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Predictors of Papanicolaou Smear Return in a Hospital-Based Adolescent and Young Adult Clinic

From the Division of Adolescent Medicine, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; and Division of Adolescent/Young Adult Medicine, Children’s Hospital, Boston, Massachusetts.

Address reprint requests to: Jessica A Kahn, MD, MPH, Cincinnati Children’s Hospital Medical Center, Division of Adolescent Medicine, MLC 4000, 3333 Burnet Avenue, Cincinnati, OH 45229-3039; E-mail: jessica.kahn{at}chmcc.org.

	ABSTRACT

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
OBJECTIVE: Sexually active young women have relatively high rates of abnormal cervical cytology, yet compliance with return for Papanicolaou smear screening and follow-up appointments is poor. The aim of this study was to determine whether a theory-based model could explain compliance with return visits.

METHODS: Participants in this longitudinal cohort study were sexually active young women 12–24 years of age presenting to a hospital-based adolescent clinic. Participants completed self-administered surveys and were then followed for up to 15 months to assess for the outcome measure, return. Logistic regression modeling was used to determine variables independently associated with return. RESULTS: The outcome measure, return, was available for 439 of 490 participants (90%). Mean participant age (± standard deviation) was 18.3 (± 2.2) years, 49% were black, 23% were Hispanic, and 51% had Medicaid health insurance. Variables independently associated with return included belief that the Papanicolaou smear will not be painful (odds ratio [OR] 1.73, 95% confidence interval [CI] 1.08, 2.83), belief that return for follow-up will prevent cervical cancer (OR 1.83, 95% CI 1.12, 3.07), likelihood that the doctor will be honest (OR 4.07, 95% CI 1.37, 17.5), and low self-reported impulsivity (OR 1.66, 95% CI 1.06, 2.63). Family history of cervical cancer was associated with decreased likelihood of return (OR 0.28, 95% CI 0.08, 0.78).

CONCLUSION: Specific beliefs about Papanicolaou smears and providers, low self-reported impulsivity, and no family history of cervical cancer are associated with return for Papanicolaou smear screening and follow-up visits. These findings may guide the design of interventions to increase compliance with recommendations for Papanicolaou smear return.

Genital human papillomavirus (HPV) is one of the most common sexually transmitted infections, with prevalence rates of 28–46% in sexually active adolescent and young adult women.^1,2 Infection with certain high-risk HPV types, such as 16, 18, 31, and 45, is associated with the development of cervical dysplasia, carcinoma in situ, and invasive cervical cancer.^3–6 Screening in adolescents currently is dependent on the use of the Papanicolaou smear for early detection of cytologic abnormalities. Compliance with appointments for Papanicolaou smear screening and with follow-up appointments to evaluate and treat high-grade precursor lesions are important to decrease cervical cancer mortality.^7,8 However, the estimated rates of noncompliance with Papanicolaou smear follow-up appointments are unacceptably high, ranging from 23% to 80%.^9–12

In an effort to strengthen the evidence for interventions targeting adolescent and young adult women, we developed a conceptual model to explain return for Papanicolaou smear follow-up. The model was based on four theories shown to predict cancer prevention behaviors in adults: the Theory of Planned Behavior,¹³ Health Belief Model,¹⁴ Social Cognitive Theory,¹⁵ and the Transtheoretical Model and Stages of Change.¹⁶ In a previously published, cross-sectional study, we reported that intention to return was associated neither with knowledge of HPV and Papanicolaou smears nor with previous behaviors. However, patient attitudes did predict intention to return, including personal beliefs about return, normative beliefs about return, perceived control over return, and cues to obtain a Papanicolaou smear.¹⁷ After revising the theoretical model based on these findings (Figure 1), we designed the prospective, longitudinal study described in this article to test the following hypotheses: 1) intention to return partially mediates the association between attitudes and actual return (that is, intention to return is the mechanism through which attitudes impact on return), and 2) knowledge about Papanicolaou smears and HPV, attitudes about Papanicolaou smear follow-up, risk behaviors, impulsivity, and sociodemographic factors independently predict actual return. The model essentially proposes that knowledge, attitudes, behaviors, impulsivity, and sociodemographic factors impact directly on return for Papanicolaou smear screening and follow-up visits, and that attitudes also impact indirectly–hrough intention to return–n return.

