Cylopathology 1992,3,79-83
An audit of cervical cancer deaths in Nottingham S. H. W I L S O N A N D J. J O H N S O N * Department of Public Health Medicine and Epidemiology, University of Nottingham, Medical School, Queen’s Medical Centre and *Department of Cytopathology, City Hospital, Nottingham, UK Accepted f o r publication 26 November 1991
WILSON S. H. AND JOHNSON J.
(1992) Cytopathology 3,79-83
An audit of cervical cancer deaths in Nottingham Death certificates were reviewed and 57 women were identified whose primary cause of death was cervical cancer. Their cervical smear records were reviewed from laboratory files. Only nine had participated in the cervical cancer screening programme before the diagnosis of cervical cancer was made. One woman had an abnormal smear as a result of cervical screening but failed to attend for follow-up. The problem of false negative smears is also addressed and the value of review of negative smears for the purposes of cytology audit is emphasized. Keywords: audit, cervical cancer deaths
INTRODUCTION The recent review of the national cervical cancer screening programme has shown that many women who are at high risk of cervical cancer do not come forward for screening’. Moreover, there is evidence that even when women participate in the cervical screening programme the tumour may be missed and they may still die from the disease2. In order to remedy this unsatisfactory situation, it has been suggested that a confidential enquiry into each death from cervical cancer should be carried out3. In order to audit the quality of the screening programme in Nottingham, a review of all cervical cancer deaths in the Nottingham district over a period of 2 years was carried out in 1988. We report our findings and discuss the lessons we have learnt from the analysis of these data. METHODS Death certificates issued between 1 January 1986 and 31 December 1987 in the Nottingham district were examined, and women for whom cervical cancer was recorded as a primary Correspondence: Dr S . H. Wilson, Department of Public Health Medicine and Epidemiology, University of Nottingham, Medical School, Queen’s Medical Centre, Nottingham NG7 2UH, UK.
80 S. H. Wilson & J.Johnson
cause of death were identified. The cytology records at the City Hospital, Nottingham were searched for evidence of a cervical smear from these women. It was the practice of the cytology laboratory at the time of this study to store all abnormal cervical smears; however, all smears reported as negative were discarded after approximately 1 year due to limited storage capacity. Thus, it was possible to review the previous abnormal smears of women who had an abnormal smear history, but it was not possible to review all previous negative smears. The gynaecological tumour registry held by the Department of Public Health Medicine, University of Nottingham was also consulted for clinical and histological information about these cases. Histology records at the University Hospital were also searched. RESULTS 57 women were identified in whom cervical cancer was recorded as the primary cause of death. Their ages ranged from 29 to 92 years (mean age 61 years); 16 women were under the age of 50 (28%). The social and demographic characteristics of the women have been previously described4. Records of 36 women were retrieved from tumour registry files. A diagnostic biopsy was available for review from 48 women. Search of the histology and cytology records revealed that 49 women had a diagnostic smear and/or biopsy processed by one of the two pathology laboratories in the district. In 33 of the 49 cases (67%) a smear had been taken as part of the diagnostic workup when the patient presented at the gynaecological clinic with symptoms. In nine cases, smears had been taken as part of the national cervical screening programme for the prevention of cervical cancer. No clinical, histological or cytology record could be found for eight women. Screening histories and clinical details of the nine patients who had had a smear taken as part of the national screening programmes are presented in Table 1. Their case histories are summarized below. Case 1
A routine smear taken 11 years prior to the diagnosis of cervical cancer contained no malignant cells. There were no arrangements for routine recall in this case. A second smear taken at the out-patient clinic at the time of diagnosis showed severe dyskariosis and invasive cancer was suspected. Stage 2 cervical cancer was confirmed 1 month later; the patient survived 2 months. Case 2 A routine smear taken in 1971contained no malignant cells. A second routine smear taken in 1979 showed mild dyskariosis. Although a repeat smear was requested at this time it was not taken, despite reminder letters to the general practitioner from the laboratory. Moreover, the woman received no notification of her abnormal smear results. She presented with postmenopausal bleeding at the hospital clinic 6 years later with stage 1b cervical cancer, and died within 8 months. Case 3 A normal smear report was issued 7 years before the patient presented with postmenopausal bleeding and stage 3 cervical cancer was diagnosed. The negative smear was not available for
Cervical cancer deaths 8 1 Table 1. Screening histories of women dying from cervical cancer in Nottingham in 1986 and 1987
Interval between
Case no.
