Our Publications

Recommendations for cervical cancer prevention in sub-saharan Africa


Denny LA, Sankaranarayanan R, De Vuyst H, Kim JJ, Adefuye PO, Alemany L, Adewole IF, Awolude OA, Parham G, de Sanjosé S, Bosch FX

Vaccine. 2013 Dec 29;31 Suppl 5:F73-4

PMID: 24331750

The burden of human papillomavirus infections and related diseases in sub-saharan Africa


De Vuyst H, Alemany L, Lacey C, Chibwesha CJ, Sahasrabuddhe V, Banura C, Denny L, Parham GP.

Vaccine. 2013 Dec 29;31 Suppl 5:F32-46

PMID: 24331746


Despite the scarcity of high quality cancer registries and lack of reliable mortality data, it is clear that human papillomavirus (HPV)-associated diseases, particularly cervical cancer, are major causes of morbidity and mortality in sub-Saharan Africa (SSA). Cervical cancer incidence rates in SSA are the highest in the world and the disease is the most common cause of cancer death among women in the region. The high incidence of cervical cancer is a consequence of the inability of most countries to either initiate or sustain cervical cancer prevention services. In addition, it appears that the prevalence of HPV in women with normal cytology is higher than in more developed areas of the world, at an average of 24%. There is, however, significant regional variation in SSA, with the highest incidence of HPV infection and cervical cancer found in Eastern and Western Africa. It is expected that, due to aging and growth of the population, but also to lack of access to appropriate prevention services and the concomitant human immunodeficiency virus (HIV)/acquired immunodeficiency syndrome (AIDS) epidemic, cervical cancer incidence and mortality rates in SSA will rise over the next 20 years. HPV16 and 18 are the most common genotypes in cervical cancer in SSA, although other carcinogenic HPV types, such as HPV45 and 35, are also relatively more frequent compared with other world regions. Data on other HPV-related anogenital cancers including those of the vulva, vagina, anus, and penis, are limited. Genital warts are common and associated with HPV types 6 and 11. HIV infection increases incidence and prevalence of all HPV-associated diseases. Sociocultural determinants of HPV-related disease, as well as the impact of forces that result in social destabilization, demand further study. Strategies to reduce the excessive burden of HPV-related diseases in SSA include age-appropriate prophylactic HPV vaccination, cervical cancer prevention services for women of the reproductive ages, and control of HIV/AIDS. This article forms part of a regional report entitled “Comprehensive Control of HPV Infections and Related Diseases in the Sub-Saharan Africa Region” Vaccine Volume 31, Supplement 5, 2013. Updates of the progress in the field are presented in a separate monograph entitled “Comprehensive Control of HPV Infections and Related Diseases” Vaccine Volume 30, Supplement 5, 2012.

Utilization of cervical cancer screening services and trends in screening positivity rates in a ‘screen-and-treat’ program integrated with HIV/AIDS care in Zambia


Mwanahamuntu MH, Sahasrabuddhe VV, Blevins M, Kapambwe S, Shepherd BE, Chibwesha C, Pfaendler KS, Mkumba G, Vwalika B, Hicks ML, Vermund SH,Stringer JS, Parham GP.

PLoS One. 2013 Sep 18;8(9):e74607

PMID: 24058599



In the absence of stand-alone infrastructures for delivering cervical cancer screening services, efforts are underway in sub-Saharan Africa to dovetail screening with ongoing vertical health initiatives like HIV/AIDS care programs. Yet, evidence demonstrating the utilization of cervical cancer prevention services in such integrated programs by women of the general population is lacking.


We analyzed program operations data from the Cervical Cancer Prevention Program in Zambia (CCPPZ), the largest public sector programs of its kind in sub-Saharan Africa. We evaluated patterns of utilization of screening services by HIV serostatus, examined contemporaneous trends in screening outcomes, and used multivariable modeling to identify factors associated with screening test positivity.


Between January 2006 and April 2011, CCPPZ services were utilized by 56,247 women who underwent cervical cancer screening with visual inspection with acetic acid (VIA), aided by digital cervicography. The proportion of women accessing these services who were HIV-seropositive declined from 54% to 23% between 2006-2010, which coincided with increasing proportions of HIV-seronegative women (from 22% to 38%) and women whose HIV serostatus was unknown (from 24% to 39%) (all p-for trend<0.001). The rates of VIA screening positivity declined from 47% to 17% during the same period (p-for trend <0.001), and this decline was consistent across all HIV serostatus categories. After adjusting for demographic and sexual/reproductive factors, HIV-seropositive women were more than twice as likely (Odds ratio 2.62, 95% CI 2.49, 2.76) to screen VIA-positive than HIV-seronegative women.


