Breitkopf, Carmen Radecki PhD*; Catero, Jennifer*; Jaccard, James PhD†; Berenson, Abbey B. MD*
Regular Papanicolaou (Pap) screening, followed by appropriate treatment when abnormalities are detected, can prevent over 90% of cervical cancer mortality.1–3 However, 20–70% of women who attend screening and are diagnosed with a premalignant lesion fail to return for follow-up monitoring or treatment.4–6 Few data are available on the contribution of nonadherence to follow-up on cervical cancer rates; one report has shown that inadequate or delayed follow-up was an important factor in 10.8% of cases of invasive cervical cancer.7 In the United States, the majority of cervical cancers occur in women who have never been screened, who have not been screened within the past 5 years, or who have not received appropriate follow-up for identified abnormalities.8 For these reasons, cervical cancer remains a common malignancy among women and is expected to claim approximately 3,900 lives in 2004 in the United States alone.9 Minority women and women of low socioeconomic strata are at greatest risk for nonadherence10,11 and experience a disproportionate burden of cervical cancer incidence and mortality.9,12,13 Although numerous studies have addressed factors that influence uptake of Pap screening, little is understood about the factors that influence the decision to attend follow-up testing once abnormalities are detected.14
The purpose of this study was to understand the relevant perceptions surrounding a patient's motivation to return for follow-up if faced with an abnormal Pap test result. To accomplish this, we applied a general theoretical framework, the unified theory of behavior, which considers multiple influences on motivation and behavior, including cognitive, social, emotional, and environmental factors.15,16 The variables that make up the unified theory are organized into 2 sequences (Fig. 1). The first sequence outlines the determinants of behavioral intention or an individual's motivation to perform the behavior, whereas the second sequence focuses on the immediate determinants of behavior.
The present study examined social, emotional, cognitive, and environmental factors related to abnormal Pap follow-up within a multiethnic sample of socioeconomically disadvantaged women who present for health care and represent a relevant patient group for the issue of adherence. The use of a theory-driven, qualitative approach permitted us to comprehensively examine the ways in which women characterize adherence to follow-up for abnormal Pap results.
MATERIALS AND METHODS
The University of Texas Medical Branch provides primary care for a predominantly low-income population living in Southeast Texas. Female outpatients attending one of two University of Texas Medical Branch family planning clinics between May 1, 2001, and August 23, 2001, were recruited to participate in an interview about the Pap test. The majority of patients interviewed attended clinics staffed by 6 to 8 nonphysician health care providers, including certified nurse midwives and nurse practitioners. For subsequent clinic visits, patients are scheduled for the next available provider unless they indicate an individual provider preference that can be accommodated. Eligible patients were nonpregnant, African-American, Hispanic, or Caucasian women, aged 25–50 years, who presented for routine contraceptive or gynecologic care. The research protocol and informed consent process were approved by the University of Texas Medical Branch Institutional Review Board.
During the recruitment period, 213 women met eligibility criteria and were approached by the interviewer. Of those approached, 178 (84%) women were recruited to participate, and 35 (16%) refused. Of the 178 women who initially agreed to participate, 121 completed interviews, whereas 57 women left the clinic before being interviewed. Women who initially agreed to participate but left the clinic without being interviewed generally indicated that their appointment took too long and they no longer had time to complete the interview. Bias analyses on available data showed that the 57 women who initially accepted but did not complete the interview did not differ from women who accepted and completed the interview in race/ethnicity (P = .86) or age (P = .97). One interview recording was inaudible and was excluded from analysis. Data are reported for 120 interviews.
Interviews were semistructured and contained 26 open-ended questions that reflected each component of the unified theory. The specific theory components include factors that influence motivation to perform the behavior, including attitudes (overall feelings of favorability or unfavorability toward performing the behavior), normative beliefs (beliefs about what important others feel one ought to do regarding the behavior), expectancies (beliefs about the consequences of performing the behavior), self-concept, affect (emotion), and self-efficacy surrounding the behavior. In addition, the theory specifies that, for behavior to occur, the individual must intend or be motivated to perform the behavior and must possess the requisite knowledge or skills. Moreover, the behavior must be salient (important and memorable) to the individual and not prohibited by external constraints.
