Cervical cancer occurs mainly in low-resource, underserved regions as part of a complex of diseases linked to poverty, race/ethnicity, and/or other health disparities (27
). However, it is important to recognize that the only two significant determinants of cervical cancer incidence are persistent carcinogenic HPV infection and lack of access to screening. There is no evidence to date to suggest that any population defined by race or ethnicity is more susceptible than another to cervical cancer, once all confounding factors such as behaviors, access to screening, and timely follow-up of screen positives are taken into account.
It has been shown that women at high risk of cervical cancer either do not have adequate access to preventive services or choose not to utilize these services for a number of reasons ranging from measurable structural barriers (e.g., transportation) to subjective intrapersonal barriers (e.g., fear of results, mistrust of the health care system). Community-based interventions that account for cultural beliefs, attitudes and behaviors aiming at increasing knowledge about HPV and its link to cervical cancer, cervical cancer screening, sexual risk reduction, and HPV vaccination uptake may represent a promising approach to minimize current disparities that exist in high-risk populations. The following sections describe the cervical cancer burden and approaches used to address cervical cancer primary and/or secondary prevention among specific high-risk populations.
A. South Carolina: A Faith-Based Approach to Screening and HPV Vaccination (Brandt)
Cervical cancer incidence and mortality rates for South Carolina, Alabama, and Mississippi exceed the national rates, with African-American women accounting for much of this difference. Incidence rates for invasive cervical cancer were 9.3 for African Americans versus 6.9 for whites in South, Carolina, 11.1 and 8.0 in Alabama, and 9.4 and 6.4 respectively in Mississippi. Mortality rates were 5.5 versus 1.8 respectively in South Caroline, 6.8 versus 2.4 in Alabama, and 6.0 and 2.4 in Mississippi (28
Cancer prevention and control research and programs have been successfully implemented in faith-based settings, particularly in African American churches. In general, there is an attitude among African American church members in which they embrace health and well being with the potential to intervene at multiple levels of change. Among African American adults, approximately 67% attend church at least monthly; therefore, the church emerges as an important setting for public health programming (29
In South Carolina, statewide faith- and community-based approaches have been undertaken to address excessive cervical cancer incidence and mortality with a focus on prevention and control among African-American women (27
). Prompted by advertisements for Gardasil®, the State Baptist Young Woman's Auxiliary (YWA) of the Woman's Baptist Education and Missionary Convention Health Ministry approached researchers at the University of South Carolina about a partnership to address cervical cancer among African-American women. Formative research was conducted, by partnering with five Baptist Education and Missionary Convention churches in a rural region of South Carolina to conduct 20 in-depth interviews and 10 focus groups with 116 African-Americans (mean age=38.8; 92% female), to explore the acceptance of and opportunities for promotion of the vaccine in faith-based settings using a community-based participatory approach. Preliminary results indicate that less than half (41%) correctly identified HPV as a main cause of cervical cancer, but 75% of participants had heard of HPV. Most participants (77%) favored a school requirement for HPV vaccination. Most participants felt that the church was an appropriate setting for HPV and HPV vaccine education, and the involvement of youth in such efforts was emphasized.
While most of the faith- and community-based partners were supportive of HPV vaccination, a few vocal opponents swayed opinions in faith-based settings and in public forums. Some who delivered educational programs or worked directly with the partnering churches were asked explicitly if they were paid by Merck (the maker of Gardasil®) to “push the vaccine.” To avoid “controversy” associated with Gardasil®, a balanced message of preventing cervical cancer through regular Pap tests, adherence to recommended follow-up care of abnormal results, and making informed decisions about Gardasil® was adopted. Information provided about Gardasil® was non-industry sponsored and none of the related activities have involved industry support. These decisions proved fruitful as even the most opposed to the vaccine joined forces to prevent cervical cancer using the agreed upon messages.
