O International Epldemlotogical Association 1996 Printed In Great Britain
Surveillance for Equity in Cervical
Cytology Screening
R S BAILIE AND D BOURNE
Bailie R S (Department of Community Health, University of Cape Town Medical School, Observatory 7925, South Africa) and Bourne D. Surveillance for equity In cervical cytology screening. International Journal of Epidemiology 1996; 25: 46-52.
Background. The opportunistic basis on which screening has been conducted in South Africa has resulted in multiple rescreenlng of a small proportion of the population (which excludes most women at high risk) and low population coverage. There has consequently been a failure of screening to Impact on the Incidence of cervical cancer In most of the population.
Aim. To propose the use of the ratio of smears showing cervical intra-eplthelial neoplasia (CIN) III: smears showing signs of malignancy as an indicator for the surveillance of equity in cervical cytology screening, and to apply this indicator to an area of the Western Cape of South Africa.
Results. Marked inequity In screening is demonstrated between metropolitan and non-metropolitan areas, and between different non-metropolitan districts. Inequity in screening between different age groups of women is also found, and this is associated with an inappropriately young age distribution of screening activity.
Conclusion. The application of this indicator in the routine surveillance of screening activity may be useful in monitoring progress towards the implementation of more equitable screening programmes, and the validity of the indicator should be tested in other settings.
Keywords: cervical cytology, screening, equity, surveillance
Cervical cancer is the leading cause of death due to neoplasms in women in the developing world. Pre-vention of cervical cancer relies primarily on cervical cytology screening,1 and screening has been conducted in a range of settings internationally with varying degrees of success.2"3
The opportunistic fashion in which cervical cytology screening has been conducted in South Africa has been inefficient, with low population coverage, and multiple rescreening of a small proportion of the population which excludes most women at high risk.6-7 There has consequently been a failure to impact significantly on the incidence of cervical cancer in the population overall, with considerable waste of resources. Given the deficiency of resources in South Africa and other developing countries it is essential that the resources which are currently spent on screening should be used to maximal effect through the implementation of inter-nationally accepted guidelines for cervical cytology screening programmes.1 These guidelines emphasize the requirements of reaching relatively high risk groups and maximizing coverage.
Department of Community Health, University of Cape Town Medical School, Observatory 7925, South Africa.
Application of the principle of equity in health care delivery serves to render services more efficient and more effective.8 Equity is one of the foremost princi-ples of primary health care and refers to the distribution of services according to demonstrable need rather than on the basis of political or socioeconomic privilege.8
The application of this principle to cervical cytology screening requires the shifting of resources and effort from those groups which are relatively 'overscreened' in relation to their risk of developing cervical cancer to those which are relatively 'underscreened'. This in turn requires the surveillance of screening activity in relation to the risk of developing cervical cancer in different groups. A simple method is needed to focus on groups where screening can be applied intensively to promote equity. This paper proposes indicators for such surveil-lance, and applies these to a defined study area in the Western Cape, South Africa.
The study area includes a large part of greater Cape Town, and the secondary towns and rural area extending east along the Cape south coast. The area encompasses several magisterial districts, with the non-metropolitan districts each encompassing at least one town from which primary level health services are provided. Some towns also have a district hospital. 46
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Socioeconomic conditions vary to a great extent within, and less so between, districts.
The risk of developing carcinoma of the cervix in individual women is reflected by the presence of pre-malignant lesions of the cervix. It is such lesions which cervical cytology screening aims to detect at a stage which allows the application of a relatively minor in-vasive procedure to prevent the development of cancer. The premalignant lesions are referred to as cervical intra-epithelial neoplasia (CIN) and are graded CIN I—III. There is a natural progression from CIN I to CIN III and on to invasive cancer. However, progression is not inevitable, and the various grades of CIN may regress or remain static. Women with smears showing CIN III are booked for colposcopy at which time they may receive definitive treatment. The usual time for pro-gression from CIN m to invasive cancer is estimated to be 10-15 years.1
METHOD
The proportion of smears showing CIN III in a defined group of women may be used as an indicator of the risk of developing cervical cancer in that group. The proportion of smears showing signs of malignancy in a defined group reflects the extent to which screening has failed in that group.
It follows that the ratio of
the number of smears showing CIN III the number of smears showing signs of malignancy may provide an indicator of the extent of screening in relation to risk for those women who have been reached by the screening programme. A high ratio indicates that the women being screened are at low risk for the development of invasive cervical cancer. This may be because a high level of screening activity allows the detection and treatment of the majority of cervical abnormalities in that community, and/or that the women who are being screened are at relatively low risk of developing cervical cancer due to some other determinant (such as age), despite having developed CIN III.
