© 2008 Reproductive Health Matters.

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Reproductive Health Matters 2008;16(32):41–49
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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: rianorlu2004@gmail.com

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

C
ERVICAL cancer is a preventable and cur-
able 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 sub-
Saharan 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 sub-
Saharan 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- deve-
loping 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 inci-
dence rates in Uganda, Mali and Zimbabwe
appear to be on the rise.2,3 The age-specific inci-
dence 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
 RI Anorlu / Reproductive Health Matters 2008;16(32):41–49
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 repre-
sents a small fraction of women dying from cer-
vical 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 suc-
cessful 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%, respec-
tively, while during the same period the rate was
72% 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 and
relative survival at three years were 44.2% and
45.2%, respectively.7 The survival rate for cervi-
cal 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 dis-
ease; 6,7,11–13 large tumour at presentation; 14
poor quality care provided by many health ser-
vices;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 mar-
riages 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 recog-
nised, 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
 RI Anorlu / Reproductive Health Matters 2008;16(32):41–49
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 condi-
tions, 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 geographi-
cally) good health care, thus making chronic
and persistent infections very common.
Several studies have demonstrated the asso-
ciation 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 sig-
nificantly higher prevalence of squamous intra-
epithelial 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 HIV-
negative 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 pub-
lished 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 nega-
tive 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, sub-
Saharan 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 know-
ledge 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% respec-
tively 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
 RI Anorlu / Reproductive Health Matters 2008;16(32):41–49
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 pro-
viders 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. Nonethe-
less, 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 sub-
Saharan Africa may be attributed to impairment
in cellular immunity as a result of chronic cervi-
cal inflammation, parasitic infection, micronutri-
ent deficiency and HIV, which are very prevalent
in the region.49,50
Several 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 in
71.7% and 80.0% of invasive cervical cancers
in women in Mozambique and Uganda, respec-
tively.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 vac-
cine 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 unavail-
able in many places in the region. It is to be
hoped that it may become accessible geographi-
cally 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 them-
selves 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 cervi-
cal 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 screen-
ing 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 ante-
natal 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 inci-
dence 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
 RI Anorlu / Reproductive Health Matters 2008;16(32):41–49
continent, mainly sponsored by international
agencies. 6,24 Results from these studies are
quite promising and support its use as an alter-
native 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 cen-
tres.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 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 cancer
The management of invasive cervical cancer
continues to be a major challenge in many sub-
Saharan African countries, due to the lack of
surgical facilities, skilled providers and radio-
therapy services.59 Facilities for clinical man-
agement 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 cervi-
cal 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 gynaeco-
logical 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 pau-
city 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 recom-
mendation. 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 medi-
cal 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
 RI Anorlu / Reproductive Health Matters 2008;16(32):41–49
(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 physi-
cal 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 con-
sumed 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, reg-
ulatory and pricing obstacles, ignorance, and
false 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 health
care workers adequately trained in palliative
care and poor priority accorded to palliative care
by African governments are all obstacles to effec-
tive 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 offi-
cers, 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 pre-
scribe 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 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 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 low-
technology 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 cer-
vical cancer screening programme using this
approach has been set up.
• Overly restrictive laws on opioids need to be
reviewed, 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 and
trials using HPV vaccine for the primary pre-
vention of this deadly disease. Primary pre-
vention 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 govern-
ment. 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.
 RI Anorlu / Reproductive Health Matters 2008;16(32):41–49
References
1. Parkin DM, Ferlay J,
Hamdi-Cherif M, et al. Cancer
in Africa: Epidemiology and
Prevention. IARC Scientific
Publications. No.153. Lyon:
IARC Press, 2003.
2. Parkin DM, Whelan SL, Ferlay J,
et al, editors. Cancer Incidence in
Five Continents, Vol VIII. IARC
Scientific Publication No.155.
Lyon: IARC, 2002.
3. Wabinga HR, Parkin DW,
Wabwire-Mangen F, et al.
Trends in cancer incidence in
Kyadondo County, Uganda,
1960–1997. British Journal of
Cancer 2000;82(9):1585–92.
4. Chokunonga E, Levy LM, Bassett
MT, et al. Zimbabwe cancer
registry. In: Parkin DM, Whelan
SL, Ferlay J, et al, editors. Cancer
Incidence in Five Continents.
