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

Date Published: May 17, 2011

Publisher: Public Library of Science

Author(s): 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

Abstract: 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.

Partial Text: Invasive cervical cancer (ICC) is a leading cause of cancer-related mortality and
morbidity among women in the developing world [1]. Numerous demonstration projects
have proven the efficacy of simplified “screen and treat” approaches
(such as visual inspection with acetic acid [VIA] and immediate
cryotherapy) for cervical cancer prevention in low income countries [2]–[5]. Yet, rarely have they
been adopted and scaled up by governments in such settings, and as a result rates of
screening coverage in the developing world remain low [6]. In Zambia, which has the
world’s second highest annual cervical cancer incidence and mortality rates
[1], we
initiated a unique partnership for providing cervical cancer prevention services
within the public sector health care system. The Cervical Cancer Prevention Program
in Zambia (CCPPZ), launched in 2006 and initially targeting the highest risk
HIV-infected women, has cumulatively provided services to over 58,000 women
(regardless of HIV status) over the past 5 years [7],[8] (Figure 1). Our previous reports have described
the disease burden [9],[10],[11], program implementation experience [7], telecommunications matrix
utilized for distance consultation and quality assurance [8], outcomes of a referral system
for women ineligible for treatment with cryotherapy [12], common myths and
misconceptions surrounding cervical cancer [13], and an analysis of outcomes
and effectiveness of screening among women with HIV [11]. In this article, we discuss
the unique attributes of the program’s successful implementation, including its
adoptability to the conditions of a resource-constrained environment, integration
with infrastructure of an HIV/AIDS program, use of innovative quality assurance
measures, and the potential for sustainability and collateral impact (Figure 2). The global “call
to action” for cancer control in low income countries is emerging [14], yet funding
for stand-alone cancer prevention initiatives is virtually non-existent. Our
experience may provide insights and guidance for advancing cancer prevention
initiatives in resource-constrained settings.

CCPPZ is a unique partnership between Zambian and United States partner institutions
from the academic (University Teaching Hospital [UTH] in Lusaka and
University of Alabama at Birmingham [UAB]), research (Centre for
Infectious Disease Research in Zambia [CIDRZ]), and governmental (Zambian
Ministry of Health) sectors. Prevention efforts have been rapidly scaled up, taking
advantage of a historical circumstance of increased attention and funding in the
HIV/AIDS sector through the US President’s Emergency Plan for AIDS Relief
(PEPFAR) program [15]. Trained nurses form the backbone of the program,
providing free personalized clinical screening examinations for all eligible women
who attend the clinic [7],[11]. VIA aided by a low-cost digital camera adaptation
(“digital cervicography”) is used to provide results immediately [11]. Decisions
about offering immediate cryotherapy (“screen-and-treat”) or referral
are made independently by nurses in most cases, or aided by telemedicine
consultations with local doctors [11]. VIA-negative women are advised to follow-up after 1
year, VIA-positive and cryotherapy-eligible women are treated by the nurses, and
those needing referral are advised to attend the Gynecologic Cancer Prevention Unit
in the UTH [12]. Administrative support is provided by CIDRZ, while program
operations are integrated with the Zambian Ministry of Health’s public sector
health care infrastructure [7]. From 2006 to March 2011, over 58,000 women, regardless of
HIV status, have been screened in this program. Of the initial 21,010 women who were
provided services in the program (31% of whom had HIV), 38% were VIA
positive, of whom 62% were eligible for cryotherapy and 38% were
referred for histologic evaluation. Forty-nine percent of patients referred for
histologic evaluation complied, and pathology results revealed benign abnormalities
in 8%, CIN1 in 28%, CIN2/3 in 26%, and ICC in 19% (of
which 55% were early stage).

The dearth of adequately trained cytotechnologists and pathologists, and the
requirement for multiple patient visits, preclude successful utilization of cervical
cytology (“Pap smears”) in most of the developing world [5].
Testing for cervical human papillomavirus (HPV) is a highly accurate screening
approach, [16],[17] but the high cost of current commercially available HPV
testing technology makes routine implementation in low income countries impractical,
if not impossible [18]. VIA linked to cryotherapy has unique strengths (it can
be done by mid-level health care providers, and has immediate results that allow
linking screening and treatment in the same visit), but also antecedent weaknesses
(higher potential for false-positive results, and limitations in ensuring quality
assurance [5]). Nonetheless, VIA remains the only available option for a
setting like Zambia. We enhanced its application through the use of digital
photography (cervicography) as a routine adjunct to ensure quality as well as help
with patient education and electronic record keeping, and rapid distance
consultation with the limited number of available physician experts, when necessary
[8]. Our model
facilitated program scale-up, despite limited resources. In fact, our experience
suggests that while the accuracy of a screening test is an important attribute, it
is only a small part of the equation for mitigating cervical cancer. Ultimately, the
success of cervical cancer prevention interventions is largely determined by how
screening and treatment activities are integrated within the routine health care
system to ensure maximal impact, an enduring goal of our program.