View larger version (23K): [in this window] [in a new window]   Figure 1. Hypothetical compliance model: knowledge about Papanicolaou (Pap) smears and human papillomavirus (HPV), attitudes, risk behaviors, and impulsivity hypothesized to influence intention to return and actual return for Papanicolaou smear follow-up. Kahn. Papanicolaou Smear Return. Obstet Gynecol 2003.

	MATERIALS AND METHODS

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

We conducted a longitudinal cohort study, consisting of a survey administered at baseline and longitudinal follow-up for up to 15 months to determine return for recommended Papanicolaou smear screening and follow-up visits. The self-administered, pencil-and-paper survey instrument was completed during a clinic visit by those adolescent and young adult women who provided informed consent. Items were chosen based on theories of health behavior and the findings of preliminary qualitative data collection.¹⁸ Previous reports describe the items and scales measuring knowledge about HPV and Papanicolaou smears, attitudes, and behaviors.^17,19–21 Attitudes assessed included behavioral beliefs, normative beliefs (beliefs of people important to the participant regarding whether she should return for Papanicolaou smear follow-up), perceived behavioral control (perceived control over returning), health beliefs (perceived severity of and susceptibility to abnormal cervical cytology and cervical cancer), and communication with the provider regarding Papanicolaou smears. Behaviors assessed included risk behaviors and associated health outcomes linked to the development of abnormal Papanicolaou smears or cervical cancer, and past compliance with Papanicolaou smear follow-up. Impulsivity was measured using 13 items from the Eysenck impulsivity scale.^22,23

Past compliance with Papanicolaou screening and follow-up was assessed using computerized medical and cytology records from the hospital’s electronic medical record, supplemented by the paper record when necessary. Past compliance, derived from practices standard in the clinic, was defined as having kept an appointment for 1) a routine Papanicolaou smear within 15 months of the prior test, 2) a follow-up Papanicolaou smear within 6 months of a smear demonstrating atypical squamous cells of undetermined significance (ASCUS), or 3) colposcopy within 2 months of a second smear demonstrating ASCUS or a first smear demonstrating low-grade squamous intraepithelial lesion (SIL) or high-grade SIL. Participants were followed prospectively to determine current compliance with Papanicolaou screening and follow-up, using the Papanicolaou smear performed prior to the survey as the index Papanicolaou smear. Criteria for current compliance, the outcome measure, were similar to those for past compliance but also included having returned specifically for a pelvic examination or Papanicolaou smear within the follow-up period. We assessed the outcome using clinic notes from the electronic medical record. During the follow-up period, all clinicians were asked to record in the electronic and paper medical record the reason for each visit as reported by the patient. If a participant had not returned to the clinic at all after the survey was completed, a research assistant attempted to contact her. The participant was asked if she had obtained any gynecologic care elsewhere since the survey was completed, and if so, the research assistant obtained permission to contact that facility and obtain any records of Papanicolaou smears or colposcopy. Sociodemographic factors assessed were age, race, ethnicity, and insurance status. All independent variables that were assessed are summarized in Table 1.

The scale assessing knowledge about Papanicolaou smears and HPV was dichotomized into zero (none of items was answered correctly) and greater than or equal to one, because the scale was highly skewed, and the majority of participants received a score of zero. Individual items constituting the scales measuring behavioral beliefs about Papanicolaou smear follow-up, normative beliefs, perceived behavioral control, communication with the provider, health beliefs, cues to return, and impulsivity were analyzed as dichotomized variables.¹⁷ Intention to return was analyzed as a dichotomous variable: Responses of very or somewhat sure were categorized as "intends to return," and responses of neither sure nor unsure, somewhat unsure, or very unsure were categorized as "does not intend to return." Items were dichotomized both because responses to most items were highly skewed and for theoretical reasons: Responses to Likert-type scales are frequently dichotomized for analysis into neutral through negative responses and positive responses. The outcome variable was defined as having returned or not returned for recommended follow-up and was therefore dichotomous.

