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Characteristics of Respondents to a Cervical Cancer Screening Program in a Developing Country
Archives of Medical Research 33 (2002) 295–300
ORIGINAL ARTICLE
Characteristics of Respondents to a Cervical Cancer Screening Program in a Developing Country Gabriela Torres-Mejía,a Jorge Salmerón-Castro,b Martha M. Téllez-Rojo,a Eduardo C. Lazcano-Ponce,a Sergio A. Juárez-Márquez,c Irene Torres-Torijad and Leobardo Gil-Abadíee a
Centro de Investigación en Salud Poblacional, Instituto Nacional de Salud Pública (INSP), Cuernavaca, Morelos, Mexico Unidad de Investigación Epidemiológica y Servicios de Salud, cCoordinación de Investigación Médica, dCoordinación de Educación Médica, Instituto Mexicano del Seguro Social (IMSS), Centro Médico Nacional Siglo XXI, Mexico City, Mexico e Oficina de Prestaciones Médicas, Delegación Morelos, IMSS, Cuernavaca, Morelos, Mexico
b
Received for publication April 25, 2001; accepted January 16, 2002 (01/059).
Background. Characteristics associated with the response to a personalized, mailed invitation for the Papanicolaou (Pap) test vary among women. This study assesses the relationship between selected characteristics (e.g., demographic, obstetric, Pap history) and the response to a letter of invitation to undergo a Pap test among Mexican women affiliated with the Mexican Social Security Institute (IMSS). Methods. Study subjects were 328 women affiliated with the IMSS who received and responded to a mailed letter of invitation, and 247 age- and clinically matched controls who received but did not respond to the letter of invitation. Statistical analysis consisted of multivariate conditional regression model. Results. Having better housing conditions was one of the factors associated with letter response (medium level vs. low level, odds ratio [OR] 3.17, 95% confidence interval [95% CI] 2.46–4.09; high level vs. low level, OR 2.65, 95% CI 2.06–3.41). Other factors positively associated with letter response were greater number of pregnancies, previous Pap testing, being pleased at receipt of the letter of invitation, and knowing another woman who had received the invitation. Factors associated negatively to letter response were 7 or more years of formal education (7 years vs. 0–6 years, OR 0.50, 95% CI 0.40–0.63), having a current job, availability of other medical services in addition to the IMSS, and willingness to receive Pap results by mail. Conclusions. Low educational level is not a limitation for cervical cancer screening call and recall among women affiliated with the IMSS. © 2002 IMSS. Published by Elsevier Science Inc. Key Words: Call and recall, Cervical cancer, Papanicolaou, Invitation for screening.
Introduction Cervical cancer (CC) is second only to breast cancer as the most common neoplasia in the world (1). Mortality from cervical cancer has not decreased in the past 30 years in countries of Latin America and the Caribbean, and incidence rates are the highest in the world (2). In Mexico,
Address reprint requests to: Gabriela Torres-Mejía, Center for Research in Population Health, INSP, Av. Universidad #655, Col. Sta. Ma. Ahuacatitlán, 62508 Cuernavaca, Morelos, México. Tel.: (52) (77) 73112343; FAX: (52) (77) 7311-1148; E-mail: [email protected]
4,500 women die each year due to CC (3,4). The Mexican Social Security Institute (IMSS) provides medical services to nearly 60% of the population nationwide. At this Institution, CC is the most frequent neoplasia, as well as being the primary cause of death due to cancer in women (5,6). In several countries cervical cancer-screening programs based on the Pap test (CCSP) have shown to be effective in lowering morbidity and mortality from CC (7–11). In developing countries, the CCSP has not proven effective, mainly due to quality and coverage deficiencies (1,12–14). In Mexico, although the National CCSP has existed for 20 years, CC continues to be a major public health problem; a low
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level of coverage and delayed utilization of health services by women at risk have been shown as the principal causes of the low impact of the CCSP (15). Inviting women on an individual basis, either by telephone or by mail, has shown to be an effective CCSP recruitment mechanism (11,16–18). Selected characteristics (e.g., demographic, obstetric, and Pap history, among others) are known to be associated with responding to a personalized mailed invitation to undergo a Papanicolaou (Pap) test; these characteristics vary among women. For instance, in an Australian study, factors associated with a positive response to a screening invitation by mail were having a mate, higher level of education, access to a female family doctor, knowledge of the screening interval, and being more recently screened (19). However, women having one or more previous Pap tests were more likely to attend a new Pap test independently of the recall system (19,20). Fear of being diagnosed with cancer and embarrassment and fear of the procedure were some of the reasons for refusal to participate in a UK study (21). In the present study, the relationship between demographic characteristics, obstetric and Pap history, and characteristics related to health services are assessed as predictors of response to a personalized invitation to undergo a Pap test in Mexican women affiliated with the IMSS.