The increasing expansion, over the past decade, of bilateral (e.g., PEPFAR) and
multilateral (e.g., Global Fund) donor funding for HIV/AIDS programs has transformed
health care delivery in resource limited settings, particularly in sub-Saharan
Africa [19]. With
support from PEPFAR and private donations, CCPPZ’s cervical cancer prevention
clinics are co-located within public health clinics offering HIV/AIDS care and
treatment. Manifold advantages of this strategy include resource and infrastructure
sharing, availability of a wider range of women’s health services for
HIV-infected/at-risk women, and opportunities for referral between the clinic
systems and maximization of participation in both programs. Yet, the stigma
associated with HIV/AIDS continues to be a challenge in Zambia, which drove our
decision to keep service provisions and the identities of the cervical cancer and
HIV/AIDS care programs distinct, albeit in the same premises. Women attending
cervical cancer screening clinics with unknown HIV status are offered HIV testing
within the confidential environment of the screening rooms. Indeed, cervical cancer
itself is stigmatized, and anxiety and fear often keep women from getting screened
[13]. In
response, the program is branded as a “Cervical Health” program, which
deemphasizes cancer while denoting a positive (“health”) connotation to
the effort.

One of the most enabling and transforming aspects of the program involves utilizing
information technology tools for enhancing the program’s operations and
enabling quality assurance. Telemedicine consultation through the “electronic
cervical cancer control” model [8] is a mobile health application
that has enhanced clinical care services and improved quality assurance of nurse-led
VIA. The use of community volunteers as patient-tracking officers, taking advantage
of the wide usage of cell phone–based communication among the patient
population, is now promoting adherence to the already minimized follow-up visit
requirements. The use of point-of-care online data entry (undertaken by nurses and
their community volunteer assistants), and a centralized Web-based patient clinical
and laboratory records management system are enhancing program monitoring and
outcomes evaluation.

The program is, by design, integrated with the operations of the public health system
run and operated by the Zambian Ministry of Health, a model that has helped its
transition from being a foreign-funded/led project to a locally/nationally
“owned” program. Program nurses are recruited from the public sector
health care system, with add-on financial incentives to facilitate retention. The
program also employs community-based volunteers to serve as “peer
educators” to facilitate community awareness, counteract misconceptions and
myths, and serve patient support functions [13]. All referral services are
located within UTH, the only state-run tertiary hospital in Zambia, which permits
medical and surgical services (including loop electrosurgical excision procedures
[LEEP], hysterectomy, radiation, and chemotherapy) at low-to-no cost to
patients. The need for coordination of various administrative, clinical, and
laboratory (referral-level) services are achieved through locally employed Zambian
nationals, with technical assistance from expatriate American clinicians and
administrators living within the country, in a “shared leadership” model
(Figure 3). The motto of the
program (“Every woman has the right to live a life free from cervical
cancer”) encapsulates the rights-based approach to women’s health,
designed to promote community-based acceptance of this program. The program’s
infrastructure has facilitated the development of a linked clinical,
epidemiological, and translational research platform supported by numerous
extramural research and training grants and contracts. Opportunities abound for
engaging Zambian and foreign clinical and research trainees. The program’s
successful expansion in the Lusaka area has leveraged political will for nationwide
expansion, as well as eventual roll out of HPV vaccination and HPV-based screening
[20] as the
logical next steps in its evolution (Figure 2). As with any expanding program, unique challenges may arise
with future geographic expansion, yet we believe that the lessons learnt during our
initial years as well as the improved awareness that the program has engendered,
will likely generate unique solutions.

For cancer prevention initiatives to succeed in the developing world, programs must
avoid placing additional burdens on health systems already stretched thin due to
competing priorities. We have demonstrated a strategy for using the availability,
momentum, and capacity-building efforts of vertical HIV/AIDS care and treatment
programs to implement other disease-specific initiatives such as cervical cancer
prevention [19]. By
integrating a setting-appropriate protocol for cervical cancer prevention into
public health infrastructures, and promoting shared leadership with government
ownership, our program has not just saved lives [11], but has also established a new
solution for routine prevention intervention in resource-constrained



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