Polygyny - Cervical Cancer Association

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2008 Reproductive Health Matters.All rights reserved.

Reproductive Health Matters 2008;16(32):41490968-8080/08 $ see front matterPII: S 0 9 6 8 - 8 0 8 0 ( 0 8 ) 3 2 4 1 5 - Xwww.rhm-elsevier.com www.rhmjournal.org.uk

Cervical cancer: the sub-Saharan African perspectiveRose 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 leadingcause of cancer deaths in developing countries. While incidence and mortality rates of cervical cancerhave fallen significantly in developed countries, 83% of all new cases that occur annually and 85% ofall 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. Knowledgeand awareness of this disease on the continent are very poor and mortality still very high. Facilities forthe prevention and treatment of cervical cancer are still very inadequate in many countries in theregion. Governments in sub-Saharan Africa must recognise cervical cancer as a major public healthconcern 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 andchildhood immunisations. 2008 Reproductive Health Matters. All rights reserved.

Keywords: cervical cancer and screening, health policies and programmes, sub-Saharan Africa

CERVICAL cancer is a preventable and cur-able disease, preventable by vaccination

and screening and curable if identified atan early enough stage. It is gradually becominga rare disease in many developed countries; thisis not the case with many countries in sub-Saharan Africa. Cervical cancer is the mostcommon cancer in women in sub-SaharanAfrica and second to breast cancer in northernAfrica. In sub-Saharan African, it accounts for22.2% of all cancers in women and it is alsothe most common cause of cancer death amongwomen.1 About 6075% of women in sub-Saharan Africa who develop cervical cancer

live in rural areas,2 and mortality is very high.1Many of the women who develop cervicalcancer are untreated, mostly due to lack ofaccess (financial and geographical) to healthcare. Women in sub-Saharan Africa lose moreyears to cervical cancer than to any other typeof cancer. Unfortunately, it affects them at atime of life when they are critical to the socialand economic stability of their families.

The objective of this review was to criticallyappraise the incidence, mortality, knowledge,

prevention and treatment of cervical cancer insub-Saharan Africa. A computerised literature

search was conducted for published articles.Mesh phrases used for the search were cervicalcancer, cervical cancer Africa, cervical cancerscreening Africa, cervical cancer screening- deve-loping countries, radiotherapy Africa, palliativecare Africa. Hand searches of journals and theproceedings of major conferences were also done.

Incidence of cervical cancer in Africa

The incidence of cervical cancer is still very highin sub-Saharan Africa; the rate can be up to

15 times higher in poor countries comparedwith industrialised ones (Table 1).1 The inci-dence rates in Uganda, Mali and Zimbabweappear to be on the rise.2,3 The age-specific inci-dence rate in Uganda was 17.7 per 100,000 in1960 and this increased to 44.1 per 100,000 in199597.3An estimated 57,000 cases of cervicalcancer occurred in the year 2000, comprising22.2% of all cancers in women, equivalent toan age-standardised incidence rate of 31 per100,000.2 The age-specific incidence rate in black

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African populations in Harare4 and Durban5

were 55.0 per 100,000 and 45 per 100,000,respectively. Nonetheless, the true incidence ofcervical cancer in many African countries isunknown as there is gross under-reporting.Only a very few countries have functionalcancer registries and record-keeping is minimalor non-existent. Some of the figures quoted inthe literature are hospital-based, which repre-sents a small fraction of women dying from cer-vical cancer, as most women cannot accesshospital care and die at home.

