Special Theme Noncommunicable Diseases

Effective screening programmes for cervical cancer

in low- and middle-income developing countries
Rengaswamy Sankaranarayanan,1 Atul Madhukar Budukh,2 & Rajamanickam Rajkumar 3

Abstract Cervical cancer is an important public health problem among adult women in developing countries in
South and Central America, sub-Saharan Africa, and south and south-east Asia. Frequently repeated cytology
screening programmes either organized or opportunistic have led to a large decline in cervical cancer
incidence and mortality in developed countries. In contrast, cervical cancer remains largely uncontrolled in high-risk
developing countries because of ineffective or no screening. This article briefly reviews the experience from existing
screening and research initiatives in developing countries.
Substantial costs are involved in providing the infrastructure, manpower, consumables, follow-up and
surveillance for both organized and opportunistic screening programmes for cervical cancer. Owing to their limited
health care resources, developing countries cannot afford the models of frequently repeated screening of women
over a wide age range that are used in developed countries. Many low-income developing countries, including most
in sub-Saharan Africa, have neither the resources nor the capacity for their health services to organize and sustain
any kind of screening programme. Middle-income developing countries, which currently provide inefficient
screening, should reorganize their programmes in the light of experiences from other countries and lessons from
their past failures. Middle-income countries intending to organize a new screening programme should start first in a
limited geographical area, before considering any expansion. It is also more realistic and effective to target the
screening on high-risk women once or twice in their lifetime using a highly sensitive test, with an emphasis on high
coverage (>80%) of the targeted population.
Efforts to organize an effective screening programme in these developing countries will have to find
adequate financial resources, develop the infrastructure, train the needed manpower, and elaborate surveillance
mechanisms for screening, investigating, treating, and following up the targeted women. The findings from the
large body of research on various screening approaches carried out in developing countries and from the available
managerial guidelines should be taken into account when reorganizing existing programmes and when considering
new screening initiatives.

Keywords Cervix neoplasms/diagnosis/prevention and control; Cervix uteri/cytology; Vaginal smears/utilization;

Mass screening/organization and administration; Developing countries; Central America; South America; Africa
South of the Sahara; South Africa; India; South-East Asia (source: MeSH ).
Mots cles Tumeur col uterus/diagnostic/prevention et controle; Col uterin/cytologie; Frottis vaginal/utilisation;
Depistage systematique/organisation et administration; Pays en developpement; Amerique centrale; Amerique du
Sud; Afrique subsaharienne; Afrique du Sud; Inde; Asie Sud-Est (source: INSERM ).
Palabras clave Neoplasmas del cuello uterino/diagnostico/prevencion y control; Cuello uterino/citologa; Frotis
vaginal/utilizacion; Tamizaje masivo/organizacion y administracion; Pases en desarrollo; America Central; America
del Sur; Africa del Sur del Sahara; Sudafrica; India; Asia Sudoriental (fuente: BIREME ).
Bulletin of the World Health Organization, 2001, 79: 954962.

Voir page 960 le resume en francais. En la pagina 961 figura un resumen en espanol.

Introduction and Central America, sub-Saharan Africa, and south

and south-east Asia, where it is the most or second
Cervical cancer is an important public health problem most common cancer among women. The vast
for adult women in developing countries in South majority of cervical cancer cases are caused by
infection with certain subtypes of human papilloma
1
Scientist, International Agency for Research on Cancer, 150 cours virus (HPV), a sexually transmitted virus that infects
Albert Thomas, 69372 Lyon Cedex 08, France (email: [email protected]). cells and may result in precancerous lesions and
Correspondence should be addressed to this author.
2 invasive cancer (1). Developing countries accounted
Programme Manager, Cervical Cancer Prevention Programme, Tata
Memorial Centre Rural Cancer Project, Nargis Dutt Memorial Cancer for 370 000 out of a total of 466 000 cases of cervical
Hospital, Barshi, Solapur District, Maharashtra, India. cancer that were estimated to occur in the world in
3
Medical Officer, Christian Fellowship Community Health Centre, the year 2000 (2). Worldwide, cervical cancer claims
Ambillikai, Dindigul District, Tamil Nadu, India. the lives of 231 000 women annually, over 80% of
Ref. No. 01-1311 whom live in developing countries. A conservative