This is the first ‘real world’ demonstration in a public sector implementation program in a sub-Saharan African setting that with successful program scale-up efforts, nurse-led cervical cancer screening programs targeting women with HIV can expand and serve all women, regardless of HIV serostatus. Screening program performance can improve with adequate emphasis on training, quality control, and telemedicine-support for nurse-providers in clinical decision making.

World Health Organization Guidelines: Use of cryotherapy for cervical intraepithelial neoplasia


Santesso N, Schünemann H, Blumenthal P, De Vuyst H, Gage J, Garcia F, Jeronimo J, Lu R, Luciani S, Quek SC, Awad T, Broutet N; World Health Organization Steering Committee for Recommendations on Use of Cryotherapy for Cervical Cancer Prevention (of which Dr. Groesbeck Parham is a member).

Int J Gynaecol Obstet. 2012 Aug;118(2):97-102

PMID: 22727415



In 2008, cervical cancer was responsible for 275000 deaths, of which approximately 88% occurred in low- and middle-income countries. In 2009, the World Health Organization (WHO) committed to updating recommendations for use of cryotherapy for cervical intraepithelial neoplasia (CIN).

Methods and Results

We followed the WHO Handbook for Guidelines Development to develop present guidelines. An expert panel was established, which included clinicians, researchers, program directors, and methodologists. An independent group conducted systematic reviews and produced evidence summaries following the GRADE approach. GRADE evidence profiles were created for 16 key questions about the effects of cryotherapy in the presence of histologically confirmed CIN compared with no treatment and with loop electrosurgical excision procedure, as well as the use of different cryotherapy techniques. We identified a small number of randomized controlled trials or independently controlled observational studies. Surrogate outcomes were reported when evidence about outcomes critical to decision making were not available. The panel made 14 recommendations and documented factors that determined the strength and direction of the recommendations in decision tables.


The present document summarizes new evidence-based WHO recommendations about the use of cryotherapy in women with histologically confirmed CIN for low-, middle-, and high-income countries.

Motivations and experiences of women who accessed “see-and-treat” cervical cancer prevention services in Zambia


Heather L. White, Chishimba Mulambia, Moses Sinkala, Mulindi H. Mwanahamuntu, Groesbeck P. Parham, Sharon Kapambwe, Linda Moneyham, Mirjam C. Kempf, Eric Chamot

J Psychosom Obstet Gynaecol; 2012; 33(2): 91-8

PMID: 22369192



In Zambia, a country with a generalized HIV epidemic, age-adjusted cervical cancer incidence is among the highest worldwide. In 2006, the University of Alabama at Birmingham-Center for Infectious Disease Research in Zambia and the Zambian Ministry of Health launched a visual inspection with acetic acid (VIA) -based “see and treat” cervical cancer prevention program in Lusaka. All services were integrated within existing government-operated primary health care facilities.


Study aims were to (i) identify women’s motivations for cervical screening, (ii) document women’s experiences with screening and (iii) describe the potentially reciprocal influences between women undergoing cervical screening and their social networks.

Design and Methods

Focus group discussions (FGD) and in-depth interviews (IDI) were conducted with women who accepted screening and with care providers. Low-level content analysis was performed to identify themes evoked by participants. Between September 2009 and July 2010, 60 women and 21 care providers participated in 8 FGD and 10 IDI.


Women presented for screening with varying needs and expectations. A majority discussed their screening decisions and experiences with members of their social networks. Key reinforcing factors and obstacles to VIA screening were identified.


Interventions are needed to gain support for the screening process from influential family members and peers.

‘Worse than HIV’ or ‘not as serious as other diseases’? Conceptualization of cervical cancer among newly screened women in Zambia


Heather L. White, Chishimba Mulambia, Moses Sinkala, Mulindi H. Mwanahamuntu, Groesbeck P. Parham, Linda Moneyham, Diane M. Grimley, Eric Chamot