Cervical cancer mortality in AfricaMortality from cervical cancer in Africa is veryhigh. A mortality rate of 35 per 100,000 isreported in Eastern Africa (Table 1).6 Reportedmortality rates in developed countries with suc-cessful screening programmes seldom exceed5 per 100,000 women. The five-year relativesurvival rates in Kampala, Uganda and Harare,Zimbabwe in 1990 were 18% and 30%, respec-tively, while during the same period the rate was72% in the USA.6 In Harare, 77% of 284 regis-tered cervical cancer patients died within three

years of follow-up.7 The overall observed andrelative survival at three years were 44.2% and45.2%, respectively.7 The survival rate for cervi-cal cancer in sub-Saharan Africa in 2002 was21% compared with 70% and 66% in the UnitedStates and Western Europe, respectively.8

The causes of high mortality and low survivalrates are: poor access to medical facilities (worstin the rural areas, where 6070% of women whoget cervical cancer reside); poor nutrition andco-morbid conditions, e.g. anaemia, malaria;9

HIV infection;10 late presentation with the dis-ease;6,7 ,1113 large tumour at presentation;14

poorquality care provided by many health ser-vices;7 high rate of loss to follow-up;7,15 andwomen not completing treatment due to barriersimposed by poverty.6 Facilities for treatment arealso limited, and where they are available arenot affordable to most women in the region.

Factors responsible for cervical cancerin Africa

Socio-cultural factorsHuman papillomavirus (HPV), the necessary cause

of cervical cancer, is endemic in Africa.16,17Many of the factors that increase both HPVacquisition and promote the oncogenic effectof the virus are also very widespread in Africa.These include: early marriage, polygamous mar-riages and high parity. Polygamy is accepted inmany societies in sub-Saharan Africa. In somecultures very young girls, usually virgins, aregiven out to marriage to much older men, somewith three or more wives.18,19 This may increasethe likelihood of a girl catching HPV infection atfirst intercourse with her husband. Polygamy is

reported to increase the risk of cervical cancertwo-fold and the risk increases with increasingnumber of wives.18 High parity, which is thenorm in some cultures in Africa, is also a recog-nised, independent, HPV-related co-factor for thedevelopment of cervical cancer.18,2022

Socio-economic factorsWorldwide women of low socio-economic statushave a greater risk of cervical cancer. Cervicalcancer is often referred to as a disease of poverty23

RI Anorlu / Reproductive Health Matters 2008;16(32):4149

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and of poor women.24 Poverty is endemic insub-Saharan Africa. A recent study in Mali in West Africa showed that within a populationwidely infected with HPV, poor social condi-tions, high parity and poor hygienic conditions

were the main co-factors for cervical cancer.18

Poverty, in its many ramifications, is also avery important barrier to the prevention andtreatment of this disease.

Biological factorsPoor nutritional status and infections, e.g. malaria,HIV and TB, are ravaging sub-Saharan Africa andhave made many people immuno-compromised.Reproductive tract infections are also endemic.Recent studies have linked sexually transmittedinfections (STIs) other than HPV with cervical

cancer.25

Herpes simplex type 2,26

Chlamydiatrachomatis27,28 and Neisseria gonorrhoea29

have all been associated with an increased riskfor cervical intraepithelial neoplasia (CIN) andinvasive cervical cancer, after accounting forinfection with high-risk types of HPV. Theseinfections excite chronic inflammatory responsewhich causes the generation of free radicals,which are thought to play an important role inthe generation and progression of cancers.25

Unfortunately, many women who get theseinfections receive incomplete treatment, because

they cannot access (financially or geographi-cally) good health care, thus making chronicand persistent infections very common.

Several studies have demonstrated the asso-ciation of HIV with HPV. The prevalence of CINhas been estimated to be as high as 2040% inHIV-positive women.30,31 HIV-positive women aremore likely to have persistent HPV infections thanHIV-negative women. In a study of 2,198 womenwho attended gynaecological clinics in Abidjan,C.te d'Ivoire,32 HIV-positive women had a sig-nificantly higher prevalence of squamous intra-

epithelial lesion (SIL, OR 3.6) for low-grade SILand 5.8 for high-grade SIL. Temmerman et al33

reported a five-fold increased risk of high-gradeSIL among 513 HIV-positive women in a familyplanning clinic in Kenya.

