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Family Practice Vol. 19, No. 2, 189-192
© Oxford University Press 2002


Original Paper

Prevention of cervical cancer in a poor population in Brazil

Edmundo C Mauada, Uilho A Gomesb, Jarbas L Nogueirab, Armando GF Melanic, Denise L Lemosc and Geraldo S Hidalgod

a Department of Clinical Oncology,
c Department of Gynecological Oncology and
d Department of Anatomic Pathology, Fundação Pio XII, Barretos and
b Faculdade de Medicina de Ribeirão Preto (USP), Ribeirão Preto, São Paulo, Brazil.

EC Mauad, Rua Vinte 221, Centro, CEP:14780-070, Barretos, São Paulo, Brazil.

Mauad EC, Gomes UA, Nogueira JL, Melani AGF, Lemos DL and Hidalgo GS. Prevention of cervical cancer in a poor population in Brazil. Family Practice 2002; 19: 189–192.

Received 19 January 2001; Revised 6 September 2001; Accepted 1 November 2001.


    Abstract
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 
Objective. The purpose of this study was to determine the possibility of providing a cervical screening facility to a poor population.

Methods. A cross-sectional study was conducted in the period from December 1994 to December 1997, with 1384 women from the poor districts of Barretos, São Paulo and three other neighbouring cities. Performed by a nurse, the programme included door-to-door interviews and cervical screening. The Papanicolaou smears were taken either at the community centre or at home using a portable gynaecological table transportable by bicycle, developed by the Institution.

Results. From 1384 interviewed women, 1044 (75.4%) agreed to undergo the examimation and 499 (47.8%) had never had the test or had not had it repeated within the last 3 years. Among 1044 examined women, seven cases of carcinoma ‘in situ’, one invasive squamous cell carcinoma (stage IB) and two polyps were found.

Conclusions. This study shows that programmes of cancer prevention in poor populations can be as successful as those carried out in more developed countries by taking advantage of innovations in the delivery of care.

Keywords. Active prevention, cervical cancer screening, developing countries, portable gynaecological table.


    Introduction
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 Abstract
 Introduction
 Methods
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 Discussion
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Cervical cancer is the second most frequent malignancy among women worldwide.1 The incidence of cervical cancer is not high in the USA; 80 700 new cases were predicted to be diagnosed in 1996, 65 000 of them in situ and 15 700 invasive, with the occurrence of ~4900 deaths.2 However, the incidence and mortality of the disease are considered to be very high in Africa and Latin America, with an estimated 1999 incidence of 20 650 new cases in Brazil (of 26.28 cases per 100 000 women) and ~6900 deaths (a rate of 9.2 cases/100 000 women).3,4 Mandeblatt and colleagues5 have reported that low-income populations tend to have low coverage with the Papanicolaou test, which could explain the high rates of mortality.

The objective of the present study was to assess whether response rates could be improved by informing a poor population in Brazil about the Papanicolaou test using easily understandable language and offering an unthreatening environment for the test close to women's homes.


    Methods
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 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 
A cross-sectional study involving an active search for cases was planned in order to reach sexually active women residing in the five poorest neighbourhoods of Barretos, State of São Paulo, Brazil, and in four poor neighbourhoods in three nearby small towns. The total number of women older than 14 years living in the urban zone of these four towns was 44 939, and 1472 of them lived in extremely poor neighbourhoods. The neighbourhoods were classified by the local government offices. The study was carried out in two steps, i.e. dissemination of the procedure and detection of cervical cancer.

Dissemination phase
The participants were one of the authors, a physician acting as co-ordinator of the study and a nurse, who together developed actions for the dissemination of information and collection of material, a community leader who facilitated access to the population and a radio announcer who presented a popular programme directed at a large audience. The following activities were developed: interviews with the co-ordinator dur-ing the radio programme, a loudspeaker service passing through the streets of the neighbourhoods to announce the programme and inviting women to submit to the exam, and a home visit by the nurse accompanied by the community leader to extend a personal invitation and to deliver easily understood printed material. This phase lasted 1–2 weeks in each neighbourhood before the collection of material.

Detection phase
All women older than 14 years were interviewed at home by the nurse and a questionnaire was filled out in order to determine the patient's knowledge about cancer, a history of previous examination for prevention of cervical–uterine cancer and demographic data. The women were then instructed about the importance of the Papanicolaou test and invited to have one done at no cost. As part of the instruction, a T-shirt with a drawing showing self-examination of the breast was offered together with a plastic food container as an incentive. A visit for material collection was scheduled for those who accepted the test, to be performed at the community centre or at the closest health centre of easy access, from Monday to Friday, from 8:00 to 17:00 h. On the assumption that the women would have some difficulty in arriving at the scheduled time, a flexible timetable was offered for collection after 17:00 h or when required on Saturdays or Sundays. When a woman did not arrive for her visit, the nurse visited her at home twice more, recording the reasons for failing to show up and encouraging her participation. When a woman continued to fail to present herself and when greater difficulties were foreseen, the test was offered at home using a collapsible portable gynaecological table transportable by bicycle, specifically designed for this purpose. The table was first used when the development of the project was already in progress. In every case, the collection of material was performed using a disposable kit (speculae, etc.). The slides with the smears were delivered to the Pathology Laboratory of São Judas Tadeu Hospital within 5 days. The results were delivered to the women who had been examined after 10 days, accompanied by standardized instructions. When the colpocytological result was normal, the woman was discharged from the project. When the result showed infection or inflammation, the woman was referred to the doctor at the health centre. If cervical intraepithelial neoplasia (CIN I, II or III) or infil-trative malignant neoplasia was detected, the patient was sent to the Department of Gynaecology of São Judas Tadeu Hospital for definitive diagnosis and treatment.

