A literature review on cancer of the cervix

Commissioned by Soul City for the Soul City 7

research process

June 2003

Prepared by
Dr M Kawonga

Women’s Health Project

University of the Witwatersrand Johannesburg

1. Introduction

1.1. Burden of disease

Cancer of the cervix is a significant public health problem globally,

especially in developing countries where it is the most common cancer in

women. Developing countries bear a disproportionate burden of the

disease, experiencing age-standardised mortality rate that are twice

those experienced in developed countries. Every year, approximately half

a million new cases of cancer of the cervix are reported globally, 80% of

which occur developing countries, where the disease is also the leading

cause of cancer-related death among women1,2. The huge disparities in

morbidity and mortality between developed and developing countries exist

largely because over the last few decades, developed countries have

implemented effective programmes for the prevention of cancer of the

cervix, in some countries reducing incidence and mortality by up to

80%1,2,3.

Southern Africa has one of the highest reported age-standardised

incidence rates of cancer of the cervix (higher than 40 per 100,000

women) 1 and existing data indicates that the incidence of disease is

actually increasing in some parts of Sub-Saharan Africa1. In South

Africa, cancer of the cervix causes significant cancer-related morbidity

and mortality among women4. It has been estimated that 5000 new cases

of the disease are reported annually, accounting for 16.7% of all cancers

reported annually in the country5. Though the disease is the second most

common cancer among all women, amongst black women it is the

commonest 6. Though easily preventable, it is the leading cause of cancer

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death amongst women in South Africa5,6, accounting for about 1500

deaths annually. However, death rates are differentially distributed in

the different ethnic groups, the highest mortality occurring in Black

women (25 per 100 000 women) and the lowest in White women (5 per 100

000 women) 7. Though this data was reported in the late 1980’s it is

unlikely that these patterns have changed much over the last 20 years.

These differences in mortality by race reflect past and present

differential access to cancer of the cervix prevention programmes among

the races in South Africa.

1.2. What is cancer of the cervix?

Cancer in general can be described as an abnormal growth of cells. Cancer

of the cervix is a cancer involving the squamous cells of the cervix. Thus,

cancer of the cervix means there is “abnormal growth” of the squamous

cells of the cervix (commonly referred to as the mouth of the uterus).

That is the squamous cells of the cervix start “behaving” in a way that

they shouldn’t – they grow at an abnormally fast rate, function

differently and start looking different from the normal squamous cells of

the cervix. At a more advanced stage, the cancer cells spread to

surrounding tissue such as the bladder, and even spread to distant ti ssue

such as bones and lungs, through the blood stream.

What causes cancer of the cervix?

The primary underlying cause of cancer of the cervix is Human Papilloma

Virus (HPV) 8,9,10. HPV is a common sexually-transmitted disease that does

not always cause symptomatic disease in infected individuals. Existing

evidence indicates that more than 97% of all cancers of the cervix are

associated with persistent infection HPV.

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Cancer of the cervix is a disease with a long latent period, which means it

develops over a long period of time. The natural history of the disease is

such that the disease is induced by HPV and persistent HPV infection

progresses onto a pre-invasive (pre-cancer) stage, characterised by the

presence of pre-cancerous cells in the cervix (broadly called dysplasia).

Women are most commonly infected with HPV in their teens, 20s, or early

30s, but it may take as long as 15-20 years for the disease to progress

from HPV infection through low-grade to high-grade dysplasia and finally

to cancer of the cervix. High grade dysplasia is a precursor for cancer of

the cervix. The natural history of the disease is illustrated in figure 1.

What are the main risk factors?

Age: Any woman who has ever had sex is at risk of developing cancer of

the cervix, but the risk increases as a woman gets older. Currently, age is

the most reliable predictor of risk for cancer of the cervix. The risk is

greater in women over 35 years of age.

