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RHO archives : Topics : Cervical Cancer Prevention

Annotated Bibliography

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Cervical cancer and HIV

Abercrombie, P.D. and Korn, A.P. Lower genital tract neoplasia in women with HIV infection. Oncology 12(12):1735-1739 (December 1998).
This article reviews the current body of knowledge about lower genital tract neoplasia in HIV-infected women. Issues discussed in the article include human papillomavirus (HPV) infection in HIV-infected women, lower genital tract neoplasia, and cancer. The authors recognize that knowledge about the pathophysiology and clinical management of lower genital tract neoplasia in HIV-infected women is incomplete, and that more research in this area is needed. Regular performance of cervical Pap smears can be of critical importance. Careful examination of the entire lower genital tract of HIV-infected women is crucial, because of the multifocal nature of HPV-related neoplasms. The authors recommended that women who have high-grade intraepithelial neoplasia or cervical cancer be offered testing for HIV infection.

Chirenje, Z.M. et al. Association of cervical SIL and HIV-1 infection among Zimbabwean women in an HIV/STI prevention study. International Journal of STD & AIDS 13:765-768 (2002).
This article presents results from a cross-sectional study of the association of cervical squamous intraepithelial lesions (SIL) and HIV-1 infection in Zimbabwe. Among the 554 women in the study, the prevalence of HIV-1 was 36.8 percent. Compared to HIV-negative women, HIV-infected women had twice the risk of having abnormal cervical cells (relative risk 2.47, odds ratio 10.14, P < 0.001), The prevalence of both low-grade squamous intraepithelial lesions and high-grade squamous intraepithelial lesions was associated with HIV infection; this association was statistically significant. These results agree with other studies showing that HPV infection and the presence of cervical lesions are associated with HIV infection. The authors suggest that, in resource-poor settings, careful decisions about resource allocation must be made because of the many competing health needs of HIV-positive women. In Zimbabwe, although HIV-infected women have higher rates of HSIL, the Zimbabwe National Cancer Registry has not recorded an increase in invasive cervical cancer cases. Due to scarcity of resources and anti-retroviral drugs, the authors hypothesize that many HIV-infected women may be dying of other opportunistic infections prior to presenting with invasive cervical cancer.

French, A.L., Kirstein, L.M., Massad, L.S., et al. Association of vitamin A deficiency with cervical squamous intraepithelial lesions in human immunodeficiency virus-infected women. Journal of Infectious Diseases 182:1084-1089 (October 2000).
This study examined the association between vitamin A deficiency and the development of cervical squamous intraepithelial lesions (SILs) in 1,314 HIV-infected women. Retinol (vitamin A) concentrations were measured at a baseline visit and compared to cervical samples (Pap smears and cervicovaginal lavage fluid). At baseline 204 women had retinol levels that met the definition of vitamin A deficiency (<1.05umol/L). Pap smear results showed 216 women with SILs. Multivariate statistical analyses suggest low retinol concentrations were independently associated with SILs (OR 1.63; P = .04). The analysis was repeated in a subset of women who had tested positive for HPV DNA. Mulitvariate analysis again showed an association between retinol deficiency and cervical SILs (OR 1.75; P = .02). These findings, which contradict several earlier studies, suggest that vitamin A deficiency in HIV-infected women may play a role in the development of cervical SILs and suggest that further study of this association is necessary.

Fruchter, R.G. et al. Is HIV infection a risk factor for advanced cervical cancer? Journal of Acquired Immune Deficiency Syndromes and Human Retrovirology 18(3):241-245 (July 1, 1998).
The goal of this study was to compare HIV-infected and HIV-negative women with invasive cervical cancer with respect to predictors of advanced disease. The study compared 28 HIV-infected and 132 HIV-negative cervical cancer patients with regard to stage of disease, demographic and behavioral variables, and risk factors for advanced disease. Results from a retrospective analysis of the data showed that HIV-infected women had a fivefold greater rate of cervical intraepithelial neoplasia or unevaluated abnormal smears than the HIV-negative women. A univariate analysis indicated that HIV infection was associated with a threefold increase in advanced-stage cervical cancer. However, a multiple logistic regression analysis showed that the major predictors of advanced cervical cancer in HIV-infected and HIV-negative women were similar and that only lack of cytologic screening and prolonged duration of symptoms were significant predictors of advanced disease. The authors stated that it is likely that a large proportion of HIV-infected women with cervical cancer acquire HIV infection after the initiation of the neoplastic process rather than as a result of immunodeficiency, demonstrating an association of the common behavioral risk factors of the two diseases rather than a causal effect of HIV immunodeficiency.