Other reports from the region show thatwomen with HIV develop cervical cancer at anearlier age than women who are HIV-negative.10,34

Gichangi et al in Kenya10 found that young womenunder the age of 35 who had invasive cervicalcancer 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 Senegalfound invasive cervical cancer in 0.3% of HIV-negative women, compared with 1.9% in HIV-1positive women (OR 6.7, 95% CI 2.121.7),

4.5% in HIV-2 positive women (OR 16.0, 95%CI 3.867.7) and 6.9% in dually-infected women(OR, 37.2; 95% CI 6.6210).35 A recently pub-lished study from Tanzania showed prevalenceof HIV-1 was much higher among the cervicalcancer patients (21.0%) than among the controls(11.6%). HIV-1 was a significant risk factor forcancer of the cervix (OR=2.9, 95% CI=1.45.9).36

The mean ages of the HIV-1 positive and nega-tive women with cervical cancer were 44.3 and54 years respectively (p=0.0001).36

However, there are conflicting reports on

whether HIV-positive women are more likelyto develop cervical cancer than HIV-negativewomen.37,38 Moodley and his group in SouthAfrica did not find an excess of cervical cancerin HIV-positive women.37 However, sub-Saharan Africa harbours 67% of the world'spopulation of people living with HIV and AIDS.39

Awareness and knowledge of cervical cancerin AfricaCervical cancer is yet to be recognised as animportant public health problem in sub-Saharan

Africa. Several studies have shown poor know-ledge of the disease in Africa, which even cutsacross different literacy levels.5,4043 Among500 attendees of a maternal and child healthclinic in Lagos-Nigeria only 4.3% were foundto be aware of cervical cancer.43 In 2004, alsoin Lagos, 81.7% of 139 patients with advancedcervical cancer had never heard of cervicalcancer before, and 20%, 30% and 10% respec-tively thought the symptoms they had weredue to resumption of menses, lower genitalinfection and irregular menses (unpublished

report). Almost all the women (98%) believedthat their advanced disease was curable, 12%thought it was not a serious disease and only9% understood that it was cancer and thereforeserious. Similar studies in Kenya and Tanzaniaalso reported very poor knowledge of the diseasein patients.44,45 Poor knowledge is not limitedto patients alone, however; health care workerswho are supposed to be better informed do nothave good knowledge of the disease either.4548

In Lagos, delay by primary health care providers


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in referring cases of cervical cancer was foundto be an important cause of women presentingwith late-stage disease.11 It took a mean of9.35 12.9 months for primary health care pro-viders to diagnose and refer women with cervical

cancer to a tertiary hospital for management.11

Prevention of cervical cancer insub-Saharan Africa

HPV and HPV vaccinationThere are few studies of the prevalence of HPVin sub-Saharan Africa. Available publishedreports are usually on specific populations inspecific geographic areas of a country. Nonethe-less, a recent International Agency for Researchon Cancer (IARC) pooled analysis showed the

age-standardised HPV prevalence in womenwith normal cytology is approximately fivetimes higher in sub-Saharan Africa than inEurope.49Also sub-Saharan Africa has the highestprevalence of all HPV types. HPV-positive womenin sub-Saharan Africa are also more likely tohave multiple infection with other high-risktypes.49 The high prevalence of HPV in sub-Saharan Africa may be attributed to impairmentin cellular immunity as a result of chronic cervi-cal inflammation, parasitic infection, micronutri-ent deficiency and HIV, which are very prevalent

in the region.49,50Several studies have shown that HPV 16 and

18 are found in about 70% of all cervical can-cers worldwide. HPV 16 and 18 were found in71.7% and 80.0% of invasive cervical cancersin women in Mozambique and Uganda, respec-tively.51,52 The Mozambique study also reportedthat HPVs 16, 18, 31 and 45 were detected in80.9% of cervical cancer tissue. The findings inthese two studies imply that the HPV16,18 vac-cine could potentially prevent the occurrence ofmore than 70% of invasive cervical cancer in the

region. However, the present high cost of thevaccine may make it unaffordable and unavail-able in many places in the region. It is to behoped that it may become accessible geographi-cally and economically in the near future throughthe collaboration of governments, internationalagencies and the pharmaceutical industry.

