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Cervical Cancer Screening for Women Living With HIV
Cervical Cancer Screening for Women Living with HIV crystal lambert chaPman allyssa l. harris
10 DEC
Appointment Reminder Hi Sara! You have an appointment scheduled for Tuesday, December 10th at 9:45am.
Women living with HIV are at greater risk for human papillomavirus (HPV) infection, cervical dysplasia, and cervical cancer than are uninfected women (Abraham et al., 2013; Grulich, van Leeuwen, Falster, & Vajdic, 2007). A national longitudinal cohort study consisting of women living with HIV and uninfected women suggests that women living with HIV are about two to eight times more likely to develop cervical cancer than uninfected women, and severely immune-suppressed women living with HIV have the highest risk (Abraham et al., 2013). Despite these greater risks, recent studies suggest that as many as 50% of these women are not being screened appropriately (Baranoski, Horsburgh, Cupples, Aschengrau, & Stier, 2011; Lambert et al., 2015; Simonsen et al., 2014). In this article we provide an overview of cervical cancer screening for women living with HIV. Abstract: Studies suggest that women living with HIV are not being adequately screened for cervical cancer. In this article we review the latest recommendations for cervical cancer screening in women with HIV and make recommendations for clinical practice. http://dx.doi.org/10.1016/j.nwh.2016.07.002 Keywords: cervical cancer screening | HIV | HPV | Pap test | women’s health
HPV, the most common sexually transmitted infection in the United States, is responsible for about 99% of cervical cancer cases (Centers for Disease Control and Prevention [CDC], 2015b). Almost 80 million Americans are currently infected with one or more subtypes of HPV, and approximately 15 million Americans will become infected annually (CDC, 2016). The HPV virus is transmitted person to person during skin-toskin contact, including sexual contact. HPV is a group of viruses with more than 150 subtypes, of which approximately 40 subtypes can infect the genital areas (National Cancer Institute, 2015). There are many highrisk types of HPV. High-risk types HPV-16 and HPV-18 are responsible for approximately 70% of cervical cancer cases. Women living with HIV are more likely to have persistent coinfection with HPV, a history of abnormal Pap test results, and a degree of immune suppression leading to an increase in prevalence and incidence of cervical cancer (American College of Obstetricans and Gynecologists [ACOG], 2010; Massad et al., 2010). A meta-analysis of HPV types among women with HIV found that 36% of the women were infected with some type of HPV and that 12% were infected with multiple types (Clifford, Gonçalves, Franceschi, & HPV and HIV Study Group, 2006). Because HPV persistence in women living with HIV is common, the rates of cervical cancer are likely to be greater in this population. Persistent HPV infections lead to more cases of abnormal cervical cytology, including squamous intraepithelial lesions and atypical cells of undetermined significance, which are more common in women with HIV (Tello et al., 2010). In addition to HPV, other risk factors that increase a woman’s chances of cervical cancer are smoking, chlamydia infection, obesity, long-term oral contraceptive use, family history, poverty, having three or more full-term pregnancies, and a diet poor in fruits and vegetables (Akers, Newmann, & Smith, 2007; American Cancer Society, 2014). Therefore, conducting a careful health history and providing education on reducing modifiable risk factors are essential components in clinicians’ care of women to improve their awareness of HPV prevention measures.
Women and HIV Despite advances in raising awareness about HIV infection, women continue to experience significant HIV infection rates. Women account for 20% of all new HIV infections
Crystal Lambert Chapman, PhD, CRNP, FNP-BC, is an assistant professor in the School of Nursing at the University of Alabama at Birmingham in Birmingham, AL. Allyssa L. Harris, PhD, RN, WHNP-BC, is an assistant professor in the William F. Connell School of Nursing at Boston College in Chestnut Hill, MA. The authors report no conflicts of interest or relevant financial relationships. Address correspondence to: [email protected].
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and approximately 25% of individuals living with HIV (CDC, 2015a). Therefore, the topic of women and HIV is timely and relevant for nurses and other clinicians working in women’s health care. Advances in antiretroviral therapy over the past three decades have improved life expectancy and decreased the incidence of many AIDS-defining cancers (i.e., Kaposi sarcoma and non-Hodgkin lymphoma) among people living with HIV. However, the incidence of cervical cancer, also an AIDS-defining malignancy, has not decreased. Several studies suggest that cervical cancer is more prevalent in women with lower CD4 T lymphocytes (Abraham et al., 2013; Keller et al., 2012). However, despite CD4 T-lymphocyte count, incidences of cervical cancer are higher among women living with HIV than women who are not infected with HIV. Findings from the Women’s Interagency Health Study showed that cervical cancer incidences were generally greater in women living with HIV and specifically greater among severely immunosuppressed women living with HIV (Abraham et al., 2013). This multicohort prospective study found that women with HIV had a twoto fivefold greater incidence of invasive cervical cancer rates than women without HIV, and the incidence of invasive cervical cancer rates increased with lower CD4 counts (Abraham et al., 2013). Therefore, treatment alone is not sufficient to reduce cervical cancer incidence.