Materials and Methods Study population The study population was selected from women aged 20–64 years who participated in a randomized field trial carried out to assess the efficacy and effectiveness of a mailed invitation as a recruitment strategy during 1997 in the Mexican state of Morelos (18). Of 103,978 women who registered at 23 IMSS clinics, 4,802 women were selected by probabilistic multistage method to participate in the randomized field trial. Four to five clinics were randomly selected from each of three zones of residence (i.e., urban, suburban, and rural) and one or two family physicians were randomly selected from each clinic. Women who were patients of these physicians were ordered by age, and within each age group (20–34 years, 35–49 years, and 50–64 years) women were systematically assigned to an intervention or control group (18). At the end of the follow-up period, the nurses in charge of each clinic program identified the women in the sample (n 4,802) who had a Papanicolaou test done at their clinic during the 12 months prior to the study, as well as those who died or had a hysterectomy. These women were excluded from analysis of the trial (300 in the intervention group and 283 in the control group) (18) and therefore from the present study. A total of 1,268 of the 2,419 women in the intervention group received the invitation letter and were eligible to participate in the present case-control study. Of women who received the invitation, 425 had the Pap test done at IMSS after receiving the letter and 843 did not. The
total follow-up period allowed for attending the clinic for Pap testing following the invitation was 8.5 weeks (18). Cases. These included women aged 20–64 years who did not have a Pap test at the IMSS during the 12 months previous to the study and who received a mailed invitation to have a Pap test done and had it at IMSS during the follow-up study. Of 425 eligible cases, 97 did not complete the questionnaire mainly because they went to their clinic on busy days when nurses were not able to apply the questionnaire because they were caring for other women waiting for their Pap tests. Thus, data on 328 women aged 20– 64 years were available for general analysis for an overall response rate of 77.2%. Controls. Controls were randomly selected from women who also received the invitation but who did not attend the Pap test during the follow-up period. Of 843 eligible controls, 425 women were randomly selected to yield an age and health care unit distribution similar to the cases. We were unable to contact 129 women because 11.5% had moved, 7.5% addresses were not found, 4.7% did not open the door, 3.8% were working, and 2.8% due to other reasons. Data from 296 women were available for general analysis with an overall response rate of 69.7%. Data collection. According to an approved protocol (Comisión Nacional de Investigación Científica, IMSS, October 8, 1996) the nurses in charge of the program at each health care unit participating in the field trial registered the women who arrived for the Pap test and applied a questionnaire for data collection. Women who did not attend were interviewed at their homes. The questionnaire collected information on demographic characteristics, health care services, obstetric and Pap history, and invitation data. Analysis. After applying the questionnaire, 49 women were identified as having had the Papanicolaou test done outside of the IMSS during the 12 months prior to the study and therefore were excluded from the analysis. Outcome of interest was having/not having a Pap test done at IMSS clinics after receiving a mailed invitation. Independent variables were classified as demographic, health care services, obstetric and Pap history, and invitation issues. Table 1 shows the categorization of these variables. To evaluate the association between the characteristics of several women and their responses to the invitation, multivariate conditional logistic regression was used for the analysis (22). First, odds ratios (ORs) and 95% confidence intervals (95% CIs) were computed for Pap test utilization and each of the variables of interest, taking into account the matching characteristics (age group and clinic). Second, multivariate regression model was constructed, leaving in the model only statistically significant variables (p 0.05). Likelihood ratio tests for trend were used as appropriate.
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Table 1. Characteristics of women and their association with response to a mailed invitation to undergo a Papanicolaou test (Morelos IMSS a, 1997)
Variables Demographic characteristics Years of schooling 06 7 Current job No Yes Living conditions Low Medium High Health care services IMSSa users No Yes Other medical care in addition to IMSSa No Yes Obstetric and PAP history Number of pregnancies 0 12 3 Previous Pap test No Yes Knowledge on the use of PAP test No Yes Invitation issues Knowledge of another woman who received an invitation No Yes Pleased with receipt of the letter No Yes Would like to receive mailed results No Yes
No. of respondentsb
%
No. of non-respondentsb
%
ORc
95% CI
211 106
64.3 32.3
137 110
55.5 44.5
1.00 0.46
0.380.55
0.001
208 100
63.4 30.5
153 94
61.9 38.1
1.00 0.52
0.440.62
0.001
91 127 105
27.7 38.7 32.0
105 68 72
42.5 27.5 29.2
1.00 3.02 1.94
2.443.74 1.572.40
0.001 0.001 0.001d
9 318
2.7 96.9
15 231
6.1 93.5
1.00 1.45
1.052.02
0.026
291 37
88.7 11.3
209 38
84.6 15.4
1.00 0.73
0.570.92
0.007
13 57 258
3.9 17.4 78.7
18 58 171
7.3 23.5 69.2
1.00 2.46 3.35
1.713.54 1.394.69
0.001 0.001 0.001d
52 275
15.8 83.8
58 187
23.5 75.7
1.00 2.06
1.672.53
0.001
14 287
4.3 87.5
18 225
7.3 91.1
1.00 0.70
0.981.02
0.06
247 79
75.3 24.1
195 50
78.9 20.2
1.00 1.46
1.151.84
0.002
13 301
4.0 91.8
9 218
3.6 88.3
1.02
0.731.42
0.893
102 224
31.1 68.3
31 215
12.6 87.0
1.00 0.37
0.310.45
0.001
p
a
Instituto Mexicano del Seguro Social; btotal numbers may vary due to missing values; codds ratios obtained by a logistic model conditioned on age and clinic groups, observations were weighted by inverse of probability of selection; dtest for trend: p 0.001.