Cervical cancer screeningVery few women in sub-Saharan Africa areever screened for cervical cancer. None of the

500 women attending a maternal and childhealth clinic in a poor area of Lagos in 1999had ever had a Pap smear.43 Less than 1% ofwomen in fourWest African countries had everbeen screened.53 Only 9% of health care workers

in two health institutions in Nigeria had ever hada Pap smear.47,48 Some of the few women whodo have access to screening do not get them-selves screened because they have wrong beliefsabout cervical cancer. Low levels of awarenessand poor knowledge of cervical cancer coupledwith unavailability and inaccessibility of cervi-cal cancer screening services are responsiblefor only a very small number of women beingscreened in sub-Saharan Africa.

Moreover, there are very few cervical screen-ing services in Africa and many of them are

based in secondary and tertiary health carefacilities located in urban areas. Only 5% of504 general practitioners in Lagos in 2004screened their patients.54 Screening for cervicalcancer is opportunistic and it is more oftenthan not limited to women who attend ante-natal and family planning clinics. Women whouse these services are generally young, andsmears are thus being taken from a relativelylow-risk group. This type of service does notreach women most at risk, i.e. older womenaged 3560 years, especially those who live in

rural areas.Cytology-based screening, which is used in

developed countries, is resource intensive, anddifficult to realise in very many countries insub-Saharan Africa because of poor health careinfrastructure and lack of resources. There arevery few cytopathologists, cytoscreeners andcytotechnicians; some have inadequate training.Quality control is inadequate. Histopathologicalservices are extremely limited in many countries.Malawi, a country with a cervical cancer inci-dence rate of 47 per 100,000 women, has one

pathologist, one colposcope, no cyto-techniciansand no facilities for cervical cancer screening ortreatment.55 The default rate among those withcytological abnormalities reaches 6080% dueto the absence of effective mechanisms forrecall of women with abnormal smears.15

The effectiveness of direct visual inspection(visual inspection with acetic acid and visualinspection with Lugol's iodine) as a form ofpopulation-based screening is currently beingstudied in some ongoing projects across the


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continent, mainly sponsored by internationalagencies.6,24 Results from these studies arequite promising and support its use as an alter-native to cervical cytology.55

Treatment of pre-cancersIt may not be too wrong to say that there areapparently more cases of invasive cancer thanpre-invasive cancer; this is mainly because thereare very few facilities for screening and very pooraccess to the screening services. Because so fewwomen are ever screened, not many cases ofpre-cancerous lesions are diagnosed or detected.Colposcopy is available only in very few cen-tres.56 Hysterectomy and cone biopsy are theusual treatment modalities for pre-cancerous

lesions, as the equipment and expertise for largeloop 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 notavailable in very many places either. A recentsurvey of methods used by Nigerian gynae-cologists to treat CIN II/III found 51.5%, 33.6%,7.5% and 0.7% performed cone biopsy, hysterec-tomy, electro-diathermy and LEEP respectively.57

Treatment of invasive cervical cancerThe management of invasive cervical cancercontinues to be a major challenge in many sub-Saharan African countries, due to the lack ofsurgical facilities, skilled providers and radio-therapy services.59 Facilities for clinical man-agement of those cases who do present at astage where therapy might be successful areoften very inadequate. Currently, almost all thecentres for management of invasive disease arefound in urban areas. Follow-up is very poor asmany of the women who get the disease are poor,

live in rural areas and cannot afford the cost ofgoing back to urban centres for follow-up afterinitial treatment.

Management of women with invasive cervi-cal cancer requires a multidisciplinary approach,including: gynaecologists, radiation oncologistsand medical oncologists, pathologists, medicalphysicists, technicians, nurses and counsellors.These people are lacking in many places acrossthe continent, and where they exist they tend towork in isolation rather than in teams.