Participants were therefore asked to provide information about how they characterize the following: the advantages and disadvantages of attending and not attending a follow-up visit (expectancies), their feelings and emotions associated with such visits (affect), their perceived ability to attend a follow-up visit (self-efficacy), who might encourage or discourage their decision to attend follow-up (normative influences), their characterization of the type of person who does not follow-up an abnormal Pap result and how their own self-concept maps onto such characterizations (self-concept), and whether in general they favored or did not favor returning for follow-up (attitude). Additionally, women were asked to discuss potential obstacles to adherence (environmental constraints), the meaning of an abnormal result (knowledge), how they would arrange a follow-up appointment (skills), how likely it is that they personally would come back for follow-up given an abnormal result (motivation), and strategies they use to remember follow-up appointments (salience).
A total of 116 interviews were conducted in English, and 4 were conducted in Spanish; all interviews were conducted by the same individual. Sessions were audio-recorded, transcribed, and verified twice for completion and accuracy.
Two individuals independently conducted content analysis; both were experienced in qualitative methodology and familiar with the constructs of the unified theory. Content analysis was undertaken using a 3-step process of listing responses to each question (description), reviewing the data to identify consistent and relevant themes (reduction), and describing the way in which the themes reflect the constructs of the unified theory (interpretation).17,18 Merging of themes was accomplished by consensus and was performed conservatively (ie, disagreement led to maintaining separate themes rather than merging). Before coding, decision rules were established regarding the handling of repeated responses from the same subject (responses were not tallied more than once per subject) and the fidelity to participant wording (themes reflect patient's language usage). Transcripts were subsequently divided into 3 groups on the basis of participant race/ethnicity to examine patterns within groups.
Responses were tallied and verified across all interviews and by race/ethnicity. Interview findings are organized by the theory components and reflect the most frequently elicited responses. The presentation of qualitative findings includes representative quotations of frequent responses or illustrative points from the interviews. Quotations are extracted from transcripts of the interview sessions and convey the precise wording of the respondent. Bias analyses comparing women who refused and women who agreed to the interview on general demographic factors and Pap history were conducted by using t tests for comparison of continuous data, Wilcoxon rank sum (z) with exact P values for ordered categorical data, and Fisher exact test for unordered categorical data. Descriptive and analytical statistics were generated using SPSS 12.1 statistical software (SPSS, Chicago, IL).
Participants were of African-American, Hispanic, and Caucasian race/ethnicity (n = 40 per group). The median age of participants was 30. Over half of the women (n = 62) reported a high school education or less. Approximately 80% (n = 94) of interview participants were covered by Medicaid or classified as zero-pay (indigent). Nearly 60% (n = 70) of the women reported that they had experienced an abnormal Pap result in the past. Women who participated in the interview did not differ from women who refused on age (P = .95), household income (P = .60), or race/ethnicity (P = .55). A marginal (P = .049) effect of education was observed, with participants reporting higher education levels than women who refused. Refusal rates were 27% among women who had never experienced an abnormal Pap test result and 5% among women who reported experiencing an abnormal Pap result in the past (P < .01). The findings for each theoretical construct are presented below.
A majority of the sample (74%) described their attitude toward returning for follow-up to be favorable using a semantic rating scale. The percentage of women indicating a favorable rating was similar across race/ethnicity (75% Caucasian, 70% African American, 77% Hispanic, P = .75).
The most frequently mentioned normative influences for encouraging follow-up were “mother” and “mate or spouse.” Over 10% of women indicated that there was a person in their life who would discourage them from attending follow-up. When asked whose opinion would be the most important to them, “mother” was indicated most frequently, followed by “mate or spouse” and “self” for Caucasian and Hispanic women. For African-American women, “self” was the most important influence: “You need to be the one to take control…”; “I would be the number one factor there ′cause it my body.”
Perceived advantages of returning for follow-up primarily conveyed practical consequences of the behavior, whereas perceived disadvantages of attending follow-up included affective beliefs and practical constraints (Table 1). When asked about the positive consequences of not coming back for follow-up, nearly 60% of women mentioned “there are no good consequences” to not coming back. Other positive and negative consequences of not attending follow-up included, respectively, saving time and money and needing more extensive treatment later (Table 1).
The type of woman who would not adhere to follow-up recommendations was described by nearly all participants as one who is unconcerned, feels afraid or scared, does not want to know about or ignores the problem, has a low income, has family problems or conflicts with her mate, is confused or does not know what to do, and is uneducated. Not having time to come back was mentioned by African-American and Caucasian women but not by Hispanic women; the absence of a support system, family, or kids was mentioned exclusively by African-American and Hispanic women. Several Caucasian women indicated that someone who failed to follow-up probably suffered from “low self-esteem”; similarly one Hispanic woman stated “women don't feel worthy.” In contrast, very few African-American women conveyed beliefs about self worth, but several mentioned laziness or stubbornness. Women who would avoid follow-up were characterized by several minority women, but by no Caucasians, as promiscuous or diseased, “one that has sex with anybody and everybody and don't care”; “She got somethin' that's just plumb nasty.”
