had any health insurance coverage. Finally, hysterectomy status was measured using a dichotomous variable, indicating whether or not the respondent had ever received a hysterectomy. Analyses

All analyses were conducted in Stata 14.1, using weights to account for differential selection probability, stratification,

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and clustering of data. Means and frequencies were calculated for all study variables, as appropriate (Table 2). A series of logistic regression models calculating two outcomes were fit as follows. (1) Models among all women, age 21 and older, calculating odds of ever having a Pap test (Table 3) and (2) models among women between 21 and 65 years of age (n = 1527), calculating odds of having had a Pap test in the past 3 years (n = 1038) (Table 4). In this way, analyses mirror the age-specific recommendations for cancer screening. Three groups of logistic regression models were fit for each of the two outcomes. For the first group, bivariate associations between each of the nine ACE measures and the outcome were modeled. For the second group, confounders were added to these models. In the final group, a model, including all ACE measures simultaneously and confounders, was fit. Results

Table 2 shows the sample characteristics. A majority of respondents had ever received a Pap test (93.55%). A smaller majority had received a Pap test in the last 3 years (85.44%). Emotional abuse was the most commonly experienced ACE measure (27.93%) and living with someone who was jailed (6.92%) was the least commonly experienced. On average, respondents were 49.32 years old. About four-fifths of respondents were non-Latino white (81.88%). Respondents, on average, had some college education (13.8 years of education). Under a third of participants had received a hysterectomy (30.84%). Table 3 shows the result of logistic regression models predicting odds of ever receiving a Pap test, among women aged 21 and older. In bivariate models (Model 1), living in a household in which adults treated each other violently was associated with a 104% increase in odds of receiving a Pap test (odds ratio [OR] = 2.04; 95% confidence interval [CI] = 1.13, 3.68). This relationship remained significant after accounting for confounders (Model 2) and after accounting for confounders and other ACEs (Model 3). No other ACEs were associated with odds of ever receiving Pap tests. Table 4 shows the result of logistic regression models predicting odds of receiving a Pap test in the past 3 years

Table 3. Logistic Regression Calculating Odds of Ever Having a Pap Smear, Women Aged 21+, BRFSS 2009 (N = 1527) Model 1: bivariate

Model 2: controls

Variable

OR

AOR

Physical abuse Sexual abuse Emotional abuse Lived with someone who was mentally ill Lived with problem drinker Lived with drug user Lived with someone who was jailed Parents divorced or separated Adults in household treated each other violently

1.10 1.25 1.33 0.74 1.11 0.78 0.87 1.09 2.04

95% CI (0.56, (0.62, (0.72, (0.37, (0.62, (0.32, (0.30, (0.55, (1.13,

2.17) 2.53) 2.44) 1.50) 2.00) 1.93) 2.52) 2.14) 3.68)

1.16 1.39 1.17 0.59 1.23 0.62 0.77 1.01 2.25

95% CI (0.56, (0.65, (0.93, (0.29, (0.66, (0.25, (0.26, (0.48, (1.19,

2.42) 2.98) 1.09) 1.21) 2.29) 1.57) 2.25) 2.12) 4.27)

Model 3: All ACE measures and controls AOR 0.87 1.37 1.05 0.54 1.35 0.57 0.93 1.03 2.36

95% CI (0.33, (0.62, (0.40, (0.22, (0.70, (0.17, (0.27, (0.46, (1.14,

2.33) 3.01) 2.78) 1.33) 2.61) 1.90) 3.20) 2.32) 4.88)

Significant associations denoted in bold. Model 1 includes unadjusted bivariate associations. Model 2 adds age, gender, race, years of education, hysterectomy status, and insurance status as controls to bivariate models. Model 3 introduces all ACEs simultaneously while also controlling for age, gender, race, years of education, hysterectomy status, and insurance status to bivariate models. AOR, adjusted odds ratio; CI, confidence interval; OR, odds ratio.