An index of housing conditions was constructed, including number of persons living per number of bedrooms in the house, toilet/sewage conditions, and housing/floor materials. Observations were weighted by the inverse of the probability of being selected for the field trial. The probability of selection was as follows: ni/Ni x mi/Mi, in which ni number of physicians selected in each clinic, Ni total number of physicians per clinic, mi number of clinics selected per residence stratum, and Mi total number of clinics per residence stratum. On average, each physician attends the same number of women. Additional weight was given to observations from clinics with large numbers of women to
achieve better representation of the results for women registered at all 23 IMSS clinics in the state of Morelos. Results The dataset consisted of 575 women who received an invitation for a Pap test. However, several women were excluded from the analyses basically due to missing information. Table 1 shows a general description of the study population according to their characteristics and response to the invitation. Index of living conditions showed that 32% of women in the low level had houses with a dirt floor, 7%
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had no toilet, and households were inhabited by 3.2 persons per bedroom. Corresponding numbers for the medium level were 2, 5, and 2.4%, and for the high level 0, 0, and 1.4%, respectively. Table 1 shows the relative odds of response to the letter among the categories of the different characteristics analyzed in the present study, which were conditioned on age and clinic group using conditional logistic regression model. With respect to demographic characteristics, women with 7 or more years of formal education had lower odds of response to the letter than women with 0–6 years of formal education (OR 0.46, 95% CI 0.38–0.55). There was evidence that having a job decreased odds of response to the letter relative to having no job. Women with medium and high living conditions had higher odds of response to the letter than women with low living conditions. Regarding health care services, women who had attended an IMSS clinic at least once had higher odds of response to the invitation than those who had never attended, even though the latter were also affiliated with the IMSS. Compared to women who belonged to only IMSS medical services, women with other available medical services in addition to the IMSS had lower odds of response to the letter. Regarding obstetric and Pap history, a highly significant trend was observed for odds of response to increase with an increasing number of pregnancies (p 0.001). Women who had a previous Pap test had increased odds of response to the letter compared to women with no previous Pap test (OR 2.06, 95% CI 1.67–2.53). Knowledge concerning the use of the Pap test decreased odds of having responded to the invitation. With respect to invitation issues, knowledge of other women receiving the invitation increased odds of response to the letter (OR 1.46, 95% CI 1.15–1.84). Women who want to receive their Pap results by mail in the future had lower odds of response to the letter than women who would not like to receive their results by mail. Women who were pleased with receiving a mailed invitation had greater odds of response to the letter than women who did not like to receive the invitation by mail. Table 2 shows the results from the multivariate model. All variables except the use of IMSS services and knowledge of the use of Pap test were kept in the model. Compared with non-respondents to the mailed invitation, women who attended a clinic for a Pap test were more likely to have fewer years of formal education, no current job, better housing conditions, no medical care other than IMSS, more pregnancies, and a previous Pap test. These women were also more likely to know someone who also received the invitation and was pleased with the letter but not pleased with receiving the Pap results by mail (Table 2). Discussion Study results show that several factors appear to affect odds of response to a mailed invitation. Better housing conditions,
Table 2. Multivariate model of factors associated with response to an invitation by mail to undergo a Papanicolaou test (n 498) (Morelos IMSS a, 1997) Variables Demographic characteristics Years of schooling 0–6 7 Current job No Yes Living conditions Low Medium High
ORb
95% CI
p
1.00 0.50
0.400.63
0.001
1.00 0.70
0.57 0.85
0.001
1.00 3.17 2.65
2.464.09 2.063.41
0.001 0.001 0.001c
0.550.97
0.029
1.383.49 2.195.22
0.001 0.001 0.001c
Health care services Other medical care in addition to the IMSS No 1.00 Yes 0.73 Obstetric and PAPd history Number of pregnancies 0 1.00 1–2 2.19 3 3.38
Previous PAPd test No 1.00 Yes 2.83 2.173.69 Invitation issues Knowledge of another woman who received an invitation No 1.00 Yes 1.41 1.081.84 Pleased with receipt of the letter No 1.00 Yes 1.56 1.032.35 Would like to receive mailed results No 1.00 Yes 0.33 0.260.42
0.001
0.012
0.035 0.001
a
Instituto Mexicano del Seguro Social; bOR obtained with logistic model conditioned on age and clinic groups; all data were adjusted for all variables in the table; observations were weighted by inverse of probability of selection; ctest for trend: p 0.001; dPapanicolaou test.