Vol. VIII. Lyon: IARC Press,
2002. pp.104–05.
5. Walker ARP, Michelow PM,
Walker BF. Cervix cancer in
African women in Durban,
South Africa. International
Journal Gynecology &
Obstetrics 2002;79:45–46.
6. Sankaranarayanan R, Ferlay J.
Worldwide burden of
gynaecological cancer: the size
of the problem. Best Practice and
Research Clinical Obstetrics &
Gynaecology 2006;20(2):207–25.
7. Chokunonga E, Ramanakumar
AV, Nyakabau AM, et al.
Survival of cervix cancer
patients in Harare, Zimbabwe,
1995–1997. British Journal of
Cancer 2003;89:65–69.
8. Parkin DM, Bray F, Ferlay J,
et al. Global Cancer Statistics,
2002. CA: A Cancer Journal for
Clinicians 2005;55:74–108.
9. Odida M, Schmauz R, Lwanga
SK. Grade of malignancy of
cervical cancer in regions of
Uganda with varying malarial
endemicity. International
Journal of Cancer 2002;99:
737–41.
10. Gichangi PB, Bwayo J,
Estambale B, et al. Impact of HIV
infection on invasive cervical
cancer in Kenyan women. AIDS
2003;17(13):1963–68.
11. Anorlu RI, Orakwue CO,
Oyeneyin L, et al. Late
presentation of cervical cancer
in Lagos: what is responsible?
European Journal of
Gynaecological Oncology 2004;
25(6):729–32.
12. Rogo KO, Omany J, Onyango JN,
et al. Carcinoma of the cervix in
the African setting. International
Journal of Gynecology &
Obstetrics 1990;33:249–55.
13. Chirenje ZM, Rusakaniko S,
Akino V, et al. A review of
cervical cancer patients
presenting in Harare and
Parirenyatwa Hospitals in 1998.
Central African Journal of
Medicine 2000;46(10):264–67.
14. Levin V, el Gueddari B,
Meghzifene A. Radiation
therapy in Africa: distribution
and equipment. Radiotherapy
and Oncology 1997;52:79–83.
15. Cronje HS. Screening for
cervical cancer in developing
countries. International Journal
of Gynecology & Obstetrics
2004;84:101–08.
16. Schmauz R, Okong P, de Villiers
EM, et al. Multiple infections in
cases of cervical cancer from a
high incidence area in tropical
Africa. International Journal of
Cancer 1989;43:805–09.
17. Serwadda D, Wawer MJ, Shah
KV, et al. Use of a hybrid capture
assay of self-collected vaginal
swabs in rural Uganda for
detection of human papilloma-
virus. Journal of Infectious
Diseases 1999;180(4):1316–19.
18. Bayo S, Bosch FX, de Sanjose S,
et al. Risk factors of invasive
cervical cancer in Mali.
International Journal of
Epidemiology 2002;31:202–09.
19. Chaouki N, Bosch FX, Munoz N,
et al. The viral origin of cervical
cancer in Rabat, Morocco.
International Journal of Cancer
1998;75(4):546–54.
20. Brinton LA, Reeves WC, Brenes
MM, et al. Parity as a risk factor
for cervical cancer. American
Journal of Epidemiology 1989;
130:486–96.
21. Hildesheim A, Herrero R, Castle
PE, et al. HPV co-factors related
to the development of cervical
cancer: results from a
population-based study in Costa
Rica. British Journal Cancer
2001;84(9):1219–26.
22. Munoz N, Franceschi S, Bosetti
C, et al. Role of parity and
human papillomavirus in
cervical cancer. The IARC
multicentre case-control study.
Lancet 2002;359:1093–101.
23. Palacio-Mejía LS, Range-Gomez
G, Hernandez Avila M, et al.
Cervical cancer, a disease of
poverty: mortality difference
between urban and rural areas in
Mexico. Salud Pública de
México 2003;45(Suppl 3):
S315–25.
24. Denny L. The prevention of
cervical cancer in the developing
world. BJOG 2005;112:1204–12.
25. Hawes SE, Kiviat NB. Are genital
infections and inflammation
cofactors in the pathogenesis of
invasive cervical cancer?
Journal of National Cancer
Institute 2002;94:1592–93.