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Table 4. Logistic Regression Calculating Odds of Having a Pap Smear in the Past 3 Years, Women Aged 21–65, BRFSS 2009 (N = 1038) Model 1: bivariate Variable

OR

Physical abuse Sexual abuse Emotional abuse Lived with someone who was mentally ill Lived with problem drinker Lived with drug user Lived with someone who was jailed Parents divorced or separated Adults in household treated each other violently

0.54 0.49 0.80 0.69 0.77 1.27 1.05 0.90 1.10

95% CI (0.31, (0.30, (0.49, (0.42, (0.46, (0.61, (0.50, (0.55, (0.62,

0.94) 0.81) 1.30) 1.14) 1.28) 2.64) 2.20) 1.48) 1.95)

Model 2: controls AOR 0.58 0.55 0.75 0.63 0.95 1.25 1.09 0.89 1.23

95% CI (0.32, (0.32, (0.45, (0.37, (0.56, (0.58, (0.51, (0.51, (0.65,

1.05) 0.94) 1.23) 1.07) 1.63) 2.69) 2.35) 1.52) 2.31)

Model 3: all ACE measures and controls AOR 0.63 0.57 1.03 0.65 0.99 1.95 0.92 0.94 1.71

95% CI (0.29, (0.30, (0.52, (0.33, (0.51, (0.72, (0.39, (0.51, (0.86,

1.38) 1.07) 2.04) 1.26) 1.90) 5.23) 2.51) 1.72) 3.39)

Significant associations denoted in bold. Model 1 includes unadjusted bivariate associations. Model 2 adds age, gender, race, years of education, hysterectomy status, and insurance status as controls to bivariate models. Model 3 introduces all ACEs simultaneously while also controlling for age, gender, race, years of education, hysterectomy status, and insurance status to bivariate models.

among women aged 21–65. In bivariate models (Model 1), physical abuse was associated with 46% lower odds of receiving a Pap test in the past 3 years (OR = 0.54; 95% CI = 0.31, 0.94). Also, sexual abuse was associated with 51% lower odds of receiving a Pap test in the past 3 years (OR = 0.49; 95% CI = 0.30, 0.81). After accounting for confounders (Model 2), sexual abuse was associated with 45% lower odds of receiving a Pap test in the past 3 years (OR = 0.55; 95% CI = 0.32, 0.94). Physical abuse was no longer associated with odds of receiving a Pap test in the past 3 years. Follow-up analyses that individually introduced confounders into the model with physical abuse revealed that the greatest attenuation of this relationship resulted with the introduction of educational attainment into the model. In this sample, higher educational attainment was associated with higher odds of receiving a Pap test in the past 3 years and lower odds of reporting physical abuse. In Model 3, no ACEs were associated with odds of receiving a Pap test in the past 3 years. However, when education was treated as a categorical variable, sexual abuse was still associated with lower odds of receiving a Pap test. Discussion

The present study offered important insight into how ACEs are associated with cervical cancer screenings. Findings revealed that specific ACEs are associated with both the uptake and continued use of Pap tests. This is important for a few reasons. First, it provides support for a growing body of research that has shown an association between specific ACEs and cancer overall27,28,30,31 and cervical cancer specifically.32 That is, the negative association of some ACEs on current compliance with cervical cancer recommendations may be a reason why ACEs are associated with increased odds of cancer. Next, because only specific ACEs were associated with cervical cancer screening and because associations were both positive and negative and associations depended on outcome, this research highlights the benefits of disaggregating items in the ACE scale. These items, as shown in this study, are not equally prevalent in the population. As a result, some of them may be more normative and potentially less harmful than others. Also, by analyzing specific ACEs, the field can ex-