number of pregnancies, previous Pap testing, knowledge of other women receiving the invitation letter, and being pleased with receiving the invitation letter were positively associated with the response. Negatively associated factors were 7 or more years of formal education, having a current job, availability of other medical services in addition to the IMSS, and being pleased with the idea of receiving the Pap results by mail in the future (Table 2). With respect to demographic characteristics, an Australian study reported that women with more years of formal education were positively associated to response to a mailed invitation (19). In our study, response to the letter was greater in women with fewer years of formal education than in women with 7 or more years of formal education. This effect persisted even after adjustment for having a previous Pap test and for using other medical services in addition to
Cervical Cancer Screening in a Developing Country
the IMSS. This behavior could be explained by the fact that 14% of women with 7 or more years of formal education and a previous Pap test answered that they had their previous Pap test in the private sector, as compared to 11% of women with 6 or fewer years of formal education (data not shown). In Sweden, younger and better-educated women were less likely to attend a clinic for Pap testing in response to an invitation, but two thirds of non-participants provided reasons indicating that they had attended elsewhere (19,23). In a Mexican study, more years of education were associated with higher rates of attendance; however, this study was carried out in women of the general population (24). Level of education has been analyzed more than economic status in relation to response to an invitation letter. However, lower rates of attendance for screening have been found among women with lower socioeconomic status (25,26). Our study showed that women at the lower level of living conditions had the lowest response. An Australian study showed that women who had been screened more recently were likely to have a positive response to the invitation (19). In our study, women who had been screened at least once had a greater response to the invitation when compared to those not previously screened. Nevertheless, of 110 women who never had a Pap test 47.3% had a Pap test after receiving the letter. Among women who were not invited (control group from the randomized field trial, data not shown), the proportion was 20.6%, indicating that the letter doubled the proportion of response. Two thirds of women who did not respond to an invitation in a Swedish population gave reasons indicating that they had attended elsewhere (23). In our study, women affiliated with medical care institutions other than the IMSS responded less often to the invitation. A survey made in a rural UK community assessed acceptability to individual invitations. Satisfaction with receiving a personalized invitation was stated by 78% of women; 94% stated that such letters should be sent to all women and 83% said they wished to be reminded regularly by mail (19,27). In our study, 81% were pleased with receiving the invitation. Additionally, when we inquired about the main reason, 28.01% expressed that it was a good way to remind them to undergo Pap testing and 32.94% responded that they appreciated the IMSS caring about their health. The quality offered by the cancer screening program might influence the response of women to a mailed invitation. In this study, 68% of respondents and 87% of non-respondents answered in the interview that they would like to receive their results by mail. Among non-respondents who would like to receive their results by mail, 40% agreed that sending the results by mail would be a good idea because in that way they would not have to return often to the IMSS to inquire about their results. However, only 10% of respondents gave the same answer. This could explain why more women who have not attended the Pap test wanted their re-
299
sults by mail, and that one of the reasons that they had not responded was their non-conformity with the delay in receiving the results. To reinforce this explanation, we detected that from all women who had their last Pap test at the IMSS, only 47% received their results, while 86% of those who had done the test privately were informed of their results. There is a potential misclassification bias due to the fact that questionnaires were completed in different settings. However, to reduce this bias with respect to the information provided for the majority of the characteristics evaluated in this study (i.e., demographic characteristics, health care services, and obstetric and invitation issues) all interviewers were trained by one of the authors of this paper. In addition, all women in this study received in their invitation a brief description of the importance and benefits of a Papanicolaou test. It is unlikely that the characteristics evaluated in this study were collected in a differential manner; thus, this potential bias may not have had a strong influence on our results. Our results suggest that low educational level is not a limitation for using this strategy. However, timely delivery of Pap results and accuracy of women’s addresses could improve the efficacy of this strategy. Acknowledgments The Mexican Institute of Social Security (IMSS) supported this research. The National Council for Science and Technology (CONACYT, Mexico) and the National Institute of Public Health (INSP, Mexico) provided additional support. The authors are grateful to Drs. Ignacio Méndez and Héctor Guiscafré for their valuable recommendations, to Drs. Patricia Alonso and Aurelio Cruz for their commentaries, to Betania Allen and Ana Ma. Chávez for their advice, to Drs. Rosado and Guerrero for their special help, to all clinic directors who allowed their patients to be interviewed, to the nurse-interviewers who collected the data, and to all IMSS patients for their time and valuable information. The following clinics participated in this study: Cuernavaca No. 1; Cuernavaca No. 20; Cuautla No. 7; Jiutepec No. 3; Jojutla No. 4; Oacalco No. 14; Zapata No. 18; Tepoztlán No. 19; Xochitepec No. 2; Zacatepec No. 5; Tlaltizapán No. 9; Chinameca No. 10; Miacatlán No. 13, and Jantetelco No. 21.
