In the 60 years since its introduction in the United States, Pap test screening has been responsible for a 90% decrease in deaths from cervical cancer.1 Despite this achievement, an estimated 11,000 women will develop cervical cancer in the year 2003, and 4,000 women will succumb to this potentially preventable disease.2 Despite implementation of many state and national screening programs, cervical cancer screening rates stabilized in late 1980s and did not increase significantly in the 1990s.3 Furthermore, approximately half of the women diagnosed with cervical cancer reported suboptimal screening.4–6
Efforts to improve cervical cancer mortality through outreach to underscreened women require an understanding of barriers women experience. Prior studies have focused on the inadequacies in Pap test collection and interpretation (Piper DM. Pap smear update—the Bethesda [nomenclature] System [letter]. West J Med 1991;154:325).7 However, physical, financial, cultural, and spiritual barriers also exist.8–14 Prior studies defining these barriers have focused on specific ethnic groups, analyzed a restricted number of potential barriers, or focused on general screening populations. Studies of barriers in women who have actually developed cervical cancer have queried retrospectively identified patients.5,6 The purpose of our current study was to 1) investigate the overall frequency of selected potential barriers to screening in an urban population with cervical cancer and 2) determine if there were any differences in the occurrence of selected risk factors and cultural characteristics between women with cervical cancer who had Pap test screening and those who did not. To attain this goal, a multidisciplinary team composed of clinical psychologists, clergy, nurses, physicians, patients, and patient advocates designed a questionnaire that we administered to newly diagnosed cervical cancer patients during their initial visit to the gynecologic oncology service of 3 Chicago urban hospitals.
MATERIALS AND METHODS
One hundred forty-eight consecutive women with newly diagnosed invasive cervical cancer presenting to the gynecologic oncology divisions of the departments of obstetrics and gynecology at Rush-Presbyterian-St. Luke's Medical Center, Mount Sinai Medical Center, and Cook County Hospital between August 2001 and July 2002 were asked to participate in this questionnaire study (English or Spanish versions). No identifying information was collected. Women with limited literacy were given the option of having the questionnaire read to them. Questions were adapted from the cancer control supplement of the National Health Interview Survey and expanded on the basis of input from the advisory panel for this project. This panel included physicians, patients, patient advocates, nurses, clergy, and clinical psychologists. Questions from published studies were added to establish comparisons to existing literature.15,16 The questionnaire was translated into Spanish and back-translated by certified medical translators using standard methods.17 The questionnaire was pretested on a selected group of patients eligible for, but not included in, the study. Participants who did not speak English or Spanish or were not able to understand the questionnaire were excluded. The study was previously reviewed and approved by the Institutional Review Boards of Rush-Presbyterian-St. Luke's Medical Center, Cook County Hospital, and Mount Sinai Hospital (Chicago, IL).
We divided the study participants into 2 groups according to whether they had reported never receiving a Pap test in the past (“never Pap”) or had received a screening Pap test before their cancer diagnosis (“ever Pap”). Diagnostic Pap tests performed during evaluation for a suspected cancer were excluded. Subsequently, we compared the frequency of selected demographic characteristics between the 2 groups. We then explored differences in lifestyle and attitudes between the 2 groups. The questions pertained to fatalistic attitudes, lifestyle, quality of interaction with the medical profession, and knowledge of the Pap test. We also asked participants about the acceptance of home screening.
The data were analyzed with SPSS 11.0 (SPSS Inc, Chicago, IL). Associations were tested with the χ2 or Fisher exact test and reported as the odds ratio (OR) with 95% confidence interval (CI). Significant variables in univariate analysis were entered in a multiple logistic regression model. Differences in the means of continuous variables were compared using the Student t test. Questionnaire internal validity was assessed by analyzing responses to similar questions with the Cronbach α.
Of 148 women offered the questionnaire, 146 (99%) chose to respond. Twenty-five percent (36/146) of respondents reported no prior screening (“never Pap” group), and the remaining 75% (110/146) reported having had at least one previous screening Pap test (“ever Pap” group). Table 1 presents and compares the sociodemographic characteristics of women in the “never Pap” and “ever Pap” groups. Mean age of the entire cohort was 49 years and was not significantly different between groups. The majority of participants presented to the public hospital, and public hospital patients were marginally more likely to report never having been screened.