A variable that functions as a mediator accounts for the relation between the independent variable and the dependent variable. That is, the independent variable influences the mediator which, in turn, influences the dependent variable; the mediator is the mechanism through which the independent variable impacts on the dependent variable.²⁴ To test the first hypothesis, whether intention to return partially mediated the association between attitudes and return, we used the following criteria.²⁴ First, the mediating variable must be associated significantly with both the independent variables (individual attitudes) and the dependent variable (return). Associations between intention to return and attitudes (Figure 1, path A) have been reported previously.¹⁷ The association between intention to return and return (Figure 1, path B) was assessed using a ² test. Second, when the mediating variable is added to logistic regression models estimating the associations between individual attitudes and return, there is a reduction in the ß coefficient (effect size) associated with each attitude.

To test the second hypothesis, whether knowledge, attitudes, behaviors, impulsivity, and sociodemographic factors independently predict return, we first examined bivariate associations between predictor variables and return (Figure 1, paths C and D). We used a ² test if predictor variables were dichotomized or categorical, and a Wilcoxon rank-sum test, Student t test, or univariate logistic regression if predictor variables were ordinal or continuous. Those variables associated with return at P < .10 were eligible for the stepwise logistic regression procedure to identify variables independently associated with return.²⁵ We did not perform a test of multiple comparisons because the purpose of these bivariate analyses was only to determine which independent variables were eligible for the logistic regression. Only those variables significantly associated with return at P < .05 remained in the final model. We also used the best subsets model selection technique, with identical results.²⁶ Adjusted odds ratios (OR) and 95% confidence intervals (CI) are reported for the models. We performed statistical analyses using SAS 8.2 (SAS Institute Inc., Cary, NC).

	RESULTS

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
The outcome measure, return for follow-up, was available for 439 of the 490 participants (90%). Those who remained in the study did not differ from those lost to follow-up in terms of age, risk behaviors, or selected attitudinal variables, but were more likely to report they were white (P = .04). Mean participant age was 18.3 years (standard deviation 2.2 years), approximately half of the participants were black, and approximately half reported Medicaid insurance (Table 2). Although 360 (82%) participants intended to return at baseline, only 133 participants (30%) actually returned for Papanicolaou smear follow-up appointments.

Those independent variables associated at P < .10 with return (that is, those eligible for the logistic regression analysis) are as follows. Age (analyzed both as a dichotomous and as a continuous variable), race, ethnicity, and insurance status were not associated with return. Higher knowledge of HPV and Papanicolaou smears was associated with return. Fewer of those who returned, compared with those who did not return, had a low score on the scale measuring knowledge (49% of those who returned compared with 60% of those who did not return, P = .036). Three behavioral beliefs were associated with return. Those who returned, compared with those who did not return, were more likely to believe that returning for Papanicolaou smear follow-up would help prevent cancer (80% versus 69%, P = .021) and were more likely to believe that the follow-up Papanicolaou smear would not be painful (77% versus 65%, P = .013). Those who returned, compared with those who did not return, were also more likely to believe that their provider would communicate well with them at the follow-up visit (90% versus 83%, P = .05). One item measuring perceived control over return, belief that one has high control over coming in for the next Papanicolaou visit, was associated with return: 80% of those who returned, compared with 72% of those who did not return, reported high perceived control over return (P = .074). Four items measuring communication with the provider were associated with return. Those who returned, compared with those who did not return, were more likely to believe the provider would be honest at the follow-up visit (98% versus 91%, P = .008), would answer all her questions (98% versus 94%, P = .081), would know about the health issues of teenagers (93% versus 87%, P = .092), and would respect her (96% versus 92%, P = .092).