Gichangi, P.B. et al. Impact of HIV infection on invasive cervical cancer in Kenyan women. AIDS 17:1963-1968 (2003).
Data on the interaction between HIV and invasive cervical cancer (ICC) are scarce. In this case-control study, authors examine this association in a population of Kenyan women where the prevalence of both HIV and ICC are substantial. The Cases were recruited from women with cervical cancer at the radiotherapy unit in Kenyatta National Hospital. Controls were women with uterine fibroids diagnosed by ultrasound. After controlling for confounding factors of educational level, number of partners, and previous history of an STD, women with invasive cervical cancer who also were HIV-positive were on average 10 years younger than HIV-negative women with invasive cervical cancer. In fact, ICC patients less than 35 years of age were 2.6 times more likely to be HIV-positive than patients with uterine fibroids of the same age. HIV-positive ICC patients also had greater risk of having poorly differentiated tumors as compared to HIV-negative ICC patients (77% vs. 53%; OR, 3.1; P=0.038), which is indicative of a poor prognosis.

La Ruche, G. et al. Squamous intraepithelial lesions of the cervix, invasive cervical carcinoma, and immunosuppression induced by human immunodeficiency virus in Africa. Cancer 82(12):2401-2408 (June 15, 1998).
Squamous intraepithelial lesions (SILs) are associated with human immunodeficiency virus (HIV), but the factors associated with SILs and cervical cancer, and their prevalence must be considered in context. This study screened 2,198 women from three outpatient gynecological clinics in Abidjan, C�te d'Ivoire, for cervical disease and HIV infection. The prevalence of HIV infection was 21.7 percent, and 11.7 percent had dysplasia or neoplasia (7.6 percent low grade SILs, 3.3 percent high grade SILs, and .8 percent invasive cervical cancer). Multivariate analysis found that the factors associated with low grade SILs were: HIV-1 seropositivity, age less than 24 years, parity greater than one, consultation for genital infection, and no use of oral contraceptives in the past. For high-grade SILs, the factors were HIV-1 seropositivity, chewing tobacco use, low educational level, and parity greater than one. Cervical cancer was associated with age over 33 years, parity greater than three, and illiteracy. Cancer was associated with HIV-2 infection, but not HIV-1 infection. The factors associated with precancerous and cancerous lesions are different. HIV-positive women should receive screening for cervical cancer, and women with cervical cancer should be offered HIV testing. However, cervical cancer screening should not depend on HIV screening because the requirements of the two programs differ. Cervical cancer screening could be directed toward women with low educational levels or multiparity or both, as indicated by the risk factors identified in this study.

La Ruche, G. et al. Human papillomavirus and human immunodeficiency virus infections: relation with cervical dysplasia-neoplasia in African women. International Journal of Cancer 76:480-486 (1998).
The goal of this study was to assess the factors associated with squamous intraepithelial lesions (SILs) and invasive cervical cancer, with special attention to human immunodeficiency virus (HIV) and human papillomavirus (HPV). Women were recruited from three outpatient gynecology clinics of Abidjan, Cote d'Ivoire, and screened for cervical abnormalities. The women were placed into three case-control groups: 151 women with low-grade SILs and 151 controls, 60 women with high-grade SILs and 240 controls, and 13 women with invasive cancer and 65 controls. Results from multivariate analyses showed that factors associated with low-grade SILs were HPV positivity, HIV-1 seropositivity, and parity greater than 3. Factors associated with high-grade SILs were HPV positivity, chewing tobacco, HIV-1 seropositivity, and illiteracy. The only factor associated with invasive cancer was HPV positivity. The results show that, in HIV-infected women, SILs occurred at an early stage of HIV disease. Women infected with both HIV and HPV were at a much higher risk of SILs than women infected with either of the two viruses separately. Based on the study findings, the authors suggest that cervical screening could be directed preferentially to women with low educational levels or women of high parity.

Leroy, V. et al. Cervical dysplasia and HIV type 1 infection in African pregnant women: a cross sectional study, Kigali, Rwanda. Sexually Transmitted Infections 75:103-106 (1999).
The goal of this study was to determine the prevalence of cervical squamous intraepithelial lesions (SILs) and their association with HIV-1 infection and immunodeficiency among pregnant women in Kigali, Rwanda. A total of 103 HIV-positive and 107 HIV-negative women participated in the study. The participants were recruited at the maternity ward of the Centre Hospitalier de Kigali. At inclusion, the women were screened for sexually transmitted infections (STIs) including syphilis, gonorrhea, chlamydia, and trichomoniasis. CD4 cell counts were measured and Pap smears were performed. The study results showed that the prevalence of SILs was significantly higher in HIV-infected women than in HIV-negative women: 24.3 percent versus 6.5 percent, respectively. Furthermore, SIL-positive women tended to have more STIs than SIL-negative women (37.5% and 24.7%, respectively), but this did not reach a statistical difference. The authors conclude that the prevalence of SILs was high in this population of pregnant women with high STI/HIV prevalence. They note that this cross-sectional study cannot establish a causal relation between HIV infection and SILs. Other factors such as age, age at first intercourse, parity, STIs, and number of sexual partners may be confounding factors in the analysis of this association.