B. Alabama and Mississippi: Screening and Self-Collected Sampling for HPV Testing among African-American women (Scarinci, Partridge, Castle)
The Deep South Network for Cancer Control (DSN) was established to develop sustainable community infrastructure to promote cancer awareness among African-Americans residing in the Alabama Black Belt and the Mississippi Delta (31
). The development and implementation of the program was based on principles of Community-Based Participatory Research (CBPR) and the Empowerment Model (32
), in which volunteer community health workers (CHWs), investigators, and partners jointly developed the action plan to provide public education and promote screening for breast and cervical cancer. We have trained and retained over 500 CHWs who are “natural helpers” in their respective communities to provide cancer awareness messages and resources to their communities. We focused specifically on breast and cervical cancer screening because it has been shown that screening decreases mortality and, most importantly, we could provide screening and treatment through the National Breast and Cervical Cancer Early Detection Program (NBCCEDP) to uninsured women who were within 200% of poverty levels or worse. There has been a continuous increase in innovative cancer awareness activities within the communities with examples ranging from hat contests to cancer awareness walks, town hall meetings, fashion shows, local medial messages, and one-on-one messages (34
The most compelling data regarding the impact of the program on breast and cervical cancer disparities is based on data obtained through the Alabama NBCCEDP in our targeted counties in Alabama among women between the ages of 50 and 64. In 2004-2005, only 2% of eligible white women and 6% of eligible African-American women obtained a mammogram through this program. In 2007-2008, this percentage was 8% and 29% respectively. That is, an increase of 6% among whites and 23.6% increase among African Americans. With regard to Pap smear in the Alabama targeted counties, 0.8% of eligible white women between the ages of 50 and 64 obtained a Pap smear in 2004-2005 as compared to 3.6% in 2007-2008. For African Americans, Pap utilization increased from 2% in 2004-2005 to 9.2% in 2007-2008.
Although the data above show an increase in breast and cervical cancer screening among African-American women in the targeted counties, there is still a hard-to-reach group, which, despite our efforts, has not engaged in these behaviors. As such, alternative approaches to cytology screening must be considered since a large percentage of eligible women were not going to the clinics to obtain their Pap smear. Through the community-based participatory process in our targeted communities, DSN and the U.S. National Cancer Institute have partnered to explore the acceptability of self-collected sampling for HPV testing among African-American women in three of our targeted counties in the Mississippi Delta. Preliminary data among African-American women who reported not having a Pap smear in the past three years indicate that almost 60% agreed to participate, and among those more than 90% mailed their self-collected material for analysis.
Throughout this experience we have learned two major lessons: 1) “Built it and they will come” may not make for a successful strategy because women may not come. Unscreened women have reported that they are embarrassed, and they do not want others in their communities to know that they are not taking care of their health. In order to recruit participants for the self-collected sampling HPV testing, we have used door-to-door canvassing. However, in order for this approach to be successful it was necessary to build trust and credibility in the community by promoting screening so when women were approached individually they were more receptive to the message while keeping their privacy; 2) Credibility and trust take time and effort.
C. Haitian Immigrants Living in Miami, FL (Little Haiti): Self-Collected Sampling for HPV Testing and Understanding of Feminine Hygiene Practices (Kobetz)
In Miami, Florida, cervical cancer incidence is highest among Haitian women, particularly those who are recent immigrants, and reside in Little Haiti, a large ethnic enclave located just northeast of the City center. Between 2004-2007, the estimated incidence of disease for Little Haiti was 38/100,000 (35
To address this disparity, community leaders from Little Haiti and academic investigators from University of Miami created a campus-community collaborative known as Patne en Akyson (Partners in Action). This Partnership aims to improve cancer outcomes among Haitian women through CBPR (36
). Currently, the partnership oversees five complementary research initiatives that address the excess cervical cancer burden in Little Haiti. The success of such research can be primarily attributed to our reliance on CHWs to recruit participants and collect study data (37
). The CHWs are women of Haitian descent, who speak English and Haitian Kreyol fluently, and are employed by a community-based organization located in Little Haiti. The affiliation between the CHWs and this organization is critical to the success of Partnership research initiatives. By providing our studies with a “community home,” we are able to dissuade widespread distrust of research in Little Haiti associated with the misidentification of Haitian ancestry as a risk factor for HIV/AIDS (39
The advisory board, which is comprised primarily of community members, drives the Partnership's research agenda. To date, we have:
- Documented the prevalence of lifetime and routine Pap test use in Little Haiti. Among nearly 1,000 survey respondents, one third had never had a Pap test, and less than half of women with prior screening experience reported having a Pap test in the past three years (36);
- Identified primary barriers to screening, including language difficulties, limited access to care, and socio-cultural concerns about modesty;
- Examined the acceptability of self-sampling as an alternative to Pap test, and found that nearly 90% of participants with a history of having had a Pap test (n=189) prefer self-sampling;
- Conducted formative research to understand the potential influence of a culturally-bounded, feminine hygiene practice on HPV susceptibility.