HPV infection: not all women who are infected with HPV develop cancer of

the cervix and it is not currently possible to predict which women with

HPV infection will actually develop cancer of the cervix. In fact, only

about 5% of women infected with HPV go on to develop cancer of the

cervix later in life1. However, in recent years, research ha s shown that

particular types of HPV (high risk types) , in association with other co-

factors, such as smoking and immune suppression, are largely responsible

for most cases of cancer of the cervix8,9,10. Thus, women who are infected

with these high risk types of HPV are considered to be at higher risk of

developing cancer of the cervix than women infected with the other low

risk types of HPV. Furthermore, women with persistent HPV infection

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who are over the age of 35 years are at greater risk of developing the

precursor lesions of cancer of the cervix. A lot is not yet known about the

exact nature of the role of HPV in the development of cancer of the

cervix, but some facts are certain:

o
HPV infection does precede high-grade dysplasia8
o
Persistent infection with HPV plays a central role in the

development of cervical dysplasia11, 12

o
High risk HPV infection is a good predictor of subsequent high

grade dysplasia in young women, and an even better predictor in

older women.

Smoking1: tobacco use may influence whether a woman with dysplasia is

likely to develop cancer of the cervix.

Immune suppression1: exact role is not known, but immune suppression,

especially related to HIV infection, also plays a mediation role.

Hormonal factors1: use of contraceptives, early age at first birth and

high parity also play a role in mediating the disease.

Sexual behaviour 1: younger age at first intercourse and having multiple

sex partners have frequently been cited at risk factors for cancer of the

cervix, but these are now thought to be indicators of exposure to HPV

infection and are not independent risk factors.

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Figure 1: Natural History of Cancer of the cervix1

Source: PATH

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Prevention of cancer of the cervix

Cancer of the cervix is one of very few preventable cancers known in the

health field. There are two main strategies that can be used for

prevention:

1. Primary prevention

This involves preventing exposure to and transmission of HPV infection by

means of safer sex practices. Strategies that promote behaviour change

such as: abstinence from sexual intercourse, mutual monogamy , and the

use of barrier methods (male or female condoms), are included in primary

prevention. However, there is little evidence that infection with the HPV

types that cause cancer of the cervix can be avoided by condom use13.

Furthermore, because HPV infection is asymptomatic in most infected

individuals and sexual behaviour is not easy to control, stemming

transmission of HPV is a major public health challenge. In this regard,

primary prevention is not an effective prevention strategy at a population

level. It is an individual-based approach and thus would result in only a

minor reduction in incidence of cancer of the cervix. However, such an

approach can be integrated in existing behaviour-change programmes for

STI/HIV prevention but must be complementary to population-based

approaches (such as screening – see below).

Because of the limited effectiveness of behaviour change strategies,

researchers are increasingly looking into the possibility of vaccines that

could be used to prevent HPV infection. Most recently, researchers have

shown success with HPV vaccine research9. They found that

administration of an HPV vaccine to HPV-negative women reduced the

incidence of HPV infection and of cervical dysplasia. This study

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demonstrated the potential of HPV vaccines in reducing the incidence of

cancer of the cervix, but more work is required as results need further

evaluation.

2. Secondary prevention (cervical cancer screening)

Secondary prevention (early detection and treatment of disease) is the

most effective and realistic strategy for prevention of cancer of the

cervix. Secondary prevention of cancer of the cervix refers to early

detection and treatment of precursors [high grade pre-cancerous lesions]

of cancer of the cervix. Early detection of precursor s of cancer of the

cervix is achieved by cervical cancer screening. The point of cervical

cancer screening is to screen women into two groups:

i) Those women that are more likely to develop cancer of the

cervix (the presence of certain precancerous lesions in the

cervix of these women indicates that they are more likely to

develop cancer of the cervix). If these precancerous lesions are

identified and treated early, these women will not develop

cancer of the cervix.

ii) Those women that are less likely to develop cancer of the

cervix.

Because cancer of the cervix has a long latent period and starts with a

pre-invasive stage that is curable, it is possible to detect the disease

early and take necessary steps to prevent progression to life-threatening

incurable disease10. There are several cervical cancer screening methods

that can be employed in cervical cancer screening programmes. The

commonest and most well-established method is that of cervical cytology

(Box 1), the method currently recommended for use in South Africa.

Cervical cytology refers to the following process:

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 o Cells are scraped from the cervix by means of a simple test. The

simple test that is employed to obtain cells from the cervix is

called a Papanicolaou (Pap) smear.

o The cells are smeared and fixed onto a glass slide

o The slide is sent to a cytology laboratory to be examined under the

microscope for precancerous lesions. Precancerous lesions may be

of low grade or high grade.

o Women with high grade precancerous lesions are treated.