Pap Test Guidelines for Women Living With HIV In recent years, guidelines on Pap test screening for the general population have changed from screening annually to screening every 3 years for women ages 21 to 65 years (ACOG, 2016; Fontaine, Saslow, & King, 2012). Women with abnormal results are scheduled for more frequent screening and additional testing with a specialist (Massad et al., 2013). Pap test guidelines differ for women living with HIV. Until recently, Pap testing was recommended at the time of initial HIV diagnosis, 6 months from baseline, and annually thereafter (ACOG, 2010; U.S. Department of Health & Human Services & Health Resources and Services Administration, 2013). Currently, Pap testing is recommended at the time of HIV diagnosis, 6 to 12 months from baseline, and annually thereafter until three consecutive normal Pap test results are obtained (Panel on Opportunistic Infections in HIV-Infected Adults and Adolescents, 2015). After three consecutive normal Pap test results, screening is recommended every 3 years (Panel on Opportunistic Infections in HIV-Infected Adults and Adolescents, 2015). Despite the increased risk of developing invasive cervical cancer, women living with HIV are less likely to have cervical cancer screening. Recent data report that 22% to 56% of women with HIV had not received an annual Pap test after baseline (Baranoski et al., 2011; Lambert et al., 2015; Oster, Sullivan, & Blair, 2009; Simonsen et al., 2014; Tello et al., 2010),
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Opening photo © iStock Collection / thinkstockphotos.com
Risk Factors
Pap test rates among women living with HIV are suboptimal, and the reasons for suboptimal screening are complex and multilayered and approximately 75% had not received the second recommended Pap test during their first year in care (Logan, Khambaty, D’Souza, & Menezes, 2010). Pap test rates among women living with HIV are suboptimal, and the reasons for suboptimal screening are complex and multilayered.
Photo © Deirdre Rusk / thinkstockphotos.com
Reasons for Poor Screening In general, there are multiple reasons that women are not being screened. These include poor health habits, misunderstanding of changing Pap test guidelines by women and their health care providers, current abstinence from sexual activity, fear of pelvic examinations, and/or history of pelvic trauma, as well as systemic barriers that include health care access issues, lack of health care and health insurance, transportation and child care issues, and fatalistic attitudes (Coughlin, King, Richards, & Ekwueme, 2006; Downs, Smith, Scarinci, Flowers, & Parham, 2008; Garbers & Chiasson, 2004; McMullin, De Alba, Chávez, & Hubbell, 2005). For example, fear of pain is one barrier to Pap testing. Findings from a longitudinal study of 420 women with unknown HIV status suggest that perceptions of pain influence Pap testing by limiting women’s willingness to schedule a Pap test (Gauss, Mabiso, & Williams, 2013). Additionally, cultural
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practices may influence Pap testing. The literature is mixed on racial and ethnic barriers (Baranoski et al., 2011). Women living with HIV have additional barriers to cervical cancer screening. This population often requires complex care that involves multiple clinicians, such as infectious disease clinicians, primary care providers, and women’s health providers. Sometimes women and their health care providers lose sight of routine preventive primary care needs (i.e., Pap testing), focusing instead on what they deem as more urgent care (i.e., HIV care). Women may not be receiving all of their care at one site and may have to make additional appointments with women’s health or primary care providers. Lack of centralized care can be cumbersome for some women, and they may forgo preventive health care services and focus only on their HIV care needs. Also, women living with HIV fear disclosing their status to additional health care providers because of HIV-related stigma (Audet, McGowan, Wallston, & Kipp, 2013). Research suggests that health literacy is associated with poor cervical cancer screening awareness and use, but again the data are mixed. Among a sample of 145 women living with HIV, women with low health literacy were less likely to report having an annual Pap test (Bynum et al., 2013). In the same study,
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women with low health literacy reported having at least two Pap tests in the first year after initial screening, which may suggest confusion among women who reported low health literacy. Many women confuse Pap testing with a general pelvic examination, which could explain the mixed results. HIV care also has