26. Smith JS, Herrero R, Bosetti C,
et al. Herpes simplex virus-2
as a human papillomavirus
cofactor in the aetiology of
invasive cervical cancer. Journal
of National Cancer Institute
2002;94:1604–10.
27. Smith JS, Muñoz N, Herrero R,
et al. Evidence for Chlamydia
trachomatis as a human
papillomavirus cofactor in the
aetiology of invasive cervical
cancer in Brazil and the
Philippines. Journal of
Infectious Diseases 2002;185:
324–31.
28. Wallin KL, Wiklund F,
Luostarinen T, et al. A
population-based prospective
study of Chlamydia trachomatis
infection and cervical
carcinoma. International Journal
of Cancer 2002;101:371–74.
47
 RI Anorlu / Reproductive Health Matters 2008;16(32):41–49
29. Skapinyecz J, Smid I, Horvath A,
et al. Pelvic inflammatory
disease is a risk factor for
cervical cancer. European
Journal of Gynaecological
Oncology 2003;24(5):401–04.
30. Maiman M, Fruchter RG, Sedlis
A, et al. Prevalence, risk factors,
and accuracy of cytologic
screening for cervical
intraepithelial neoplasia in
women with the human
immunodeficiency virus.
Gynaecologic Oncology 1998;
68:233–39.
31. Wright TC Jr, Ellerbrock TV,
Chiasson MA, et al. Cervical
intraepithelial neoplasia in
women infected with human
immunodeficiency virus:
prevalence, risk factors, and
validity of Papanicolaou smears.
Obstetrics and Gynecology
1994;84(4):591–97.
32. La Ruche G, You B,
Mensah-Ado I, et al. Human
papillomavirus and human
immunodeficiency virus
infections: relation with
cervical dysplasia-neoplasia in
African women. International
Journal of Cancer 1998;76:
482–86.
33. Temmerman M, Tyndall MW,
Kidula N, et al. Risk factors for
human papillomavirus and
cervical precancerous lesions:
the role of concurrent HIV-1
infection. International Journal
Gynecology and Obstetrics
1999;65:171–78.
34. Moodley M, Moodley J,
Kleinschmidt I. Invasive cervical
cancer and human
immunodeficiency virus (HIV)
infection: a South African
perspective. International
Journal of Gynecological Cancer
2001;11(3):194–97.
35. Hawes SE, Critchlow CW,
Faye-Niang MA, et al. Increased
risk of high-grade cervical
squamous intraepithelial lesions
and invasive cervical cancer
among African women with
human immunodeficiency virus
Type 1 and 2 infections. Journal
48
of Infectious Diseases 2003;188:
555–63.
36. Chirenje ZM. HIV and cancer of
the cervix. Best Practice and
Research Clinical Obstetrics
Gynaecology 2005;19(2):
269–76.
37. Moodley JR, Hoffman M,
Carrara H, et al. HIV and
pre-neoplastic and neoplastic
lesions of the cervix in South
Africa: a case-control study.
BMC Cancer 2006;6135.
38. Kahesa C, Mwaiselage J,
Wabinga HR, et al. Association
between invasive cancer of the
cervix and HIV-1 infection in
Tanzania: the need for dual
screening. BioMed Central
Public Health 2008;8:262.
39. UNAIDS. AIDS Epidermic
Update, 2008.
40. Buga GA. Cervical cancer
awareness and risk factors
among female university
students. East African Medical
Journal 1998;75(7):411–16.
41. Ajayi IO, Adewole IF. Knowledge
and attitude of out patients'
attendants in Nigeria to cervical
cancer. Central African Journal
of Medicine 1998;44(2):41–44.
42. Wellensiek N, Moodley M,
Moodley J, et al. Knowledge of
cervical cancer screening and
use of cervical screening
facilities among women from
various socioeconomic
backgrounds in Durban,
Kwazulu Natal, South Africa.
International Journal of
Gynecological Cancer 2002;12:
376–82.
43. Anorlu RI, Banjo AAF,
Odoemhum C, et al. Cervical
cancer and cervical cancer
screening: level of awareness in
women attending a primary
health care facility in Lagos.
Nigeria Postgraduate Medical
Journal 2000;70:25–28.
44. Gichangi P, Estamble B, Bwayo
J, et al. Knowledge and practice
about cervical cancer and Pap
smear testing among patients at
Kenyatta National Hospital,
Nairobi, Kenya. International
Journal of Gynecological Cancer
2003;13:827–33.