Ageat diagnosis (years)
last screening smear& diagnosis (years)
1 2
53 60
11 6
3
75
7
37 32 39 33 29 30
Result of last screening smear
Clinical stage at diagnosis
Problem identified
NMC TV+ mild dyskariosis; repeat in 4/12 requested NMC
2 Ib
No routine recall NOfollow-up
3
NMC NMC TV+pus+ pus+ +NMC pus+ NMC pus+ +NMC
2b lb
No routine recall ?falsenegative report ?False negative report ?False negative report Inadequate follow-up NOfollow-up NOfollow-up NOfOllOw-up
+
+ ++ +
++
Ib 4
2b 2 ~~
NMC = n o malignant cells; TV = Trichomas vaginalis
review and the possibility that a false negative report had been given could not be excluded. She survived 2 months.
Case 4 This woman had two normal smears at 3-yearly intervals before presenting with clinical symptoms of cervical cancer. Biopsy revealed stage 2b cervical cancer and she survived 17 months. Routine negative smears had been discarded so it was not possible to exclude false negative reporting in this case. Case 5
This woman had a normal cervical smear 1 year prior to a diagnosis of cervical cancer stage 1b. She was referred for biopsy by the smear-taker because of the suspicious appearance of her cervix. The possibility of a false negative report cannot be excluded as the smear was not available for review. She died within 9 months of diagnosis.
Case 6 A cervical smear, taken 12 months before the clinical diagnosis of cervical cancer was made, was found to contain Trichomonas and numerous pus cells. No malignant cells were seen.
82 S. H . Wilson & J. Johnson The patient was referred for biopsy because the smear taker noted an ‘unhealthy looking cervix’ and stage 1b cervical cancer was diagnosed. She survived 1 month after diagnosis. Case 7
An abnormal smear in 1978 had been followed by six normal smears over a 4-year period. A smear taken in 1983contained no malignant cells, although many pus cells were noted on the report. She had no further smear but in 1987 a biopsy confirmed stage 4 cervical cancer. Despite radical surgery she survived only 9 months. Case 8
A smear was taken in an ante-natal clinic and reported to contain many pus cells but no malignant cells were seen. She received no follow-up and subsequently presented 5 years later with stage 2b cervical cancer and died at the age of 30,14 months after diagnosis. Case 9
A routine smear taken by a general practitioner was reported as containing many pus cells but no malignant cells were seen and the patient was never followed-up. Diagnosis of stage 2 cervical cancer was made 3 years later. Six months after a hysterectomy her smear was normal, but she died 26 months later. There was no record of any other post-hysterectomy smear being taken. DISCUSSION Screening rate
Only nine of the 57 women who died from cervical cancer in 1986 and 1987 had ever participated in the national screening programme. In this district in 1986 the screening rates were 3 5 4 5 % for the 50-64-year age-group and 4 6 5 8 % for the 36-49-year age-group. The screening rate in the group of women who died was low (16%) but is unlikely to reflect the true picture because of the limited access to complete records. The issue of invitations for screening and the emphasis on targets for screening in the new UK general practitioner contract5should improve district screening rates in the future. It is encouraging to report that 65% of unscreened women aged 4 5 4 6 responded to the first phase of the computerized call scheme in this district6. Adequacy of follow-up of abnormal smears
The evidence that some women who had availed themselves of the screening programme had nevertheless developed invasive cervical cancer is a cause for concern. In 1984 Elwood’ reported that only 59% of Nottingham women with abnormal smears received adequate follow-up. Subsequently it was shown that women with an abnormal smear report who were inadequately followed-up had a 29% chance of harbouring CIN 2 or worse’. In our study, case 2 might have received adequate treatment if her abnormal smear had been conscientiously followed-up. As a result of our study the screening laboratory now has a computerized system for the follow-up of abnormal smears and, although follow-up remains
Cervical cancer deaths 83
the responsibility of the smear taker, default in recall automatically generates reminder letters. Delegation of follow-up to the general practitioner of abnormalities detected in hospital clinics has to be notified to the laboratory so that subsequent reminder letters are correctly addressed and responsibility for follow-up made explicit. False negative results