the potential to be complex and burdensome. This may result in increased health literacy challenges for women living with HIV. Therefore, women living with HIV could benefit from interventions aimed at improving health literacy and awareness of the significance of screening. Psychosocial barriers such as depression have been associated with lack of testing. For example, researchers at the Johns Hopkins HIV clinic examined barriers to adherence with gynecologic care among 200 women living with HIV. In this study, moderate and severe depression was associated with missing gynecology appointments and lack of a documented Pap test (Tello et al., 2010). Likewise, in Boston, Baranoski et al. (2011) assessed risk factors for inadequate Pap testing. Results showed that depression was associated with poor Pap test adherence in a diverse sample of women living with HIV. Individuals who engage in unhealthful behaviors, such as drug use and tobacco use, are potentially unlikely to be engaged in preventive health behaviors (i.e., Pap testing). Baranoski et al. (2011) conducted a chart review of 549 women living with HIV to assess factors associated with poor Pap test follow-up. Current or former drug use or cigarette smoking was associated with increased odds of poor Pap test adherence (Baranoski et al., 2011). Laboratory test results, such as level of CD4 T-lymphocyte cells (also known as T cells), provide a measure of immune health in people living with HIV. Lower numbers of T cells indicate advanced HIV disease. Data are mixed regarding the association of Pap test adherence among women living with
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HIV and CD4 T-lymphocyte count. For example, the results of Baranoski et al. (2011) suggests that Pap test adherence is associated with T-cell counts of less than 200 cells/mm3, yet Tello et al. (2010) suggest that, according to their research, a relationship does not exist. Authors of the former study obtained laboratory test values from medical records, whereas authors of the latter administered a survey to each participant requesting self-reported laboratory test results. Self-report measures may be less accurate because of participant recall error. Therefore, laboratory values from Baranoski et al. (2011) are likely more accurate because of lack of recall bias. As researchers continue to investigate the relationship between Pap test adherence and T-cell count, clinicians must educate, encourage, and improve access for all women living with HIV and specifically women with advanced HIV disease.
Implications for Nursing Practice Nurses, advanced practice nurses, and other women’s health care clinicians must stay abreast of current cervical cancer screening guidelines generally for all women and specifically for those women at greater risk. It is important to assess women’s perceptions and attitudes related to cervical cancer and screening.
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women living with HIV could benefit from interventions aimed at improving health literacy and awareness of the significance of screening
Understanding their attitudes and beliefs enables clinicians to provide education to increase awareness and, hopefully, Pap testing uptake. It’s critical to increase awareness, stress the importance of screening, and pay particular attention to barriers. In today’s HIV health care environment, disease management guidelines are consistently changing as evidence improves through research. HIV-specific guidelines are rapidly changing, and it is essential for nurses and other health care providers to be aware of the latest updates (Panel on Opportunistic Infections in HIV-Infected Adults and Adolescents, 2015). Currently, differences exist between the recommendations of the Panel on Opportunistic Infections in HIV-Infected Adults and Adolescents (2015) and those of ACOG (2010). The latter organization recommends Pap testing at the time of HIV diagnosis, 6 to 12 months from baseline, and annually thereafter until three consecutive Pap tests yield normal results. However, the former organization recently released guidelines recommending extending screening to every 3 years after three consecutive normal Pap test results. These discrepancies have the potential to result in confusion and missed opportunities to provide preventive health care. It is important that health care providers unfamiliar with HIV management seek assistance from an HIV specialist.
Limiting Barriers Reasons for poor Pap test adherence are multifaceted. The literature has identified several barriers to Pap screening, including lack of provider knowledge, complex care plans, psychological factors (i.e., fear and embarrassment), systematic factors (i.e., lack of insurance), and individual factors (i.e., lack of transportation, competing demands, and lack of child care). Although nurse practitioners and nurses have a key role in staying abreast of new guidelines, they can also play a critical role in accessing and limiting barriers to screening. Some examples include establishing reminder systems for women to improve adherence and using electronic sources such as e-mail and text messaging to remind women of an upcoming appointment. Creating systematic processes to reduce barriers, such as limiting multiple appointment burdens, could also improve adherence. Systematic processes could include establishing a woman-centered practice that focuses specifically on the health needs of women. This clinic could operate daily or weekly with consistent nurses and nurse practitioners. Another option is to hire a women’s health nurse practitioner to deliver evidence-based care during primary care appointments. Another strategy is to use social media to increase awareness and stress importance of cervical cancer screening. A renowned HIV ambulatory care clinic in the southeastern United States uses media (i.e., brochures, posters, and a brief verbal message) to engage women receiving HIV care (Raper, 2014). These strategies can be used to improve cervical cancer screening awareness and stress the importance of screening.