954 # World Health Organization 2001 Bulletin of the World Health Organization, 2001, 79 (10)
 Screening of cervical cancer in developing countries

estimate of the global prevalence (based on the high. In most developed countries, women are
number of patients still alive 5 years after the advised to have their first smear test soon after
diagnosis) suggests that each year there are 1.4 mil- becoming sexually active and subsequently once
lion cases of clinically recognized cervical cancer. It is every 15 years. Many national guidelines are
also likely that 37 million women worldwide may currently moving towards less frequent smear tests
have high grade dysplasia. (once every 35 years) because it is recognized that
Some of the developing countries that have cervical lesions develop slowly over several years.
data on cancer incidence and/or mortality have Women with low-grade lesions are generally advised
registered either a stable or slowly declining trend in to return for routine follow-up smears. Women with
cervical cancer incidence, most likely due to socio- high-grade precursor lesions are further evaluated via
demographic changes rather than to early detection/ colposcopy, biopsy, and subsequent treatment of
prevention efforts (3). On the other hand, some confirmed lesions. Organized programmes with
regions in sub-Saharan Africa have registered an systematic call, recall, follow-up and surveillance
increased incidence in recent years (4). Despite the systems that have shown the greatest effect (e.g. in
declining trends in incidence observed in some Finland and Iceland), even though they use fewer
regions, the total burden of cervical cancer is rising in resources than unorganized programmes (e.g. in the
high-risk developing countries, mostly due to USA).
increasing populations. Cervical cytology is considered to be a very
In developed countries, initiation and suste- specific test for high-grade precancerous lesions or
nance of cervical cytology programmes involving the cancer but, even if the quality of collection and
screening of sexually active women annually, or once spreading of cells, fixation, and staining of smears,
in every 25 years, have resulted in a large decline in and reporting by well-trained technicians and
cervical cancer incidence and mortality (Fig. 1 and cytopathologists are good, its sensitivity is only
Fig. 2) over the last 4050 years (58). The aim of moderate. The results of meta-analyses suggest that
these programmes is to detect precancerous lesions cytological screening has a very wide range of
and treat them before they progress to invasive sensitivity to detect lesions (11, 12); for example,
cancer. In contrast, the risks of disease and death cytology is estimated to have a mean sensitivity of
from such lesions have remained largely uncontrolled 58% and a mean specificity of 69% (11). Also,
in high-risk developing countries, mostly because of estimates of sensitivity of conventional cytology (for
the lack of screening programmes or because of their high-grade lesions) vary greatly in individual studies,
ineffectiveness. This paper reviews existing experi- by as much as 3087% (mean, 47%) (12). Both
ences, achievements, constraints, and lessons learned sampling and detection (reading) errors probably
in community-based, cervical cancer intervention contribute to the low-to-moderate sensitivity of
programmes in developing countries. The sensitivity cytology. Assuming that cytology is only moderately
and specificity values that we report for various sensitive, it seems likely that the observed decline in
screening tests correspond to the detection of high- the risk of cervical cancer in developed countries may
grade lesions (cervical intraepithelial neoplasia II and have arisen from the high screening frequency.
III) and invasive cancer. Cervical neoplasia is a disease that progresses slowly,
and many low-grade precancerous lesions regress
spontaneously or do not progress further. High-
Cervical cytology screening grade lesions that are missed in a given screening
round would probably be detected during the
programmes worldwide subsequent rounds in a frequently repeated cytolo-
To date, cervical cancer prevention efforts worldwide gical screening programme. A critical review of
have focused on screening sexually active women conventional cervical cytology in developed coun-
using cytology smears and treating precancerous tries, where it was shown to be effective in cervical
lesions. It has been widely believed that invasive cancer control, provides valuable leads for public
cervical cancer develops from dysplastic precursor health policy decisions in low-resource environ-
lesions, progressing steadily from mild to moderate to ments. Current procedures, involving screening
severe dysplasia, then to carcinoma in situ, and finally women once every 15 years, have considerable cost
to cancer. It now appears that the direct precursor of and resource implications. The limited health care
cervical cancer is high-grade dysplasia, which in about budgets in most developing countries preclude
a third of instances may progress to cervical cancer initiating and sustaining such programmes, even in
over a period of 1015 years, while most low-grade a limited geographic setting.
dysplasias regress spontaneously (9, 10).
Even though the impact of cytology screening
has never been proved through randomized trials, it Cervical cancer screening programmes
has been shown to be effective in reducing the
incidence and mortality from cervical cancer in
in developing countries
developed countries (58). The incidence of cervical Cytology-based screening programmes for cervical
cancer can be reduced by as much as 80% if the cancer have been introduced in some developing
quality, coverage, and follow-up of screening are countries, particularly in South and Central America,