As is often true for CBPR initiatives, this agenda is born out of lessons learned and significant compromise (38
). The academic investigators, in particular, must continually relinquish their assumptions about how data should be collected, by whom, and in what context (37
). All partners must invest considerable time to establish and maintain trust, as well as, foster mutual respect for each other, despite occasionally divergent ideas about the research process. Doing so is essential for effectively engaging residents in research, and for collecting quality data that may advance community health and social change in Little Haiti and other similarly disenfranchised communities.
D. U.S.-Mexico Border Region: HPV Vaccination, Screening, and Follow-Up among Hispanic Women (Garcia)
Cervical cancer incidence and mortality rates for the United States-Mexico border region exceed those of the rest of the nation, with Hispanic women accounting largely for this differential (42
). Age-adjusted cervical cancer rates for Hispanic women living in border counties are twice those of their non-Hispanic peers in the same communities (13.9/100,000 vs. 7.0/100,000), and significantly higher than for other Hispanics in the U.S. (13.2/100,000)(45
). Hispanic border residents are more likely to present with squamous disease (11.0 compared to 9.7 for Hispanics in non-border states) and late stage disease with earlier age at presentation.
Factors associated with non-adherence to cervical cancer screening in this population include low income, lack of health insurance, limited access to health care services, lack of clinician recommendation, length of residency in the U.S., limited English language proficiency, acculturation and lack of awareness (46
). Most of these are not easily addressed through standard public health strategies. Interventions that promote patient awareness of cancer screening and cervical cancer, those that facilitate access to health care services, and clinician recommendations may have a positive effect in Hispanic border populations. For example, women for whom both breast and cervical cancer screenings were recommended were more likely (odds ratio [OR] = 7.7) to get a mammogram than women told only to get a mammogram (OR = 2.4) or when no recommendation was made (OR = 1.0, reference). They were also more likely to get a Pap smear within the last 5 years (OR = 14) than women told only to get a Pap smear (OR = 2.3) or when no recommendation was made (OR = 1.0, reference).
In particular, awareness promoting cancer education interventions especially when delivered by CHWs (promotoras
) may be particularly useful among isolated, low educated, acculturated women of Mexican origin in this area (53
). The addition of molecular based HPV screening technologies to the screening paradigm whether clinician or patient collected has been demonstrated to be feasible in this population (55
). Although self collection promises to overcome important cultural, geographic and access barriers, its use will still be hindered by the same cost issues faced by cytology-based screening programs.
The Pima County Cervical Cancer Prevention Partnership (PCCCPP) funded by the CDC under the REACH U.S. initiative attempts to foster a sustainable systemic response to cervical cancer prevention. PCCCPP, which includes school districts, community health centers, county government and community-based organizations, has grown out of a community-based participatory process, and has as its mission to increase awareness and knowledge of cervical cancer screening, prevention, and management, as well as to facilitate access to diagnostic and treatment services for women throughout Pima county. In its first 18 months PCCCPP has developed and disseminated a CHW training program, which has trained nearly 75 promotoras (all Mexican origin women) and reached more than 2,000 individuals through small group sessions and home visits. Current efforts are focused on developing school-based parent education interventions to facilitate HPV vaccination decision making, and developing navigation strategies for women with abnormal screenings who are concurrently at higher risk of cancer and being lost to clinical follow up.
Although publicly funded initiatives like the NBCCEDP have increased screening coverage in this area, the diagnostic and therapeutic follow up of these patients is highly variable and dependent on state specific Medicaid residency requirements which in Border States may exclude from coverage recent and/or illegal immigrants. This is particularly problematic given that foreign-born women living in the U.S. have significantly increased mortality compared to their U.S.-born counterparts (56
). Additionally, although many of the screening related determinants (age, access, acculturation, clinician recommendation, etc.) likely apply to primary prevention, little is known about the knowledge, acceptability and uptake of the HPV vaccine in border communities (57
). Despite distribution of vaccine through the CDC's Vaccine for Children program, the major public health concern is to ensure that the populations with the greatest burden of risk and disease (in this case the children of immigrants) are able to access these services without compromising their own or their parents legal status in the country.