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ORIGINAL ARTICLE
Characteristics of Respondents to a Cervical Cancer Screening Program in a Developing Country Gabriela Torres-Mejía,a Jorge Salmerón-Castro,b Martha M. Téllez-Rojo,a Eduardo C. Lazcano-Ponce,a Sergio A. Juárez-Márquez,c Irene Torres-Torijad and Leobardo Gil-Abadíee a
Centro de Investigación en Salud Poblacional, Instituto Nacional de Salud Pública (INSP), Cuernavaca, Morelos, Mexico Unidad de Investigación Epidemiológica y Servicios de Salud, cCoordinación de Investigación Médica, dCoordinación de Educación Médica, Instituto Mexicano del Seguro Social (IMSS), Centro Médico Nacional Siglo XXI, Mexico City, Mexico e Oficina de Prestaciones Médicas, Delegación Morelos, IMSS, Cuernavaca, Morelos, Mexico
b
Received for publication April 25, 2001; accepted January 16, 2002 (01/059).
Background. Characteristics associated with the response to a personalized, mailed invitation for the Papanicolaou (Pap) test vary among women. This study assesses the relationship between selected characteristics (e.g., demographic, obstetric, Pap history) and the response to a letter of invitation to undergo a Pap test among Mexican women affiliated with the Mexican Social Security Institute (IMSS). Methods. Study subjects were 328 women affiliated with the IMSS who received and responded to a mailed letter of invitation, and 247 age- and clinically matched controls who received but did not respond to the letter of invitation. Statistical analysis consisted of multivariate conditional regression model. Results. Having better housing conditions was one of the factors associated with letter response (medium level vs. low level, odds ratio [OR] 3.17, 95% confidence interval [95% CI] 2.46–4.09; high level vs. low level, OR 2.65, 95% CI 2.06–3.41). Other factors positively associated with letter response were greater number of pregnancies, previous Pap testing, being pleased at receipt of the letter of invitation, and knowing another woman who had received the invitation. Factors associated negatively to letter response were 7 or more years of formal education (7 years vs. 0–6 years, OR 0.50, 95% CI 0.40–0.63), having a current job, availability of other medical services in addition to the IMSS, and willingness to receive Pap results by mail. Conclusions. Low educational level is not a limitation for cervical cancer screening call and recall among women affiliated with the IMSS. © 2002 IMSS. Published by Elsevier Science Inc. Key Words: Call and recall, Cervical cancer, Papanicolaou, Invitation for screening.
Introduction Cervical cancer (CC) is second only to breast cancer as the most common neoplasia in the world (1). Mortality from cervical cancer has not decreased in the past 30 years in countries of Latin America and the Caribbean, and incidence rates are the highest in the world (2). In Mexico,
Address reprint requests to: Gabriela Torres-Mejía, Center for Research in Population Health, INSP, Av. Universidad #655, Col. Sta. Ma. Ahuacatitlán, 62508 Cuernavaca, Morelos, México. Tel.: (52) (77) 73112343; FAX: (52) (77) 7311-1148; E-mail: [email protected]
4,500 women die each year due to CC (3,4). The Mexican Social Security Institute (IMSS) provides medical services to nearly 60% of the population nationwide. At this Institution, CC is the most frequent neoplasia, as well as being the primary cause of death due to cancer in women (5,6). In several countries cervical cancer-screening programs based on the Pap test (CCSP) have shown to be effective in lowering morbidity and mortality from CC (7–11). In developing countries, the CCSP has not proven effective, mainly due to quality and coverage deficiencies (1,12–14). In Mexico, although the National CCSP has existed for 20 years, CC continues to be a major public health problem; a low
0188-4409/02 $–see front matter. Copyright © 2002 IMSS. Published by Elsevier Science Inc. PII S0188-4409(02)00 3 6 3 - 6
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level of coverage and delayed utilization of health services by women at risk have been shown as the principal causes of the low impact of the CCSP (15). Inviting women on an individual basis, either by telephone or by mail, has shown to be an effective CCSP recruitment mechanism (11,16–18). Selected characteristics (e.g., demographic, obstetric, and Pap history, among others) are known to be associated with responding to a personalized mailed invitation to undergo a Papanicolaou (Pap) test; these characteristics vary among women. For instance, in an Australian study, factors associated with a positive response to a screening invitation by mail were having a mate, higher level of education, access to a female family doctor, knowledge of the screening interval, and being more recently screened (19). However, women having one or more previous Pap tests were more likely to attend a new Pap test independently of the recall system (19,20). Fear of being diagnosed with cancer and embarrassment and fear of the procedure were some of the reasons for refusal to participate in a UK study (21). In the present study, the relationship between demographic characteristics, obstetric and Pap history, and characteristics related to health services are assessed as predictors of response to a personalized invitation to undergo a Pap test in Mexican women affiliated with the IMSS.