Box 1: Cervical cytology – screening for cancer of the cervix

o A Pap smear is done to obtain cells to detect abnormalities in the

cervix. Thus, it is a test that is predictive of disease and is not for

making a diagnosis of cancer of the cervix.

o The aim of cervical cytology is to detect cancer of the cervix in the

population at risk in its early asymptomatic form when it can be

successfully treated.

o If these abnormalities are detected early, they can be treated, thus

preventing morbidity and mortality associated with cancer of the

cervix.

o Early detection is possible because the natural history of cancer of the

cervix is such that it may take up to 20 years for the disease to

progress from pre-cancer lesions to invasive cancer.

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2. Cervical cancer screening Programmes
As previously mentioned, cancer of the cervix is a preventable disease.

Concrete evidence exists demonstrating that well planned and instituted

cervical cytology screening programmes can effectively reduce the

incidence and mortality due to cancer of the cervix14. For example, the

implementation of an organised national cervical cancer screening

programme in Finland in 1963 decreased the incidence of cancer of the

cervix to 5.5 per 100,000 women, one of the lowest incidents in the

world2. On the other hand the large numbers of premature deaths due to

cancer of the cervix in developing countries are attributed to the lack of

effective cervical cancer screening programmes in those countries.

Studies have shown that only about 5% of women in developing have had a

Pap smear, compared to more than 40% of women in many developed

countries.

The challenges involved in preventing cancer of the cervix in low resource

settings are immense. In order to effectively reduce incidence and

mortality from cancer of the cervix, a cervical cytology screening

programme must target women most at risk (older women) and must have

a number of essential components1, 15:

o Information, education and communication programme using

culturally-appropriate field-based strategies targeted at both men

and women in the community to ensure the appropriate age group

for cervical cancer screening attends for the service

o Education and training of service providers – to increase awareness

about the screening programme and upgrade their skills

o Training service providers in technical skills

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 o Training health providers in counselling skills – to enable

them to provide appropriate information to women and

allay fears and anxieties about the procedure

o Provision of cervical smears in appropriately equipped health

facilities

o System for delivering specimens to cytology laboratories and

reporting cytology results back to health facilities

o Mechanisms to ensure results of Pap smears are given to clients,

including follow-up of women with abnormal results who do not

return for results

o Setting up referral systems to ensure patients with abnormal Pap

smear results are referred to the appropriate level of care for

further tests and treatment

o Facilities for treatment of precursor lesions and cancer of the

cervix must be in place

o Systems in place to collect statistics to enable monitoring and

evaluation of the programme

No organised national screening programmes are in place in any of the

Sub-Saharan African countries, most of which have female populations at

high risk for cancer of the cervix2. Where cervical cancer screening

services are available in the developing countries of Latin America, Africa

and Asia, they have had limited impact if any, on incidence and

mortality 1,2. The reasons for this limited impact include1,2,16:

o Programmes are not organised and are mainly opportunistic.

Opportunistic screening services usually target younger women,

who are at low risk for precursors of cancer of the cervix. In

addition, because it is less effective, opportunistic screening is

more costly than organised screening programme.

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 o Pap smear testing is of poor quality due to inadequate training of

screeners or poor quality laboratory services;

o Inadequate number of trained cytologists to examine specimens

o Poor utilisation of services by women due to lack of appropriate

out-reach programmes to increase awareness, cultural barriers

(gynaecological examination is cause of embarrassment or a taboo)

or health service barriers.

o Inadequate investment of resources to maintain an organised

screening service

It is evident from the above description of the components of a cytology-

based cervical cancer screening programme that such a multi-faceted

programme would be a challenge to implement in low-resource settings17,18.

However, it is not an impossible task. In fact, guidelines for

implementation in low-resource settings have been developed1.

Furthermore, a study in East, Central and Southern African countries

found that though the basic infrastructure for provision of cervical

cytology was available, it was not optimally utilised and screening coverage

remained extremely low19.

Notwithstanding the limited resources and numerous competing priorities

in developing countries, it undisputable that action must be taken to

prevent the numerous premature deaths that occur due to cancer of the

cervix annually. The consequences of not taking action are potentially

grave, including:

o Impact on the health of women in society: increased morbidity and

mortality. Social impact of loss of mothers, carers at a productive

phase of their lives.

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 o Impact on health services: it is much more costly to treat women

with already established cancer (highly specialised health care are

required, usually at tertiary or academic hospital level) than to

treat early stages of disease that can be picked up by cervical

screening. Cost analyses applied to the South African setting and

elsewhere have established that treating only invasive cancer would

cost 80% more than screening and early treatment of precursors4.