Bulletin of the World Health Organization, 2001, 79 (10) 955

Special Theme Noncommunicable Diseases

Cervical cancer mortality rates did not change much

in the period from 1970 to 1985 after the introduc-
tion of the programme (Fig. 2). A recent evaluation of
the programme indicated that more than 80% of the
married women in Chile have been screened at least
once. The programme was reorganized in the early
1990s, and mortality from cervical cancer has
subsequently begun to decline.
Colombia. In Colombia, the Colombian Na-
tional League against Cancer (a part of the public
health system) and private organizations such as
PROFAMILIA have been offering cytology screening
since the 1970s (13). Subsequently, the cervical cancer
mortality rate in the country has, however, remained
stable (Fig. 2). Nevertheless, there has been a steady
and substantial decline in the incidence of cervical
cancer in the city of Cali (Fig. 1), possibly as a result of
the ongoing screening activities carried out there since
1967, including educational and early detection
campaigns. In 1990, a 5-year nationwide cervical
cancer control programme was initiated to provide
cytology smears to more than 60% of women aged 25
69 years over a 3-year period and to provide follow-up
to over 90% of the women screened. The programme
trained over 4000 nurses, 40 gynaecologists, and
36 pathologists. Cytology services were centralized
and extensive community information and education
campaigns were launched. Midway through the
project, the centralized national health care system
was reorganized and several services were decentra-
lized to encourage the creation of efficient networks of
services and surveillance. However, 5 years after the
initiation of the programme, cervical cancer mortality
data suggested that the situation had remained
unchanged.
Costa Rica. In Costa Rica nationwide cytology
services have been available to women aged
515 years since 1970. Information/education cam-
paigns have been used to encourage sexually active
women to have annual cytology smears. Invariably in
all pelvic examinations a Pap smear is also obtained
(14). Annually, around 250 000 smears have been
performed and reported. Coverage has varied
considerably according to region, with coverage of
rural areas being inadequate in each given round of
over the last 30 years, but generally have achieved screening. Despite this, it seems that more than 85%
very limited success. In contrast, a comparison of the of eligible women have been screened at least once.
performance of conventional cytology and its Though cervical cancer incidence remained virtually
potential alternatives in detecting cervical cancer unchanged from 1983 to 1991, a significant decline
and its precursors is ongoing in Asia, Africa, and Latin has been observed more recently (i.e. a 3.6% decrease
America. Both these approaches are briefly reviewed in annual incidence in 199397 compared with that in
below since they provide potentially useful informa- 198892) (Fig.1). However, the cervical cancer
tion for directing public health policy on introducing mortality rates have remained unchanged over the
new and effective programmes in low-resource last 25 years (Fig. 2) (15, 16). In an ongoing cohort
settings and for reorganizing existing programmes. study of more than 9000 women in Guanacaste
Province, the cross-sectional sensitivity of HPV
South and Central America testing was found to be higher than that of
Since the 1970s there have been efforts to organize conventional cytology (88% versus 78%) but the
cervical cytology screening programmes nationally or specificity was lower (89% versus 94%) (17).
regionally in selected Latin American countries. Cuba. In Cuba a cervical cytology screening
Chile. In Chile the cervical cancer screening pro- programme, offering smears every two years to
gramme has been in operation since the early 1970s. women aged 520 years, was implemented through