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Conclusion Cervical cancer is a highly preventable cancer (CDC, 2012), yet screening via Pap testing is suboptimal for all women generally and especially for women living with HIV. Women living with HIV are at greater risk for cervical cancer than women without an HIV diagnosis. It is important for women’s health care nurses to be aware of the cervical cancer screening guidelines for women living with HIV, focusing on providing education and information on the importance of Pap testing adherence. Women living with HIV encounter many barriers—individual, psychological, systematic, and complexity of care—potentially limiting their ability to engage in screening. It is important for women’s health nurses and other clinicians to be aware of the specific health care challenges facing women living with HIV. NWH
References Abraham, A. G., D’Souza, G., Jing, Y., Gange, S. J., Sterling, T. R., Silverberg, M. J., . . . North American AIDS Cohort Collaboration on Research and Design of IeDEA. (2013). Invasive cervical cancer risk among HIV-infected women: A North American multicohort collaboration prospective study. Journal of Acquired Immune Deficiency Syndromes, 62(4), 405–413. doi:10.1097/ QAI.0b013e31828177d7 Akers, A. Y., Newmann, S. J., & Smith, J. S. (2007). Factors underlying disparities in cervical cancer incidence, screening, and treatment in the United States. Current Problems in Cancer, 31(3), 157–181. doi:10.1016/j.currproblcancer.2007.01.001 American Cancer Society. (2014). Cervical cancer. Atlanta, GA: Author. Retrieved from http://www.cancer.org/acs/groups/cid/ documents/webcontent/003094-pdf.pdf American College of Obstetricans and Gynecologists. (2010). ACOG Practice Bulletin No. 117: Gynecologic care for women with human immunodeficiency virus. Obstetrics & Gynecology, 116(6), 1492–1509. doi:10.1097/AOG.0b013e3182054cae American College of Obstetricians and Gynecologists. (2016). Practice bulletin no. 157: Cervical cancer screening and prevention. Obstetrics & Gynecology, 127(1), e1–e20. doi:10.1097/ AOG.0000000000001263 Audet, C. M., McGowan, C. C., Wallston, K. A., & Kipp, A. M. (2013). Relationship between HIV stigma and self-isolation among people living with HIV in Tennessee. PLOS One, 8(8), e69564. doi:10.1371/journal.pone.0069564 Baranoski, A. S., Horsburgh, C. R., Cupples, L. A., Aschengrau, A., & Stier, E. A. (2011). Risk factors for nonadherence with Pap testing in HIV-infected women. Journal of Women’s Health, 20(11), 1635–1643. doi:10.1089/jwh.2010.2465 Bynum, S. A., Wigfall, L. T., Brandt, H. M., Richter, D. L., Glover, S. H., & Hébert, J. R. (2013). Assessing the influence of health literacy on HIV-positive women’s cervical cancer prevention knowledge and behaviors. Journal of Cancer Education, 28(2), 352–356. doi:10.1007/s13187-013-0470-4
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Centers for Disease Control and Prevention. (2012). Cervical cancer screening with the HPV test and the Pap test in women ages 30 and older. Retrieved from http://www.cdc.gov/cancer/cervical/ pdf/HPV_Testing_2012_English.pdf
Logan, J. L., Khambaty, M. Q., D’Souza, K. M., & Menezes, L. J. (2010). Cervical cancer screening among HIV-infected women in a health department setting. AIDS Patient Care and STDs, 24(8), 471–475. doi:10.1089/apc.2009.0295
Centers for Disease Control and Prevention. (2015a). HIV among women. Retrieved from http://www.cdc.gov/hiv/group/gender/ women/
Massad, L. S., Einstein, M. H., Huh, W. K., Katki, H. A., Kinney, W. K., Schiffman, M., . . . 2012 ASCCP Consensus Guidelines Conference. (2013). 2012 updated consensus guidelines for the management of abnormal cervical cancer screening tests and cancer precursors. Journal of Lower Genital Tract Disease, 17(5 Suppl. 1), S1–S27. doi:10.1097/LGT.0b013e318287d329