Six women in our review had a negative screening smear within 5 years of the diagnosis of cervical cancer being made. These slides were not available for review. The possibility of false negatives cannot be excluded. Storage space for at least the previous 3 years’ slides is now available and is being expanded to ensure that previous negative smears can be reviewed. Adequacy of smears
There are four cases in our review (cases 6 9 ) where masking by pus and blood cells should have resulted in the smear being rejected as unsatisfactory and a repeat smear requested. The laboratory now has a written policy about adequacy of smears based on the guidelines set out by the British Society for Clinical Cytology. The usefulness of audit
This exercise was valuable in demonstrating significant deficiencies in both the organisational and technical aspects of the screening programme. The results were of interest to both clinicians and managers and led to some important changes in practice. This audit is a good example of cooperation between Health Authority managers, cytology staff and Public Health physicians. ACKNOWLEDGEMENTS We are grateful to the staff at the University and City Hospitals’ Pathology Departments for extracting cytology and histology reports, to the District Cytology Group for its support, and to the secretarial staff in the Department of Public Health Medicine and Epidemiology for preparing the manuscript.
REFERENCES 1 IARC Working Group on Evaluation of cervical
cancer screening programmes. Screening for squarnous cervical cancer: duration of low risk after negative results of cervical cytology and its irnplications for screening policies. Br Med J 1986 293 659-64. 2 Paterson MEL, Peel KR, J o s h CAF. Cervical smear histories of 500 women with invasive cervical cancer in Yorkshire. Br Med J 1984; 289 8 9 6 8 . 3 Mills A. Confidential enquiry into deaths from cervical cancer? Br J Family Planning 1987; 13 1. 4 Wilson S, Fowler P. The social and demographic
5
6
7
8
characteristics of women dying from cervical cancer in Nottingham. Public Health 1990; 104.449-55. General Practice in the National Health Service: The 1990 Contract. London: Health Departments of Great Britain, 1989. Wilson SH, Johnson J. Abnormalities detected in unscreened women invited for cervical cancer screening. Health Trends 1990; 2 1 6 7 7 . Elwood JM, Cotton R, Johnson J et al. Are patients with abnormal cervical smears adequately managed? Br Med J 1984; 289 890-4. Cotton RE, Elwood JM, Jones G. Results of delayed follow-up of abnormal cervical smears. Br MedJ 1986; 292:799-800.
An audit of cervical cancer deaths in Nottingham S. H. W I L S O N A N D J. J O H N S O N * Department of Public Health Medicine and Epidemiology, University of Nottingham, Medical School, Queen’s Medical Centre and *Department of Cytopathology, City Hospital, Nottingham, UK Accepted f o r publication 26 November 1991
WILSON S. H. AND JOHNSON J.
(1992) Cytopathology 3,79-83
An audit of cervical cancer deaths in Nottingham Death certificates were reviewed and 57 women were identified whose primary cause of death was cervical cancer. Their cervical smear records were reviewed from laboratory files. Only nine had participated in the cervical cancer screening programme before the diagnosis of cervical cancer was made. One woman had an abnormal smear as a result of cervical screening but failed to attend for follow-up. The problem of false negative smears is also addressed and the value of review of negative smears for the purposes of cytology audit is emphasized. Keywords: audit, cervical cancer deaths
INTRODUCTION The recent review of the national cervical cancer screening programme has shown that many women who are at high risk of cervical cancer do not come forward for screening’. Moreover, there is evidence that even when women participate in the cervical screening programme the tumour may be missed and they may still die from the disease2. In order to remedy this unsatisfactory situation, it has been suggested that a confidential enquiry into each death from cervical cancer should be carried out3. In order to audit the quality of the screening programme in Nottingham, a review of all cervical cancer deaths in the Nottingham district over a period of 2 years was carried out in 1988. We report our findings and discuss the lessons we have learnt from the analysis of these data. METHODS Death certificates issued between 1 January 1986 and 31 December 1987 in the Nottingham district were examined, and women for whom cervical cancer was recorded as a primary Correspondence: Dr S . H. Wilson, Department of Public Health Medicine and Epidemiology, University of Nottingham, Medical School, Queen’s Medical Centre, Nottingham NG7 2UH, UK.