One item assessing perceived risk, personal likelihood of dying of cervical cancer, was associated negatively with return. Those who returned, compared with those who did not return, were less likely to perceive their likelihood of dying to be high (29% versus 40%, P = .028). One cue to action, having received a letter or call from the clinic about the follow-up visit, was associated negatively with return: Those who returned, compared with those who did not return, were less likely to have received a cue to return (22% versus 31%, P = .059). One of the items measuring impulsivity, which assessed whether the participant considered herself an impulsive person, was negatively associated with return: Those who returned were less likely to consider themselves impulsive than those who did not return (29% versus 40%, P = .027). Two behaviors/associated outcomes were associated with return. Those who returned, compared with those who did not return, were less likely to have had a previous pregnancy (27% versus 36%, P = .086) and were more likely to have been compliant with past follow-up appointments (71% versus 59%, P = .05). Reported family history of cervical cancer was negatively associated with return: Those who returned were less likely than those who did not to report a positive family history (9% versus 25%, P = .024). History of an abnormal Papanicolaou smear was not associated significantly with return. Of those with a history of all normal Papanicolaou smears, 32% returned for follow-up, and of those with a history of an abnormal Papanicolaou smear, 26% returned for follow-up (P = .25).

Of the 15 variables associated with return at P < .10 in bivariate analyses, five made up the logistic regression model predicting return. However, only those variables that had been associated with return in bivariate analyses at P < .05 ultimately entered into the logistic regression model. Variables independently associated with return in the logistic regression model included two beliefs about Papanicolaou smear follow-up (the Papanicolaou smear will not be painful and the follow-up visit may prevent cervical cancer), one belief about communication with the provider (provider will be honest), low self-reported impulsivity, and no family history of cervical cancer (Table 3). We attempted to stratify the study sample into those with a normal index Papanicolaou smear (whose recommendation was for a screening Papanicolaou smear) and those with an abnormal Papanicolaou smear (whose recommendation was for a follow-up smear or colposcopy) to determine whether predictors of return differed in the two groups. We did not report these results because when stratified logistic regression models were run, the models were unstable; this is likely owing to the small sample sizes within each strata. However, we did estimate a logistic regression model identical to the model shown in Table 3, but controlling for screening versus follow-up Papanicolaou smear recommendation. The variable representing screening versus follow-up recommendation was not significantly associated with return, and the ß coefficients and P values associated with the other predictor variables were essentially unchanged. Thus, it does not appear that recommendation for a screening versus follow-up visit affects which variables predict return.

	DISCUSSION

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

There are several potential explanations for why intention did not predict return in our study. First, it is possible that a short-term association between intention and return extinguished over the 15-month follow-up period. Second, adolescents may have reported high intention to return because they perceived it to be a socially desirable response. Responses to the item assessing intention to return were skewed, with only 78 (18%) participants indicating that they did not intend to return. This restricted variance may have limited the power to detect an association between intention and return, and thus to determine whether intention mediates the association between attitudes and behavior. Finally, adolescents may intend to return but subsequently encounter barriers to return, such as difficulty obtaining transportation to the clinic, change in insurance coverage, or concerns about breach of confidentiality. Further research is needed to clarify the link between intention and specific behaviors in adolescent populations, but these data suggest that a clinical assessment of whether an adolescent intends or does not intend to return for follow-up may not be useful in predicting whether or not she will actually return.

Although intention to return was not associated with return, we identified several independent predictors of return. As hypothesized, attitudes and impulsivity were independently associated with return. Three of the variables associated with follow-up–belief that the Papanicolaou smear will not be painful, that returning for follow-up may prevent cervical cancer, and that the provider will be honest during a Papanicolaou smear visit–are potentially modifiable factors in the clinical setting. Impulsivity is not a construct incorporated into most theories of preventive health behavior, although it has been associated with risk behaviors.^20,30–32 These data and prior qualitative work suggest that impulsivity may be an important issue to consider in adolescents who do not return for follow-up appointments. Report of a family history of cervical cancer was negatively associated with return for follow-up. Young women who believe that they have a family history of cervical cancer may perceive themselves to be at high risk. They may avoid follow-up appointments for the same reasons some adult women report: They fear the diagnosis of cancer, wish to avoid medical procedures such as colposcopy, or would prefer not to know about the diagnosis because they perceive cervical cancer to be an incurable disease.^33–36

Participants with higher knowledge about HPV and Papanicolaou smears were more likely to return, but this variable did not enter into the final logistic regression. Knowledge may be operating as a confounder of the association between attitudinal variables and return. A confounding variable is an extrinsic factor that is associated with the independent variable and is a cause of the outcome, or dependent, variable. For example, knowledge is associated with return for follow-up (OR = 1.56, 95% CI 1.03, 2.38), and is also associated both with belief that Papanicolaou smear follow-up will prevent cervical cancer (Spearman r = .15, P < .05) and likelihood that the doctor will be honest (Spearman r = .15, P < .05). When both knowledge and belief about prevention of cervical cancer are entered into the model predicting return, both become nonsignificant.