Luque, A.E. et al. Association of human papillomavirus infection and disease with magnitude of human immunodeficiency virus type 1 (HIV-1) RNA plasma level among women with HIV-1 infection. Journal of Infectious Diseases 179:405-409 (June 1999).
The goal of this cross-sectional study was to evaluate the relationship between plasma HIV-1 RNA levels and coincident cervical infection and disease caused by human papillomaviruses (HPVs). A total of 93 women recruited from the University of Rochester's Strong Memorial Hospital enrolled in the study. The women underwent a standardized history and physical examination that included a gynecologic history and pelvic examination. The study results showed that HIV-1 RNA plasma levels of greater than 10,000 copies/mL were highly associated with high-risk HPV DNA in cervical specimens. In addition, similar HIV-1 RNA plasma levels were associated with abnormal Pap smears. Eighty-one percent of women with high-risk HPV cervical infection had abnormal Pap smears. Among the women with detectable HPV DNA, the most frequent abnormality reported in Pap smears was low-grade SIL on specimens from 54 percent of patients with high-risk HPV DNA. The authors conclude that measurements of HIV-1 RNA plasma levels may help to identify a subgroup of HIV-infected women at increased risk for cervical HPV infection and disease and that women with moderate to high levels of plasma HIV-1 RNA may profit from aggressive gynecologic monitoring.

Palefsky, J.M. et al. Cervicovaginal human papillomavirus infection in human immunodeficiency virus-1 (HIV)-positive and high-risk HIV-negative women. Journal of the National Cancer Institute 91(3):226-236 (February 3, 1999).
The goal of this study was to determine the prevalence of and risk factors for cervicovaginal HPV infection in HIV-positive women. A total of 1,778 HIV-positive and 500 HIV-negative women were recruited from a pool of women enrolled in the Women's Interagency HIV Study. The study results confirmed earlier observations that HPV infection is significantly more common among HIV-positive women than in high-risk HIV-negative women. Compared with HIV-negative women, HIV-positive women with CD4 cell count of less than 200/mm3 were at the highest risk of HPV infection, regardless of HIV RNA load, followed by women with a CD4 cell count greater than 200/mm3 and an HIV RNA load greater than 20,000 copies/mL, and women with CD4 count greater than 200/mm3 and an HIV RNA load less than 20,000 copies/mL. Other risk factors among HIV-positive women included racial/ethnic background (African American versus Caucasian, OR = 1.64), current smoking (yes versus no, OR = 1.55), and younger age (age <30 years versus >40 years, OR = 1.75). The study results suggest that detection of HPV in HIV-positive women more likely reflects either reactivation or persistence of pre-existing HPV types rather than recent HPV acquisition.

Tate, D. and Anderson, R. Recurrence of cervical dysplasia among women who are infected with the human immunodeficiency virus: a case-control analysis. American Journal of Obstetrics and Gynecology.186(5, Part 1):880-882 (2002).
This case-control study compared cervical dysplasia treatment outcomes for 43 HIV-positive women and 103 HIV-negative women. The women received cryotherpy, laser ablation, LEEP, conization, or hysterectomy as treatment for CIN. For all treatment modalities, women who were HIV-positive had higher recurrence rates than HIV-negative women (73% versus 27%; P = .019). Overall, for all treatment modalities, patients with CD4 cell counts <200 had higher recurrence rates than women with higher CD4 counts.

Wright, T.C. et al. Human immunodeficiency virus 1 expression in the female genital tract in association with cervical inflammation and ulceration. American Journal of Obstetrics and Gynecology 184(3):279-285 (February 2001).
This study quantified the change in HIV-1 RNA shedding in women who had been treated for cervical squamous intraepithelial lesions. HIV-1 RNA levels in the cervicovaginal secretions were measured before and after treatment in 14 HIV-positive women with cervical lesions. At two to four weeks post-treatment, when the cervix visually was still inflamed and ulcerated, cervicovaginal HIV-1 shedding had increased as much as 10,000 fold (from 1.0 to 4.4 log 10; mean log 10 increase was 2.3). Between 8 and 14 weeks after treatment, when the cervix had healed, HIV-1 RNA levels had returned to pre-treatment levels. Additional tests were performed to rule out contamination of the cervicovaginal secretions by HIV virus in the found in the blood and it was concluded that blood was an unlikely explanation for the significant increase of HIV-1 RNA found in the genital secretions. The authors recommend that HIV positive women undergoing treatment for cervical lesions should be counseled to abstain from sexual intercourse for at least four weeks following the treatment to avoid transmitting HIV to their partners.