amine more nuanced research questions and arrive at more meaningful conclusions. Notably, the findings suggest that different ACEs are important for determining ever use and continued use of Pap tests. Women who were exposed to violence among adults in the household were more likely to have ever received a Pap test. While it is unclear why this factor was protective, it is consistent with the general pattern observed among ACEs and utilization of healthcare services.16 It is also possible that experiencing vicarious violence may lead to posttraumatic growth or positive change resulting from dealing with the crisis.33 That is, women may have an increased motivation to take care of their health following exposure to violence and the potential ramifications that this violence has on others. Because this association was not observed for current Pap test compliance (i.e., in past 3 years), it is possible that this association is limited to first time screening and does not extend to repeat screening. However, because posttraumatic growth is observed in response to a wide range of adversities,33 further research should examine this as a potential explanation for the observed association between household violence and life time cervical cancer screening. Interestingly, physical and sexual abuse were each associated with reduced odds of recent cervical cancer screenings. That is, these experiences discourage regular Pap tests. It is possible that these women avoid screening altogether. However, given the high prevalence of ever screening among women in the sample, it is more likely that abuse is discouraging repeat screening. As previously mentioned, because Pap tests may lead to retraumatization and discomfort for survivors of sexual abuse,6,7 it is conceivable that these women would elect to avoid these procedures after initial negative experiences with them. Because the association between physical abuse and receiving a Pap test in the past 3 years became nonsignificant with the introduction of educational attainment into the model, educational attainment may mediate the association between physical abuse and cervical cancer screening. In this sample, higher education was associated with lower odds of abuse, but only among women aged 21–65. However, proper mediation cannot be tested in this study because, at present, binary independent variables and full weights cannot be done with Stata. Comparatively, the association with sexual abuse

CHILDHOOD ADVERSITY AND CERVICAL CANCER SCREENING

remained significant until other ACEs were accounted for, suggesting that overlap in these adversities is notable. There are limitations to consider when interpreting the results of the present study. Because the data are cross-sectional, several problems are inherent (i.e., directionality of relationships cannot be established and recall bias cannot be accounted for). However, given that cervical cancer screening does not start until adulthood, it is unlikely that screening will have led to adversity. Also, the study sample is limited to Tennessee, which is different from many other states in the country given its low population density (average of 153.9/mile2) and the fact that one-third of residents live in rural settings.34 Therefore, generalizations must be made cautiously. Next, while weights and adjustments created by BRFSS attempt to make the survey representative of the underlying population, nonresponse bias has still been a documented issue with the BRFSS.35 Consequently, the present analyses may not be fully representative of the noninstitutionalized adult population in Tennessee. Also, because of the way the BRFSS asked questions about cervical cancer screening, we cannot determine if women have undergone alternative cervical cancer screening procedures or when their hysterectomies occurred relative to their last recommended screening date. Finally, as noted previously, recommendations for screening intervals changed in 2012.26 As the data included in this analysis were from 2009, guidelines from 2003 were considered contemporary in this study. The 2012 addition of cotesting (cytology plus HPV DNA testing) for women aged 30–65 may have an impact on screening adherence, as the interval for screening with this method was extended to every 5 years. However, more research is needed to explore this effect. Limitations not withstanding, findings highlight opportunities to improve the cervical cancer screening procedures for women who are survivors of sexual and physical abuse. Healthcare providers may be able to mitigate the fears and concerns of patients undergoing Pap tests better if they screen for a history of child abuse. This is especially important given that few women who experience sexual abuse disclose this information to their physicians.36 This is further complicated by the fact that most women who have experienced sexual abuse as children are not asked about their experiences.37 This is perhaps due to reluctance on the part of physicians to screen for child abuse because they feel uncomfortable doing so or they do not see a medical need to do so.38 However, if and when women make a history of childhood sexual abuse known to their healthcare providers, efforts to make the examination more comfortable, such as sharing control of procedures with the patient and adjusting the position of the examination,6 can be made. In all, findings highlight groups of women that would greatly benefit from care that acknowledges and addresses their past childhood adversities. Author Disclosure Statement

No competing financial interests exist. References

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Address correspondence to: He´ctor E. Alcala´, PhD Department of Public Health University of Virginia 560 Ray C. Hunt Drive Charlottesville, VA 22903 E-mail: [email protected]