CERVICAL cancer is a preventable and curable

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Cervical cancer: the sub-Saharan African perspective Rose I Anorlu Consultant and Senior Lecturer, Department of Obstetrics and Gynaecology, College of Medicine, University of Lagos, Lagos University Teaching Hospital, Lagos, Nigeria. E-mail: [email protected]

Abstract: Cervical cancer is the second most common cancer in women worldwide and the leading cause of cancer deaths in developing countries. While incidence and mortality rates of cervical cancer have fallen significantly in developed countries, 83% of all new cases that occur annually and 85% of all deaths from the disease occur in developing countries. Cervical cancer is the most common cancer among women in sub-Saharan Africa. The incidence is on the increase in some countries. Knowledge and awareness of this disease on the continent are very poor and mortality still very high. Facilities for the prevention and treatment of cervical cancer are still very inadequate in many countries in the region. Governments in sub-Saharan Africa must recognise cervical cancer as a major public health concern and allocate appropriate resources for its prevention and treatment, and for research. Indeed, cervical cancer in this region must be accorded the same priority as HIV, malaria, tuberculosis and childhood immunisations. ©2008 Reproductive Health Matters. All rights reserved. Keywords: cervical cancer and screening, health policies and programmes, sub-Saharan Africa


ERVICAL cancer is a preventable and curable disease, preventable by vaccination and screening and curable if identified at an early enough stage. It is gradually becoming a rare disease in many developed countries; this is not the case with many countries in subSaharan Africa. Cervical cancer is the most common cancer in women in sub-Saharan Africa and second to breast cancer in northern Africa. In sub-Saharan African, it accounts for 22.2% of all cancers in women and it is also the most common cause of cancer death among women.1 About 60–75% of women in subSaharan Africa who develop cervical cancer live in rural areas,2 and mortality is very high.1 Many of the women who develop cervical cancer are untreated, mostly due to lack of access (financial and geographical) to health care. Women in sub-Saharan Africa lose more years to cervical cancer than to any other type of cancer. Unfortunately, it affects them at a time of life when they are critical to the social and economic stability of their families. The objective of this review was to critically appraise the incidence, mortality, knowledge,

prevention and treatment of cervical cancer in sub-Saharan Africa. A computerised literature search was conducted for published articles. Mesh phrases used for the search were cervical cancer, cervical cancer Africa, cervical cancer screening Africa, cervical cancer screening- developing countries, radiotherapy Africa, palliative care Africa. Hand searches of journals and the proceedings of major conferences were also done.

Incidence of cervical cancer in Africa The incidence of cervical cancer is still very high in sub-Saharan Africa; the rate can be up to 15 times higher in poor countries compared with industrialised ones (Table 1).1 The incidence rates in Uganda, Mali and Zimbabwe appear to be on the rise.2,3 The age-specific incidence rate in Uganda was 17.7 per 100,000 in 1960 and this increased to 44.1 per 100,000 in 1995–97.3 An estimated 57,000 cases of cervical cancer occurred in the year 2000, comprising 22.2% of all cancers in women, equivalent to an age-standardised incidence rate of 31 per 100,000.2 The age-specific incidence rate in black 41

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African populations in Harare 4 and Durban 5 were 55.0 per 100,000 and 45 per 100,000, respectively. Nonetheless, the true incidence of cervical cancer in many African countries is unknown as there is gross under-reporting. Only a very few countries have functional cancer registries and record-keeping is minimal or non-existent. Some of the figures quoted in the literature are hospital-based, which represents a small fraction of women dying from cervical cancer, as most women cannot access hospital care and die at home.

Cervical cancer mortality in Africa Mortality from cervical cancer in Africa is very high. A mortality rate of 35 per 100,000 is reported in Eastern Africa (Table 1).6 Reported mortality rates in developed countries with successful screening programmes seldom exceed 5 per 100,000 women. The five-year relative survival rates in Kampala, Uganda and Harare, Zimbabwe in 1990 were 18% and 30%, respectively, while during the same period the rate was 72% in the USA.6 In Harare, 77% of 284 registered cervical cancer patients died within three years of follow-up.7 The overall observed and relative survival at three years were 44.2% and 45.2%, respectively.7 The survival rate for cervical cancer in sub-Saharan Africa in 2002 was 21% compared with 70% and 66% in the United States and Western Europe, respectively.8 The causes of high mortality and low survival rates are: poor access to medical facilities (worst in the rural areas, where 60–70% of women who get cervical cancer reside); poor nutrition and co-morbid conditions, e.g. anaemia, malaria;9 42

HIV infection;10 late presentation with the disease; 6,7,11–13 large tumour at presentation; 14 poor quality care provided by many health services;7 high rate of loss to follow-up;7,15 and women not completing treatment due to barriers imposed by poverty.6 Facilities for treatment are also limited, and where they are available are not affordable to most women in the region.