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Cost-effectiveness and cost implications

Brown, A.D., Raab, S.S., Suba, E.J., et al. Cost-effectiveness studies on cervical cancer. Acta Cytologica 45:509-514 (2001).
This article reviews recommendations generated at the International Consensus Conference on the Fight Against Cervical Cancer. These recommendations include: (1) Cost-effectiveness analyses should, whenever possible, use a reference case to report baseline results. (2) Cost-effectiveness analyses should use a single standard of evidence when evaluating interventions. (3) Further research is necessary to provide information on questions including quality of life after receiving a false positive result and the costs of various aspects of screening and treatment strategies. (4) Further research on cost-effectiveness is necessary in developing countries. (5) Detailed methodology, including assumptions used in the cost-effectiveness model, should be made available in an accessible place such as the Internet. (6) Comparisons of available models should be made. (7) Conflicts of interest of researchers should be disclosed, with subsequent opportunity for publication.

Goldie, S.J., Kuhn, L., Denny, L., et al. Policy analysis of cervical cancer screening in low-resource settings: clinical benefits and cost-effectiveness. JAMA 285(24):3107-3115 (June 27, 2001).
This study utilizes a mathematical model to compare the clinical benefits and cost-effectiveness of various screening and treatment strategies for cervical cancer prevention, including HPV DNA testing, direct visual inspection (DVI)—also commonly referred to as visual inspection with acetic acid (VIA)—and cytology. Data inputs include data from an existing South African study being implemented by EngenderHealth, Columbia University, and the University of Cape Town; existing schedules and surveys of fees; and other literature. Policy analysis using this model suggests that, using a hypothetical population of previously unscreened South African women, a single lifetime screening followed with immediate treatment at age 35 offered the best balance of costs and benefits. As compared to no screening, DVI followed with immediate treatment with cryotherapy can decrease subsequent cervical cancer incidence by 26 percent and was cost saving. The most effective strategy, HPV testing followed by a second visit for treatment, reduced cervical cancer incidence by 27 percent and cost $39/YLS (years of life saved). One-visit strategies, however, as compared to two-visit or three-visit strategies, reduced costs and loss to follow up. Authors note that cost-effectiveness analyses are but one important input into a policy decision, and cultural norms, health infrastructure, costs for equipment, supplies, and training may all be country- or region-specific and will need to be considered as well. This policy analysis, however, has important implications for decisions around cervical cancer screening in developing countries, offering countries with limited resources evidence of cost-effective screening and treatment strategies.

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Client perceptions

Adanu, R.M.K. Cervical cancer knowledge and screening in Accra, Ghana [letter to the editor]. Journal of Women's Health & Gender-Based Medicine 11(6):487-488 (2002).
In this letter, the author discusses the results from a questionnaire on cervical cancer knowledge and screening practices that was completed by 175 well-educated women in Accra, Ghana. Women participants were categorized as medical students, non-medical undergraduate students, nurses, and senior university workers. Among these 175 women, 93 percent said they had heard of cervical cancer, although only 37 percent had adequate knowledge of the disease. Only 39 percent of women had adequate knowledge of Pap smears and, of those, only 8.5 percent had ever had a Pap smear. Medical students and nurses had the most knowledge of cervical cancer and Pap smears, while actual Pap smear use was highest among university staff. The author discusses how the level of knowledge is not necessarily translated into use. The author highlights the need for an organized cervical cancer screening program that would includes better public education of nonmedical personnel and increased initiative from medical doctors to perform routine Pap smears.

Ajayi, I.O. and Adewolfe, I.F. Knowledge and attitude of general outpatient attendants in Nigeria to cervical cancer. Central African Journal of Medicine 44(2):41-43 (1998).
This cross-sectional study of women between the ages of 20 and 65 investigated Nigerian women's knowledge about cervical cancer, their source of information, and their general attitude about cancer. A total of 254 women were randomly selected from patients and accompanying persons attending a general outpatient clinic at a tertiary hospital in Ibaadan, Nigeria, to complete a structured questionnaire. The authors found that 90 percent of these women had heard of cancer (most commonly breast cancer [64.5 percent]). Only 15 percent had heard of cancer of the cervix. Media and peers were the major sources of information on cancer. Over half of the respondents had no knowledge of the description of cervical cancer, clinical presentation, or causes. The authors conclude that knowledge of cervical cancer is poor and that there is a need to educate women about cervical cancer and its early warning signs in Nigeria.

Dzuba, I.G. et al. The acceptability of self-collected samples for HPV testing vs. the Pap test as alternatives in cervical cancer screening. Journal of Women�s Health & Gender-based Medicine 11(3):265-275 (2002).
This study evaluated the acceptability of self-collected samples for HPV testing as compared to the Pap test among 1,069 women in Mexico. Women were asked questions about their experiences with both methods of screening and ranked each test on discomfort, pain, embarrassment, privacy, perception of treatment during the Pap test, and clarity of the instructions for the self-collection for HPV. Results showed that overall the women rated the self-collection method as more acceptable to the Pap smear. When women reported a preference for a test, they more often chose the self-sampling method. The reasons for preferring the self-sampling method included less discomfort and less embarrassment. Women indicated no difference in the level of pain or level of privacy experienced during the two tests. Authors suggest that offering self-collection could increase participation in cervical cancer screening among women who are uncomfortable with Pap tests.