Women who would adhere to follow-up recommendations were described in terms of emotional status, education, social situation, and values. Across race/ethnicity, women believed that those who would come back for follow-up would be stressed and anxious: “…maybe deal with it inside to where it causes stress –most of the time once you get to that point, they come back,” scared: “…frightened, because it might be something she might not want to hear,” optimistic: “She's gonna be hopeful… that something good's gonna result by coming back.” “Probably positive, thinking that maybe something was wrong with the test…,” curious about their body: “Basically the person that come back will be just full of questions –just wantin' to know what's goin' on and why,” educated: “Somebody who…had training in reproductive organs,” concerned about their family: “Doin' not only for herself but for her family, thinkin' she has to be healthy for her children or an elder or something,” and secure: “She's confident about herself. …” “Love theyself, first of all. …”
Compared with Caucasian and Hispanic women, African Americans stated with greater frequency that adherent women are concerned about themselves and are responsible: “She listens to doctors and do what she needs to be doing.” Alternatively, Hispanic women focused on taking care of oneself to live longer and benefit others: “She would think of how she'd have to be there for her family,” “I have a family and my kids don't have a father…I wanna live,” and on the negative emotions affecting women who would come back: “She feel devastated, ashamed, like she's just been ruined,” “She feel kind of dirty…downgraded.” Finally, Caucasian and Hispanic women indicated that women who attend follow-up have family support and want to improve themselves; no African-American woman expressed these beliefs.
Fear was the most frequently mentioned emotional response to follow-up for an abnormal Pap result. Specifically, women feared finding out something was wrong, cancer, not knowing what to expect, having something life threatening, and finding out something bad or serious about their bodies for which there was no treatment. Women also stated fears about having a sexually transmitted disease and issues surrounding their relationship or partner, such as losing one's mate, being rejected, or finding out one's mate slept around. For example, one woman noted, “…women depend on a guy to take care of ‘em and that's their lifeline, just one person - and if they take a Pap test, it's abnormal and they gotta tell their boyfriend or husband…their husband or boyfriend gonna look at them like ′I don't want you' and that's gonna cause a family problem especially if you got kids involved.” Another woman indicated “You'd be scared to tell a man ′cause you think that'll run him off.” Additional fears included pain, an inability to have kids, death, human immunodeficiency virus (HIV)/acquired immunodeficiency syndrome (AIDS), other people knowing, and surgery.
In addition to being afraid, women reported feeling nervous, worried, and depressed when considering follow-up. About 15% of African-American women mentioned that they would feel calm or relaxed; this was not expressed by Caucasian or Hispanic women. For instance, “I'd probably be calm, ′cause there's no need getting irrational with it - I mean, if there's something wrong down there then you need to keep the rest pretty much calm ′cause your nerves can pretty much agitate your whole body.” Embarrassment was mentioned by Hispanic and African-American women but not by Caucasian women.
Over 1 in 5 women interviewed indicated that they would not find it easy to come back for follow-up of an abnormal Pap result within the recommended time frame using a semantic easy-difficult scale. Thirty-five percent of Caucasian and 25% of Hispanic women indicated that it would be difficult or not easy, whereas only 8% of African-American women described returning for follow-up as difficult or not easy to do. In general, African-American women indicated that women who could not overcome obstacles were only “making excuses.” Several Hispanic women looked toward faith rather than their own actions when asked about their perceived ability to return for follow-up: “If it's bad, well, God will come and do His job.”
Women expected to learn of an abnormal result by receiving a phone call or letter. Less than one quarter of women mentioned that they would take it upon themselves to call the clinic or come in to request their results. Some women looked toward physical symptoms to know when they would have an abnormal result. For instance, vaginal discharge, unusual bleeding, yellow urine, and pain were mentioned as signs of an abnormality. General skills for arranging follow-up, such as calling the clinic, were obvious to nearly all women; more specific skills, such as prearranging transportation and setting up a payment plan, were rarely mentioned. Only one woman mentioned figuring out where she would be in her menstrual cycle as an important skill for appointment scheduling.