Materials and Methods Study population The study population was selected from women aged 20–64 years who participated in a randomized field trial carried out to assess the efficacy and effectiveness of a mailed invitation as a recruitment strategy during 1997 in the Mexican state of Morelos (18). Of 103,978 women who registered at 23 IMSS clinics, 4,802 women were selected by probabilistic multistage method to participate in the randomized field trial. Four to five clinics were randomly selected from each of three zones of residence (i.e., urban, suburban, and rural) and one or two family physicians were randomly selected from each clinic. Women who were patients of these physicians were ordered by age, and within each age group (20–34 years, 35–49 years, and 50–64 years) women were systematically assigned to an intervention or control group (18). At the end of the follow-up period, the nurses in charge of each clinic program identified the women in the sample (n 4,802) who had a Papanicolaou test done at their clinic during the 12 months prior to the study, as well as those who died or had a hysterectomy. These women were excluded from analysis of the trial (300 in the intervention group and 283 in the control group) (18) and therefore from the present study. A total of 1,268 of the 2,419 women in the intervention group received the invitation letter and were eligible to participate in the present case-control study. Of women who received the invitation, 425 had the Pap test done at IMSS after receiving the letter and 843 did not. The
total follow-up period allowed for attending the clinic for Pap testing following the invitation was 8.5 weeks (18). Cases. These included women aged 20–64 years who did not have a Pap test at the IMSS during the 12 months previous to the study and who received a mailed invitation to have a Pap test done and had it at IMSS during the follow-up study. Of 425 eligible cases, 97 did not complete the questionnaire mainly because they went to their clinic on busy days when nurses were not able to apply the questionnaire because they were caring for other women waiting for their Pap tests. Thus, data on 328 women aged 20– 64 years were available for general analysis for an overall response rate of 77.2%. Controls. Controls were randomly selected from women who also received the invitation but who did not attend the Pap test during the follow-up period. Of 843 eligible controls, 425 women were randomly selected to yield an age and health care unit distribution similar to the cases. We were unable to contact 129 women because 11.5% had moved, 7.5% addresses were not found, 4.7% did not open the door, 3.8% were working, and 2.8% due to other reasons. Data from 296 women were available for general analysis with an overall response rate of 69.7%. Data collection. According to an approved protocol (Comisión Nacional de Investigación Científica, IMSS, October 8, 1996) the nurses in charge of the program at each health care unit participating in the field trial registered the women who arrived for the Pap test and applied a questionnaire for data collection. Women who did not attend were interviewed at their homes. The questionnaire collected information on demographic characteristics, health care services, obstetric and Pap history, and invitation data. Analysis. After applying the questionnaire, 49 women were identified as having had the Papanicolaou test done outside of the IMSS during the 12 months prior to the study and therefore were excluded from the analysis. Outcome of interest was having/not having a Pap test done at IMSS clinics after receiving a mailed invitation. Independent variables were classified as demographic, health care services, obstetric and Pap history, and invitation issues. Table 1 shows the categorization of these variables. To evaluate the association between the characteristics of several women and their responses to the invitation, multivariate conditional logistic regression was used for the analysis (22). First, odds ratios (ORs) and 95% confidence intervals (95% CIs) were computed for Pap test utilization and each of the variables of interest, taking into account the matching characteristics (age group and clinic). Second, multivariate regression model was constructed, leaving in the model only statistically significant variables (p 0.05). Likelihood ratio tests for trend were used as appropriate.
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Table 1. Characteristics of women and their association with response to a mailed invitation to undergo a Papanicolaou test (Morelos IMSS a, 1997)
Variables Demographic characteristics Years of schooling 06 7 Current job No Yes Living conditions Low Medium High Health care services IMSSa users No Yes Other medical care in addition to IMSSa No Yes Obstetric and PAP history Number of pregnancies 0 12 3 Previous Pap test No Yes Knowledge on the use of PAP test No Yes Invitation issues Knowledge of another woman who received an invitation No Yes Pleased with receipt of the letter No Yes Would like to receive mailed results No Yes
No. of respondentsb
%
No. of non-respondentsb
%
ORc
95% CI
211 106
64.3 32.3
137 110
55.5 44.5
1.00 0.46
0.380.55
0.001
208 100
63.4 30.5
153 94
61.9 38.1
1.00 0.52
0.440.62
0.001
91 127 105
27.7 38.7 32.0
105 68 72
42.5 27.5 29.2
1.00 3.02 1.94
2.443.74 1.572.40
0.001 0.001 0.001d
9 318
2.7 96.9
15 231
6.1 93.5
1.00 1.45
1.052.02
0.026
291 37
88.7 11.3
209 38
84.6 15.4
1.00 0.73
0.570.92
0.007
13 57 258
3.9 17.4 78.7
18 58 171
7.3 23.5 69.2
1.00 2.46 3.35
1.713.54 1.394.69
0.001 0.001 0.001d
52 275
15.8 83.8
58 187
23.5 75.7
1.00 2.06
1.672.53
0.001
14 287
4.3 87.5
18 225
7.3 91.1
1.00 0.70
0.981.02
0.06
247 79
75.3 24.1
195 50
78.9 20.2
1.00 1.46
1.151.84
0.002
13 301
4.0 91.8
9 218
3.6 88.3
1.02
0.731.42
0.893
102 224
31.1 68.3
31 215
12.6 87.0
1.00 0.37
0.310.45
0.001
p
a
Instituto Mexicano del Seguro Social; btotal numbers may vary due to missing values; codds ratios obtained by a logistic model conditioned on age and clinic groups, observations were weighted by inverse of probability of selection; dtest for trend: p 0.001.