956 Bulletin of the World Health Organization, 2001, 79 (10)

 Screening of cervical cancer in developing countries

the primary health care services in 1968 (18). Pap nistic cytology smears is carried out in different
smears are taken by a nurse in the family doctors regions.
office and are processed in one of the 36 regional Peru has also recorded a high incidence of
cytology laboratories. It has been suggested that cervical cancer; there are no organized screening
more than 80% of Cuban women aged 2060 years programmes in the country. A large demonstration
have been screened at least once. However, no project of cervical cancer screening with visual
reduction in cervical cancer incidence and mortality inspection with acetic acid (VIA) is currently on-
(Fig. 2) has been observed since the introduction of going in San Martin region of Peru.
the programme. An early detection programme for cervical
Mexico. A national cervical cancer screening cancer was established in Puerto Rico in the 1960s.
programme was initiated in Mexico in 1974 (19, 20) This covered the metropolitan areas until 1962, and
and now operates in the Federal District and all was later expanded to all health regions of the island.
31 states of the country. Cytology smears are offered Cytology smears are offered to women aged
annually to women aged 2565 years and the 515 years and about 150 000 smears are processed
programme is integrated with the existing health annually. The incidence and mortality from cervical
care services. Mexico reportedly had 463 cyto- cancer have declined steadily over the last three
technologists, 251 reading centres, 70 dysplasia decades (Fig. 1 and Fig. 2). The average, annual age-
clinics, and 540 gynaecological oncology units in standardized incidence dropped from 38 per
1996. However, the infrastructure and resources 100 000 women during 195054 to 19.9 per
were sufficient to carry out only 3.5 million smears 100 000 women in 1990, and the mortality rate
annually for a target population of 16.5 million dropped from 19.1 per 100 000 women to 5.2 per
women (data for 1996); annual screening was 100 000 women in the same period.
nevertheless the norm for the programme.
Realistically, this infrastructure is sufficient to screen Sub-Saharan Africa
the targeted women only once every 5 years. The There are no organized or opportunistic screening
Ministry of Health (MOH) has a total of 120 cervical programmes for cervical cancer in any of the high-
cancer screening centres (CCSCs) where 230 cyto- risk sub-Saharan African countries. While data from
technologists are employed. These screening centres Uganda indicate that, at least in some areas of the
are intended to carry out cytology screening of country, substantial increases in the incidence of
6.5 million women who are not covered by social cervical cancer may have occurred (4), there is no
security. The Mexican Institute for Social Security evidence of an increase in incidence over time in
(IMSS) is responsible for screening women covered Zimbabwe (23). Studies in Zimbabwe and South
by social security. In 1992, the MOHs screening Africa have assessed the performance characteristics
centres carried out 1.02 million smears and the IMSS of potentially alternative screening tests such as visual
1.3 million smears. There is a wide variation in the inspection with acetic acid (VIA) and HPV testing. A
coverage of women on the national level. Studies cross-sectional screening study in Zimbabwe re-
indicate that less than 30% of the women in rural ported that the sensitivity and specificity to detect
areas have been screened so far. There is no high-grade dysplasias and cancer was 77% and 64%,
systematic effort to coordinate the programme respectively, for VIA compared to 43% and 91% for
through a central organization for call, recall, and cytology (24). The sensitivity and specificity of HPV
follow-up of screened women. testing using Hybrid Capture II assay (Digene
An evaluation of the cervical cytology tests Corporation, Gaithersburg, USA) were 81% and
provided within the Mexican programme indicated 62%, respectively (25); the sensitivity and specificity
that the validity and reproducibility varied greatly of HPV testing was, respectively, 91% and 41% for
within and between the screening carried out by HIV-infected women and 62% and 75%, respec-
the MOH and the IMSS (21). Among the CCSCs tively, for HIV-negative women (26). It is also
the sensitivity to detect high-grade lesions varied reported that the sensitivity and specificity of VIA
from 46% to 90% and that of the specificity from and HPV testing, when used sequentially, was 64%
48% to 96%. The false-negative rate varied from and 82%, respectively (27).
10% to 54%, with an average false-negative rate of South Africa. The South African Institute of Medical
35%. Review of a random sample of 6011 nega- Research organized the infrastructure for mass
tive smears indicated that 64.0% of the smears screening of the female population of Soweto
were of insufficient quality. There has been no (Project Screen Soweto) so that 90 000 cytology
decline in mortality from cervical cancer in Mexico smears could be tested annually (28). However, the
since the initiation of the screening programme lack of a planned population education and motiva-
(Fig. 2) (22). tion programme resulted in poor participation of the
Brazil, Peru, and Puerto Rico. There are no target population in the programme. In a cross-
organized cervical cancer screening programmes in sectional study that addressed the comparative
Brazil. A high-risk of the disease (incidence >40 per performance of cytology, VIA, cervicography, and
100 000 women) is reported from the north-east HPV testing in South Africa, the sensitivity was
region. Low-level sporadic screening with opportu- found to be 78%, 67%, 53%, and 73%, respectively;