A primary goal of this study was to provide information that could be used to increase compliance with Papanicolaou smear screening and follow-up visits in adolescent and young adult women. Although our return rate of 30% is somewhat lower than that reported in some previous studies, perhaps because we rigorously defined return as a visit specifically for a Papanicolaou smear or colposcopy, other reported return rates are also unacceptably low.^9,10,12,37 A number of investigators have conducted interventions aimed at improving compliance with Papanicolaou smear screening or follow-up visits.^38–44 Although older adolescents were eligible for some of these interventions, the study samples predominantly consisted of adult women. Yabroff et al conducted a meta-analysis of those interventions designed to improve follow-up after abnormal Papanicolaou smears, categorizing interventions into cognitive, behavioral, sociologic, or combined strategies.⁴⁵ Cognitive strategies, such as educational pamphlets and telephone counseling, and behavioral strategies, such as telephone reminders, increased follow-up modestly, whereas the sociologic intervention of videotaped peer discussions of Papanicolaou smears did not change return rates. Recently, Sheeran and Orbell showed that an intervention consisting of specifying implementation intentions (that is, when, where, and how participants would make a follow-up appointment) was associated with higher return rates.²⁷

Although there are a number of descriptive studies and reviews of compliance with follow-up appointments among adolescents,^46–50 there are few published interventions aimed at enhancing adolescent compliance with appointments.⁵¹ A potential application of our findings is the design of interventions that combine information on adolescent-specific predictors of return for Papanicolaou smear follow-up with the types of intervention strategies that have been used successfully in adults. The constructs identified as predictors of Papanicolaou follow-up may be used as content in cognitive, behavioral, or sociologic interventions targeting adolescents. For example, an individualized counseling session or educational pamphlet might focus on avoidance of discomfort during the pelvic exam, the role of screening in cervical cancer prevention, and reassurance that the provider will give all pertinent information in an honest and straightforward way. Providers might consider inquiring about a family history of cervical cancer and exploring how this might impact follow-up.

There are several limitations to this study. First, the participants were recruited from an urban, hospital-based clinic with a high proportion of minority and low-income young women. Results may not be generalizable to other populations of young women. Second, items comprising several of the scales were created for the purposes of this study because there were no existing instruments available to measure knowledge and attitudes about Papanicolaou smears in adolescents. Although the items were chosen based on prior qualitative work and behavioral theory, there were no existing data on validity and reliability of these measures.

Despite these limitations, this study provides new data on identifiable predictors of Papanicolaou smear screening and follow-up appointments in adolescent and young adult women that may be applied in clinical settings. Ultimately, improving compliance with cervical cancer prevention recommendations in young women is likely to require comprehensive interventions at the individual and population levels.⁵² At the individual level, both patient and provider education regarding cervical cancer screening and adherence are needed. At the population level, social marketing strategies that enhance public awareness of cervical cancer prevention may help create a milieu that supports individual decisions to seek screening. Future research should focus on testing interventions to enhance follow-up that are theoretically grounded, evidence-based, and achievable in the office setting.

	Footnotes

 
Funding for this research was provided by The Deborah Munroe Noonan Memorial Fund; Projects No. 5 T71 MC 00009-09 and 5 T71 MC 00001-24 from the Maternal-Child Health Bureau, Health Resources and Services Administration, U.S. Department of Health and Human Resources; and a Research Career Award from the National Institute of Allergy and Infectious Diseases (K23 AI50923-01, Principal Investigator JAK).

PII S0029-7844(02)02592-9

Received May 20, 2002. Received in revised form July 29, 2002. Accepted August 8, 2002.

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