An abnormal Pap test result was ubiquitously perceived as a sign of cancer or a sexually transmitted infection; the words “dysplasia” or “precancer” were rarely mentioned. Many women indicated “I don't know” to the question “what might an abnormal Pap result mean?” Answers such as “warts” or “HPV” (human papillomavirus), “cervical infection,” and “growth” were mentioned by less than 5% of the sample.
A number of misconceptions about Pap testing were revealed during the interviews. For example, causes of an abnormal Pap test result included “something you ate,” improper hygiene, and using unclean “sprinkled on” toilet paper. Pap testing was confused with biopsy: “…they take the little tissues…”; and sexually transmitted infection testing: “…I had another partner and I would tell him… I went and took the Pap smear test … you need to go take one.” Several women stated that an abnormal Pap test result could indicate drug use, something pregnancy-related, that you had sex with the wrong person, or were menstruating at the time of the test. Abnormal results were also attributed to scar tissue, infection (vaginal, bladder, bacterial, yeast), or a problem with the ovaries. Nine percent of those interviewed stated an abnormal Pap result could be just a clinic error.
The low socioeconomic status of our sample yielded a number of practical constraints to follow-up, such as lack of transportation, lost wages or no time off from work, no child care, and an inability to afford treatment. Lack of child care was identified as a barrier more frequently by Caucasian than African-American or Hispanic women.
When the same question regarding perceived barriers in the environment was asked with reference to other women, issues surrounding partners were revealed. Specifically, women indicated that other women might have to deal with a discouraging partner, threats of violence, and fear of losing their mate when considering whether to attend recommended follow-up.
Twenty-four percent of the sample indicated there were “no obstacles” to attending follow-up for an abnormal Pap test result. Of the women indicating no obstacles, 48% were Hispanic, 38% were African American, and only 14% were Caucasian.
Salience was asked with regard to the ability to remember the appointment and the perceived importance of the appointment. For about 15% of the sample, follow-up for an abnormal result was highly salient. African-American women in particular conveyed the idea that they “just wouldn't forget” about coming back. Nevertheless, one quarter of the women we interviewed indicated it was difficult to remember follow-up appointments. Several African-American and Hispanic participants indicated that women who say they forget are covering up for being afraid or embarrassed. When asked about ways in which the clinic could help with remembering, frequent responses included reminder calls the day before and mailed letters.
Factors associated with increasing the perceived importance of follow-up primarily addressed communication. Respondents made these suggestions: telling the patient the importance of coming back, talking to the patient and keeping the patient informed, telling the patient the risks or consequences of not coming back, giving encouragement, providing reassurance, and having “good” communication between doctor and patient. “Good” communication was described as understandable, open, and “just like one person talking to another person.” Finally, several women indicated that it was particularly meaningful when providers actually (ie, physically) sat down with patients to explain examination findings or test results.
Deficiencies in provider-patient communication, including an unconcerned or uncaring attitude, failure to give adequate explanation or information, and rude or inconsiderate behavior, were the most frequently indicated clinic-based deterrents to follow-up. In addition, women mentioned a long wait time, receiving bad service, and being rushed through the appointment. Ten percent of women stated that “scaring the patient” would decrease the likelihood that they would return for follow-up.
This study used the framework of the unified theory of behavior to understand how women conceptualize returning for follow-up of an abnormal Pap test result. We revealed a number of potential barriers to follow-up that are perhaps more amenable to change or intervention than the socioeconomic and demographic factors identified in previous research among low-income women.5,19–24 An important finding of this study was our observation that good provider-patient communication is a critical component of patient willingness to return for follow-up. This finding is consistent with previous research establishing a relationship between provider-patient rapport and adherence among adolescent patients25 and represents one facet of adherence that clinicians can strongly influence. Further, we were able to identify several key elements to include in patient encounters. For instance, many women reported that providers failed to mention the significance of an abnormal result or emphasize the importance of returning for follow-up. It is possible that providers' attempts to minimize fear and worry surrounding an abnormal result can encourage complacency among patients. In fact, several women reported that someone who is scared would be more likely to come back. This finding is consistent with those of Crane,26 in which a high negative emotional response toward an abnormal Pap test result was associated with greater adherence to follow-up recommendations. Further research is needed to understand the role of fear in patient adherence to follow-up and to identify the threshold at which fear motivates or inhibits behavior. At the provider-patient level, an individual assessment of fear and an evaluation of the potential effect of the patient's fear on her behavior may be beneficial in delivering a tailored message that will encourage follow-up for that patient.