Bulletin of the World Health Organization, 2001, 79 (10) 957

Special Theme Noncommunicable Diseases

the specificity was 94%, 83%, 89%, and 86%, testing, VIA, and visual inspection with Lugols
respectively (29). In another study in South Africa, iodine (VILI) as well as the detection rates associated
HPV testing using self-collected vaginal samples was with them.
found to be more sensitive than cytology (66% versus
61%), but less specific (83% versus 88%) (30). In an
South Asia
earlier study in South Africa, the sensitivity of VIA
India. India accounts for one-fifth of the world
was found to be 65% (31). A recent study of the cost-
burden of cervical cancer. There are no organized or
effectiveness of several cervical cancer screening
high-level opportunistic screening programmes for
strategies, based on the South African experience,
cervical cancer in any of the provincial states. Data
indicated that strategies using VIA or HPV DNA
testing may offer attractive alternatives to cytology- from population-based cancer registries in different
based screening programmes in low-resource set- regions indicate a slow, but steady, decline in the
tings (32). When all the strategies were analysed on incidence of cervical cancer (Fig. 1). However, the
the basis of a single lifetime screening at age 35 years rates are still too high, particularly in the rural areas,
compared with no screening, it was found that HPV and the absolute number of cases is on the increase
testing, followed by treatment of screen-positive due to population growth. Efforts to improve
women at a second visit, cost US$ 39 per year of life awareness of the population have resulted in early
saved (27% reduction in cancer incidence); VIA, detection of and improved survival from cervical
coupled with immediate treatment of screen-positive cancer in a backward rural region in western India (33,
women at the first visit, was the next most cost- 34). Also in two subdistricts of western India where
effective (26% reduction in cancer incidence) and the literacy among women is less than 20% there have
was cost saving; cytology, followed by treatment of been attempts to evaluate the role of improved
screen-positive women at a second visit, was the least awareness in the early detection and control of
effective (19% reduction in cancer incidence) at a cervical cancer (35). Person-to-person and group
cost of US$ 81 per year of life saved (32). health education on cervical cancer were provided to
Currently, cytology smears are provided on 97 000 women in Madha Tehsil, Solapur district,
demand in antenatal, postnatal, gynaecology, and Maharashtra State, in western India; 79 000 women in
family planning clinics in South Africa. Work to Karmala Tehsil served as the control population. This
develop a cervical screening policy for South Africa, programme was initiated in 1995 and the preliminary
based on the models of natural history, has been results for 199599 indicate that, compared with the
ongoing for some time. It is proposed to initiate control area, in the intervention subdistrict a
screening at the age of 30 years with three smears substantially higher proportion of women presented
being carried out in a womans lifetime. However, with cervical cancer in earlier stages with significantly
there has been debate about both whether this policy reduced case fatality (Table 1).
should be implemented and how. A pilot project to Visual inspection-based approaches to cervical
set up screening services using the health systems cancer screening have been extensively investigated
development approach is currently being undertaken in India. The performance characteristics of unaided
by three provincial departments of health (Western visual inspection (without acetic acid), also known as
Cape, Northern Cape, and Gauteng) in cooperation downstaging, has been addressed in several studies
with nongovernmental organizations. This approach (36). This approach suffers from low sensitivity and
seeks to set up programme components such as specificity to detect cervical neoplasia, particularly the
reaching the target population, providing a compe- precursor lesions, and is no longer recommended as a
tent screening service, relaying the results, and screening approach. Currently there are several
organizing referral, investigation, treatment and ongoing, cross-sectional studies being carried out
follow-up of screening-positive women. It is ex- on other screening approaches such as VIA, VIA
pected that these tested methods will be applied in with magnification (VIAM), and VILI, as well as
the provinces and then nationally. HPV testing as alternative screening approaches.
A three-arm, prospective randomized interven- Results from two reported studies indicate that the
tion trial in South Africa is currently addressing the sensitivity of VIA to detect high-grade lesions was
comparative safety, acceptability and efficacy of similar or higher than that of conventional cytology
screening women with VIA and HPV DNA testing but that its specificity was lower (37, 38).
and immediately treating screen-positive women with There are three large, ongoing cluster-rando-
cryotherapy performed by nurses in a primary health mized intervention trials in India in Dindigul
care setting. Outcome measures include reduction of district (Tamil Nadu), in Mumbai, and in Osmanabad
high-grade cervical cancer precursors in treated versus district (Maharashtra) to evaluate the effectiveness
untreated women, followed over a 12-month period. of VIA, in reducing cervical cancer incidence and
Other countries. Cross-sectional/randomized mortality. The intervention programme in Osmana-
screening intervention studies are currently ongoing bad district aims to address the comparative efficacy
in several African countries Burkina Faso, Congo and cost-effectiveness of three different primary
(Brazzaville), Ghana, Guinea (Conakry), Kenya, Mali, screening approaches in reducing the incidence and
Niger, and Nigeria to address the accuracy of mortality: VIA, conventional cervical cytology, and
various screening approaches such as cytology, HPV HPV testing. The results of these studies are likely to