Treatment of invasive cervical cancer: surgeryThere are few cases that present in the operablestage of the disease. In Lagos less than 10% ofcases 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 certifiedgynaecologists who perform radical gynaeco-logical cancer surgery. Follow-up after surgeryis often very poor as some patients who believethey have been cured never come back. Others just cannot afford the cost of transportationback to urban centres for follow-up.

Treatment of invasive cervical cancer: radiationFor patients who present late, radiotherapybecomes the preferred treatment. Unfortunately,only a few receive this treatment due to the pau-

city of resources and very advanced disease atpresentation. Chirenje found in Harare13 thatin 70% of patients, radiotherapy was the mostcommonly used treatment modality, as manyof the cases presented with stage 2B and above.Radiotherapy is not available in many places,however. In 1997, radiotherapy was not availablein 32 African countries.14 In 2003, 15 countriesin Africa did not have a single radiotherapymachine.60 Nigeria, the most populous countryin Africa, had only five radiotherapy centres in2007: four government-owned and one privately

owned. WHO recommends 0.4 radiotherapymachines per million of population.61 Nigeria'sfive machines to 140 million people translatesto 0.04 per million, well below WHO's recom-mendation. In contrast, in the United States,there are 12 machines per million people.61

Besides few machines, those that exist frequentlydo not function most of the time because theresources for proper maintenance and repair ofthem do not exist. In addition, there is a shortageof trained staff such as radiotherapists and medi-cal physicists, as well as essential materials.

Treatment of invasive cervical cancer:palliative carePain is the most common presenting symptomin many cancer patients in Africa because of latepresentation. In a survey of terminally ill patientsin five countries in Africa Uganda, Ethiopia,Tanzania, Zimbabwe and Botswana the greatestneed expressed by the patients was pain relief.62

In another study63 comparing the concerns ofterminally ill patients in a developed country


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(Scotland) and an African country (Kenya), itwas found that the main concern of the Scottishpatients was the emotional pain of facing death,while for their counterparts in Kenya it was physi-cal pain and financial worries. Unfortunately,

there is inadequate availability ofpain-relievingmedications, especially opioids.6265 Only 11out of 47 African countries use morphine forchronic pain and of these 11, the amount con-sumed is small.64 Oral morphine is not availableto very many cancer patients in sub-SaharanAfrica. Insufficient funds due to low priorityaccorded to palliative care by governments, reg-ulatory and pricing obstacles, ignorance, andfalse beliefs are responsible. In some instances,where drugs are available to patients, sustain-ability of pain relief is hampered by poverty, as

many cannot afford the cost of the drugs.Poverty, poor infrastructure, lack of healthcare workers adequately trained in palliativecare and poor priority accorded to palliative careby African governments are all obstacles to effec-tive palliative care in sub-Saharan Africa. Thereare very few hospices to take care of terminallyill patients. However, countries like South Africa,Uganda, Kenya, Tanzania and Zimbabwe havemade some progress in palliative care. Ugandais the first African country to follow the WHOguidelines on palliative care. It has made oral

morphine freely available to districts that havespecialist palliative care nurses or clinical offi-cers, and has promoted morphine use down tothe villages. Laws have also been passed to allowtrained nurses, especially those in the rural areas,where there are very few or no doctors, to pre-scribe morphine.64

Cancer is believed in certain cultures to be apunishment from the gods, and terminally illpatients often seek help from traditional healersand spiritual leaders. A good model for pallia-tive care in Africa should therefore integrate

the culture, beliefs and traditions of the people.Some countries are making efforts in this direc-tion by incorporating traditional healers intomainstream medicine.64 Nonetheless, a feasible,accessible, and effective palliative care is yet tobe developed in sub-Saharan Africa.64

Recommendations

The problem of cervical cancer in sub-SaharanAfrica can be tackled effectively if there is

political will. Governments must recognisecervical cancer as a serious public healthproblem and allocate appropriate resources toits prevention and treatment, and for research.