Factors responsible for cervical cancer in Africa Socio-cultural factors Human papillomavirus (HPV), the necessary cause of cervical cancer, is endemic in Africa.16,17 Many of the factors that increase both HPV acquisition and promote the oncogenic effect of the virus are also very widespread in Africa. These include: early marriage, polygamous marriages and high parity. Polygamy is accepted in many societies in sub-Saharan Africa. In some cultures very young girls, usually virgins, are given out to marriage to much older men, some with three or more wives.18,19 This may increase the likelihood of a girl catching HPV infection at first intercourse with her husband. Polygamy is reported to increase the risk of cervical cancer two-fold and the risk increases with increasing number of wives.18 High parity, which is the norm in some cultures in Africa, is also a recognised, independent, HPV-related co-factor for the development of cervical cancer.18,20–22 Socio-economic factors Worldwide women of low socio-economic status have a greater risk of cervical cancer. Cervical cancer is often referred to as a disease of poverty23

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and of poor women.24 Poverty is endemic in sub-Saharan Africa. A recent study in Mali in West Africa showed that within a population widely infected with HPV, poor social conditions, high parity and poor hygienic conditions were the main co-factors for cervical cancer.18 Poverty, in its many ramifications, is also a very important barrier to the prevention and treatment of this disease. Biological factors Poor nutritional status and infections, e.g. malaria, HIV and TB, are ravaging sub-Saharan Africa and have made many people immuno-compromised. Reproductive tract infections are also endemic. Recent studies have linked sexually transmitted infections (STIs) other than HPV with cervical cancer.25 Herpes simplex type 2,26 Chlamydia trachomatis 27,28 and Neisseria gonorrhoea 29 have all been associated with an increased risk for cervical intraepithelial neoplasia (CIN) and invasive cervical cancer, after accounting for infection with high-risk types of HPV. These infections excite chronic inflammatory response which causes the generation of free radicals, which are thought to play an important role in the generation and progression of cancers. 25 Unfortunately, many women who get these infections receive incomplete treatment, because they cannot access (financially or geographically) good health care, thus making chronic and persistent infections very common. Several studies have demonstrated the association of HIV with HPV. The prevalence of CIN has been estimated to be as high as 20–40% in HIV-positive women.30,31 HIV-positive women are more likely to have persistent HPV infections than HIV-negative women. In a study of 2,198 women who attended gynaecological clinics in Abidjan, Cô.te d'Ivoire,32 HIV-positive women had a significantly higher prevalence of squamous intraepithelial lesion (SIL, OR 3.6) for low-grade SIL and 5.8 for high-grade SIL. Temmerman et al33 reported a five-fold increased risk of high-grade SIL among 513 HIV-positive women in a family planning clinic in Kenya. Other reports from the region show that women with HIV develop cervical cancer at an earlier age than women who are HIV-negative.10,34 Gichangi et al in Kenya10 found that young women under the age of 35 who had invasive cervical cancer were 2.6 times more likely to be HIV-

positive than controls of similar age (35% vs. 17%, OR 2.6, p=0.043). Hawes et al. in Senegal found invasive cervical cancer in 0.3% of HIVnegative women, compared with 1.9% in HIV-1 positive women (OR 6.7, 95% CI 2.1–21.7), 4.5% in HIV-2 positive women (OR 16.0, 95% CI 3.8–67.7) and 6.9% in dually-infected women (OR, 37.2; 95% CI 6.6–210).35 A recently published study from Tanzania showed prevalence of HIV-1 was much higher among the cervical cancer patients (21.0%) than among the controls (11.6%). HIV-1 was a significant risk factor for cancer of the cervix (OR=2.9, 95% CI=1.4–5.9).36 The mean ages of the HIV-1 positive and negative women with cervical cancer were 44.3 and 54 years respectively (p=0.0001).36 However, there are conflicting reports on whether HIV-positive women are more likely to develop cervical cancer than HIV-negative women.37,38 Moodley and his group in South Africa did not find an excess of cervical cancer in HIV-positive women. 3 7 However, subSaharan Africa harbours 67% of the world's population of people living with HIV and AIDS.39 Awareness and knowledge of cervical cancer in Africa Cervical cancer is yet to be recognised as an important public health problem in sub-Saharan Africa. Several studies have shown poor knowledge of the disease in Africa, which even cuts across different literacy levels.5,40–43 Among 500 attendees of a maternal and child health clinic in Lagos-Nigeria only 4.3% were found to be aware of cervical cancer.43 In 2004, also in Lagos, 81.7% of 139 patients with advanced cervical cancer had never heard of cervical cancer before, and 20%, 30% and 10% respectively thought the symptoms they had were due to resumption of menses, lower genital infection and irregular menses (unpublished report). Almost all the women (98%) believed that their advanced disease was curable, 12% thought it was not a serious disease and only 9% understood that it was cancer and therefore serious. Similar studies in Kenya and Tanzania also reported very poor knowledge of the disease in patients.44,45 Poor knowledge is not limited to patients alone, however; health care workers who are supposed to be better informed do not have good knowledge of the disease either.45–48 In Lagos, delay by primary health care providers 43