958 Bulletin of the World Health Organization, 2001, 79 (10)

 Screening of cervical cancer in developing countries

provide valuable leads to the development of public Table 1. Outcome of information/education on the control of
health policies to control cervical cancer in developing cervical cancer, Solapur District, Maharashtra, India, 199599
countries. A recently held national workshop on
control of cervical cancer in India reviewed the various Intervention Control
methodologies for the early detection of cervical area (Madha area (Karmala
neoplasia and considered both good quality conven- Tehsil) Tehsil)
tional cytology and VIA as suitable tests for early
Total number of women 96 908 76 084
clinical diagnosis (39). In view of the inadequately
developed cytology services, VIA was recommended No. of womenyears 352 628 380 805
as the immediate option for the introduction of
No. of incident cervical cancers 80 64
cervical cancer control initiatives as part of the district
cancer control programmes in 54 districts in India. Stage I and II cancers (%) 65.1 32.8
a
Age-standardized incidence (per 100 000) 26.3 18.7
South-east Asia
In Singapore, a high level of opportunistic screening No. of deaths from cervical cancer 17 30
for cervical cancer has been operating over the last Age-standardized mortality rate (per 100 000) b
5.6 8.6
few years, but has had only minimal impact on the
a
overall incidence and mortality from cervical cancer Incidence rate ratio: 1.41 (95% CI: 1.001.98).
b
(3). However, a substantial decline in cervical cancer Mortality rate ratio: 0.65 (95% CI: 0.361.18).
incidence and mortality has been observed among
the Singapore Indian community, with stable trends
find adequate financial resources, develop the
among the Chinese and Malay communities. Efforts
infrastructure, train the needed manpower, and
are currently underway to provide an organized
elaborate surveillance mechanisms for screening,
screening programme by restructuring the existing
investigating, treating, and follow-up of the targeted
opportunistic programme. A test-and-treat approach
women. Quite often, considerable discussion is
following VIA is currently being evaluated in Thai-
focused on which screening test to use cytology
land. A cytology-based demonstration programme
or alternatives to cytology, such as VIA or HPV
on screening is currently being implemented by the
testing or which combinations/sequence of
MOH in Nakornpanam Province in north-east
screening tests should be used for screening in
Thailand. The comparative performance of VIA
developing countries. Choosing a suitable screening
and VILI in detecting cervical neoplasia is being
test is only one aspect of a screening programme. A
addressed in Vientiane, Lao Peoples Democratic
more fundamental and challenging issue is the
Republic. Ongoing studies in rural China are
organization of the programme in its totality.
addressing the accuracy of cytology and non-
Whichever screening test is to be used, the challenges
cytology-based screening approaches.
in organizing a screening programme are more or less
the same. However, screening tests (e.g. cytology,
Summary HPV testing) that require additional recalls and
Although cytological screening is being carried out in revisits for diagnostic evaluation and treatment may
some developing countries/regions, there are no pose added logistic difficulties and these may emerge
organized programmes and the testing is often of as another barrier for participation in low-resource
poor quality and performed inadequately and settings.
inefficiently among the population. As a result, there The choice of screening test in countries/
has been a very limited impact on the incidence of regions that plan to initiate new programmes should
cervical cancer, despite the large numbers of be based on the comparative performance character-
cytological smears taken in some countries such as istics of cytology and its potential alternatives such as
Cuba and Mexico. The findings from completed and VIA, their relative costs, technical requirements, the
ongoing research on various approaches to screening level of development of laboratory infrastructure,
(in terms of accuracy and effectiveness) and to and the feasibility in a given country/region. Since
treatment (in terms of long-term safety) such as programmes cannot afford the luxury of frequently
cryotherapy and loop electrosurgical excision proce- repeated testing of women, a highly sensitive test
dures, carried out in field conditions, and test-and- should be provided. If cytology is chosen, consider-
treat approaches should be taken into account able attention should be given to obtaining good
when considering new programmes and when quality smears, staining, and reporting so that a
reorganizing existing programmes. moderately high sensitivity to detect lesions is
ensured. If a potential alternative to cytology, such
as VIA, is chosen for screening, considerable
Effective screening programmes attention should be given to the proper monitoring
and evaluation of the programme inputs and out-
in developing countries comes before further expansion, since VIA is still an
Efforts to organize effective cervical cancer screen- experimental option for cervical cancer screening and
ing programmes in developing countries will have to it remains to be demonstrated whether VIA-based