Fylan, F. Screening for cervical cancer: a review of women's attitudes. Knowledge, and behaviour. British Journal of General Practice 48:1509-1514 (August 1998).
The article reviews the psychological consequences of receiving an abnormal cervical smear result and undergoing secondary screening and treatment, and examines reasons for women's nonparticipation in screening programs. Reasons for nonparticipation include administrative failures, unavailability of female screeners, inconvenient clinic times, lack of awareness of the test's indications and benefits, considering oneself not to be at risk of cervical cancer, and fear of embarrassment, pain, or the detection of cancer. Receiving an abnormal result and referral for colposcopy causes high levels of distress owing to limited understanding of the meaning of the smear test; many women believe the test aims to detect existing cervical cancer. The article discusses ways in which health professionals can increase their patients' participation in screening programs and minimize the distress experienced by women who require secondary screening and treatment.

Holroyd E, Twinn S, Adab P. Socio-cultural influences on Chinese women’s attendance for cervical screening. Journal of Advanced Nursing. 2004;46(1):42-52.
Authors investigated the sociocultural influences on women’s attendance for cervical cancer screening in Hong Kong. Data were gathered from 10 focus groups with 54 previously screened and unscreened women and from interviews with 28 Hong Kong doctors. The focus groups revealed several themes. For women who had sought screening, the decision was more often prompted by marriage or childbirth rather than self-initiated for health protection. Having a friend or relative with cancer also influenced women’s decisions to seek screening. The focus groups identified a preference for female providers among both screened and unscreened women. Perceived risk factors for cervical cancer identified by the women included promiscuity, marriage, youth and old age, poor personal hygiene of husbands and selves, and the use of tampons. Unscreened women in particular tended to associate seeking health services with illness, not prevention. Barriers to attending screening included time away from work and family, costs, embarrassment, and perceptions of pain. Data from the interviews with doctors showed doctors perceived low educational status, poverty, and lack of knowledge of cervical cancer as barriers to women attending screening. They also described fatalism, modesty, and low perceived susceptibility as factors affecting women’s intentions to seek screening. Finally, several doctors suggested that long waits for services at the clinic posed barriers for women who do not have the time to come for several visits. Authors conclude that there is a need for ensuring all cervical cancer screening programs are conducted in culturally sensitive ways. They recommend education for providers so that they can address the social and cultural factors in the community that act as barriers and can better promote seeking preventive health care and cervical cancer screening services.

Idestrom, M. et al. Women’s experience of coping with a positive Pap smear: a register-based study of women with two consecutive Pap smears reported as CIN 1. Acta Obstetrica et Gynecologica Scandinavica 82(8):756-761 (August 2003).
This study examines how receiving positive Pap smear results affects women’s daily lives and decisions to return for follow-up and treatment. Questionnaires were mailed to 324 Swedish women who five years prior had received two consecutive positive Pap smears showing CIN 1 and should have returned for investigative follow-up. Of these women, 242 (74%) returned the questionnaire. The mean age of women completing the questionnaire was 45 years (range 24-81 years). Two hundred and thirty-three women (96%) returned for follow-up, and for 178 of these women follow-up included a biopsy. The majority of women reported a good or positive experience with the follow-up exams, with older women more frequently reporting a positive experience than younger women. Overall, however, 142 women (59%) reported worry and anxiety over receiving positive Pap smear results and over the significance of the positive result. Twenty women (8%) reported a continued negative effect on their sexuality and their sexual relationships. Most women reported receiving information about Pap smears and dysplasia from their doctor or midwife. Less frequently reported sources of information included media, the health care system (written information), school education, and friends and family. The authors conclude that better sources of information are needed because many women were not receiving the message that mild dysplasia was not a diagnosis of cancer, causing undue worry and stress in their lives when they received a positive Pap smear result.

Jameson, A. et al. Barriers to Pacific women's use of cervical screening services. Australian and New Zealand Journal of Public Health 23(1):89-92 (1999).
This study explored perceived barriers to cervical screening information services from the perspective of Pacific Island women living in New Zealand. Face-to-face, in-depth interviews based on a snowballing technique were used to assess attitudes among 20 Pacific women. Women identified numerous barriers, including a perception that Pacific women were being defined as socially problematic, a belief in the sacred nature of human sexuality, anxiety about a lack of confidentiality within community groups, and the perceived relationship between cervical smears and sexual activity. Study participants also voiced a strong preference for formal and interpersonal rather than informal sources of information. Formal sources included doctors, nurses, clinics, hospitals, and women's health centers. Talking with female rather than male professionals was strongly preferred. Women also agreed that the preferable role of a Pacific Island health professional would be in disseminating information, rather than taking Pap smears. They recommended that multi-racial images of women be used in advertising, illustrating that Pap smears are necessary for all women.