Overall, the majority of participants were African American (73/146, 50%), followed by Hispanic (39/146, 27%), Caucasian (29/146, 20%), and other (5/146, 3%). Significantly more Hispanic women were in the “never Pap” group (OR 3.0, 95% CI 1.4–6.7). Furthermore, respondents answering the Spanish version of the questionnaire were significantly more likely to be in the “never Pap” group (OR 4.1, 95% CI 1.8–9.6). A significantly higher proportion of women with cervical cancer in the “never Pap” group reported living in the United States for less than 5 years (OR 5.7, 95% CI 2.0–16). Similarly, compared with the “ever Pap” group, a significantly higher proportion of women in the “never Pap” group lacked health insurance (OR 3.9, 95% CI 1.6–9.7) and had not completed a high school education (OR 3.6, 95% CI 1.6–8.0). Adjusted OR was not calculated for demographic variables because of colinearity in the multivariate model.
Responses to questions addressing fatalism are listed and analyzed in Table 2. Fatalistic responses to 2 questions were significantly different between the 2 groups. Compared with women who reported having had a screening Pap test, women in the “never Pap” group were more likely to think that cancer was the result of bad luck (OR 2.6, 95% CI 1.0–6.6) and state that they did not wish to be informed that they had cancer (OR 3.6, 95% CI 1.2–10). After controlling for the effects of ethnicity (as a marker of the colinear variables questionnaire language, time living in the United States, insurance status, and education), women in the “never Pap” group were still more likely to think that cancer was the result of bad luck (adjusted OR 2.6, 95% CI 1.0–6.9) and did not wish to be informed that they had cancer (adjusted OR 3.0, 95% CI 1.0–9.4). Internal validity, as measured by responses to 3 similar nonconsecutive questions, was 0.63 (Cronbach α).
Responses to questions about lifestyle, attitudes, quality of interaction with the medical profession, and knowledge of the Pap test are outlined and analyzed in Table 3. Controlling for ethnicity, a significantly higher number of women in the “never Pap” group had no family support at the time of their diagnosis (adjusted OR 3.5, 95% CI 1.1–11). Specifically, these women were more likely to respond “I have to support and care for others” or “I am all alone” rather than “I have a lot of family around to support me” or “I have some family support.” Furthermore, women in the “never Pap” group were more likely to not know that it is possible to get cervical cancer (adjusted OR 2.6, 95% CI 1.1–6.4). Fewer than 40% of either group knew that a Pap test involves scraping of cells from the cervix as a cancer prevention measure. However, ignorance about Pap test screening was no more common among women in the “never Pap” group. Twelve percent of participants thought that the Pap test was a treatment for cancer.
As a secondary analysis, we compared other variables potentially associated with fatalism and physician trust. Education level and ethnicity were not associated with fatalistic attitudes. Respondents who stated that religious beliefs influenced their health care decisions were more likely to not want to know they had cancer (OR 3.8, 95% CI 1.1–13). Hispanic respondents were more likely to trust their doctors than Caucasian or African-American respondents (OR 4.1, 95% CI 1.9–8.9). Only 16% (22/146; 95% CI 10–22%) of respondents stated they would rather do a home Pap test if one was available than have the doctor do the test. There was no correlation between interest in home testing and Pap test compliance.
We found that fatalistic attitudes, lack of family support, and lack of information about the risk of cervical cancer have a significant association with lack of Pap screening in women presenting with cervical cancer. This supports the current literature, which also identifies minority patients as well as those who are recent immigrants, have completed fewer grades of formal education, and lack health care coverage as facing barriers to Pap test screening.18–22
A similar prospective study of prior screening in women diagnosed with cervical cancer enrolled 97 women. Women were seen in 2 Brooklyn hospitals, and results were reported in 1980. Fifty-two percent of participants had no previous Pap test, and these were more likely to be older than participants reporting a previous Pap test. Although overall ethnicity, education, and time in the United States were reported, these were not compared between groups. Additionally, fatalistic attitudes and beliefs were not queried.5 A retrospective study of 664 Connecticut residents diagnosed with cervical cancer between 1985 and 1990 also showed a high noncompliance rate with any prior Pap test screening. Mean age in the nonscreened population was 64 years, compared with 46 years in the screened population. This study focused mainly on inadequacies in Pap test analysis and did not analyze other factors such as demographics or fatalism in relation to Pap test screening.4
Existing studies addressing fatalism as a barrier to cervical cancer screening have compared general Hispanic and Caucasian populations using telephone interviews.10,15,23 In these studies, Hispanic populations with suboptimal Pap test screening have consistently stated that they would not want to know if they had cervical cancer. In addition, they were more likely to believe cancer is a death sentence or God's punishment and to believe that there is little one can do to prevent cancer.23 Our results in urban cancer patients of all ethnic origins agree with those of a previous study of fatalism on self-reported use of Pap tests, which was conducted by means of telephone interviews of a Hispanic population.15 This suggests that fatalistic attitudes exist independently of a recent cancer diagnosis and are associated with lack of screening. Because fatalistic attitudes were found to be independent of ethnicity, fatalism may have a broader impact among women from all ethnic backgrounds in an urban setting. Public health messages aimed at increasing participation in screening should address this fatalism.