Bulletin of the World Health Organization, 2001, 79 (10) 959

Special Theme Noncommunicable Diseases

screening programmes are associated with a reduc- planned investments in order to improve the capacity
tion in cervical cancer incidence and mortality. In of their health services to diagnose and treat cervical
developing countries, existing ineffective cytology- cancer precursors and early invasive cancers, before
based programmes should be urgently reorganized considering even limited screening programmes.
and monitored. VIA may be considered as a suitable early detection
Quantitative studies have shown that after two test in the context of early clinical diagnosis in low-
or more negative cytology smears, even screening income countries, particularly in those regions with-
once every 10 years yields a 64% reduction in the out extensive cytology laboratory facilities.
incidence of invasive cervical cancer, assuming 100% Those middle-income developing countries
compliance (6, 40). Further studies based on this with inefficient cytology screening programmes
model indicate that once-in-a-lifetime screening may should focus their attention on reorganizing the
yield around 2530% reduction in the incidence of programme in the light of lessons from their past
cervical cancer (41, 42). failures and experiences from elsewhere. Many of
To have an impact on cervical cancer incidence these programmes work with the unrealistic notion
and mortality, efforts must be focused on the of offering frequently repeated screening tests (e.g.
following: increasing the awareness of women about every year) targeted at women of wide age ranges (e.g.
cervical cancer and preventive health-seeking beha- 2065 years). It would be more realistic and effective
viour; screening all women aged 3550 years at least to screen high-risk women (e.g. those aged 35
once, before expanding the services and providing 49 years or 3050 years) only once or twice with a
repeated screening (e.g. once in every 10 years); good quality and highly sensitive test, with an
providing a screening test with high sensitivity (since emphasis on wide coverage (>80%) of the targeted
women have less frequent opportunities for repeated women. It should also be ensured that women with
screening); treating women with high-grade dysplasia identified abnormalities attend for diagnosis, man-
and cancer; and monitoring programme inputs and agement and follow-up. Additional investments
evaluating the outcomes. should also be made to improve the manpower
resources and infrastructure that would sustain the
programmes in these countries. Adequate informa-
Conclusion tion systems should also be incorporated within the
Programmes for organized screening of cervical programme for monitoring inputs and outcomes.
cancer (e.g. in England and Finland) or for Middle-income countries without any programmes
opportunistic/spontaneous screening (e.g. in the for cervical cancer screening, but planning to
USA and Canada) involve substantial costs to provide implement such a programme, should consider
for the associated infrastructure, manpower, con- organizing and sustaining it in a limited geographical
sumables, follow-up, and surveillance. In our view, region before expanding to cover a wider area.
many low-income developing countries, particularly Managerial guidelines are now available to help in
most of those in sub-Saharan Africa, currently have planning and implementing appropriate programmes
neither the financial and manpower resources nor the in low-resource settings (13, 43). n
capacity in their health services to organize and
sustain a screening programme of any sort. Low-
income developing countries should consider Conflicts of interest: none declared.

Resume
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a revenu faible ou moyen
Le cancer du col constitue un important probleme de Le cout de linfrastructure, du personnel, des
sante publique chez les femmes adultes des pays en produits renouvelables, du suivi et de la surveillance
developpement dAmerique du Sud, dAmerique cen- est eleve, quil sagisse de programmes de depistage
trale, dAfrique subsaharienne, dAsie du Sud et dAsie organises ou ponctuels. Les ressources quils peuvent
du Sud-Est. Dans les pays developpes, des programmes consacrer aux soins de sante etant limitees, les pays en
repetes de depistage cytologique, soit organises soit developpement ne peuvent adopter les programmes
ponctuels, ont conduit a une baisse importante de en usage dans les pays developpes, qui comportent
lincidence du cancer du col et de la mortalite qui lui est des depistages frequemment repetes sur une tranche
associee. En revanche, le cancer du col reste une dage plus etendue. Les services de sante de nombreux
affection le plus souvent non matrisee dans les pays en pays en developpement a faible revenu, dont la
developpement a haut risque en raison de labsence ou plupart en Afrique subsaharienne, nont ni les
de linefficacite du depistage. Le present article passe ressources ni la capacite dorganiser et de poursuivre
brievement en revue les initiatives actuelles en matiere de des programmes de depistage quels quils soient. Les
depistage et de recherche dans ces pays. pays en developpement a revenu moyen, dans lesquels