The women interviewed were classified socio-economically according to the criteria of the Brazilian Association of Market Research.

In order to avoid ethical problems, during the visits prior to the collection of material, the nurse carefully avoided forcing acceptance of the examination. Her attitude was always to give enough information about the disease, prevention and so on for the patient to be able to make an informed decision.

The data were processed and analysed statistically using Epi Info-6 software.


    Results
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 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 
Of the 1472 women older than 14 years, 1384 were interviewed from December 1994 to December 1997. The following socio-demographic data were obtained: mean age, 37.4 years (range 14–91 years); 194 (l4.0%) were illiterate; 1013 (73.2%) had 1–4 years of schooling; 109 (8.0%) had 5–8 years of schooling; and 68 (4.9%) had >8 years of schooling. Socio-economic classification showed that 362 (26.1%) belonged to class E and 815 (59.0%) to class D (both very poor), 195 (l4.0%) belonged to class C, 12 (0.9%) belonged to class B and none belonged to class A. A total of 317 (22.9%) of the women interviewed had never had a Papanicolaou test. This negative response was more common among women aged <35 years and >=50 years, among women with less schooling and among women of lower socio-economic classification (P < 0.005) (Table 1Go).


View this table:
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TABLE 1 Data concerning the application of the Papanicolaou test to the 1384 women interviewed, according to age, schooling and socio-economic class
 
Of the 1384 women interviewed, 1044 (75.4%) took the Papanicolaou test: 993 of them at community centres—using the usual gynaecological table—and 51 (3.7%) at home using the portable gynaecological table. The women who used the portable gynaecological table, being unable to attend a community centre, tended to live at a greater distance from the centres, to be older or to have small children, but some had no apparent reason for preferring the portable table. Of the 1044 women who submitted to the test, 499 (47.8%) had never done so before or had not repeated the test in the last 3 years. Of the 340 women who refused the Papanicolaou test, 141 (41.47%) had been tested during the previous year, making new examination unnecessary and 199 did not accept it. Seven women with abnormal cytology compatible with in situ carcinoma (ICN III) were identified, as well as one with invasive squamous cell carcinoma (IB) and two with polyps (TNM-UICC). The cases with a confirmed diagnosis of malignancy were referred to and treated at an Oncological Institution (São Judas Tadeu Hospital). The treatments applied to these patients were two conizations and five hysterectomies with high-dose external radiotherapy. The cost of this study over the 3 year period was US$ 29 245.46, corresponding to the salary of the nurse, broadcasting on the radio, using a loudspeaker in the street, slides (the price paid by the Unified Health System for each examination was used), leaflets distributed at home, the cost of the portable gynaecological table and bicycle, and small prizes (T-shirt or plastic food container).

The project was funded partly by the Pio XII Foundation (of the São Judas Tadeu Hospital) and partly by the Brazilian Unified Health System (through the payment for each examination).


    Discussion
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 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 
In Brazil, the Papanicolaou test is offered free of charge to the entire female population at official health units. A government decree regulating the role and responsibility of local governmental bodies establishes that disease prevention is a responsibility of the Municipalities, with aid from the State.

A 1988 survey based on data from 198 laboratories of pathological anatomy and cytology in the State of São Paulo revealed that only 9.2% of the 10.7 million women older than 14 years residing in the state had taken the Papanicolaou test at public services.6 This low coverage has also been detected in other developing countries: <5% of women in developing countries submitted to the Papanicolaou test in the last 5 years.7 On the other hand, in Finland, the rate of participation in programmes of early detection of cervical cancer is ~70–80% and the prevalence of invasive cases after the introduction of these programmes currently is 20% of all cases.8

In our study, we obtained coverage of 74.4% of the target population. Excluding women who had taken the test during the year of the study and who therefore refused to repeat it, coverage was >80%.

This high rate of coverage may have been due to several factors. These include a broadcasting campaign before and, at times, during the project, with an easy to understand message, the use of means of dissemination having higher credibility in this population, i.e. radio announcers highly accepted by the population; offering preventive measures near the homes of the women, the presence of a nurse that captivates them, listening attentively to their problems and demonstrating a sincere desire to help; offering facilities for the examination such as collection of material after working hours and on Saturdays and Sundays, if necessary; availability of a person in the programme to accompany them to the hospital when necessary for colposcopy or treatment; credibility of the service behind the project; and the possibility of home collection using a gynaecological table transported by bicycle. The women who availed themselves of home collection were those who lived far from the community centre, older women, women with small children and some with no apparent motive. The number of women who had the material drawn for Papanicolaou exam with the use of the portable gynaecological table was not as large as it might have been because this method was first used some time after the beginning of the project.

