Abstract
Cervical cancer is a highly preventable disease that disproportionately affects women in developing countries and women with HIV. As integrated HIV and cervical cancer screening programs in Sub-Saharan Africa mature, we have an opportunity to measure the impact of outreach and education efforts and identify areas for future improvement. We conducted a cross-sectional survey of 106 women enrolled in care at an integrated HIV clinic in the Nyanza Province of Kenya 5 years after the start of a cervical cancer screening program. Female clinic attendees who met clinic criteria for cervical cancer screening were asked to complete an oral questionnaire assessing their cervical cancer knowledge, attitudes, and screening history. Ninety-nine percent of women had heard of screening, 70 % felt at risk, and 84 % had been screened. Increased duration of HIV diagnosis was associated with feeling at risk and with a screening history. Nearly half (48 %) of women said they would not get screened if they had to pay for it.
Keywords: HIV/AIDS, Cervical cancer screening, Knowledge and attitudes, Behavior, Sub-Saharan Africa
Introduction
Cervical cancer, a highly preventable disease with early screening and treatment, remains a leading cause of cancer and cancer-related mortality in Sub-Saharan Africa [1]. Eastern Africa has the highest cervical cancer incidence and mortality in the world with 34.5 cases and 25.3 deaths per 100,000 women [1]. High incidence and mortality rates are attributable to several factors, specifically a lack of programs for early detection and treatment, compounded by high rates of HIV and human papillomavirus (HPV) [2, 3]. Cervical cancer screening rates across Sub-Saharan Africa are estimated to be 0.5–20 %, and in Kenya are estimated to be only 2.4–4 % [4]. Furthermore, HIV increases a woman’s risk of having persistent HPV infection, high-grade cervical precancerous lesions, and invasive cervical cancer [5]. Additionally, as HIV positive individuals are living longer on antiretroviral (ARV) therapy, they face an increasing burden of comorbid chronic conditions, including cancer [6]. In a recent study in Kenya, 26 % of HIV positive women screened for cervical cancer had abnormal results [7]. To address this synergistic relationship and capitalize on the relatively well-funded and developed infrastructure supporting HIV care and treatment programs, an increasing number of programs are integrating cervical cancer screening into their existing HIV service delivery model [6, 8]. As cancer screening programs emerge within the existing HIV healthcare infrastructure, programs need to evaluate not only their ability to provide high-quality clinical services, but also their effectiveness in increasing patient awareness and knowledge about cervical cancer screening.
The World Health Organization (WHO) has suggested metrics for evaluating the success of new cervical cancer screening programs. Outcome measures include ensuring that >80 % of women ages 35–59 years are informed about cervical cancer screening and that >80 % of women ages 35–59 years have been screened at least once during their lifetime [9]. Although the ultimate measure of success is decreasing the incidence of invasive cancer, these intermediate outcomes are important and measureable factors that ensure programs will be able to achieve that goal.
Family AIDS Care and Education Services (FACES) provide integrated HIV services in the Nyanza Province of Kenya, the region with the highest HIV prevalence in the country at an estimated 15 % [10]. In 2007, FACES began offering free cervical cancer screening and prevention (CCSP) services using visual inspection with acetic acid (VIA) in their Lumumba Health Center in Kisumu, Kenya and has since provided screening to over 6000 women [8]. Myths about cervical cancer risk factors and treatment options are common, and inadequate knowledge, not feeling at risk, and stigma have been identified as significant barriers to screening uptake in Sub-Saharan Africa [5, 11–13]. Therefore, one key aspect of the program is the community and clinic awareness campaign. All clinic staff underwent general cervical cancer education, with specialized training for health educators, counselors, and clinicians. Cervical cancer information is incorporated into health education talks given at enrollment into HIV care and while waiting for appointments. Personalized counseling is done by nurses and clinical officers during clinic visits, after which eligible women are offered screening. In this study, we assessed knowledge, personal risk perception, stigma, and screening uptake among women enrolled in the FACES clinic 5 years after the start of the CCSP program.