960 Bulletin of the World Health Organization, 2001, 79 (10)

 Screening of cervical cancer in developing countries

le depistage est actuellement inefficace, devront Pour organiser un programme de depistage

reorganiser leurs programmes a la lumiere de efficace dans ces pays, il faudra trouver des ressources
lexperience des autres pays et des lecons de leurs financieres suffisantes, developper les infrastructures,
echecs passes. Ceux de ces pays qui envisagent former le personnel necessaire et elaborer des meca-
dorganiser un nouveau programme de depistage nismes de surveillance pour depister, examiner, traiter et
devront commencer par une region geographique suivre les femmes appartenant au groupe cible. On
limitee avant de songer a une quelconque extension. Il tiendra compte des resultats des nombreuses recherches
est egalement plus realiste et plus efficace daxer le portant sur les diverses approches du depistage dans les
depistage sur les femmes a haut risque, qui seront pays en developpement ainsi que des directives de
soumises une fois ou deux dans leur vie a un test tres gestion existantes lorsquon reorganisera des program-
sensible, en cherchant a obtenir une couverture elevee mes en cours ou que lon envisagera de nouvelles
(>80 %) de la population visee. initiatives en matiere de depistage.

Resumen
Programas eficaces de cribado del cancer cervicouterino en los pases en desarrollo
de ingresos bajos y medios
El cancer cervicouterino representa un importante de forma sostenida programa alguno de cribado. Los
problema de salud publica entre las mujeres adultas de pases en desarrollo de ingresos medios, que aplican hoy
los pases en desarrollo de America del Sur y medidas de cribado ineficientes, deberan reorganizar
Centroamerica, el Africa subsahariana y Asia meridional sus programas a la luz de las experiencias de otros pases
y sudoriental. Los programas de cribado citologico y de las lecciones extradas de sus pasados fracasos. Los
frecuente, organizados o puntuales, han logrado reducir pases de ingresos medios que decidan organizar un
considerablemente la incidencia de cancer cervicouterino nuevo programa de cribado deberan ensayarlo prime-
y la mortalidad asociada en los pases desarrollados. En ramente en un area geografica limitada, antes de
cambio, este tipo de cancer sigue sin controlarse apenas estudiar su eventual ampliacion. Es mas realista y eficaz
en los pases en desarrollo de alto riesgo, donde las intentar cribar a las mujeres de alto riesgo una o dos
medidas de cribado son ineficaces o inexistentes. El veces a lo largo de su vida mediante una prueba de alta
artculo analiza brevemente la experiencia de las sensibilidad, procurando sobre todo asegurar una amplia
iniciativas de cribado e investigacion llevadas a cabo cobertura (> 80%) de la poblacion destinataria.
actualmente en pases en desarrollo. Como parte de las actividades desplegadas para
La infraestructura, los recursos humanos, el organizar un programa de cribado eficaz en esos pases
material fungible, el seguimiento y la vigilancia que en desarrollo, habra que hallar recursos financieros
requieren los programas de cribado del cancer cervicou- suficientes, desarrollar la infraestructura oportuna,
terino tanto los organizados como los puntuales capacitar al personal necesario e idear mecanismos de
entranan grandes costos. Debido a lo limitado de sus vigilancia para el cribado, investigacion, tratamiento y
recursos de atencion sanitaria, los pases en desarrollo no seguimiento de las mujeres destinatarias. A la hora de
pueden permitirse el cribado frecuente que durante un reorganizar los programas existentes y de planear nuevas
amplio intervalo de edades aplican los pases desarro- iniciativas de cribado, deberan tenerse en cuenta los
llados. Muchos pases en desarrollo de bajos ingresos, en resultados de las numerosas investigaciones realizadas
particular la mayora de los pases del Africa subsaha- sobre los diversos enfoques de cribado aplicados en los
riana, no poseen ni los recursos ni la capacidad pases en desarrollo, as como las directrices de gestion
necesarios para que sus servicios de salud organicen disponibles.

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