Uterine Cervical Cancer Prevention in Eritrea: Development and Results of a Pilot Project

Background: Uterine cervical cancer (UCC) is the fourth most common cancer worldwide; almost 85%-90% of UCCs, and UCC-related deaths occur in low-income countries. No UCC prevention programs are currently running in Eritrea. Aims: This manuscript describes a stepwise initiative aiming to establish an UCC prevention project in Eritrea, which combines Pap-smear and colposcopy. Methods: In 2013, an Italian multidisciplinary team submitted a project to the Eritrean Ministry of Health with a view to establishing an Eritrean-Italian UCC prevention task force. The project’s starting point was an educational initiative to train local technicians on both Pap-smear assessments and colposcopy. Results: An intensive academic course organized by the University of Padova (Italy) under the patronage of the Eritrean Ministry of Health was successfully held in Asmara to train Eritrean technicians, nurses and midwifes to conduct Pap-smear assessments. Two subsequent pilot projects (2014-2016; 2016-2018) monitored the diagnostic competence of the Eritrean cyto-screeners. These pilot schemes resulted in an initial assessment of 2,014 Pap-smears, which provided information on the main operative issues involved in newly establishing a cancer prevention initiative in a sub-Saharan country. They also generated preliminary data on the prevalence of cancer and precancerous cervical lesions. The second pilot study is additionally providing further insight on the problems faced in expanding the prevention project to the Asmara population as a whole. Conclusions: Anti-HPV vaccination, the most effi cient primary UCC prevention strategy, entails basic requirements that are not always available in low-income countries. In terms of secondary UCC prevention, this Eritrean experience suggests that the low cost of “Pap testing” and the availability of local human resources could lower the incidence of UCC and related deaths in Eritrea. Procedures Uterine Cervical Cancer Prevention in Eritrea: Development and Results of a Pilot Project Massimo Rugge1*, F.A.C.G1, Michele Cosentino1, Kebreab Mehari WG2, Paola Bassan1, Elisabetta Marcato1, Zewdi Ghebremedhin Andemicael2, Simon Gebrehiwet2, Kibrom Hailu Ghebremicael3, Tesfamariam Mehari Halki3, Egle A Insacco4, Gianlibero Onnis1 and Daria Minucci4 1Department of Medicine (DIMED), Surgical Pathology & Cytopathology Unit, University of Padova; Padova, Italy 2Department of Gynecology & Obstetrics; Orotta National Referral Hospital, Asmara, Eritrea 3Department of Anatomic Pathology & Laboratory Medicine, Orotta National Referral Hospital, Asmara, Eritrea 4Department of Women’s and Child’s Health University of Padova Hospital, AOUP, Padova, Italy Received: 08 January, 2018 Accepted: 16 January, 2018 Published: 17 January, 2018 *Corresponding author: Massimo Rugge, Surgical Pathology & Cytopathology Unit, Department of Medicine (DIMED), University of Padova, Via Aristide Gabelli 61, 35121 Padova, Italy; Tel: (+39) 049 8218990; Fax: (+39) 049 8272277; E-mail:


Introduction
Of the 9 million people worldwide diagnosed with cancer in 2017, more than 60% live in Africa, Asia, or Central and South America. These regions also account for about 70% of the world's cancer-related deaths ( Figure 1). Uterine cervical cancer (UCC) is the fourth most common cancer worldwide, and the second cause of cancer-related death. Almost 90% of UCC and UCC-related deaths occur in low-income countries, mostly affecting young women in critical socio-economic conditions [1].
In high-income countries, joint efforts by public and private healthcare networks usually do the operational groundwork needed to run oncological screening programs successfully. In UCC secondary prevention, in particular, excellent results have been achieved by combining Pap smears with colposcopy [6]. Such favorable conditions are often unavailable in low-income countries, however. No established UCC prevention programs (be the primary or secondary) are currently running in Eritrea [7]. This manuscript describes an educational project that aimed to pave the way to locally-run screening programs for UCC secondary prevention in Eritrea [8].
The geopolitical landscape and early action undertaken in 2013-2017 -The geopolitical landscape Eritrea is a sub-Saharan country (land area: 101,000 km 2 ) with a population of fi ve million (51% female). The median age of the resident population is 18.9 years, with a fertility rate of 4.32. The Eritrean population density is 50 per km 2 , and about one in three Eritreans live in urban areas. At the time of writing (2017), the country's annual per capita gross domestic product (GDP) was almost 1000 USD.
No reliable epidemiological information is available on the incidence of UCC in Eritrea [7]. In sub-Saharan Africa, 34.8 per 100,000 women are diagnosed with UCC each year, and 22.5 per 100,000 die of this disease [9].
The project, teaching timetable, and available resources -The project In 2013, a team of Italian specialists (gynecologists, pathologists, and experienced cyto-screeners) submitted a project to the Eritrean Ministry of Health (Mrs. Amina Nurhussien) that proposed to establish a national UCC secondary prevention initiative ( Figure 2). The fi rst step in the project involved training local technicians to conduct Pap smear assessments. This step was considered crucial to the subsequent establishment of a screening-based secondary prevention program.
-Teaching program management and timetable (years