Materials and Methods
We conducted a cross-sectional survey of HIV positive women attending an HIV clinic in Kisumu Kenya on their knowledge and attitudes about cervical cancer screening. Women were eligible to participate in they were clinic attendees at Lumumba Health Center in Kisumu, Kenya and met the clinic’s eligibility criteria for cervical cancer screening (non-pregnant women ages 23–64 years). On four separate clinic days over the course of 1 month in April 2013, all eligible women attending the FACES Lumumba Health Center clinic for their regular HIV care were asked at clinic registration if they would be willing to participate in the survey. A total of 106 women were enrolled in the study. This sample size was felt to be adequate to estimate overall clinic screening rates and cervical cancer knowledge and was powered to detect an 11 % difference in knowledge scores. In a private room, trained interviewers administered the structured survey in English, Kiswahili, or Dholuo, depending on the participant’s language preference, and entered responses directly onto Open Data Kit software (opendatakit.org) on tablet computers.
The survey included sections on demographic characteristics, cervical cancer awareness, specific knowledge, perception of risk, stigma, and screening acceptability. Survey questions were based off of previous studies of common misconceptions about cervical cancer in Sub-Saharan Africa and validated questionnaires and were piloted prior to administration [9, 11, 14–16]. The awareness section consisted of five yes/no questions about whether or not participants had ever heard of cervical cancer, screening, Pap smears, visual inspection with acetic acid (VIA), and human papilloma virus (HPV). The knowledge section included 15 true/false questions about facts and common myths about cervical cancer risk factors and prevention. The risk section asked if women felt personally at risk for cervical cancer as well as malaria, breast cancer, and sexually transmitted diseases for comparison. The stigma section adapted a 9-point HIV stigma questionnaire [15] to assess perceived cervical cancer and HIV stigma. Finally, women were asked if they had been previously screened, would pay for screening, and would accept screening by a male provider.
For bivariate and multivariate regressions, we used chi-square, t-test, linear, and logistic regression models. Knowledge questions were compiled into a 15-point Knowledge Score which was used in linear regression models. Stigma was dichotomized into ‘having stigma’ if participants responded ‘yes’ to any of the nine stigma statements and ‘not having stigma’ if they responded ‘no’ to all stigma statements; exact logistic regression was used for this analysis because few participants reported any stigma. Multivariate models were created using backwards elimination including variables determined a priori to be potential confounders (age and education) and those that had a p<0.2 in the bivariate analysis; models also controlled for interviewer using hierarchical clustering. Final models included all variables found in the backwards elimination to be statistically significant (p<0.05), variables that were significant in bivariate analysis, and variables deemed important potential confounders (age and education). Knowledge Score was maintained as a continuous variable whereas all other questions were analyzed as dichotomous variables. Results were analyzed using STATA SE statistical software (version 12.1; College Station, Texas). Ethical approval was obtained from the Kenya Medical Research Institute Ethical Review Committee and the University of California, San Francisco Committee on Human Research.
Results
Demographic Characteristics
106 HIV positive women consented for participation and were interviewed during the 4-week study period. The average age of the participants was 34.9 years (SD=±7.9) and the average time since testing HIV positive was 5.3 years (SD=±3.2). The health facility or a healthcare worker was the primary source of health information for 88 % (N=93) of women and 84 % (N=89) had been previously screened for cervical cancer (Table 1).
Table 1.
Demographic characteristics
| Characteristic |
N (%) n=106 |
|---|---|
| Age (years; mean±SD) | 34.9±7.9 |
| Duration since tested HIV+ (year; mean±SD) | 5.3±3.2 |
| Knows someone with cervical cancer | 21 (20 %) |
| Transportation to clinic | |
| Motorcycle/tuktuk/bus | 78 (74 %) |
| Walking/bicycle | 28 (26 %) |
| Travel time to clinic (minute; mean±SD) | 34±26.6 |
| Education | |
| Primary school or less | 61 (58 %) |
| Secondary school or beyond | 45 (42 %) |
| Occupation | |
| Professional/technical/sales/services | 76 (72 %) |
| Housewife/farming/fishing | 31 (29 %) |
| Relationship Status | |
| Married | 58 (55 %) |
| Single/widowed/divorced | 48 (45 %) |
| Primary source of health information | |
| Health facility or healthcare worker | 93 (88 %) |
| Outside source (i.e., radio, school, and NGO) | 13 (12 %) |
| Cervical cancer risk factors | |
| Gravida (mean±SD) | 3.1±1.6 |
| Parity (mean±SD) | 3.0±1.6 |
| Age of sexual debut (mean±SD) | 16.9±2.9 |
| No. of current sexual partners (mean±SD) | 0.9±0.6 |
| No. of lifetime sexual partners (mean±SD) | 2.6±1.4 |
| Sex worker | 2 (2 %) |
| Health seeking behavior | |
| Hx of cervical cancer screening | 89 (84 %) |
| Hx of STD testing | 51 (48 %) |
| Hx of breast exam | 11 (10 %) |
| Hx of mammogram | 3 (3 %) |
| Uses family planning | 65 (61 %) |
Awareness
Nearly every participant (N=105; 99 %) had heard of cervical cancer screening, but only 42 (40 %) had heard of VIA (Table 2). On multivariate analysis, previous screening for cervical cancer, older age, and higher educational attainment were significant predictors of VIA awareness (Table 3).