An index of housing conditions was constructed, including number of persons living per number of bedrooms in the house, toilet/sewage conditions, and housing/floor materials. Observations were weighted by the inverse of the probability of being selected for the field trial. The probability of selection was as follows: ni/Ni x mi/Mi, in which ni number of physicians selected in each clinic, Ni total number of physicians per clinic, mi number of clinics selected per residence stratum, and Mi total number of clinics per residence stratum. On average, each physician attends the same number of women. Additional weight was given to observations from clinics with large numbers of women to
achieve better representation of the results for women registered at all 23 IMSS clinics in the state of Morelos. Results The dataset consisted of 575 women who received an invitation for a Pap test. However, several women were excluded from the analyses basically due to missing information. Table 1 shows a general description of the study population according to their characteristics and response to the invitation. Index of living conditions showed that 32% of women in the low level had houses with a dirt floor, 7%
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had no toilet, and households were inhabited by 3.2 persons per bedroom. Corresponding numbers for the medium level were 2, 5, and 2.4%, and for the high level 0, 0, and 1.4%, respectively. Table 1 shows the relative odds of response to the letter among the categories of the different characteristics analyzed in the present study, which were conditioned on age and clinic group using conditional logistic regression model. With respect to demographic characteristics, women with 7 or more years of formal education had lower odds of response to the letter than women with 0–6 years of formal education (OR 0.46, 95% CI 0.38–0.55). There was evidence that having a job decreased odds of response to the letter relative to having no job. Women with medium and high living conditions had higher odds of response to the letter than women with low living conditions. Regarding health care services, women who had attended an IMSS clinic at least once had higher odds of response to the invitation than those who had never attended, even though the latter were also affiliated with the IMSS. Compared to women who belonged to only IMSS medical services, women with other available medical services in addition to the IMSS had lower odds of response to the letter. Regarding obstetric and Pap history, a highly significant trend was observed for odds of response to increase with an increasing number of pregnancies (p 0.001). Women who had a previous Pap test had increased odds of response to the letter compared to women with no previous Pap test (OR 2.06, 95% CI 1.67–2.53). Knowledge concerning the use of the Pap test decreased odds of having responded to the invitation. With respect to invitation issues, knowledge of other women receiving the invitation increased odds of response to the letter (OR 1.46, 95% CI 1.15–1.84). Women who want to receive their Pap results by mail in the future had lower odds of response to the letter than women who would not like to receive their results by mail. Women who were pleased with receiving a mailed invitation had greater odds of response to the letter than women who did not like to receive the invitation by mail. Table 2 shows the results from the multivariate model. All variables except the use of IMSS services and knowledge of the use of Pap test were kept in the model. Compared with non-respondents to the mailed invitation, women who attended a clinic for a Pap test were more likely to have fewer years of formal education, no current job, better housing conditions, no medical care other than IMSS, more pregnancies, and a previous Pap test. These women were also more likely to know someone who also received the invitation and was pleased with the letter but not pleased with receiving the Pap results by mail (Table 2). Discussion Study results show that several factors appear to affect odds of response to a mailed invitation. Better housing conditions,
Table 2. Multivariate model of factors associated with response to an invitation by mail to undergo a Papanicolaou test (n 498) (Morelos IMSS a, 1997) Variables Demographic characteristics Years of schooling 0–6 7 Current job No Yes Living conditions Low Medium High
ORb
95% CI
p
1.00 0.50
0.400.63
0.001
1.00 0.70
0.57 0.85
0.001
1.00 3.17 2.65
2.464.09 2.063.41
0.001 0.001 0.001c
0.550.97
0.029
1.383.49 2.195.22
0.001 0.001 0.001c
Health care services Other medical care in addition to the IMSS No 1.00 Yes 0.73 Obstetric and PAPd history Number of pregnancies 0 1.00 1–2 2.19 3 3.38
Previous PAPd test No 1.00 Yes 2.83 2.173.69 Invitation issues Knowledge of another woman who received an invitation No 1.00 Yes 1.41 1.081.84 Pleased with receipt of the letter No 1.00 Yes 1.56 1.032.35 Would like to receive mailed results No 1.00 Yes 0.33 0.260.42
0.001
0.012
0.035 0.001
a
Instituto Mexicano del Seguro Social; bOR obtained with logistic model conditioned on age and clinic groups; all data were adjusted for all variables in the table; observations were weighted by inverse of probability of selection; ctest for trend: p 0.001; dPapanicolaou test.