In a bid to alleviate the cost of cervical screening programmes and

identify more feasible screening strategies for resource-poor countries,

researchers in South Africa and elsewhere are looking into alternatives

to Pap smears and cytology-based cervical screening programmes. It is

envisaged that less costly and less complex methods for cervical cancer

screening (such as provision of screening services as a one-stop service)

would be easier to implement and sustain in developing countries18, 20.

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3. Prevention of cancer of the cervix in South Africa

3.1. Historical context

Over the last three decades unsuccessful attempts have been made to

introduce a cervical screening programme in South Africa. Various

national policies were articulated, but rarely adequately implemented.

These varied from the Department of Health’s policy in the mid 70’s of

taking a Pap smear only if the cervix looked abnormal 4, to the Project

Screen Soweto opportunistic screening, to the Western Cape policy in the

mid 90’s, focussing on family planning clinic attendees. Previously, cervical

screening occurred in pockets around the country, often around academic

health institutions in urban centres and invariably linked to family

planning services4. Thus, those with good access to health care, who were

also often at lower risk for cancer of the cervix, had greater opportunity

to have Pap smears and were screened over and over, sometimes annually,

while those without access and beyond the age group of the family

planning clinic target group were often left out. Studies conducted in the

late 1980s in Khayelitsha found that 55% of women in the study had

never had a Pap smear 21 and a more recent multi-centre national study

found that 80% of women had never had a Pap smear 22. These findings

indicate that historical cervical cancer screening services had a low

population coverage and thus little impact on incidence or mortality.

Furthermore, the inequity of access to this crucial health service

produced and perpetuated disparities in morbidity and mortality between

black and white women and between urban and rural women.

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3.2. National policy for cervical cancer screening

In recent years, the National Department of Health (NDoH) has

demonstrated political commitment to addressing this important public

health problem by identifying cancer of the cervix as a national health

priority23. During 1999, NDoH’s National Cancer Control Programme

(NCCP) was adopted as South African health policy, a component of which

was a cervical cancer screening programme. The national cervical

screening policy states that every woman is entitled to three free

screening Pap smears (in the public sector) in her lifetime at 10-year

intervals, starting at the age of 30 years. The policy decision to screen all

women in South Africa over the age of 30 years was based on the best

available epidemiological data, taking into account resource constraints. A

recent national prevalence study found that occurrence of high grade

dysplasia was highest in women in their late 30s, validating the NDoH

rationale for commencing screening at the age of 30 years22. The policy

decisions regarding cervical scr eening were subsequently articulated in

the National Guideline for Cervical cancer screening Programme, which

provides a broad national framework for a national cervical cancer

screening programme 24.

These developments on the policy front pose a challenge to reproductive

health programme managers. National and Provincial Health Department

managers in Maternal, Child and Women’s Health (MCWH) directorates

are respectively tasked with developing a national strategy for and

implementing the national cervical cancer screening programme. The

MCWH Directorate at NDoH has led the process by establishing a

cervical cancer screening advisory committee to advise on the

development of a national strategy. A smaller task team is currently

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working on shaping the strategy before broad consultation with

stakeholders happens later this year. It is hoped the publication of a

national strategy will facilitate the implementation of an organised

national screening programme.

3.3. Programmes and services

Service provision

Though it is over two years since the National Guideline for a Cervical

Cancer Screening Programme was published, not much implementation has

happened on the ground in most provinces. Some commitment was however

demonstrated in the Gauteng and Western Cape provinces, where the

respective Provincial Governments earmarked funds for cervical cancer

screening during 2001 and 2002. However, the extra injection of

resources has not always translated into effective programme

implementation and the impacts are yet to be assessed. Most of the

other provinces have barely started preparing for provision of cervical

cancer screening, and few have made some moves toward implementation,

but there is clearly lack of uniformity across provinces. In the meantime,

the Women’s Health Project (WHP) and Women’s Health Research Unit

(WHRU) have been conducting a study in three districts (one each in

Gauteng, Western Cape and Limpopo provinces) to assess the feasibility

of implementing the national cervical cancer screening policy. Theirs and

other work in the country have identified barriers to the provision and/or

expansion of cervical cancer screening services, including:

q Programmatic and health service barriers: lack of management

capacity to plan for service services, services not in place, limited

access because services are only provided in urban centres or

hospitals, lack of appropriate equipment and poor infrastructure,

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 inadequate treatment services, poor communication between

health facilities and laboratories and between screening facilities

and treatment centres inadequate health information system to

monitor programme and failure to reach high-risk women (older

women).