Financial barriers to screening have been easily identified and have received tremendous national attention. Yet ensuring insurance coverage removes only the most superficial of barriers to care. We found lack of family support contributed to noncompliance with Pap test screening. Another study including focus group discussions of cancer prevention strategies in low-income urban women found that these women consistently prioritized care for their families over care for themselves.9 Additionally, not living independently was a significant barrier to seeking care at an urban public hospital.24 Optimum screening strategies in low-income urban women need to provide for this lack of family support.
Another barrier to obtaining screening is lack of patient education. Despite attempts at education by organizations such as The American College of Obstetricians and Gynecologists, many women are unaware of the availability and purpose of a Pap test. In a study of women presenting to the Rush dysplasia clinic, 38% were unaware that they had an abnormal Pap test as the reason for referral, and 51% did not know that a Pap screening tested for precancer cells.25 In another study of Mexican-American patients with Medicare/Medicaid, 50% did not mention a Pap test or a pelvic examination as a cervical cancer detection method.16 Women who did not speak English well were even less likely to know signs and symptoms of and risk factors and screening guidelines for cervical cancer. We did not find a difference in knowledge deficit about screening for cervical cancer between our 2 groups. This is expected because women diagnosed with cervical cancer receive some education at the time of their diagnosis. However, women with cervical cancer who did not have Pap test screening were still less likely to think they could get cervical cancer. Studies of knowledge before and after educational campaigns have shown that multifaceted education efforts can improve screening rates in low-income populations.26 Along with education comes knowledge of risk factors and perception of disease severity and health impact for a particular cancer. Perception of cancer severity is an important factor in compliance with screening and in one study overshadowed the effects of income and baseline education.27
A potential area for improvement in cervical cancer screening could be the development of less invasive techniques. Pap test screening is cumbersome, uncomfortable, and embarrassing to the patient. However, despite these problems, Pap screening had drastically diminished cervical cancer rates. To address concerns about privacy and embarrassment, investigators have suggested self-testing for human papillomavirus as an alternative.28 In our study, only a minority of respondents indicated that they would practice home testing, and we found no differences in the proportion of screened and unscreened women who considered screening embarrassing. Prospective study of home screening among various populations is needed, but our results suggest that its acceptability and impact may be low among women who develop cervical cancer.
In our study, we aimed to understand why women who presented with cervical cancer missed the opportunity for screening. To encourage answers to questions to which patient may not ordinarily respond, we did not record identifiers. Limited by this design, we did not have the opportunity to report and verify cancer stage or histologic subtype. Therefore, we cannot assess the relationship between stage at presentation and compliance with screening. Also, we cannot exclude histologic subtypes less amenable to screening, such as cervical adenocarcinomas. Furthermore, we recognize that many of the demographic variables we reported are related (ie, Hispanic ethnicity versus answering the questionnaire in Spanish), but we chose to report them to allow comparisons with the findings in the literature.
Our results show that urban U.S. women who develop cervical cancer have encountered substantial barriers to screening. Improving screening in this population should focus on culturally sensitive outreach to minority women, immigrants, and women with less than a high school education. Future studies might involve education and incorporation of peers and respected community leaders, elder family members, and clergy as intermediaries who may be more successful in combating fatalistic attitudes. The low acceptability of self-screening in our survey suggests that promotion of self-screening is unlikely to resolve inequities in screening.
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