In addition, many women we interviewed were unaware of general recommendations surrounding Pap screening intervals or follow-up of abnormal Pap results. For instance, many women were unaware of HPV testing, follow-up treatments and procedures such as colposcopy and biopsy, and a realistic timeline for resolution, and few women reported that they would be proactive about receiving their Pap results. As recommendations for Pap testing change from routine annual screening to risk-based screening that may be less frequent, it will become increasingly important to provide women with specific knowledge and individual recommendations regarding cancer prevention to guard against possible misconceptions or resistance to change.27 Furthermore, the consequences of nonadherence or long delays in adherence to follow-up must be carefully evaluated within the context of less frequent screening.
A new finding of this study is that concerns regarding relationship with a partner may influence a woman's intention of whether to attend follow-up for an abnormal Pap test. Specifically, some women responded that partners could have a direct negative impact on returning for follow-up visits by outward discouragement or threats of physical violence. Partner influences could also be more subtle; for example, the woman may fear losing her partner or being rejected if the partner learned of an abnormal result. These concerns were revealed through indirect (asking about “other women”) rather than direct inquiry (asking about themselves) and may therefore represent a barrier that is hidden to clinicians.
Several sociocultural patterns emerged when we examined the data by race/ethnicity. A positive influence of family support was seen among responses from Caucasian and Hispanic women, but not among African-American women. For example, Hispanic women stated that family members may provide emotional support to cope with bad news or provide tangible support, such as looking after the children during a clinic appointment. These data are consistent with the success of interventions that have included counseling28,29 and social support.26 In contrast, African-American women expressed strong views regarding personal responsibility for one's health and controlling one's own health. These findings suggest potentially different approaches to patient counseling about attending a follow-up visit. It is important to note that the racial/ethnic trends we report reflect consistencies in the response patterns among clinic patients responding to our interview questions. It would be inappropriate to conclude that the findings presented for a particular group necessarily apply to each individual member of the group. Nevertheless, the observed trends and patterns we report within groups and between groups can be used to stimulate further research and guide general efforts toward developing effective educational and outreach programs for targeted groups of patients.
In addition, African-American and Hispanic women were less likely than Caucasians to identify obstacles to attending follow-up. Although this study did not examine actual adherence, it is plausible that an inability to recognize and overcome obstacles in advance could lead to the poor adherence rates that have been observed among low-income and minority women in particular.22,23 One study outside the United States has shown that women who were instructed to form specific plans in advance regarding attending cervical cancer screening were more likely to attend than women not asked to develop a detailed plan.30 Our findings reveal potential barriers, such as conflict with one's mate or losing one's child care, that could potentially be overcome by assisting patients in advance to develop a specific contingency plan.
Our data show a continued need for patient education. We found many examples of poor knowledge regarding cervical cancer screening. In our study, few women understood the transient nature of some abnormal findings. For instance, several women recalled being informed of an abnormal Pap result and instructed to return for repeat Pap testing. When repeat testing yielded a normal result, they believed the initial abnormal finding was a clinic error and that attending a follow-up visit was unnecessary. If not corrected through patient education, such beliefs may reduce patient confidence in Pap test results and compromise adherence.
This study has several limitations. First, women who agreed to participate were more likely to report having an abnormal Pap result in the past than women who refused; therefore, our sample may be biased toward women with high personal involvement. Second, our sample size was small, although it relied on published guidelines for theory development and testing15,31,32 and previous qualitative studies on Pap test adherence among adolescents.25The small sample studied in this research may result in limited generalizability and nontrivial sampling error, particularly when exploring trends by race/ethnicity. Third, because of our geographic location, Hispanic women were of Mexican origin; our findings may not be relevant to Hispanic women of other backgrounds. Fourth, interview respondents had to complete reimbursement forms to participate. This criterion resulted in excluding women without social security numbers; thus, our findings may not apply to nondocumented women who receive health care in the United States. Finally, interviews conducted in Spanish were limited; our transcripts may not adequately reflect the opinions of Hispanic women who do not speak English.
The findings from this study suggest that, in addition to patient education, clinicians may facilitate adherence by directly assisting patients in their ability to anticipate obstacles, seek family support (as appropriate for the patient's racial/ethnic group), address a partner's potentially negative reaction to an abnormal result, and assign greater importance to attending recommended follow-up for an abnormal finding. Future studies are needed that examine cost- and time-effective means of performing these activities and that evaluate their impact on adherence rates in vulnerable populations.
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