In contrast, a low ratio indicates that the women being screened are at relatively high risk of develop-ing cervical cancer. This may be due to a low level of screening activity in the community generally, and/ or due to the procedure being conducted selectively on women that have gynaecological symptoms or who are at high risk for some other reason. In a given popu-lation, women's screening history (age at screen-ing, screening frequency, screening interval, screening
coverage) impacts on the numerator and/or the denom-inator of this ratio. The ratio thus provides a composite indicator of the screening history of women in that population.
The overall goal in screening should be to maxim-ize the ratio. However, the principle of equity requires that discrepancies in the ratio between groups (e.g. groups defined by age or by ease of access to preven-tive services) should be minimized. There is therefore no single optimum or overall target ratio in terms of equity. Rather, similar ratios between groups repre-sent greater equity. Nevertheless, a relatively high ratio for each of one or more groups represents a relatively low risk of developing cervical cancer in that or those groups.
The ratio assumes the sensitivity and specificity of the screening test does not vary between groups, and these aspects of the screening process should be mon-itored using routine quality control procedures within, and where necessary between, laboratories.
The information provided by this ratio may be speci-fic to that group of women which has been screened, and may not reflect the extent of screening in relation to risk in the wider target population. This may be over-come by using the incident number of cases of cervical cancer as a denominator in place of the number of smears showing signs of malignancy. In South Africa, however, women use facilities in different regions for different types of medical care (e.g. obtaining a Pap smear as opposed to having gynaecological symptoms investigated). The accurate matching of populations for screening with the base population is beyond the scope of existing health information systems in most developing countries.
A measure of the extent of screening in the target population is the number of smears done per 1000 women in a given time (screening incidence). However, the screening incidence fails to give an indication of the risk of developing cervical cancer in the screened population. A programme in which a disproportionately large number of low risk women were being screened would not be identified by monitoring the screening incidence alone.
A compromise is to use a combination of indica-tors. The screening incidence can be used as a measure of the extent of screening in a defined target group, and the ratio defined above can be used as a measure of the appropriateness (in terms of risk of develop-ing cervical cancer) of screendevelop-ing in those women who have been screened. The use of these indica-tors provides measures by which progress towards the goal of equity in cervical cytology screening can be assessed.
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TABLE 1 Incidence of screening (smears per 1000 women) by age group and area of residence. Row I: No. of women (>I4 years). Row 2: Incidence (smears per 1000 women)
Metro Level 1 All non-metro Herman us Oudtshoom Knysna George Mossel Bay Total <20 70 372 283 14 114 131 725 117 4063 64 2173 116 4885 238 2268 42 84 486 258 20-29 143 426 632 25 641 374 1733 578 5780 289 4460 324 8933 522 4735 172 169 067 593 30-39 113468 443 20 985 285 1435 508 4660 261 3676 299 7315 313 3899 165 134 453 418 Age (years) 4 0 ^ 9 76 562 219 14 996 176 1135 289 3441 205 2710 270 4963 124 2738 94 91 558 212 50-59 52 873 137 11 330 94 1134 166 2462 135 2266 80 3383 75 2085 53 64 203 130 >59 57 114 63 15017 55 2211 66 3261 95 2956 43 4092 46 2497 22 72 131 61 Total 513815 367 102 072 215 8372 296 23 667 190 18 241 210 33 571 273 18 222 109 615 887 342
Application of the Indicator in the Western Cape
All smears done in the public sector in a large and defined portion of the Western Cape region of South Africa are examined at the Groote Schuur Hospital cytopathology laboratory. Data on the number of smears taken and the abnormalities detected categor-ized by age group and area of residence were ob-tained from the computerized records for 1988-1992 inclusive.
Categories for age and area of residence were defined as follows: (1) Age in years (15-19; 20-29; 30-39; 40-^9; 50-59; 60+). (2) Area of residence: In the non-metropolitan areas this was defined by the magisterial (administrative) district in which the facility where the smear was taken was located. The three magisterial districts incorporated in the Southern part of the greater Cape Town area form the sole metropolitan area that is served by the Groote Schuur Hospital cytopath-ology laboratory. These three districts are regarded as a single unit for the purpose of this study. Within this area only smears taken at level 1 services (clinics, day hospitals, and obstetric facilities (including ma-ternity hospitals) were included in the analysis. A large portion of the procedures (including Pap smears) conducted in the level 2 and 3 facilities in the metro-politan area are part of the investigation of symptomatic or ill patients. These facilities are generally not involved in screening according to its strict definition and Pap smears taken at these facilities were excluded
from the analysis. However, the general hospitals in the non-metropolitan areas frequently serve as first level of care centres, and they have been grouped to-gether with non-metropolitan clinics.