E. Sioux/American Native Americans of the Northern Plains: Screening and Vaccination (Bell)
Cervical cancer is one of many diseases that disproportionately impact the Native American population in the Northern Plains. The Aberdeen Area of the Indian Health Service, which encompasses North Dakota, Nebraska, Iowa, and South Dakota, has a cervical cancer mortality rate of 11.5/100,000 and age-adjusted mortality rate of 4.9/100,000 for the 1994-1998 time periods (58
Increased cervical cancer incidence in the Native American population is due to many factors including behaviors (e.g., more sexual partners resulting in greater exposure to HPV) geographical issues (e.g., very rural population with poor access to care), and economic issues (59
). The unemployment rate is approximately 50%, the median household income is $20,089, 58% of the households have an annual income less than $25,000) and 68.7% of families live below the poverty level. The climate is harsh ranging from severe heat in the summer (110°F) to extreme cold in the winter (-30°F). Housing is of poor quality, often without running water or adequate heating (4
Our effort to reach this population has spanned eight years. In our initial project, we found 21.5% and 14.2% of 287 Native American patients tested positive for any HPV and carcinogenic HPV infection, respectively. Among HPV-positive women, 41% presented with multiple HPV genotypes and 48.7% were infected with HPV16 and/or HPV18 (60
). Collaborations between the state NBCCEDP program and IHS service units have begun, increasing the number of Native American women who participate in the state NBCCDEP program from 79 Native American women participated in NBCCDEP in 2000 (7% of the Pap tests performed) to 481 (18%) in 2008.
Because of the increased awareness of the problem of cervical cancer by the tribes, the tribal health board has made HPV vaccination a priority. The vaccination rates for pediatric vaccines are high among the Native American population. However, the adolescent patient is often difficult to access. To address this issue, the tribal school system has paired with the medical community to aid in school based HPV vaccination programs. To aid with diagnosis, treatment, and follow-up of cervical dysplasia and cancer, telemedicine programs are being developed to connect cancer specialists to the Native American patient remotely.
Despite making some progress with cervical cancer screening and awareness, there are persistent problems which need to be addressed. According to a recent cost model, the Indian Health Service (IHS) appropriated funding provides only 55% of the necessary federal funding to assure mainstream personal health care. It is not uncommon for the service units to “run out of funds” by the fourth fiscal quarter (1
). Most of the health care budget is spent on acute care and much less on prevention. Physician recruitment and retention continues to be problematic. The lack of continuity of care is a consistent problem, as locum tenens often staff the clinic. In the Lakota language, there is a not word for cancer, and according to Lakota beliefs, the act of looking for a bad thing such as cancer, will cause it to happen. Only when we address the cultural and socioeconomic issues of this population, will we make an impact on its cervical cancer problem.
F. Kentucky: Follow-up to Abnormal Pap Tests among Appalachian Women (Dignan)
Patient Navigation for Cervical Cancer in Appalachia was established to provide public health departments with additional support needed to increase adherence to recommendations for follow-up care for women with abnormal Pap tests. Cervical cancer incidence (11.4/100,000 during 2001-5) and mortality rates (3.1/100,000) for Appalachia have been elevated for decades (5
). Guided by Social Cognitive Theory, the project was initiated by recruiting and training of local women to work in county health departments and provide patient navigation to overcome barriers to obtaining follow-up care. The primary barriers described by women are uncertainty regarding the follow-up care they are to receive and logistics. To address uncertainty regarding follow-up care, patient navigators are prepared to provide information and describe step-by-step what women are likely to experience with follow-up medical procedures. Similarly, patient navigators are equipped to address logistical concerns, including helping women schedule appointments, arrange for transportation, and obtain other services needed follow-up care.