Centers for Disease Control and Prevention. (2015b). Human papillomavirus. Retrieved from http://www.cdc.gov/vaccines/pubs/ pinkbook/hpv.html Centers for Disease Control and Prevention. (2016). Genital HPV infection—Fact sheet. Retrieved from http://www.cdc.gov/std/ hpv/stdfact-hpv.htm Clifford, G. M, Gonçalves, M. A., Franceschi, S., HPV and HIV Study Group. (2006). Human papillomavirus types among women infected with HIV: A meta-analysis. AIDS, 20(18), 2337– 2344. doi:10.1097/01.aids.0000253361.63578.14 Coughlin, S. S., King, J., Richards, T. B., & Ekwueme, D. U. (2006). Cervical cancer screening among women in metropolitan areas of the United States by individual-level and area-based measures of socioeconomic status, 2000 to 2002. Cancer Epidemiology, Biomarkers & Prevention, 15(11), 2154–2159. doi:10.1158/10559965.EPI-05-0914 Downs, L. S., Smith, J. S., Scarinci, I., Flowers, L., & Parham, G. (2008). The disparity of cervical cancer in diverse populations. Gynecologic Oncology, 109(2 Suppl.), S22–S30. doi:10.1016/j. ygyno.2008.01.003 Fontaine, P. L., Saslow, D., &, & King, V. J. (2012). ACS/ASCCP/ ASCP guidelines for the early detection of cervical cancer. American Family Physician, 86(6), 501–508. Garbers, S., & Chiasson, M. A. (2004). Inadequate functional health literacy in Spanish as a barrier to cervical cancer screening among immigrant Latinas in New York City. Preventing Chronic Disease, 1(4), A07. Gauss, J. W., Mabiso, A., & Williams, K. P. (2013). Pap screening goals and perceptions of pain among black, Latina, and Arab women: Steps toward breaking down psychological barriers. Journal of Cancer Education, 28(2), 367–374. doi:10.1007/ s13187-012-0441-1 Grulich, A. E., van Leeuwen, M. T., Falster, M. O., & Vajdic, C. M. (2007). Incidence of cancers in people with HIV/AIDS compared with immunosuppressed transplant recipients: A meta-analysis. Lancet, 370(9581), 59–67. doi:10.1016/S0140-6736(07)61050-2 Keller, M. J., Burk, R. D., Xie, X., Anastos, K., Massad, L. S., Minkoff, H., . . . Strickler, H. D. (2012). Risk of cervical precancer and cancer among HIV-infected women with normal cervical cytology and no evidence of oncogenic HPV infection. JAMA, 308(4), 362–369. doi:10.1001/jama.2012.5664 Lambert, C. C., Chandler, R., McMillan, S., Kromrey, J., JohnsonMallard, V., & Kurtyka, D. (2015). Pap test adherence, cervical cancer perceptions, and HPV knowledge among HIV-infected women in a community health setting. Journal of the Association of Nurses in AIDS Care, 26(3), 271–280. doi: 10.1016/j. jana.2014.11.007
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Massad, L. S., Evans, C. T., Wilson, T. E., Goderre, J. L., Hessol, N. A., Henry, D., . . . Weber, K. M. (2010). Knowledge of cervical cancer prevention and human papillomavirus among women with HIV. Gynecologic Oncology, 117(1), 70–76. doi:10.1016/j. ygyno.2009.12.030 McMullin, J. M, De Alba, I., Chávez, L. R., & Hubbell, F. A. (2005). Influence of beliefs about cervical cancer etiology on Pap smear use among Latina immigrants. Ethnicity & Health, 10(1), 3–18. doi:10.1080/1355785052000323001 National Cancer Institute. (2015). HPV and cancer. Retrieved from http://www.cancer.gov/about-cancer/causes-prevention/risk/ infectious-agents/hpv-fact-sheet Oster, A. M., Sullivan, P. S., & Blair, J. M. (2009). Prevalence of cervical cancer screening of HIV-infected women in the United States. Journal of Acquired Immune Deficiency Syndromes, 51(4), 430–436. doi:10.1097/QAI.0b013e3181acb64a Panel on Opportunistic Infections in HIV-Infected Adults and Adolescents. (2015). Guidelines for the prevention and treatment of opportunistic infections in HIV-infected adults and adolescents: Recommendations from the Centers for Disease Control and Prevention, the National Institutes of Health, and the HIV Medicine Association of the Infectious Diseases Society of America. Washington, DC: U.S. Department of Health and Human Services. Retrieved from https://aidsinfo.nih.gov/contentfiles/ lvguidelines/adult_oi.pdf Raper, J. L. (2014). Going the extra mile for retention and reengagement in care: Nurses make a difference. Journal of the Association of Nurses in AIDS Care, 25(2), 108–111. doi:10.1016/j. jana.2013.10.002 Simonsen, S. E., Kepka, D., Thompson, J., Warner, E. L., Snyder, M., & Ries, K. M. (2014). Preventive health care among HIV positive women in a Utah HIV/AIDS clinic: A retrospective cohort study. BMC Women’s Health, 14(1), 37. doi:10.1186/1472-6874-14-37 Tello, M. A., Jenckes, M., Gaver, J., Anderson, J. R., Moore, R. D., & Chander, G. (2010). Barriers to recommended gynecologic care in an urban United States HIV clinic. Journal of Women’s Health, 19(8), 1511–1518. doi:10.1089/jwh.2009.1670 U.S. Department of Health & Human Services, Health Resources and Services Administration. (2013). A guide to the clinical care of women with HIV, 2013 edition. Rockville, MD: U.S. Department of Health & Human Services. Retrieved from http://hab. hrsa.gov/deliverhivaidscare/files/womenwithaids.pdf
Volume 20
Issue 4
10 DEC
Appointment Reminder Hi Sara! You have an appointment scheduled for Tuesday, December 10th at 9:45am.