Population data on the number of women aged >14 years according to magisterial district and age group was obtained from the 1991 census.9
RESULTS
Five districts submitted less than 10 smears in the period under review, preventing the meaningful calcu-lation of the indicators. These districts were excluded from further analyses.
Table 1 shows the variation in screening incid-ence between the metropolitan and non-metropolitan areas and between different districts within the non-metropolitan area. The peak age-specific screening incidence occurs in the 20-29 age range for all areas.
Table 2 shows the variation in the ratio of smears showing CIN III to malignant and suspicious smears between the metropolitan and non-metropolitan areas and between different districts within the non-metro-politan area. The peak age-specific ratio tends to occur in the 20-29 or 30-39 year age categories for all areas, although the small numbers of smears showing CIN III and signs of malignancy renders the age- and area-specific ratios unstable.
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TABLE 2 Ratio by age group and area of residence. Row I: No. of smears showing cervical intra-cpitheUal neoplasia (CIN) 111. Row 2:
Ratio (CIN III: Malignant), 'e' indicates ratio not calculable owing to denominator being zero
Metro Level 1 All non-metro Hermanus Oudtshoom Knysna George Mossel Bay Total <20 6 3.0 2 e 0 e 0 e 1 e 1 e 0 e 8 4.0 20-29 122 13.6 38 7.6 7 e 12 6.0 3 e 15 7.5 1 1.0 160 11.4 30-39 220 7.6 50 3.8 6 6 0 9 9.0 15 5.0 16 2.7 4 2.0 270 6.4 Age (years) 40-49 105 4.8 32 2.0 5 2.5 15 3.8 4 2.0 7 1.0 1 1.0 137 3.6 50-59 43 1.4 9 1.0 0 e 4 2.0 3 1.0 2 0.7 0 0 52 1.3 >59 13 0.5 6 0.3 0 0 4 1 3 0 0 2 03 0 0 19 0.4 Total 509 4.2 137 2.2 18 3.6 44 3.7 26 2.2 43 1.7 6 0.8 646 3.5
The age-specific ratios of CIN III : malignant and suspicious smears and the age-specific screening incidence show patterns of a peak in the 20-29 year age group declining to low levels for older women. Figure 1 shows these indicators for the metropolitan and non-metropolitan areas separately. The indicators for the non-metropolitan area are consistently lower than for the metropolitan area for all age groups. The age distri-bution for the two indicators follows similar patterns for each area.
The ratio and incidence for all ages together in different districts are shown in Figure 2. It can be seen from this that the consistent pattern shown between the age-specific ratios and the age-specific screening incidence is not reflected in comparing the area-specific pattern of the ratio and screening incidence. The incon-sistency in the pattern is most marked between the districts of Oudtshoom and George. Oudtshoom has the highest ratio among the non-metropolitan areas and only the fourth highest screening incidence. In contrast, George has the second highest screening incidence and only the fourth highest ratio.
The variation in age-specific screening incidence between the non-metropolitan districts is highlighted in Figure 3. Oudtshoom and Mossel Bay show relatively even distributions, with figures for Mossel Bay being the lowest in all age categories. In contrast the distri-bution for George shows a marked peak in the 20-29 year age category and low levels in the categories of 40-49 and above.
DISCUSSION
There is a marked inequity in screening practices for different age groups, as evidenced by the differences between the age-specific screening incidence (Table 1) and the differences between the age-specific ratios (Table 2). There is also a marked inequity between metropolitan and non-metropolitan areas which occurs in all age categories, as evidenced by the differences in the age-specific screening incidences and the diff-erences in the age-specific ratios for each of these two areas (Figure 1). In reflecting the age-specific inequities between the metropolitan and non-metro-politan areas the two indicators follow a consistent pattern. However, this consistent pattern is not evident in examining the non-metropolitan district specific indicators.
The contrasting patterns of the ratio and the screen-ing incidence in comparscreen-ing Oudtshoom and George shows that the practice in Oudtshoom of screening relatively less in the younger age range, and more in the older age range (Figure 3) is more efficient in that the proportion of smears showing CIN III is higher than for George (i.e. the yield of screening is higher). Further-more, the practice in Oudtshoom is more equitable for women in different age categories, in that the difference between the incidence of screening between the age groups (Figure 3) and the relative difference between the ratios for each age group is less (Table 2).