Patient navigators are working in 10 county health departments in Appalachian Kentucky, and thus far 130 women, aged 18 and older with abnormal Pap smear results have been referred for follow-up and are enrolled in the project. Of those enrolled, 31% have been told that they need a repeat Pap smear, 21% have been referred for additional follow-up at the health department, and 53% have been referred to a provider outside the health department. When asked about barriers to obtaining follow-up, concerns about health insurance (29%), child care (10%), out of pocket costs (9%), and fear of what may be found (4%) were most commonly mentioned. On the other hand, when asked about needs related to obtaining follow-up, women responded that having knowledge that cancer ‘runs in my family so I need to resolve’ the abnormal Pap smear result (22%), having support from family/friends (11%), being able to cope with financial issues (7%), and having someone to accompany them were important to obtaining follow-up.
Among the most common are health service access barriers, culturally related fear and fatalism, a lack of confidence in cancer screening, and limited awareness of variation in successful treatment. For many Appalachians, cancer is believed to be one disease that is universally fatal and therefore early detection through screening provides little if any added value to the life of the patient or their family. These beliefs added to access barriers are clearly associated with low rates of screening and low rates of obtaining recommended diagnostic procedures.
There is a long tradition of negative experiences with cancer among Appalachian women that manifests as avoidance behaviors in seeking screening and follow up because of fear of a cancer diagnosis. The avoidance is usually seen as ‘passive refusal,’ but also occurs in an active form as refusal to obtain services even when offered. This problem is compounded by poverty, which influences many parts of life and is associated with lack of transportation, child care, and exclusive reliance on public health departments and other safety net health care providers to seek cancer screening.
G. Vietnamese-Americans Living along the Eastern Seaboard: Compliance with Screening (Ma)
Among U.S. racial/ethnic groups, Vietnamese-American women have the highest incidence rate of invasive cervical cancer. The incidence rate for cervical cancer among Vietnamese women (43/100,000), is five times higher than that of White women (8.5/100,000) (62
). Vietnamese and other Asian Americans experience a dynamic state of acculturation. They acculturate at the same rate as other groups, but unlike other groups, tend to maintain strong cultural and linguistic links with their respective traditional societies. These behaviors tend to affect lifestyles as well as health care beliefs and practices. This may partially explain why some Asian subgroups lag behind other racial/ethnic groups in seeking and obtaining getting basic screening tests such as Pap smear.
Considering the rapid growth of the U.S. Vietnamese population, prevention of cervical cancer in this high risk community through screening and early detection becomes a critical public health issue. Vietnamese-American women encounter substantial healthcare system as well as cultural, educational, and linguistic barriers that prevent them from obtaining screening services (62
). Nearly two-thirds (60%) of Vietnamese women in our catchment service area in the eastern region of the U.S. are also medically underserved or uninsured and have low incomes.
Building on our previous CBPR research (67
), we are conducting a large-scale, community-based participatory group randomized intervention trial to increase cervical cancer screening and reduce health system access barriers among medically underserved and low income Vietnamese women in the eastern region of the U.S. (PA, NJ). Preliminary data from 1,020 eligible participants indicate the following characteristics of the participants: the majority-(74.0%) were married; nearly half had completed high school; less than 10 percent had college education, the majority had annual household incomes <$20,000; and overwhelming majority (97%) spoke Vietnamese at home and spoke and wrote English poorly (90%). The baseline data indicated low ever-screened percentages for cervical cancer. Few women had perceived themselves to be at risk for cervical cancer (<10%) (3% to 7%). Although most women perceived that there are benefits of obtaining a Pap test (52% to 73%), various barriers to screening were reported by a considerable percentage of women, including language difficulties, financial barriers (cost), lack of time, and lack of knowledge about what will be done during a Pap test (35% to 50%). Although no final outcome data are available at this time, we observed a significant increase (0% to 74 %) in Pap testing among non-compliant Vietnamese women in the intervention group at 12 month follow-up visit.
We have learned two major lessons through our research experience in working with the Vietnamese community: (1) Effort to reduce health disparities is not limited to health care professionals. Engaging Asian community organizations within the targeted populations from program concept and content to implementation are critical elements in building links, trust, and respect for long-term partnerships. Our engagement of community gatekeepers and organizations fostered broader community interest and participation in our cancer control intervention. The strength of this partnership determines the quality of our research outcomes; and (2) Comprehensive intervention strategies addressing a broad range of identified barriers and cultural beliefs at individual and system levels enhanced the participation and utilization of beneficial education and screening.