Lauver, D. et al. Women's uncertainties, coping, and moods regarding abnormal Papanicolaou results. Journal of Women's Health & Gender-based Medicine 8(8):1103-1112 (1999).
The goal of this study was to understand the process of coping with the news of abnormal cervical cancer screening results. The specific aims were to (1) compare women's uncertainty about the implications of abnormal Pap tests and their psychological distress over time, and (2) describe relationships among uncertainty, perceived coping ability, coping strategies that were used and helpful, and psychological distress. Women were recruited from January 1995 to March 1996 from multiple health clinics. Seventy-five women agreed to participate and completed the initial telephone interview after hearing the news of their abnormal Pap tests. Forty women completed follow-up questionnaires before their colposcopy, and 35 of these women also completed questionnaires after their colposcopy follow-up. The study results showed that women's uncertainty about abnormal Pap test results decreased over time. Negative mood scores, reflecting psychological distress, did not change over time. Uncertainty about Pap tests, ambiguity about cancer, and perceived inability to deal with Pap test results were positively related. The coping strategy of catharsis (that is, expression of emotions) was associated with greater psychological distress (high negative mood scores) after learning of the news, but acceptance was associated with less psychological distress. The authors conclude that clinical interventions can address uncertainty and promote coping strategies such as relaxation, acceptance, and diversion to reduce psychological distress among women with abnormal cervical smear results.

Lazcano-Ponce, E.C. et al. The positive experience of screening quality among users of a cervical cancer detection center. Archives of Medical Research 33:186-192 (2002).
This study used a population-based survey in the State of Morales, Mexico, to examine the factors associated with higher levels of use of the Pap test. Interviews were conducted with 3,197 randomly selected households, among which 2,094 women had previously had a Pap test and were included in the study. Factors associated with greater use of Pap smear screening services included a previous positive experience with the services, a higher level of education for the head of household, the use of two or more family planning methods, and the understanding of why the screening was necessary. Women who reported that the privacy during the Pap smear screening was acceptable and women who reported that the information given for follow-up care had been good were more likely to have had two or more Pap tests. Authors conclude that in areas of Mexico where cervical cancer screening is ineffective, programs should focus on improving quality of care as a key component of increasing utilization of screening services.

Lazcano-Ponce, E.C. et al. Barriers to early detection of cervical-uterine cancer in Mexico. Journal of Women's Health 8(3):399-408 (1999).
This qualitative study of barriers to early detection of cervical cancer included four focus groups�two in the urban setting of Mexico City and two in rural communities in the state of Oaxaca. In each setting, one focus group included women with at least one previous Pap test, and one focus group included women who had never had the test. The authors found that barriers to the Pap test included lack of knowledge about cervical cancer etiology, unawareness of the Pap test , the perception that cancer is an inevitably fatal disease, problems in client-provider relationships, giving priority to unmet needs related to extreme poverty, opposition by male sexual partners, rejection of the pelvic examination, long waits for sample collection and results, and perceived high costs for care. Based on these findings, the authors recommend that more information be given to women in an effort to create "a culture of prevention" that incorporates use of the early detection program for cervical-uterine cancer. They recommend that the campaign include information about age at which testing should begin and end, time lapse between tests, instructions for preparing for the sample, a description of the procedure for taking the sample, instructions about when and where to return for the results, and basic etiology of cervical cancer. They also suggest that multiple communication strategies be used to promote the use of the Pap test, including promotion during contacts between health personnel and women; distribution of information by radio, posters, and pamphlets; promotion through community groups; and incorporating promotion of cervical cancer prevention into existing health programs.

Lazcano-Ponce, E.C. et al. The cervical cancer screening program in Mexico: problems with access and coverage. Cancer Causes Control 8(5):698-704 (September 1997).
The goal of this cross-sectional study was to determine the main factors for predicting participation in Cervical Cytology Screening Programs in populations with high mortality due to cervical cancer. A total of 4,208 women aged between 15 and 49 years from Oaxaca State (rural area) and Mexico City (urban area) were randomly selected through a national household-sample frame. The authors found that knowledge of what the Pap smear test is used for strongly predisposes use of screening programs in Oaxaca State and Mexico City. Other predicting factors included high socioeconomic level, high education level, and access to social security. The authors confirmed low coverage of the screening programs as an important problem in Mexico.

Mauad, E.C. et al. Prevention of cervical cancer in a poor population in Brazil. Family Practice 19(2):189-192 (2002).
The authors of this study assessed and implemented strategies to increase women's participation in cervical cancer screening among a poor population in Brazil. Their activities included interviewing the program coordinator during a popular radio show, broadcasting announcements in the targeted neighborhoods by using a loudspeaker, and home visits by nurses to discuss the screening service and distribute printed materials. Their program offered flexible hours, including evenings and weekends when necessary. For women who were having difficulty making it to the nearest health center, screening services were offered to them in their home using a gynecological table that could easily be transported. Using this strategy, the study achieved coverage of 75 percent of the target population: 1,044 out of 1,384 women interviewed underwent Pap test screening. Of these, approximately 95 percent used the closest health center and approximately 5 percent were screened in their home using the portable table.