The greater equity achieved by the practice in Oudt-shoom is explained by examining the age at diagnosis
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CIN 111 : Malignant smears No. of smears per 1000 women
<20
700
20-29 30-39 40-49 50-59 >65
Age
^ Metro ratio <y Metro incidence ^"Non-metro ratio "•'Non-metro incidence
FIGURE ] Ratio and screening incidence by age and area of residence
Number of smears per 1 0 0 0 women
100 200 300 400 500
0 1 2 3 4
CIN III: Malignant and suspicious smears
^ Ratio 0 Smears per 1000 women
FIGURE 2 Ratio and screening incidence by magisterial district
of cervical cancer10 (Figure 4). Given that the time for progression from CIN III to invasive cancer is esti-mated at 10-15 years, the pattern of screening in Oudt-shoorn is more likely to identify women who are going to develop cancer during the period in which they have CIN III.
Thus the relatively high ratio in relation to incidence of screening achieved in Oudtshoorn may be explained by the age distribution of women screened. However, the situation in Mossel Bay shows that a more equitable
age distribution of screening is not in itself sufficient to influence the picture reflected by these indicators. Here the distribution of screening is relatively even, but the incidence of screening across all age categories is low. In contrast to Oudtshoorn the ratio in Mossel Bay is low both in absolute terms and in relation to the screening incidence (Figure 2). In Hermanus the age distribution of screening is relatively uneven, but the level within each age category is relatively high and the ratio is high (Figure 2).
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No. of smoars per 1000 women 20-29 50-59 >65 "+" Hormanus "*" Oudtshoorn ~*~ Knyana "•" Mossol Bay "*• George 30-39 40-49 Age
FIGURE 3 Age-specific screening incidence for non-metro magisterial districts
Incidence (per 100 000) 120 100 80 60 40 20 t o
5
O) in CN6
CN O in6
CO O) T in c C O •< \J •!• • 5-4 9 in6
in en in in ins
6
CO O) CD in CD + in A g eDrawn from data published by the National Cancer Registry of South Africa (Sitas 1 994) FIGURE 4 Cancer in the cervix in South Africa: age-specific incidence
It appears therefore that the ratio is dependent on the age distribution of screening and on the screening incidence. This indicates that the ratio may be used to monitor both the equity of screening practice in differ-ent groups and the levels of screening activity in these groups. Unlike screening incidence, calculation of the ratio does not require census data, and can be derived relatively simply from laboratory data alone. The ratio may have potential as an easily derived indicator of overall screening activity, with particular value in less
developed countries where census data and cancer reg-istration are poor or non-existent. If a minimal source of data (as required for the ratio) can provide a valid measure to change the focus of screening as part of sur-veillance for equity its application may provide guide-lines for broad shifts in screening policy in other situations.
In theory the ratio would not allow a distinction between two districts or groups where the number of CIN III and malignant and suspicious smears were in
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proportion to each other, but in which the proportion of the two categories of abnormalities in relation to the total number of smears differed for the two districts or groups. However, this situation was not encountered in applying the use of the ratio to real data as has been done here, and it may well remain only of theoretical concern. The variation in risk of developing cervical cancer between different areas as reflected by the ratio may be the result of factors unrelated to screening activity. Consistent results in applying the indicators described in this paper to data sets from other areas or at other times will provide evidence against this possibility.
The haphazard and spontaneous nature in which screening has been conducted has resulted in marked inequity in screening activity between women of dif-ferent ages and between difdif-ferent areas in South Africa. The ratio of CIN III : malignant and suspicious smears may be a useful indicator of the relative level and appro-priateness of screening activity between different groups. It is necessary that the ratio is tested in a variety of settings in order to establish its validity as an indi-cator for equity and for screening activity. The main points for consideration that emerge for the health services in the area where this study was conducted are: (1) Attention should be paid to screening women of 3=40 years, while rescreening of younger women should be reduced; (2) Attention should be paid to the appro-priate screening of women in the non-metropolitan areas; (3) The practice of screening in facilities in those areas where the ratio is shown to be low, and particu-larly from where few or no smears are being submitted, should be investigated. Similarly, the practice in those areas where the ratio is found to be especially high should be investigated.
The application of an indicator for equity presents a mechanism for use in controlling efficiency and effect-iveness of cervical cytology screening. The ratio of CIN III : malignant and suspicious smears is based solely on laboratory data and may be particularly useful in developing countries where health information systems
are deficient and cervical cancer is a major cause of mortality.
ACKNOWLEDGEMENTS
We would like to thank Dr G Learmonth for providing access to laboratory data, Ms S Wilson and Ms S Lyon for extracting the data, and Dr G Learmonth, Dr D Bradshaw, Dr M Thompson for their critical review of earlier drafts of the manuscript.
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