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in referring cases of cervical cancer was found to be an important cause of women presenting with late-stage disease.11 It took a mean of 9.35 ± 12.9 months for primary health care providers to diagnose and refer women with cervical cancer to a tertiary hospital for management.11

Prevention of cervical cancer in sub-Saharan Africa HPV and HPV vaccination There are few studies of the prevalence of HPV in sub-Saharan Africa. Available published reports are usually on specific populations in specific geographic areas of a country. Nonetheless, a recent International Agency for Research on Cancer (IARC) pooled analysis showed the age-standardised HPV prevalence in women with normal cytology is approximately five times higher in sub-Saharan Africa than in Europe.49 Also sub-Saharan Africa has the highest prevalence of all HPV types. HPV-positive women in sub-Saharan Africa are also more likely to have multiple infection with other high-risk types.49 The high prevalence of HPV in subSaharan Africa may be attributed to impairment in cellular immunity as a result of chronic cervical inflammation, parasitic infection, micronutrient deficiency and HIV, which are very prevalent in the region.49,50 Several studies have shown that HPV 16 and 18 are found in about 70% of all cervical cancers worldwide. HPV 16 and 18 were found in 71.7% and 80.0% of invasive cervical cancers in women in Mozambique and Uganda, respectively.51,52 The Mozambique study also reported that HPVs 16, 18, 31 and 45 were detected in 80.9% of cervical cancer tissue. The findings in these two studies imply that the HPV16,18 vaccine could potentially prevent the occurrence of more than 70% of invasive cervical cancer in the region. However, the present high cost of the vaccine may make it unaffordable and unavailable in many places in the region. It is to be hoped that it may become accessible geographically and economically in the near future through the collaboration of governments, international agencies and the pharmaceutical industry. Cervical cancer screening Very few women in sub-Saharan Africa are ever screened for cervical cancer. None of the 44

500 women attending a maternal and child health clinic in a poor area of Lagos in 1999 had ever had a Pap smear.43 Less than 1% of women in four West African countries had ever been screened.53 Only 9% of health care workers in two health institutions in Nigeria had ever had a Pap smear.47,48 Some of the few women who do have access to screening do not get themselves screened because they have wrong beliefs about cervical cancer. Low levels of awareness and poor knowledge of cervical cancer coupled with unavailability and inaccessibility of cervical cancer screening services are responsible for only a very small number of women being screened in sub-Saharan Africa. Moreover, there are very few cervical screening services in Africa and many of them are based in secondary and tertiary health care facilities located in urban areas. Only 5% of 504 general practitioners in Lagos in 2004 screened their patients.54 Screening for cervical cancer is opportunistic and it is more often than not limited to women who attend antenatal and family planning clinics. Women who use these services are generally young, and smears are thus being taken from a relatively low-risk group. This type of service does not reach women most at risk, i.e. older women aged 35–60 years, especially those who live in rural areas. Cytology-based screening, which is used in developed countries, is resource intensive, and difficult to realise in very many countries in sub-Saharan Africa because of poor health care infrastructure and lack of resources. There are very few cytopathologists, cytoscreeners and cytotechnicians; some have inadequate training. Quality control is inadequate. Histopathological services are extremely limited in many countries. Malawi, a country with a cervical cancer incidence rate of 47 per 100,000 women, has one pathologist, one colposcope, no cyto-technicians and no facilities for cervical cancer screening or treatment.55 The default rate among those with cytological abnormalities reaches 60–80% due to the absence of effective mechanisms for recall of women with abnormal smears.15 The effectiveness of direct visual inspection (visual inspection with acetic acid and visual inspection with Lugol's iodine) as a form of population-based screening is currently being studied in some ongoing projects across the