q Barriers at provider level: few providers trained to provide Pap

smears, poor knowledge of cancer of the cervix and the rationale

for screening, poor awareness of the screening policy, providers

reluctant to provide the service as it is perceived as “extra work”

and because they do not agree with the provisions of the screening

policy – this results in missed opportunities for screening.

These problems highlight the need for a health systems development

approach to implementing cervical screening programmes. From the above

description, it is clear that a successful cervical screening programme

requires a whole lot more than just “taking Pap smears”. It is also

important to ensure that there are health systems in place to support the

screening programme.

It has been suggested that a substantial injection of resources and

infrastructure would be required to implement and sustain a cervical

cancer screening programme in this country, research has demonstrated

that even with limited investment in health systems and infrastructure, it

is possible to provide cervical smears and report results to clients22. To

curtail excessive expenditure on infrastructure, cervical cancer screening

services in this country should ideally be integrated within primary care

clinics and community health centres, utilising existing infrastructure for

provision of Pap smears.

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Community mobilisation

An information, education and communication programme (IEC) that aims

to increase awareness about cancer of the cervix and screening is an

essential component of a cervical cancer screening service. The

experience of Project Screen Soweto in the 1980s demonstrates this

point as services were set up, but women did not attend due to lack of

community education programmes25. Cervical cancer screening requires

women who have no symptoms of disease to attend a health service for a

procedure. This is a hu ge challenge because not many people like to

attend a health service when they are not “sick”. However, before women

can even attend a clinic to demand a Pap smear they need to know about

Pap smears and cancer of the cervix. Research conducted by the Medical

Research Council in KwaZulu-Natal and by WHP and WHRU indicates that

lack of awareness is one of the major barriers to women seeking cervical

cancer screening services. Some other barriers include:

q Fear of the procedure

q Women feel embarrassed about gynaecological examinations,

especially older women

q Socio-cultural barriers (it is considered to be “a woman’s

disease” that is not discussed openly so women are not “free” to

request the service even when they know about it)

q Myths and stigmas (e.g. according to health care workers,

communities associate Pap smears with HIV testing, though recent

surveys have failed to demonstrate this)

q Poor communication between health providers and women

attending health services – services not accessible to women

To bridge the information gaps and address these barriers requires a

comprehensive and sustained IEC programme with extensive community

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outreach. The purpose of this IEC programme would be to raise

awareness about cancer of the cervix and the importance of screening as

a preventive measure, to publicise the availability of screening services in

the public sector at clinic level, and to encourage women to attend health

services for screening according to the screening policy. Taking into

account the gender and socio-cultural barriers, it is imperative that both

women and men in the community are involved. From the experience of

WHRU and WHP, it is recommended that the IEC programme should be

developed and implemented in conjunction with community

representatives and utilise culturally-appropriate outreach strategies,

including:

Development and distribution of IEC materials: pamphlets and posters

should be developed in appropriate languages. Currently, there are no

national pamphlets and posters on cancer of the cervix other than the

pamphlets developed by NGOs such as CANSA association and WHP

and WHRU. IEC materials should include key messages that

effectively inform women, such as:

o What is cancer of the cervix and what is a Pap smear?

o Who is at risk of acquiring the disease – women older than 35

years of age are more at risk of developing the disease

o The target age group that should be screened

o Cancer of the cervix can be prevented and early lesions treated

o Pap smears are done to prevent cancer of the cervix

o The Pap smear test is simple and painless

o How frequently screening should be done

o The importance of returning for results

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 Ideally any health information messages developed should be tested

with members of the intended audience to ensure they are easily

understood and are culturally appropriate. One of the big challenges

for IEC programmes is how to provide information about cancer of the

cervix that does not present it primarily as a sexually-transmitted

infection (STI) and thus associated with promiscuity, and subject to

stigma. It has been suggested that once communities link cancer of

the cervix with STIs, they perceive Pap smears as a test for STIs and

so women may not want to do the test. Thus, the IEC messages need

to be presented in a manner that clearly highl ights that all women are

at risk, and age is the best predictor of risk. Some health education

groups have steered clear of mentioning the role of HPV in

development of cancer of the cervix, reasoning that not enough is

known about the disease anyway. I am not entirely convinced this is

ideal approach to the problem though.