Soc Sci Med; 2012; 74(10): 1486-93

PMCID: PMC3328622


Invasive cervical cancer is the second most common cancer among women worldwide, with approximately 85% of the disease burden occurring in developing countries. To date, there have been few systematic efforts to document African women’s conceptualization of cervical cancer after participation in a visual inspection with acetic acid (VIA)-based “see and treat” cervical cancer prevention program. In this study, conducted between September, 2009-July, 2010, focus groups and in-depth interviews were conducted with 60 women who had recently undergone cervical cancer screening at a government-operated primary health care clinic in Lusaka, Zambia. Interviewers elicited participants’ causal representations of cervical cancer, associated physical signs and symptoms, perceived physical and psychological effects, and social norms regarding the disease. The lay model of illness causation portrayed by participants after recent exposure to program promotion messages departed in several ways from causal models described in other parts of the world. However, causal conceptualizations included both lay and biomedical elements, suggesting a possible shift from a purely traditional causal model to one that incorporates both traditional concepts and recently promoted biomedical concepts. Most, but not all, women still equated cervical cancer with death, and perceived it to be a highly stigmatized disease in Zambia because of its anatomic location, dire natural course, connections to socially-condemned behaviors, and association with HIV/AIDS. No substantive differences of disease conceptualization existed according to HIV serostatus, though HIV positive women acknowledged that their immune status makes them more aware of their health and more likely to seek medical attention. Further attention should be dedicated to the processes by which women incorporate new knowledge into their representations of cervical cancer.

Advancing Cervical Cancer Prevention Initiatives in Resource-Constrained Settings: Insights from the Cervical Cancer Prevention Program in Zambia


Mulindi H. Mwanahamuntu, Vikrant V. Sahasrabuddhe, Sharon Kapambwe, Krista S. Pfaendler, Carla Chibwesha, Gracilia Mkumba, Victor Mudenda, Michael L. Hicks, Sten H. Vermund, Jeffrey S. A. Stringer, Groesbeck P. Parham

PLoS Med; 2011; 8(5): e1001032

PMCID: PMC3096609


Groesbeck Parham and colleagues describe their Cervical Cancer Prevention Program in Zambia, which has provided services to over 58,000 women over the past five years, and share lessons learned from the program’s implementation and integration with existing HIV/AIDS programs.

Summary Points:

  • Invasive cervical cancer is a leading cause of cancer-related death and morbidity among women in the developing world.
  • Screening coverage rates are very low in developing countries despite there being proven, simple, “screen and treat” approaches for cervical cancer prevention.
  • In 2006 we initiated a partnership with the public health system in Zambia and created the Cervical Cancer Prevention Program in Zambia (CCPPZ), targeting the highest risk HIV-infected women, and have provided services to over 58,000 women (regardless of HIV status) over the past 5 years.
  • We have demonstrated a strategy for using the availability, momentum, and capacity-building efforts of vertical HIV/AIDS care and treatment programs to implement a setting-appropriate protocol for cervical cancer prevention within public health infrastructures.
  • We report our lessons learned to help other cervical cancer prevention initiatives succeed in the developing world and to avoid additional burdens on health systems.

Implementation of cervical cancer prevention services for HIV-infected women in Zambia: measuring program effectiveness


Groesbeck P Parham, Mulindi H Mwanahamuntu, Vikrant V Sahasrabuddhe, Andrew O Westfall, Kristin E King, Carla Chibwesha, Krista S Pfaendler, Gracilia Mkumba, Victor Mudenda, Sharon Kapambwe, Sten H Vermund, Michael L Hicks, Jeffrey SA Stringer, and Benjamin H Chi

HIV Ther; 2010; 4(6): 713–722

10.2217/HIV.10.52 © 2010 Future Medicine Ltd



Cervical cancer kills more women in low-income nations than any other malignancy. A variety of research and demonstration efforts have proven the efficacy and effectiveness of low-cost cervical cancer prevention methods but none in routine program implementation settings of the developing world, particularly in HIV-infected women.


In our public sector cervical cancer prevention program in Zambia, nurses conduct screening using visual inspection with acetic acid aided by digital cervicography. Women with visible lesions are offered same-visit cryotherapy or referred for histologic evaluation and clinical management. We analyzed clinical outcomes and modeled program effectiveness among HIV-infected women by estimating the total number of cervical cancer deaths prevented through screening and treatment.


Between 2006 and 2008, 6572 HIV-infected women were screened, 53.6% (3523) had visible lesions, 58.5% (2062) were eligible for cryotherapy and 41.5% (1461) were referred for histologic evaluation. A total of 75% (1095 out of 1462) of patients who were referred for evaluation complied. Pathology results from 65% (715 out of 1095) of women revealed benign abnormalities in 21% (151), cervical intraepithelial neoplasia (CIN) I in 30% (214), CIN 2/3 in 33% (235) and invasive cervical cancer in 16.1% (115, of which 69% were early stage). Using a conditional probability model, we estimated that our program prevented 142 cervical cancer deaths (high/low range: 238–96) among the 6572 HIV-infected women screened, or one cervical cancer death prevented per 46 (corresponding range: 28–68) HIV-infected women screened.