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continent, mainly sponsored by international agencies. 6,24 Results from these studies are quite promising and support its use as an alternative to cervical cytology.55 Treatment of pre-cancers It may not be too wrong to say that there are apparently more cases of invasive cancer than pre-invasive cancer; this is mainly because there are very few facilities for screening and very poor access to the screening services. Because so few women are ever screened, not many cases of pre-cancerous lesions are diagnosed or detected. Colposcopy is available only in very few centres.56 Hysterectomy and cone biopsy are the usual treatment modalities for pre-cancerous lesions, as the equipment and expertise for large loop excision of the transformation zone (LLETZ), also known as loop electrosurgical excision (LEEP), are scarce.57,58 Cryotherapy machines, which are supposed to be of low cost, are not available in very many places either. A recent survey of methods used by Nigerian gynaecologists to treat CIN II/III found 51.5%, 33.6%, 7.5% and 0.7% performed cone biopsy, hysterectomy, electro-diathermy and LEEP respectively.57

Treatment of invasive cervical cancer The management of invasive cervical cancer continues to be a major challenge in many subSaharan African countries, due to the lack of surgical facilities, skilled providers and radiotherapy services.59 Facilities for clinical management of those cases who do present at a stage where therapy might be successful are often very inadequate. Currently, almost all the centres for management of invasive disease are found in urban areas. Follow-up is very poor as many of the women who get the disease are poor, live in rural areas and cannot afford the cost of going back to urban centres for follow-up after initial treatment. Management of women with invasive cervical cancer requires a multidisciplinary approach, including: gynaecologists, radiation oncologists and medical oncologists, pathologists, medical physicists, technicians, nurses and counsellors. These people are lacking in many places across the continent, and where they exist they tend to work in isolation rather than in teams.

Treatment of invasive cervical cancer: surgery There are few cases that present in the operable stage of the disease. In Lagos less than 10% of cases are operable at the time of presentation.11 Some of the few who do present early may not have surgery as there are very few certified gynaecologists who perform radical gynaecological cancer surgery. Follow-up after surgery is often very poor as some patients who believe they have been cured never come back. Others just cannot afford the cost of transportation back to urban centres for follow-up. Treatment of invasive cervical cancer: radiation For patients who present late, radiotherapy becomes the preferred treatment. Unfortunately, only a few receive this treatment due to the paucity of resources and very advanced disease at presentation. Chirenje found in Harare13 that in 70% of patients, radiotherapy was the most commonly used treatment modality, as many of the cases presented with stage 2B and above. Radiotherapy is not available in many places, however. In 1997, radiotherapy was not available in 32 African countries.14 In 2003, 15 countries in Africa did not have a single radiotherapy machine.60 Nigeria, the most populous country in Africa, had only five radiotherapy centres in 2007: four government-owned and one privately owned. WHO recommends 0.4 radiotherapy machines per million of population.61 Nigeria's five machines to 140 million people translates to ∼0.04 per million, well below WHO's recommendation. In contrast, in the United States, there are 12 machines per million people.61 Besides few machines, those that exist frequently do not function most of the time because the resources for proper maintenance and repair of them do not exist. In addition, there is a shortage of trained staff such as radiotherapists and medical physicists, as well as essential materials. Treatment of invasive cervical cancer: palliative care Pain is the most common presenting symptom in many cancer patients in Africa because of late presentation. In a survey of terminally ill patients in five countries in Africa – Uganda, Ethiopia, Tanzania, Zimbabwe and Botswana – the greatest need expressed by the patients was pain relief.62 In another study63 comparing the concerns of terminally ill patients in a developed country 45

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(Scotland) and an African country (Kenya), it was found that the main concern of the Scottish patients was the emotional pain of facing death, while for their counterparts in Kenya it was physical pain and financial worries. Unfortunately, there is inadequate availability of pain-relieving medications, especially opioids. 62–65 Only 11 out of 47 African countries use morphine for chronic pain and of these 11, the amount consumed is small.64 Oral morphine is not available to very many cancer patients in sub-Saharan Africa. Insufficient funds due to low priority accorded to palliative care by governments, regulatory and pricing obstacles, ignorance, and false beliefs are responsible. In some instances, where drugs are available to patients, sustainability of pain relief is hampered by poverty, as many cannot afford the cost of the drugs. Poverty, poor infrastructure, lack of health care workers adequately trained in palliative care and poor priority accorded to palliative care by African governments are all obstacles to effective palliative care in sub-Saharan Africa. There are very few hospices to take care of terminally ill patients. However, countries like South Africa, Uganda, Kenya, Tanzania and Zimbabwe have made some progress in palliative care. Uganda is the first African country to follow the WHO guidelines on palliative care. It has made oral morphine freely available to districts that have specialist palliative care nurses or clinical officers, and has promoted morphine use down to the villages. Laws have also been passed to allow trained nurses, especially those in the rural areas, where there are very few or no doctors, to prescribe morphine.64 Cancer is believed in certain cultures to be a punishment from the gods, and terminally ill patients often seek help from traditional healers and spiritual leaders. A good model for palliative care in Africa should therefore integrate the culture, beliefs and traditions of the people. Some countries are making efforts in this direction by incorporating traditional healers into mainstream medicine.64 Nonetheless, a feasible, accessible, and effective palliative care is yet to be developed in sub-Saharan Africa.64