Marcus, A.C. and Crane, L.A. A review of cervical cancer screening intervention research: implications for public health programs and future research. Preventative Medicine 27:13-31 (1998).
This article provides an overview of the published literature regarding intervention strategies for promoting cervical cancer screening and reducing loss to follow-up among women with abnormal smears. The authors found that mass media campaigns have had varying effects. These campaigns may work best when multiple media are used, when they promote specific screening programs that eliminate or reduce barriers for women, or when they are used in combination with other strategies. The authors also note many positive examples of using outreach staff to promote cervical cancer screening. Mobile exam rooms also have been successful. Personalized letters to patient populations have been found to be effective, however mass or bulk mailings have not yielded impressive results. Several effective strategies were identified to reduce loss to follow-up, including multiple follow-up contacts, educational mail-outs, audiovisual programs, on-site educational presentations, transportation incentives, and economic vouchers.

Marrett, L.D. et al. A proposal for cervical screening information systems in developing countries. International Journal of Cancer 102:293-299 (2002).
In March 2001 a group of international experts came together with the Pan American Health Organization (PAHO) to discuss a framework and model for meeting the information systems needs of developing countries with respect to organized cervical cancer screening programs. This article summarizes the discussions and recommendations from the meeting. The proposed system would be modular in design to meet the needs and resources of developing countries, and would allow modules and data to be phased in as the system advances. Modules correspond to the need for "data capture," "database structure and management," and "required output." Issues that necessitate further dialogue include the need for a population register, the adequacy of the model, practicality of model, and legal issues concerning access to data.

Masood, S. A plea for worldwide volunteer cervical cancer education and awareness program. A proposal from the International Academy of Cytology Committee on Cancer Detection for Medically Underserved Women. Journal of Clinical Cytology and Cytopathology 43(4):539-543 (July-August 1999).
This editorial provides a brief review of the problem of cervical cancer and discusses the reasons why women still die from cervical cancer. The author suggests that lack of effective screening programs, especially for medically underserved women, and the continued dilemmas surrounding the practice of the cervical cytology screening test (that is, the Pap test) are the two main reasons for the medical community's failure to eradicate cervical cancer. Recommendations and strategies for overcoming these problems also are discussed. The author recommends that effective screening programs must integrate education and accessibility to health care services for all women regardless of age, race, ethnic background, and socioeconomic status. It is essential to reach women, educate them, and screening tests and responsive health care facilities. Integration of educational programs, Pap testing, and other diagnostic methods such as colposcopy in a mobile clinic is one innovative way of persuading women to utilize cancer prevention programs.

PATH (Program for Appropriate Technology in Health). Assessing Health Need/ Community Demand for Cervical Cancer Control: Results From a Study in Kenya. Reproductive Health Reports 1 (December 1996).
This report summarizes the purposes of a tool to assess the health need and community demand for cervical cancer services and results generated by use of the tool in two Kenyan sites. It also includes a complete reproduction of the tool, including questionnaires used in interviewing health care providers and prospective cervical cancer service clients about cervical and cancer and other related health services.�

Strickland, C.J. et al. Walking the journey of womanhood: Yakima Indian women and Papanicolaou (Pap) test screening. Public Health Nursing 13(2):141-150 (April 1996).
The goal of this study was to examine the understanding of Pap testing among Yakima Indian women of eastern Washington to support the community in the design of effective cervical cancer screening interventions. Using the Grounded Theory research methodology, the authors analyzed data collected from 15 interviews, focus groups, and participant observation. A major theme from the finding was "walking the journey of womanhood," which included four phases: starting the journey, blooming, heading the household, and becoming an elder. The authors confirmed previous findings that the issues of structure of care, provider-patient communications, and community education for the women must be addressed if Pap test-screening interventions for the Yakima women are to be effective. Education needs to target women heading the households and elders as they have a great influence on the younger women. Messages need to be wellness and community oriented. The authors emphasized the use of traditional methods of education, such as storytelling, talking circles, and role modeling.

Tatum, C., et al. Development and implementation of outreach strategies for breast and cervical cancer prevention among African American women. Journal of Cancer Education 12(1):43-50 (1997).
This study was designed to test the effectiveness of clinical and community outreach to improve screening rates among low-income, minority women in the United States, particularly women living in subsidized housing communities, age 40 and over. The project used five strategies to reach and influence the target population: (1) education on women's issues that included cervical and breast cancer prevention; (2) media campaigns; (3) inclusion of religious ideals and beliefs in educational classes and community outreach; (4) the use of information centers to distribute materials; and (5) a community-wide cancer awareness event. Preliminary findings indicated that maintaining uninterrupted access to the target population was critical to successful community efforts. In addition, the authors found that developing good rapport with community leaders was vital. Convenient scheduling, small incentives, and refreshments were strongly related to the degree of women's participation in the meetings. Successful education materials were those packaged in simple, logical terms, and classes emphasized participation over didactic presentations.