Our prevention efforts using setting-appropriate human resources and technology have reduced morbidity and mortality from cervical cancer among HIV-infected women in Zambia. Financial support for implementing cervical cancer prevention programs integrated within HIV/AIDS care programs is warranted. Our prevention model can serve as the implementation platform for future low-cost HPV-based screening methods, and our results may provide the basis for comparison of programmatic effectiveness of future prevention efforts.

eC3 – A Modern Telecommunications Matrix for Cervical Cancer Prevention in Zambia


Groesbeck P. Parman, Mulindi H. Mwanahamuntu, Krista S. Pfaendler, Vikrant V. Sahasrabuddhe, Daniel Myung, Gracilia Mkumba, Sharon Kapambwe, Bianca Mwanza, Carla Chibwesha, Michael L. Hicks, Jeffrey S.A. Stringer

J Low Genit Tract Dis; 2010; 14(3): 167-73

PMID: 20592550



Low physician density, undercapacitated laboratory infrastructures, and limited resources are major limitations to the development and implementation of widely accessible cervical cancer prevention programs in sub-Saharan Africa.

Materials and Methods

We developed a system operated by nonphysician health providers that used widely available and affordable communication technology to create locally adaptable and sustainable public sector cervical cancer prevention program in Zambia, one of the world’s poorest countries.


Nurses were trained to perform visual inspection with acetic acid aided by digital cervicography using predefined criteria. Electronic digital images (cervigrams) were reviewed with patients, and distance consultation was sought as necessary. Same-visit cryotherapy or referral for further evaluation by a gynecologist was offered. The Zambian system of “electronic cervical cancer control” bypasses many of the historic barriers to the delivery of preventive health care to women in low-resource environments while facilitating monitoring, evaluation, and continued education of primary health care providers, patient education, and medical records documentation.


The electronic cervical cancer control system uses appropriate technology to bridge the gap between screening and diagnosis, thereby facilitating the conduct of “screen-and-treat” programs. The inherent flexibility of the system lends itself to the integration with future infrastructures using rapid molecular human papillomavirus-based screening approaches and wireless telemedicine communications.

Myths and misconceptions about cervical cancer among Zambian women: Rapid assessment by peer educators


Susan Chirwa, Mulindi Mwanahamuntu, Sharon Kapambwe, Gracilia Mkumba, Jeff Stringer, Vikrant Sahasrabuddhe, Krista Pfaendler and Groesbeck Parham

Glob Health Promot; 2010; 17(2 Suppl): 47-50

PMID: 20595342



To make a rapid assessment of the common myths and misconceptions surrounding the causes of cervical cancer and lack of screening among unscreened low-income Zambian women.


We initiated a door-to-door community-based initiative, led by peer educators, to inform unscreened women about the existence of a new see-and-treat cervical cancer prevention program. During home visits peer educators posed the following two questions to women: 1. What do you think causes cervical cancer? 2. Why haven’t you been screened for cervical cancer? The most frequent types of responses gathered in this exercise were analyzed thematically.


Peer educators contacted over 1100 unscreened women over a period of two months. Their median age was 33 years, a large majority (58%) were not educated beyond primary school, over two-thirds (71%) did not have monthly incomes over 500,000 Zambian Kwacha (US$100) per month, and just over half (51%) were married and cohabiting with their spouses. Approximately 75% of the women engaged in discussions had heard of cervical cancer and had heard of the new cervical cancer prevention program in the local clinic. The responses of unscreened low-income Zambian women to questions posed by peer educators in urban Lusaka reflect the variety of prevalent ‘folk’ myths and misconceptions surrounding cervical cancer and its prevention methods.


The information in our rapid assessment can serve as a basis for developing future educational and intervention campaigns for improving uptake of cervical cancer prevention services in Zambia. It also speaks to the necessity of ensuring that programs addressing women’s reproductive health take into account societal inputs at the time they are being developed and implemented. Taking a community-based participatory approach to program development and implementation will help ensure sustainability and impact.