Women living with HIV are at greater risk for human papillomavirus (HPV) infection, cervical dysplasia, and cervical cancer than are uninfected women (Abraham et al., 2013; Grulich, van Leeuwen, Falster, & Vajdic, 2007). A national longitudinal cohort study consisting of women living with HIV and uninfected women suggests that women living with HIV are about two to eight times more likely to develop cervical cancer than uninfected women, and severely immune-suppressed women living with HIV have the highest risk (Abraham et al., 2013). Despite these greater risks, recent studies suggest that as many as 50% of these women are not being screened appropriately (Baranoski, Horsburgh, Cupples, Aschengrau, & Stier, 2011; Lambert et al., 2015; Simonsen et al., 2014). In this article we provide an overview of cervical cancer screening for women living with HIV. Abstract: Studies suggest that women living with HIV are not being adequately screened for cervical cancer. In this article we review the latest recommendations for cervical cancer screening in women with HIV and make recommendations for clinical practice. http://dx.doi.org/10.1016/j.nwh.2016.07.002 Keywords: cervical cancer screening | HIV | HPV | Pap test | women’s health
HPV, the most common sexually transmitted infection in the United States, is responsible for about 99% of cervical cancer cases (Centers for Disease Control and Prevention [CDC], 2015b). Almost 80 million Americans are currently infected with one or more subtypes of HPV, and approximately 15 million Americans will become infected annually (CDC, 2016). The HPV virus is transmitted person to person during skin-toskin contact, including sexual contact. HPV is a group of viruses with more than 150 subtypes, of which approximately 40 subtypes can infect the genital areas (National Cancer Institute, 2015). There are many highrisk types of HPV. High-risk types HPV-16 and HPV-18 are responsible for approximately 70% of cervical cancer cases. Women living with HIV are more likely to have persistent coinfection with HPV, a history of abnormal Pap test results, and a degree of immune suppression leading to an increase in prevalence and incidence of cervical cancer (American College of Obstetricans and Gynecologists [ACOG], 2010; Massad et al., 2010). A meta-analysis of HPV types among women with HIV found that 36% of the women were infected with some type of HPV and that 12% were infected with multiple types (Clifford, Gonçalves, Franceschi, & HPV and HIV Study Group, 2006). Because HPV persistence in women living with HIV is common, the rates of cervical cancer are likely to be greater in this population. Persistent HPV infections lead to more cases of abnormal cervical cytology, including squamous intraepithelial lesions and atypical cells of undetermined significance, which are more common in women with HIV (Tello et al., 2010). In addition to HPV, other risk factors that increase a woman’s chances of cervical cancer are smoking, chlamydia infection, obesity, long-term oral contraceptive use, family history, poverty, having three or more full-term pregnancies, and a diet poor in fruits and vegetables (Akers, Newmann, & Smith, 2007; American Cancer Society, 2014). Therefore, conducting a careful health history and providing education on reducing modifiable risk factors are essential components in clinicians’ care of women to improve their awareness of HPV prevention measures.
Women and HIV Despite advances in raising awareness about HIV infection, women continue to experience significant HIV infection rates. Women account for 20% of all new HIV infections
Crystal Lambert Chapman, PhD, CRNP, FNP-BC, is an assistant professor in the School of Nursing at the University of Alabama at Birmingham in Birmingham, AL. Allyssa L. Harris, PhD, RN, WHNP-BC, is an assistant professor in the William F. Connell School of Nursing at Boston College in Chestnut Hill, MA. The authors report no conflicts of interest or relevant financial relationships. Address correspondence to: [email protected].
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and approximately 25% of individuals living with HIV (CDC, 2015a). Therefore, the topic of women and HIV is timely and relevant for nurses and other clinicians working in women’s health care. Advances in antiretroviral therapy over the past three decades have improved life expectancy and decreased the incidence of many AIDS-defining cancers (i.e., Kaposi sarcoma and non-Hodgkin lymphoma) among people living with HIV. However, the incidence of cervical cancer, also an AIDS-defining malignancy, has not decreased. Several studies suggest that cervical cancer is more prevalent in women with lower CD4 T lymphocytes (Abraham et al., 2013; Keller et al., 2012). However, despite CD4 T-lymphocyte count, incidences of cervical cancer are higher among women living with HIV than women who are not infected with HIV. Findings from the Women’s Interagency Health Study showed that cervical cancer incidences were generally greater in women living with HIV and specifically greater among severely immunosuppressed women living with HIV (Abraham et al., 2013). This multicohort prospective study found that women with HIV had a twoto fivefold greater incidence of invasive cervical cancer rates than women without HIV, and the incidence of invasive cervical cancer rates increased with lower CD4 counts (Abraham et al., 2013). Therefore, treatment alone is not sufficient to reduce cervical cancer incidence.