2013-2014)
Before starting the training activities at the Asmara Orotta Hospital, the gynecologist (KM) acting as the Eritrean promoter of the project spent 2 months in charge of the UCC screening activities at the Gynecology Unit at Padova University Hospital in Italy. During this period, he also attended a course on colposcopy organized by the Italian Society of Colposcopy and Cervical Pathology.
A structured academic course organized by the University of Padova was then held in Asmara. The course was structured and formally recognized by the University of Padova (Decree of the Rector of the University of Padova: July/22 sd /2013). The teaching team consisted of 7 Italian specialists (2 cytoscreeners, 3 gynecologists, and 2 pathologists). An Eritrean gynecologist (KM) appointed by the Eritrean Minister of Public Heath was in charge of local organizational matters.
Twelve Eritrean nurses, midwives, and laboratory technicians, selected from among the healthcare personnel at the Orotta National Referral Hospital in Asmara, attended the residential course, which was held at the Orotta National Referral Hospital. The course included: (a) formal lectures to provide a basic theoretical knowledge of the pathology of the female genital tract; and (b) microscopy tutorials to provide the basic diagnostic criteria to apply in Pap smear assessments.

-Formal lectures
The following topics were addressed in 8 days (70 hours) of intensive teaching activity: i) anatomy of the female genital tract; ii) physiopathology and basic pathology of the female genital tract, iii) diagnostic cytopathology/microbiology techniques; iv) histological-cytological correlations; and v) diagnostic cytopathology laboratory management.
-Diagnostic Laboratory of Pap smears assessment.
In all, 180 hours of training on real Pap smear slides were delivered as practical microscopy sessions. Informal group tuition with one-to-one discussion of cases at a multi-vision microscope was also included.
After completing these teaching activities, the students were shown a series of 75 pre-assessed Pap-smears representative of normal and pathological, neoplastic and non-neoplastic conditions (all obtained using conventional thick layer methods). They were also given a pre-set diagnostic frame

The second pilot project (Pilot-II: 2017-2018): real-life testing
To preserve the professional competence gained by the Eritrean technicians, and improve the operational link between the diagnostic and any necessary therapeutic steps, a Pilot-II project was developed and is still underway (Figure 2).
The aims of this Pilot-II initiative are: • to monitor the quality of the cytology samples and the laboratory's functional organization (including its technical performance); • to establish the colposcopy clinic;

SQUAMOUS CELLS ABNORMALITIES
• to test the procedures for enabling outpatients to access Pap testing; • to obtain more reliable information on the prevalence of the target disease in the outpatient population.
The goal of Pilot-II is thus to collect at least 5,000 Pap-

Conclusions
Before the extensive implementation of screening programs, the UCC-related mortality rates were much the same in highand low-income countries. This is no longer the case, however, now that the incidence and mortality rates for UCC in Europe and North America have been drastically lowered. It is generally acknowledged that we have to thank cervical cytology (Pap-smear) combined with colposcopy for the signifi cant improvements made in this setting [11,12].
The results emerging from this Eritrean experience suggest a high prevalence of UCC in the population of Asmara, although no dependable information has been obtained as yet on the UCC incidence in Eritrea as a whole. The only (albeit weak) information potentially comparable with other African experiences concerns the association between an older mean age of the women screened and an increasing severity of the cases of cytologically identifi ed cervical disease.
As for the educational effort, our initiative demonstrates that an intensive training program can produce effi cient cytoscreeners capable of covering all the diagnostic steps of a Pap smear procedure successfully [13].
Secondary prevention strategies offer the opportunity to lower the incidence of UCC in developing countries too, even though certain practical issues may hinder the broad implementation of screening programs [14]. In 2015, a USA task force asked to design cancer prevention strategies for developing countries identifi ed two major lines of intervention for preventing UCC: i) preventing HPV infection by making vaccines more readily available; and ii) implementing screening methods "more compatible than Pap smear" with the resources available in developing countries [15].
Vaccinating against HPV is currently the most effi cient strategy for eradicating the main causative agent behind UCC, but the cost of national vaccination campaigns seems to be hardly compatible with the resources available in some areas.
As concerns secondary prevention strategies, this Eritrean experience demonstrated -despite signifi cant weaknesses (related largely to shortcomings of the health system infrastructure) -that most of the obstacles are potentially manageable. On balance, the "cons" of "Pap testing" are largely counteracted by two signifi cant "pros", i.e. low cost and the availability of local human resources [16][17][18][19]. """""""""""""