number of pregnancies, previous Pap testing, knowledge of other women receiving the invitation letter, and being pleased with receiving the invitation letter were positively associated with the response. Negatively associated factors were 7 or more years of formal education, having a current job, availability of other medical services in addition to the IMSS, and being pleased with the idea of receiving the Pap results by mail in the future (Table 2). With respect to demographic characteristics, an Australian study reported that women with more years of formal education were positively associated to response to a mailed invitation (19). In our study, response to the letter was greater in women with fewer years of formal education than in women with 7 or more years of formal education. This effect persisted even after adjustment for having a previous Pap test and for using other medical services in addition to
Cervical Cancer Screening in a Developing Country
the IMSS. This behavior could be explained by the fact that 14% of women with 7 or more years of formal education and a previous Pap test answered that they had their previous Pap test in the private sector, as compared to 11% of women with 6 or fewer years of formal education (data not shown). In Sweden, younger and better-educated women were less likely to attend a clinic for Pap testing in response to an invitation, but two thirds of non-participants provided reasons indicating that they had attended elsewhere (19,23). In a Mexican study, more years of education were associated with higher rates of attendance; however, this study was carried out in women of the general population (24). Level of education has been analyzed more than economic status in relation to response to an invitation letter. However, lower rates of attendance for screening have been found among women with lower socioeconomic status (25,26). Our study showed that women at the lower level of living conditions had the lowest response. An Australian study showed that women who had been screened more recently were likely to have a positive response to the invitation (19). In our study, women who had been screened at least once had a greater response to the invitation when compared to those not previously screened. Nevertheless, of 110 women who never had a Pap test 47.3% had a Pap test after receiving the letter. Among women who were not invited (control group from the randomized field trial, data not shown), the proportion was 20.6%, indicating that the letter doubled the proportion of response. Two thirds of women who did not respond to an invitation in a Swedish population gave reasons indicating that they had attended elsewhere (23). In our study, women affiliated with medical care institutions other than the IMSS responded less often to the invitation. A survey made in a rural UK community assessed acceptability to individual invitations. Satisfaction with receiving a personalized invitation was stated by 78% of women; 94% stated that such letters should be sent to all women and 83% said they wished to be reminded regularly by mail (19,27). In our study, 81% were pleased with receiving the invitation. Additionally, when we inquired about the main reason, 28.01% expressed that it was a good way to remind them to undergo Pap testing and 32.94% responded that they appreciated the IMSS caring about their health. The quality offered by the cancer screening program might influence the response of women to a mailed invitation. In this study, 68% of respondents and 87% of non-respondents answered in the interview that they would like to receive their results by mail. Among non-respondents who would like to receive their results by mail, 40% agreed that sending the results by mail would be a good idea because in that way they would not have to return often to the IMSS to inquire about their results. However, only 10% of respondents gave the same answer. This could explain why more women who have not attended the Pap test wanted their re-
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sults by mail, and that one of the reasons that they had not responded was their non-conformity with the delay in receiving the results. To reinforce this explanation, we detected that from all women who had their last Pap test at the IMSS, only 47% received their results, while 86% of those who had done the test privately were informed of their results. There is a potential misclassification bias due to the fact that questionnaires were completed in different settings. However, to reduce this bias with respect to the information provided for the majority of the characteristics evaluated in this study (i.e., demographic characteristics, health care services, and obstetric and invitation issues) all interviewers were trained by one of the authors of this paper. In addition, all women in this study received in their invitation a brief description of the importance and benefits of a Papanicolaou test. It is unlikely that the characteristics evaluated in this study were collected in a differential manner; thus, this potential bias may not have had a strong influence on our results. Our results suggest that low educational level is not a limitation for using this strategy. However, timely delivery of Pap results and accuracy of women’s addresses could improve the efficacy of this strategy. Acknowledgments The Mexican Institute of Social Security (IMSS) supported this research. The National Council for Science and Technology (CONACYT, Mexico) and the National Institute of Public Health (INSP, Mexico) provided additional support. The authors are grateful to Drs. Ignacio Méndez and Héctor Guiscafré for their valuable recommendations, to Drs. Patricia Alonso and Aurelio Cruz for their commentaries, to Betania Allen and Ana Ma. Chávez for their advice, to Drs. Rosado and Guerrero for their special help, to all clinic directors who allowed their patients to be interviewed, to the nurse-interviewers who collected the data, and to all IMSS patients for their time and valuable information. The following clinics participated in this study: Cuernavaca No. 1; Cuernavaca No. 20; Cuautla No. 7; Jiutepec No. 3; Jojutla No. 4; Oacalco No. 14; Zapata No. 18; Tepoztlán No. 19; Xochitepec No. 2; Zacatepec No. 5; Tlaltizapán No. 9; Chinameca No. 10; Miacatlán No. 13, and Jantetelco No. 21.
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