Table 2.
Awareness and knowledge
|
N (%) n=106 |
|
|---|---|
| Awareness (% ever heard of…) | |
| Cervical cancer | 104 (98 %) |
| Cervical cancer screening | 105 (99 %) |
| Pap smear | 48 (45 %) |
| VIA | 42 (40 %) |
| HPV | 25 (24 %) |
| Awareness Score (mean # positive out of 5) | 3.1±0.9 |
| Knowledge (% answered correctly) | |
| Screening tests look for changes on your cervix that indicate you are at risk for cancer | 91 (86 %) |
| Women should get screened for cervical cancer only if they have symptoms | 93 (88 %) |
| If a woman has abnormal vaginal bleeding, discharge, or pain, she should see a medical provider to get screened for cervical cancer | 100 (94 %) |
| Cervical cancer can be prevented | 89 (84 %) |
| Screening tests can help prevent cervical cancer | 98 (92 %) |
| There is no treatment for cervical cancer | 75 (71 %) |
| Knowledge of risk factors (% answered correctly) | |
| Family planning increases risk | 36 (34 %) |
| HIV increases risk | 80 (75 %) |
| Only HIV+ women are at risk | 92 (87 %) |
| Washing inside the vagina decreases risk | 37 (35 %) |
| Screening decreases risk | 100 (94 %) |
| Nothing can prevent cervical cancer because it is fate or the will of God | 75 (71 %) |
| Knowledge of HPV (% answered correctly) | |
| HPV is an infection that can cause cervical cancer | 24 (23 %) |
| HPV is spread during close contact like during sexual intercourse | 35 (33 %) |
| HPV infection is always symptomatic | 8 (8 %) |
| Knowledge Score (mean # correct out of 15) | 9.7±1.8 |
Table 3.
Demographic predictors of cervical cancer awareness, risk perception, stigma, and prior screening
| Awareness of VIA | Perception of risk | Stigma | Previously screened | |||||
|---|---|---|---|---|---|---|---|---|
| Unadjusted OR (95 % CI) | Adjusted OR (95 % CI) | Unadjusted OR (95 % CI) | Adjusted OR (95 % CI) | Unadjusted OR (95 % CI) | Adjusted OR (95 % CI) | Unadjusted OR (95 % CI) | Adjusted OR (95 % CI) | |
| Age >35 years | 0.8 (0.3–1.6) | 1.5 (1.1–2.2)* | 0.7 (0.3–1.6) | 0.6 (0.6–0.6)*** | 0.5 (0.2–1.5) | 0.4 (0.3–0.6)*** | 1.6 (0.5–4.8) | 1.2 (0.4–3.7) |
| Education beyond primary school | 1.4 (0.6–3.1) | 1.5 (1.2–1.9)*** | 1.3 (0.6–3.1) | 1.2 (1.0–1.3)* | 1.4 (0.5–4.0) | 1.6 (1.0–2.7) | 0.9 (0.3–2.7) | 0.9 (0.3–2.6) |
| Duration HIV+ >5 years | 0.8 (0.4–1.8) | – | 2.4 (1.0–5.7)* | 3.2 (1.2–8.6)* | 1.1 (0.4–3.2) | – | 4.1 (1.2–13.7)* | 4.0 (1.2–13.8)* |
| Health facility primary source of health info | 0.5 (0.2–1.7) | – | 0.7 (0.1–2.8) | – | 0.4 (0.1–1.5) | 0.3 (0.3–0.4)*** | 0.4 (0.1–3.6) | – |
| Sexual debut >17 years | 1.1 (0.5–2.4) | – | 1.9 (0.8–4.9) | 2.1 (1.6–2.9)*** | 1.2 (0.4–3.5) | – | 0.6 (0.2–1.9) | – |
| Knows someone who had cervical cancer | 1.5 (0.6–3.9) | – | 0.5 (0.2–1.3) | 0.5 (0.3–0.8)** | 2.4 (0.8–7.5) | – | 1.1 (0.3–4.2) | |
| Cervical cancer screeneda | 5.6 (1.2–26.1)* | 6.1 (1.7–21.8)** | 1.1 (0.3–3.3) | – | 0.5 (0.2–2.0) | – | – | – |
OR odds ratio, CI confidence interval