Media: community radio stations to air programmes or make public

announcements and local and national newspapers to publish articles

about cancer of the cervix and screening. Our study found that more

than 75% of women attending health services listen to the radio and

the radio was the commonest source of information about these

topics.

Peer educator training: training appropriately selected members of

the community on cervical cancer scr eening so that they in turn

conduct workshops and give talks on cancer of the cervix within their

communities, while also distributing pamphlets.

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 Drama and photo-comic: these methods have been employed in the

Khayelitsha Cervical cancer screening Project. More information about

these is available from the project.

Most of these IEC strategies may improve knowledge, but ultimately the

aim is to see a change in practices, i.e. to see more women attending

services for Pap smears. However, very little work has been done to

evaluate the impact of various IEC strategies on women’s attendance for

screening. Thus it is difficult to determine which strategy works best.

However, a study in RSA found that pamphlets and even photo-comics are

not as effective as peer educator programmes.

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4. Some key debates
q Is an organised cytology-based screening programme a reality?

Screening involves substantial costs and many poor countries cannot

afford to set up a screening programme, especially a cytological-based

programme. There are on-going debates questioning the feasibility of an

organised cytology-based screening programme in this country. However,

evidence based on modelling shows it is achievable.

q Impact of HIV

There have been calls from clinicians for revision of the national

screening guidelines: to commence screening at an earlier age, or develop

an alternative screening schedule for HIV positive women. This is in light

of recent research suggesting the impact of HIV on dysplasia and cancer

of the cervix (early lesions of Cancer of the cervix are more persistent

in HIV + women; cancer of the cervix affects HIV + women at younger

age, is more aggressive and early lesions are more likely to recur after

treatment) 26.

q Alternative screening strategies

What is the most appropriate cervical screening method for this

country? Is the Pap smear the best way to go? What about other “one-

step” methods that, unlike cytology-based screening, do not require

repeated visits to health facility? There are no answers but work is on-

going on this issue. Dr L Denny is the best resource person for more

information on this issue.

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5. Key stakeholders
Some of the main actors in this area, at service provision, policy,

academic, non-governmental and community levels include:, including a

brief description of their activities. Some national actors include:

o CANSA association – mainly involved in health promotion

activities, including large scale production and dissemination of

IEC materials (pamphlets and posters).

o GAP - health promotion on various gender and reproductive

health topics, including cancer of the cervix

o Khayelitsha Cervical cancer screening Project, University of

Cape Town – have worked on cancer of the cervix in the area for

years. Running a comprehensive screening service in the area,

including development of photo comic called “Nokwezi’s story”,

which has been made into a video and development of edu-

drama. The group are also conducting research looking at

alternative strategies for screening.

o National Department of Health, Maternal Child and Women’s

Health (Women and Genetics Division) – spearheading the

development of a national strategy for cervical cancer screening

in order to give guidance for implementation to provinces,

regions and districts.

o PPASA – health promotion, community education: running a

project looking at ways of involving men in cervical screening.

o Women’s Health Project, University of the Witwatersrand –

conducting research looking at the ways of implementing the

screening policy, also involved in national strategy development.

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 o Women’s Health Research Unit (in society), University of

Capetown - conducting research to inform implementation of the

screening policy and involved in national strategy development.

Concluding remarks
There is certainly an urgent need for advocacy to place cancer of the

cervix high on the programme planning agenda at provincial and regional

levels. Currently, breast cancer receives a lot of coverage in the media,

and yet cancer of the cervix causes significantly more deaths. There is a

lot of room for greater media involvement to increase the profile of

cancer of the cervix among policy makers, managers, service providers

and communities at large.

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Dr M. Kawonga. WHP
REFERENCES

1
Programme for Appropriate Technology in Health. Planning Appropriate
Cancer of the cervix Prevention programmes. 2nd edition, 2000.

2
Sankaranarayanan R, Budukh A M, Rajkumar R. Effective Screening
Programmes for Cancer of the cervix in Low- and Middle-income
developing Countries. Bulletin of the World Health Organisation. 2001, 79
(10)

3
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