One of the great advantages provided by the creation of this table was that it was easy to transport by a nurse to poor neighbourhoods or to the periphery using a bicycle, performing door-to-door visits. No similar studies have been found in the literature using this portable gynaecological table for the prevention of cervical cancer. Despite the small number of cases using this equipment, the feeling of the team is that it could certainly be used in rural areas. It is known that in the Northeast and North regions of Brazil, 36 and 34% of all women, respectively, live in rural areas. In places where dissemination of information and Papanicolaou collections are more difficult, the portable table can be transported by bicycle, motorcycle, cart or any other simple means of transportation. In poor or remote regions where nurses or sanitary agents routinely carry out home visits, material for the Papanicolaou test probably could also be collected at home using this table.

We are sure that the most efficient way of preventing this cancer is through an active, domiciliary and low cost search. The cost of each examination in the present study during the 3 years of the project was US$ 28.00 per woman. A recent study also based on a domiciliary search using a mobile clinic yielded excellent results with poor South African women, but we believe that the equipment used was not easily accessible to most developing countries.9

Another important aspect to be emphasized is the number of cases diagnosed in the present study, three times higher than the Brazilian regional mean.10 This was probably because the population studied was at ‘higher risk’, with 85.1% of the women belonging to the poorest class (categories D and E) and 87.2% having <4 years of schooling, and also because an active search was conducted.

So far, there have been no deaths among the women who presented an abnormal test or cervical polyps and who were referred to the hospital, probably due to the rapid scheduling of a visit and to the nurse personally accompanying the patient to the hospital. However, a patient who presented ‘in situ carcinoma was reluctant for 3 months to go to the hospital. In this case, a home visit to the patient and her husband by a doctor was necessary. The present study demonstrated that a well-directed programme targeted at the poor population can reach the same rates of coverage with the Papanicolaou test as those obtained for the wealthier population of higher educational level who use private preventive services.

We should also point out some of the difficulties met during the study, such as limited participation on the part of some community leaders due to their workload and the poor participation of some municipalities.

In conclusion, our study demonstrated that a project of dissemination using several low cost strategies can considerably increase the co-operation of poor women with this type of screening programme and consequently reverse this dramatic picture of advanced cases of cervical cancer in less privileged populations.


    Acknowledgments
 
The authors would like to thank Clube dos Leões do Brasil for the significant financial support. We also thank Nurse Cleusa in recognition of her arduous and pioneering work in collecting material for Papanicolaou smears at home and for being rewarded by UNICEF as Woman of the Year in the field of Health in 1998. This study was presented in part at the 17th International Cancer Congress, Rio de Janiero, Brazil, August 24–28, 1998.


    References
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 Abstract
 Introduction
 Methods
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 Discussion
 References
 
1 Wharton JT. Neoplasms of the cervix. In Holland JF, Bast RC, Jr, Norton DL, Frei E, III, Kufe DW (eds). Cancer Medicine, 4th edn. Baltimore: Williams & Wilkins, 1997: 22–27.

2 Parker SL, Tong T, Bolden S, Wingo PA. Cancer Statistics 1996, Vol. 65. CA, 1996: 5–27.

3 Whelan SL, Parkin DM, Masuyer E. Patterns of Cancer in Five Continents. Lyons: International Agency for Research on Cancer, 1990.

4 Ministério da Saúde/INCA/Pro-Onco. Estimativa da Incidência e Mortalidade por Câncer no Brasil 1999. Rio de Janeiro: INCA/Pro-Onco, 1998.

5 Mandelblatt J, Andrews H, Kerner J. Determinants of late stage diagnosis of breast and cervical cancer: the impact of age, race, social class and hospital typeAm J Publ Health 1991; 85:646–649.

6 Soares RRS. Laboratórios de Anatomia Patológica e de Citologia do Estado de São Paulo: Diagnóstico da Situação, 1988–89.

7 WHO. Control of cancer of the cervix uteri. Bull WHO 1986; 64:607–618.[Web of Science][Medline]

8 Hristova L, Hakama M. Effect of screening for cancer in the Nordic countries on deaths, costs and quality of life, up to the year 2017. Acta Oncol 1997; 36:1–60.

9 Megevand E, Wybrand VW, Bryan K, Bloch B. Can cervical cancer be prevented by a see, screen, and treat program? A pilot study. Am J Obstet Gynecol 1996; 174:923–928.[Web of Science][Medline]

10 Secretaria de Estado da Saúde. Coordenadoria da Saúde do Interior. Direção Regional de Saúde de Barretos, DIR-IX—Núcleo de Planejamento, avaliação e desenvolvimento 2, 1993 e 1994.


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