Pap Test Guidelines for Women Living With HIV In recent years, guidelines on Pap test screening for the general population have changed from screening annually to screening every 3 years for women ages 21 to 65 years (ACOG, 2016; Fontaine, Saslow, & King, 2012). Women with abnormal results are scheduled for more frequent screening and additional testing with a specialist (Massad et al., 2013). Pap test guidelines differ for women living with HIV. Until recently, Pap testing was recommended at the time of initial HIV diagnosis, 6 months from baseline, and annually thereafter (ACOG, 2010; U.S. Department of Health & Human Services & Health Resources and Services Administration, 2013). Currently, Pap testing is recommended at the time of HIV diagnosis, 6 to 12 months from baseline, and annually thereafter until three consecutive normal Pap test results are obtained (Panel on Opportunistic Infections in HIV-Infected Adults and Adolescents, 2015). After three consecutive normal Pap test results, screening is recommended every 3 years (Panel on Opportunistic Infections in HIV-Infected Adults and Adolescents, 2015). Despite the increased risk of developing invasive cervical cancer, women living with HIV are less likely to have cervical cancer screening. Recent data report that 22% to 56% of women with HIV had not received an annual Pap test after baseline (Baranoski et al., 2011; Lambert et al., 2015; Oster, Sullivan, & Blair, 2009; Simonsen et al., 2014; Tello et al., 2010),
nwhjournal.org
Opening photo © iStock Collection / thinkstockphotos.com
Risk Factors
Pap test rates among women living with HIV are suboptimal, and the reasons for suboptimal screening are complex and multilayered and approximately 75% had not received the second recommended Pap test during their first year in care (Logan, Khambaty, D’Souza, & Menezes, 2010). Pap test rates among women living with HIV are suboptimal, and the reasons for suboptimal screening are complex and multilayered.
Photo © Deirdre Rusk / thinkstockphotos.com
Reasons for Poor Screening In general, there are multiple reasons that women are not being screened. These include poor health habits, misunderstanding of changing Pap test guidelines by women and their health care providers, current abstinence from sexual activity, fear of pelvic examinations, and/or history of pelvic trauma, as well as systemic barriers that include health care access issues, lack of health care and health insurance, transportation and child care issues, and fatalistic attitudes (Coughlin, King, Richards, & Ekwueme, 2006; Downs, Smith, Scarinci, Flowers, & Parham, 2008; Garbers & Chiasson, 2004; McMullin, De Alba, Chávez, & Hubbell, 2005). For example, fear of pain is one barrier to Pap testing. Findings from a longitudinal study of 420 women with unknown HIV status suggest that perceptions of pain influence Pap testing by limiting women’s willingness to schedule a Pap test (Gauss, Mabiso, & Williams, 2013). Additionally, cultural
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practices may influence Pap testing. The literature is mixed on racial and ethnic barriers (Baranoski et al., 2011). Women living with HIV have additional barriers to cervical cancer screening. This population often requires complex care that involves multiple clinicians, such as infectious disease clinicians, primary care providers, and women’s health providers. Sometimes women and their health care providers lose sight of routine preventive primary care needs (i.e., Pap testing), focusing instead on what they deem as more urgent care (i.e., HIV care). Women may not be receiving all of their care at one site and may have to make additional appointments with women’s health or primary care providers. Lack of centralized care can be cumbersome for some women, and they may forgo preventive health care services and focus only on their HIV care needs. Also, women living with HIV fear disclosing their status to additional health care providers because of HIV-related stigma (Audet, McGowan, Wallston, & Kipp, 2013). Research suggests that health literacy is associated with poor cervical cancer screening awareness and use, but again the data are mixed. Among a sample of 145 women living with HIV, women with low health literacy were less likely to report having an annual Pap test (Bynum et al., 2013). In the same study,
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women with low health literacy reported having at least two Pap tests in the first year after initial screening, which may suggest confusion among women who reported low health literacy. Many women confuse Pap testing with a general pelvic examination, which could explain the mixed results. HIV care also has
the potential to be complex and burdensome. This may result in increased health literacy challenges for women living with HIV. Therefore, women living with HIV could benefit from interventions aimed at improving health literacy and awareness of the significance of screening. Psychosocial barriers such as depression have been associated with lack of testing. For example, researchers at the Johns Hopkins HIV clinic examined barriers to adherence with gynecologic care among 200 women living with HIV. In this study, moderate and severe depression was associated with missing gynecology appointments and lack of a documented Pap test (Tello et al., 2010). Likewise, in Boston, Baranoski et al. (2011) assessed risk factors for inadequate Pap testing. Results showed that depression was associated with poor Pap test adherence in a diverse sample of women living with HIV. Individuals who engage in unhealthful behaviors, such as drug use and tobacco use, are potentially unlikely to be engaged in preventive health behaviors (i.e., Pap testing). Baranoski et al. (2011) conducted a chart review of 549 women living with HIV to assess factors associated with poor Pap test follow-up. Current or former drug use or cigarette smoking was associated with increased odds of poor Pap test adherence (Baranoski et al., 2011). Laboratory test results, such as level of CD4 T-lymphocyte cells (also known as T cells), provide a measure of immune health in people living with HIV. Lower numbers of T cells indicate advanced HIV disease. Data are mixed regarding the association of Pap test adherence among women living with
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HIV and CD4 T-lymphocyte count. For example, the results of Baranoski et al. (2011) suggests that Pap test adherence is associated with T-cell counts of less than 200 cells/mm3, yet Tello et al. (2010) suggest that, according to their research, a relationship does not exist. Authors of the former study obtained laboratory test values from medical records, whereas authors of the latter administered a survey to each participant requesting self-reported laboratory test results. Self-report measures may be less accurate because of participant recall error. Therefore, laboratory values from Baranoski et al. (2011) are likely more accurate because of lack of recall bias. As researchers continue to investigate the relationship between Pap test adherence and T-cell count, clinicians must educate, encourage, and improve access for all women living with HIV and specifically women with advanced HIV disease.