Recommendations • The problem of cervical cancer in sub-Saharan Africa can be tackled effectively if there is 46

• •

political will. Governments must recognise cervical cancer as a serious public health problem and allocate appropriate resources to its prevention and treatment, and for research. Interventions should be put in place to increase awareness of cervical cancer and preventive health-seeking behaviour among high-risk women (especially those aged 30–50 years). These high-risk women should be targeted using a good quality and highly sensitive test at least once or twice in their lifetime. The South African government has recently taken steps in the right direction and introduced a policy to screen women at least three times, starting from age 30 and at ten-year intervals. The “single-visit approach” for prevention of cervical cancer, using low-cost and lowtechnology screening methods and treatment, is recommended for countries in the region. This method is affordable and effective. In the Niger Republic, in West Africa, a free cervical cancer screening programme using this approach has been set up. Overly restrictive laws on opioids need to be reviewed, to make these drugs available, accessible and affordable for pain relief and palliative care. Governments in sub-Saharan Africa should support and be part of ongoing research and trials using HPV vaccine for the primary prevention of this deadly disease. Primary prevention using the HPV vaccine may in the long run provide an answer to the reduction of the incidence of cervical cancer, including in Africa. The Geneva-based Global Alliance for Vaccines and Immunization (GAVI), PATH and the World Bank should work with the pharmaceutical industry to bring down the price of the vaccine to make it available and affordable in sub-Saharan Africa. Significantly more international attention needs to be paid to the burden of cervical cancer in sub-Saharan Africa. Cervical cancer screening and treatment should either be free or heavily subsidised by government. This can be achieved if there is both political and financial backing. Finally, poverty in sub-Saharan Africa needs to be addressed seriously, as poverty is an important factor in the aetiology, prevention and treatment of this disease.

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Résumé Le cancer du col de l'utérus est le deuxième cancer féminin le plus fréquent dans le monde et la principale cause de décès par cancer dans les pays en développement. Si ses taux d'incidence et de mortalité ont reculé sensiblement dans les pays développés, 83% des nouveaux cas qui se déclarent chaque année et 85% des décès dus à la maladie se produisent dans les pays en développement. Le cancer du col de l'utérus est la forme de cancer la plus fréquente chez les femmes en Afrique subsaharienne. Dans certains pays, son incidence augmente. La connaissance de la maladie sur le continent est très médiocre et la mortalité demeure très élevée. Les équipements de prévention et de traitement du cancer du col de l'utérus sont encore nettement insuffisants dans beaucoup de pays de la région. Les gouvernements d'Afrique subsaharienne doivent comprendre qu'il s'agit d'un problème majeur de santé publique et allouer assez de ressources pour sa prévention et son traitement, ainsi que pour la recherche. En fait, le cancer du col de l'utérus doit recevoir dans la région la même priorité que le VIH, le paludisme, la tuberculose et la vaccination des enfants.

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Resumen El cáncer cervical es el segundo cáncer más común en las mujeres mundialmente y la causa principal de muertes por cáncer en los países en desarrollo. Aunque la incidencia y las tasas de mortalidad por cáncer cervical han disminuido considerablemente en los países desarrollados, el 83% de todos los casos nuevos que ocurren anualmente y el 85% de todas las muertes atribuibles a esta enfermedad ocurren en países en desarrollo. El cáncer cervical es el cáncer más común entre las mujeres de África subsahariana. Su incidencia está en alza en algunos países. Existe muy poco conocimiento y conciencia de esta enfermedad en el continente, y la tasa de mortalidad continúa siendo muy alta. En muchos países de la región, los establecimientos para la prevención y el tratamiento del cáncer cervical aún son muy inadecuados. Los gobiernos de África subsahariana deben reconocer al cáncer cervical como un grave problema de salud pública y alocar los recursos necesarios para su prevención, tratamiento e investigación. Es más, en esta región se le debe dar la misma prioridad al cáncer cervical que al VIH, malaria, tuberculosis e inmunizaciones de niños.