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Key resource documents

Miller, A.B. Cervical Cancer Screening Programmes: Managerial Guidelines. Geneva: World Health Organization (1992).
These guidelines outline management issues that must be considered when setting up a cytology screening program. After reviewing the natural history of cervical cancer, the guidelines detail strategies for: deciding whether to initiate cervical cancer screening; health service sectors through which screening can be offered; issues related to age of initiation and frequency of screening, health education needs; monitoring and evaluation needs; and other areas. The guidelines then provide specific strategies for providing cervical screening in primary health care settings and outline issues surrounding information systems for cervical screening, including the goals, characteristics, and data requirements of information systems. Lastly, the guidelines describe an approach to reducing cervical cancer mortality in countries where cytological screening cannot be provided. This approach, called downstaging, focuses on detecting early cancer when it is still treatable.

PAHO (Pan American Health Organization). Cancer of the uterine cervix. Bulletin of the Pan American Health Organization (special issue) 30(4) (December 1996). (Available in English and Spanish.)
This special issue of the PAHO Bulletin includes 11 reviews and research articles on cervical cancer in the Latin American and Caribbean region. The articles include information on the epidemiology of cervical cancer in the region, the effectiveness of Pap testing in several countries, and women's knowledge and concerns about Pap testing in Chile and Mexico. Short communications on specific program activities and reports from the field also are included, as well as a list of recommended readings.

PAHO (Organización Panamericana de la Salud). Manual de normas y procedimientos para el control del cancer de cuello uterino. Organización Panamericana de la Salud, Serie PALTEX Para Ejecutores de Programas de Salud, No. 6, Washington, DC (1990).
This Spanish-language PAHO publication reviews key managerial and technical aspects regarding cervical cancer control, with an emphasis on norms and procedures appropriate for the Latin American and Caribbean setting. The document includes sections that describe basic considerations for cervical cancer control, guidelines for cytological screening, diagnostic and treatment procedures, management of an effective program, and program monitoring and evaluation. The publication also includes several useful appendices that illustrate specific equipment and supply needs, evaluation indicators for cervical cancer control programs, and clinic and cytology registry forms.

 PATH. Planning Appropriate Cervical Cancer Prevention Programs. 2nd Edition Seattle: PATH (2001). Available online at PATH/PAHO edition available in Spanish (
This revised edition of Planning Appropriate Cervical Cancer Prevention Programs, 2nd Edition, is designed for program managers, policy makers, and advocates working to launch or strengthen cervical cancer prevention efforts in their communities. The guide provides a global overview of the magnitude of the problem and outlines key recommendations for program managers and policy makers to consider as they design cervical cancer control programs. The guide summarizes recent research, profiles program experiences, and presents analyses related to cervical cancer control, with a specific focus on program and policy implications and emphazing considerations for planning programs in low-resource settings.

World Health Organization (WHO). Cytological screening in the control of cervical cancer: technical guidelines. Geneva: WHO (1988).
These guidelines were designed to be used in conjunction with the WHO managerial guidelines abstracted above (Miller 1992). After a general introduction to the problem of cervical cancer and the role of cervical cytology in cervical cancer control, the guidelines provided detailed information on collection of cervical smears; cytology laboratory processes; diagnostic, treatment, and follow-up procedures; monitoring and evaluation issues; and personnel, equipment, and supply needs. One section of the guidelines also outlines common faults of screening programs and suggested solutions.

WHO. Cancer pain relief and palliative care: report of a WHO expert committee. Technical Report Series 804. Geneva: WHO. (1990).
This report summarizes the findings of a meeting of the WHO Expert Committee on Cancer Pain Relief and Active Supportive Care. The report reviews the principles of palliative care, including obstacles to implementing effective palliative care. It defines the type of pain associated with cancer, as well as other symptoms associated with advanced cancer, and describes the drugs used to treat cancer pain. The report emphasizes that palliative care must encompass the psychosocial and spiritual needs of cancer patients and discusses ethical issues that providers may need to consider when working with terminally ill people. Lastly, the report lists key program issues that must be considered before implementing palliative care (including education and training needs) and includes recommendations to WHO and WHO member-states on key strategies for making palliative care accessible to those who need it.

World Health Organization (WHO). Cancer Pain Relief. 2nd ed. (with a guide to opioid availability). Geneva: WHO (1996)
This document updates the 1990 WHO report summarized above. In particular, opioid availability is addressed, including strategies for overcoming barriers to obtaining a regular supply of opioids.

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