p<0.05;
p<0.01;
p<0.001
Bivariate and multivariate analyses of outcomes variables (awareness, risk, and stigma) as predictors of prior screening
Knowledge
The mean Knowledge Score was 9.7 (SD=±1.8) out of 15 possible points. Most women knew that screening could help to prevent cervical cancer (N=98; 92 %) and that treatment was available (N=75; 71 %). Additionally, 75 % (N=80) of women recognized that HIV positivity increased their risk of cervical cancer and 87 % (N=92) knew that not only HIV positive women were at risk. However, other myths about risk factors were commonly reported; 66 % (N=70) believed that family planning increases risk and 65 % (N=69) believed that vaginal washing decreases risk (Table 2). On multivariate analysis, the only significant predictor of high knowledge was education beyond primary school. Knowledge Score was not significantly associated with prior cervical cancer screening (Table 4).
Table 4.
Demographic predictors of cervical cancer knowledge
| Knowledge scorea | ||
|---|---|---|
| Unadjusted coefficient (95 % CI) | Adjusted coefficient (95 % CI) | |
| Age (>35 years) | 0.1 (−0.6–0.8) | 0.2 (−5.7–6.1) |
| Education (beyond primary school) | 0.8 (0.1–1.5)* | 0.5 (0.3–0.7)* |
| Duration HIV+ (>5 years) | 0.4 (−0.6–0.7) | – |
| Source of health info (at health facility) | 0.8 (−0.3–1.8) | – |
| Sexual debut (>17 years) | 1.2 (0.5–1.9)** | 1.0 (−0.2–2.3) |
| Knows someone who had cervical cancer | 0.4 (−0.5–1.2) | – |
| Cervical cancer screened | −0.1 (−1–0.9) | – |
Other demographic characteristics were not significant and thus not included in this chart
CI confidence interval
p<0.05;
p<0.01;
p<0.001
Linear regression of score out of 15 possible points
Perception of Risk
Seventy percent of women (N=74) said they felt at risk for cervical cancer; compared to 93 % (N=99) for malaria, 60 % for breast cancer, and 53 % for an STI. Being diagnosed with HIV over 5 years ago was the only significant predictor of feeling at risk for cervical cancer on bivariate analysis. On multivariate analysis, significant predictors of feeling at risk were longer duration of HIV diagnosis, younger age, higher education, older sexual debut, and not knowing anyone with cervical cancer. There was no association between feeling at risk for cervical cancer and either Knowledge Score or history of screening (Table 3).
Stigma
Overall Cervical Cancer and HIV Stigma Scores were both low, with respective average scores of only 0.4 (±1.2) and 0.6 (±1.4) out of 9 possible points. Only 17 % (N=18) answered yes to at least one cervical cancer stigma statement and 25 % (N=26) answered yes to at least one HIV stigma question. On multivariate analysis, younger women and women who primarily used the health facility for their health information reported significantly less stigma. There was no significant association between reporting any cervical cancer stigma and prior screening (Table 3).