Interventions should be put in place to increase

awareness of cervical cancer and preventivehealth-seeking behaviour among high-riskwomen (especially those aged 3050 years).These high-risk women should be targetedusing a good quality and highly sensitive testat least once or twice in their lifetime. TheSouth African government has recently takensteps in the right direction and introduced apolicy to screen women at least three times,starting from age 30 and at ten-year intervals.

The single-visit approach for preventionof cervical cancer, using low-cost and low-technology screening methods and treatment,is recommended for countries in the region.This method is affordable and effective. Inthe Niger Republic, in West Africa, a free cer-vical cancer screening programme using thisapproach has been set up.

Overly restrictive laws on opioids need to bereviewed, to make these drugs available, acces-sible and affordable for pain relief and pallia-tive care.

Governments in sub-Saharan Africa should

support and be part of ongoing research andtrials using HPV vaccine for the primary pre-vention of this deadly disease. Primary pre-vention using the HPV vaccine may in thelong run provide an answer to the reductionof the incidence of cervical cancer, includingin Africa. The Geneva-based Global Alliancefor Vaccines and Immunization (GAVI), PATHand the World Bank should work with thepharmaceutical industry to bring down theprice of the vaccine to make it available andaffordable in sub-Saharan Africa.

Significantly more international attentionneeds to be paid to the burden of cervical cancerin sub-Saharan Africa.

Cervical cancer screening and treatment shouldeither be free or heavily subsidised by govern-ment. This can be achieved if there is bothpolitical and financial backing.

Finally, poverty in sub-Saharan Africa needsto be addressed seriously, as poverty is animportant factor in the aetiology, preventionand treatment of this disease.


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RsumLe cancer du col de l'utrus est le deuximecancer fminin le plus frquent dans le monde etla principale cause de dcs par cancer dans lespays en dveloppement. Si ses taux d'incidence

et de mortalit ont recul sensiblement dans lespays dvelopps, 83% des nouveaux cas qui sedclarent chaque anne et 85% des dcsdus la maladie se produisent dans les pays endveloppement. Le cancer du col de l'utrus estla forme de cancer la plus frquente chez lesfemmes en Afrique subsaharienne. Danscertains pays, son incidence augmente. Laconnaissance de la maladie sur le continent esttrs mdiocre et la mortalit demeure trsleve. Les quipements de prvention et detraitement du cancer du col de l'utrus sont

encore nettement insuffisants dans beaucoupde pays de la rgion. Les gouvernementsd'Afrique subsaharienne doivent comprendrequ'il s'agit d'un problme majeur de santpublique et allouer assez de ressources pour saprvention et son traitement, ainsi que pour larecherche. En fait, le cancer du col de l'utrusdoit recevoir dans la rgion la mme prioritque le VIH, le paludisme, la tuberculose et lavaccination des enfants.

ResumenEl cncer cervical es el segundo cncer mscomn en las mujeres mundialmente y lacausa principal de muertes por cncer en lospases en desarrollo. Aunque la incidencia y las

tasas de mortalidad por cncer cervical handisminuido considerablemente en los pasesdesarrollados, el 83% de todos los casos nuevosque ocurren anualmente y el 85% de todas lasmuertes atribuibles a esta enfermedad ocurrenen pases en desarrollo. El cncer cervical es elcncer ms comn entre las mujeres de fricasubsahariana. Su incidencia est en alza enalgunos pases. Existe muy poco conocimientoy conciencia de esta enfermedad en el continente,y la tasa de mortalidad contina siendo muy alta.En muchos pases de la regin, los establecimientos

para la prevencin y el tratamiento del cncercervical an son muy inadecuados. Los gobiernosde frica subsahariana deben reconocer al cncercervical como un grave problema de saludpblica y alocar los recursos necesarios para suprevencin, tratamiento e investigacin. Es ms,en esta regin se le debe dar la misma prioridad alcncer cervical que al VIH, malaria, tuberculosise inmunizaciones de nios.


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Polygyny - Cervical Cancer Association