45. Kidanto HL, Kilewo CD, Moshiro
C. Cancer of the cervix:
knowledge and attitudes of
female patients admitted at
Muhimbili National Hospital,
Dar es Salaam. East African
Medical Journal 2002;79:467–69.
46. Tarwireyi F, Chirenje ZM,
Rusakaniko S. Cancer of the
cervix: knowledge, beliefs and
screening behaviours of health
workers in Mudzi District in
Mashonaland East Province,
Zimbabwe. Central African
Journal of Medicine 2003;49:
83–86.
47. Ayinde OA, Omigbodun AO.
Knowledge, attitude and
practices related to prevention of
cancer of the cervix among
female health workers in Ibadan.
Journal of Obstetrics and
Gynaecology 2003;23(1):55–58.
48. Anya SE, Oshi DC, Nwosu SO,
et al. Knowledge, attitude, and
practice of female health
professionals regarding cervical
cancer and Pap smear. Nigerian
Journal of Medicine 2005;14(3):
283–86.
49. Clifford GM, Gallus S, Herrero R,
et al. Worldwide distribution of
human papillomavirus types in
cytologically normal women in
the International Agency for
Research on Cancer HPV
prevalence surveys: a pooled
analysis. Lancet 2005;366:
991–98.
50. Kamal SM, El Sayed Khalifa K.
Immune modulation by
helminthic infections: worms
and viral infections. Parasite
Immunology 2006;28:483–96.
51. Castellsagu X, Klaustermeier J,
Carla Carrilho C, et al.
Vaccine-related HPV genotypes
in women with and without
cervical cancer in Mozambique:
Burden and potential for
prevention. International
Journal of Cancer 2008;122:
1901–04.
52. Odida M, de Sanjosé S, Quint W,
et al. Human papillomavirus
 RI Anorlu / Reproductive Health Matters 2008;16(32):41–49

type distribution in invasive
cervical cancer in Uganda.
BioMed Central Infectious
Diseases 2008;8:85.
53. Woto-Gaye G, Critchlow C,
Kiviat N, et al. Cytological
detection of cervical cancer in
black Africa: what are the
perspectives? Bulletin du Cancer
1996;83(5):407–09.
54. Anorlu RI, Rabiu KA, Abudu OO,
et al. Cervical cancer screening
practices among general
practitioners in Lagos, Nigeria.
Journal of Obstetrics and
Gynaecology 2007;27(2):181–84.
55. Denny L, Quinn M,
Sankaranarayanan R. Screening
for cervical cancer in developing
countries. Vaccine 2006;
24(Suppl 3):S3/71–S3/77.
56. Chirenje ZM, Rusakaniko S,
Kirumbi L, et al. Situation
analysis for cervical cancer
diagnosis and treatment in east,
central and southern African
countries. Bulletin of WHO
2001;79:127–32.
57. Omigbodun AO, Ayinde OA. The
management of abnormal
cervical smears by Nigerian
gynaecologists. International
Journal Gynecology Obstetrics
2005;88:340–41.
58. Noah HE, Iyoke CA. Abnormal
Pap smears: a comparison of
total abdominal hysterectomy
and cone biopsy in
management. Journal of
Obstetrics and Gynaecology
2006;26(1):48–51.
59. Stewart BW, Kleihues P. World
Cancer Report. Lyon: IARC
Press; 2003.
60. Ashraf H. Poor nations need
more help to slow growing
cancer burden. Lancet 2003;
361:2209.
61. Jones S. Cancer in the
developing world: a call for
action. British Medical Journal
1999;319:505–09.
62. Sepulveda C, Habiyambere V,
Amandua J, et al. Quality care
at end of life in Africa. British
Medical Journal 2003;327:
209–13.
63. Murray SA, Grant E, Grant A,
et al. Dying from cancer in
developed and developing
countries: lessons from two
qualitative interview studies of
patients and their caretakers.
British Medical Journal 2003;
326:368–72.
64. Harding R, Profrene J,
Higginson PJ. Palliative care in
sub-Saharan Africa. Lancet
2005;365:1971–77.
65. Merriman A, Kaur M. Palliative
care in Africa: an appraisal.
Lancet 2005;365:1909–11.

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.
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.

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