Implications for Nursing Practice Nurses, advanced practice nurses, and other women’s health care clinicians must stay abreast of current cervical cancer screening guidelines generally for all women and specifically for those women at greater risk. It is important to assess women’s perceptions and attitudes related to cervical cancer and screening.
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women living with HIV could benefit from interventions aimed at improving health literacy and awareness of the significance of screening
Understanding their attitudes and beliefs enables clinicians to provide education to increase awareness and, hopefully, Pap testing uptake. It’s critical to increase awareness, stress the importance of screening, and pay particular attention to barriers. In today’s HIV health care environment, disease management guidelines are consistently changing as evidence improves through research. HIV-specific guidelines are rapidly changing, and it is essential for nurses and other health care providers to be aware of the latest updates (Panel on Opportunistic Infections in HIV-Infected Adults and Adolescents, 2015). Currently, differences exist between the recommendations of the Panel on Opportunistic Infections in HIV-Infected Adults and Adolescents (2015) and those of ACOG (2010). The latter organization recommends Pap testing at the time of HIV diagnosis, 6 to 12 months from baseline, and annually thereafter until three consecutive Pap tests yield normal results. However, the former organization recently released guidelines recommending extending screening to every 3 years after three consecutive normal Pap test results. These discrepancies have the potential to result in confusion and missed opportunities to provide preventive health care. It is important that health care providers unfamiliar with HIV management seek assistance from an HIV specialist.
Limiting Barriers Reasons for poor Pap test adherence are multifaceted. The literature has identified several barriers to Pap screening, including lack of provider knowledge, complex care plans, psychological factors (i.e., fear and embarrassment), systematic factors (i.e., lack of insurance), and individual factors (i.e., lack of transportation, competing demands, and lack of child care). Although nurse practitioners and nurses have a key role in staying abreast of new guidelines, they can also play a critical role in accessing and limiting barriers to screening. Some examples include establishing reminder systems for women to improve adherence and using electronic sources such as e-mail and text messaging to remind women of an upcoming appointment. Creating systematic processes to reduce barriers, such as limiting multiple appointment burdens, could also improve adherence. Systematic processes could include establishing a woman-centered practice that focuses specifically on the health needs of women. This clinic could operate daily or weekly with consistent nurses and nurse practitioners. Another option is to hire a women’s health nurse practitioner to deliver evidence-based care during primary care appointments. Another strategy is to use social media to increase awareness and stress importance of cervical cancer screening. A renowned HIV ambulatory care clinic in the southeastern United States uses media (i.e., brochures, posters, and a brief verbal message) to engage women receiving HIV care (Raper, 2014). These strategies can be used to improve cervical cancer screening awareness and stress the importance of screening.
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Conclusion Cervical cancer is a highly preventable cancer (CDC, 2012), yet screening via Pap testing is suboptimal for all women generally and especially for women living with HIV. Women living with HIV are at greater risk for cervical cancer than women without an HIV diagnosis. It is important for women’s health care nurses to be aware of the cervical cancer screening guidelines for women living with HIV, focusing on providing education and information on the importance of Pap testing adherence. Women living with HIV encounter many barriers—individual, psychological, systematic, and complexity of care—potentially limiting their ability to engage in screening. It is important for women’s health nurses and other clinicians to be aware of the specific health care challenges facing women living with HIV. NWH
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