Cervical Cancer Screening
Only 16 women (15 %) had not previously been screened for cervical cancer, of which 12 said they would agree to screening that day. Two women declined screening because they were menstruating and two declined because they did not have time to wait. Only nine women (8 %) said they would refuse screening by a male provider, whereas 51 (48 %) said they would not get screened if they had to pay. Of those who said they would pay for screening (N=55), the median amount women said they would be willing to pay for screening was KSh200 (~$2.50), with responses varying from KSh50 to 5000 ($0.75 to $75). Women who had been diagnosed with HIV more than 5 years ago were over four times as likely to have been screened for cervical cancer in both bivariate and multivariate analyses (Table 3).
Discussion
In this population, awareness of screening and screening rates were both high and well over the 80 % goal set by the WHO. Perception of risk and screening rates were higher in women with a longer duration of HIV diagnosis. Although gaps in knowledge about certain risk factors were common, most women correctly answered questions about screening and treatment as a means to prevent cervical cancer.
Additionally, knowledge in this population of women enrolled in a clinic with a CCSP program was higher than in neighboring populations with less exposure to cervical cancer screening education. The same survey tool was used to measure knowledge and attitudes of previously unscreened women attending rural health facilities newly offering cervical cancer screening in western Kenya [16]. Although responses to individual questions were similar, women surveyed in this study had consistently higher knowledge, higher risk perception, and lower stigma than in the neighboring study. Although these differences could be attributed in part to differing demographic characteristics, they could also be a reflection of ongoing CCSP activities for the past 5 years, supporting the idea that clinic-based health education can have a positive impact on patients’ knowledge and attitudes regarding screening.
This study has some limitations. We sought to describe the knowledge and behavior of women enrolled in an HIV clinic that had offered integrated cervical cancer screening for the past 5 years. This is not a representative sample of the larger community of women in this urban area who likely have much less exposure to CCSP services. However, measuring knowledge, attitudes, and screening rates in this population provides a standard for what is achievable only a few years into an integrated HIV-cervical cancer program as well as a guide for potential gaps. Another limitation of this study is that as a retrospective study, it is not possible to determine a causal relationship between cervical cancer awareness and prior screening. The power of the study to detect significant predictors of previous cervical cancer screening is also limited by the small sample size and high rates of screening.
However, this study does introduce an interesting predictor of screening: duration of HIV diagnosis. The relationship between prior cervical cancer screening and duration of HIV is unclear. Longer duration of HIV positivity may be a surrogate marker for higher acceptance of healthcare services, decreased stigma, increased exposure to health education, increased perception of vulnerability, or simply repeated opportunities for screening.
In addition to exploring how certain knowledge and attitudes affect screening behavior, further research is needed on the importance and efficiency of having repeated opportunities for education and screening in low-resource settings. Another potentially critical barrier highlighted by this study is the limited willingness to pay for screening. While pilot studies frequently provide screening and treatment for free, screening at public institutions in Kenya frequently costs between KSh50 and 200 (approximately $0.50–$2.50), and up to KSh2000 (approximately $25) for cryotherapy treatment. About half of the women surveyed said they would not get screened if they had to pay for it.
Cervical cancer screening rates are high in this population of women with repeated education and availability of free screening services. However, in order to achieve universal screening coverage, clinic-based screening programs need to be scaled-up. Screening programs have already grown to include community outreach and mobile clinic models. In order for programs to successfully reach the greatest number of women, they need to consider the importance of providing multiple opportunities for exposure to education and screening services in a low or no cost way.
Acknowledgments
This work was supported by a grant from the Doris Duke Charitable Foundation to the University of California, San Francisco to fund Clinical Research Fellow Joelle Rosser. While working on this project, M.J.H. was supported through a National Institutes of Health career development award (KL2 RR024130-04).
Footnotes
Conflict of Interest The authors have no conflicts of interest.
Contributor Information
Joelle I. Rosser, Department of Internal Medicine, University of Washington, 1959 NE Pacific Street Box 356421, Seattle, WA 98195-6421, USA
Betty Njoroge, Centre for Microbiology Research, Kenya Medical Research Institute (KEMRI), P.O. Box 54840-00200, Mbagathi Way, Nairobi, Kenya.
Megan J. Huchko, Department of Obstetrics, Gynecology and Reproductive Sciences, Bixby Center for Global Reproductive Health, University of California, San Francisco; 50 Beale Street, San Francisco, CA 94143, USA
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