Implementation of ‘see-and-treat’ cervical cancer prevention services linked to HIV care in Zambia


Mulindi H. Mwanahamuntu, Vikrant V. Sahasrabuddhed, Krista S. Pfaendler, Victor Mudenda, Michael L. Hicks, Sten H. Vermund, Jeffrey S.A. Stringer, and Groesbeck P. Parham

AIDS; 2009; 23(6): N1-5

PMCID: PMC2747794

No Abstract

Building a Cervical Cancer Prevention Program into the HIV Care and Treatment Infrastructure in Zambia


Groesbeck P. Parham, Mulindi Mwanahammuntu, Krista Pfaendler, Gricelia Mkumba, Vikrant V. Sahasrabuddhe, Michael L. Hicks, Edith Welty, and Jeffrey S.A. Stringer

In: Marlink RG, Teitelman ST, eds. From the Ground Up: Building Comprehensive HIV/AIDS Care Programs in Resource-Limited Settings. Washington, DC: Elizabeth Glaser Pediatric AIDS Foundation; 2009. http://ftguonline.org

No Abstract

Management of cryotherapy-ineligible women in a “screen-and-treat” cervical cancer prevention program targeting HIV-infected women in Zambia: Lessons from the field


Krista S. Pfaendler, Mulindi H. Mwanahamuntu, Vikrant V. Sahasrabuddhe, Victor Mudenda, Jeffrey S.A. Stringer, and Groesbeck P. Parham

Gynecol Oncol; 2008; 110(3): 402-7

PMCID: PMC2745977



We demonstrate the feasibility of implementing a referral and management system for cryotherapy-ineligible women in a “screen-and-treat” cervical cancer prevention program targeting HIV-infected women in Zambia


We established criteria for patient referral, developed a training program for loop electrosurgical excision procedure (LEEP) providers, and adapted LEEP to a resource-constrained setting.


We successfully trained 15 nurses to perform visual inspection with acetic acid (VIA) followed by immediate cryotherapy. Women with positive tests but ineligible for cryotherapy were referred for further evaluation. We trained four Zambian physicians to evaluate referrals, perform punch biopsy, LEEP, and manage intra-operative and post-operative complications. From January 2006 through October 2007, a total of 8823 women (41.5% HIV seropositive) were evaluated by nurses in outlying prevention clinics; of these, 1477 (16.7%) were referred for physician evaluation based on established criteria. Of the 875 (59.2% of 1147 referred) that presented for evaluation, 748 (8.4% of total screened) underwent histologic evaluation in the form of punch biopsy or LEEP. Complications associated with LEEP included anesthesia reaction (n=2) which spontaneously resolved, intra-operative (n=12) and post-operative (n=2) bleeding managed by local measures, and post-operative infection (n=12) managed with antibiotics.


With adaptations for a resource-constrained environment, we have demonstrated that performing LEEP is feasible and safe, with low rates of complications that can be managed locally. It is important to establish referral and management systems using LEEP-based excisional evaluation for women with cryotherapy-ineligible lesions in VIA-based “screen-and-treat” protocols nested within HIV-care programs in resource-constrained settings.

Prevalence and predictors of squamous intraepithelial lesions of the cervix in HIV-infected women in Lusaka, Zambia


Groesbeck P. Parham, Vikrant V. Sahasrabuddhe, Mulindi H. Mwanahamuntu, Bryan E. Shepherd, Michael L. Hicks, Elizabeth M. Stringer, and Sten H. Vermund

Gynecol Oncol; 2006; 103(3): 1017–1022

PMCID: PMC2748907



HIV-infected women living in resource-constrained nations like Zambia are now accessing antiretroviral therapy and thus may live long enough for HPV-induced cervical cancer to manifest and progress. We evaluated the prevalence and predictors of cervical squamous intraepithelial lesions (SIL) among HIV-infected women in Zambia.


We screened 150 consecutive, non-pregnant HIV-infected women accessing HIV/AIDS care services in Lusaka, Zambia. We collected cervical specimens for cytological analysis by liquid-based monolayer cytology (ThinPrep Pap Test®) and HPV typing using the Roche Linear Array® PCR assay.


The median age of study participants was 36 years (range 23-49 years) and their median CD4+ count was 165/μL (range 7-942). The prevalence of SIL on cytology was 76% (114/150), of which 23.3% (35/150) women had low-grade SIL, 32.6% (49/150) had high-grade SIL, and 20% (30/150) had lesions suspicious for squamous cell carcinoma (SCC). High-risk HPV types were present in 85.3% (128/150) women. On univariate analyses, age of the participant, CD4+ cell count, and presence of any high-risk HPV type were significantly associated with the presence of severely abnormal cytological lesions (i.e., high-grade SIL and lesions suspicious for SCC). Multivariable logistic regression modeling suggested the presence of any high-risk HPV type as an independent predictor of severely abnormal cytology (adjusted OR: 12.4, 95% CI 2.62-58.1, p=0.02).


The high prevalence of abnormal squamous cytology in our study is one of the highest reported in any population worldwide. Screening of HIV-infected women in resource-constrained settings like Zambia should be implemented to prevent development of HPV-induced SCC.