80 S. H. Wilson & J.Johnson
cause of death were identified. The cytology records at the City Hospital, Nottingham were searched for evidence of a cervical smear from these women. It was the practice of the cytology laboratory at the time of this study to store all abnormal cervical smears; however, all smears reported as negative were discarded after approximately 1 year due to limited storage capacity. Thus, it was possible to review the previous abnormal smears of women who had an abnormal smear history, but it was not possible to review all previous negative smears. The gynaecological tumour registry held by the Department of Public Health Medicine, University of Nottingham was also consulted for clinical and histological information about these cases. Histology records at the University Hospital were also searched. RESULTS 57 women were identified in whom cervical cancer was recorded as the primary cause of death. Their ages ranged from 29 to 92 years (mean age 61 years); 16 women were under the age of 50 (28%). The social and demographic characteristics of the women have been previously described4. Records of 36 women were retrieved from tumour registry files. A diagnostic biopsy was available for review from 48 women. Search of the histology and cytology records revealed that 49 women had a diagnostic smear and/or biopsy processed by one of the two pathology laboratories in the district. In 33 of the 49 cases (67%) a smear had been taken as part of the diagnostic workup when the patient presented at the gynaecological clinic with symptoms. In nine cases, smears had been taken as part of the national cervical screening programme for the prevention of cervical cancer. No clinical, histological or cytology record could be found for eight women. Screening histories and clinical details of the nine patients who had had a smear taken as part of the national screening programmes are presented in Table 1. Their case histories are summarized below. Case 1
A routine smear taken 11 years prior to the diagnosis of cervical cancer contained no malignant cells. There were no arrangements for routine recall in this case. A second smear taken at the out-patient clinic at the time of diagnosis showed severe dyskariosis and invasive cancer was suspected. Stage 2 cervical cancer was confirmed 1 month later; the patient survived 2 months. Case 2 A routine smear taken in 1971contained no malignant cells. A second routine smear taken in 1979 showed mild dyskariosis. Although a repeat smear was requested at this time it was not taken, despite reminder letters to the general practitioner from the laboratory. Moreover, the woman received no notification of her abnormal smear results. She presented with postmenopausal bleeding at the hospital clinic 6 years later with stage 1b cervical cancer, and died within 8 months. Case 3 A normal smear report was issued 7 years before the patient presented with postmenopausal bleeding and stage 3 cervical cancer was diagnosed. The negative smear was not available for
Cervical cancer deaths 8 1 Table 1. Screening histories of women dying from cervical cancer in Nottingham in 1986 and 1987
Interval between
Case no.
Ageat diagnosis (years)
last screening smear& diagnosis (years)
1 2
53 60
11 6
3
75
7
37 32 39 33 29 30
Result of last screening smear
Clinical stage at diagnosis
Problem identified
NMC TV+ mild dyskariosis; repeat in 4/12 requested NMC
2 Ib
No routine recall NOfollow-up
3
NMC NMC TV+pus+ pus+ +NMC pus+ NMC pus+ +NMC
2b lb
No routine recall ?falsenegative report ?False negative report ?False negative report Inadequate follow-up NOfollow-up NOfollow-up NOfOllOw-up
+
+ ++ +
++
Ib 4
2b 2 ~~
NMC = n o malignant cells; TV = Trichomas vaginalis
review and the possibility that a false negative report had been given could not be excluded. She survived 2 months.
Case 4 This woman had two normal smears at 3-yearly intervals before presenting with clinical symptoms of cervical cancer. Biopsy revealed stage 2b cervical cancer and she survived 17 months. Routine negative smears had been discarded so it was not possible to exclude false negative reporting in this case. Case 5
This woman had a normal cervical smear 1 year prior to a diagnosis of cervical cancer stage 1b. She was referred for biopsy by the smear-taker because of the suspicious appearance of her cervix. The possibility of a false negative report cannot be excluded as the smear was not available for review. She died within 9 months of diagnosis.
Case 6 A cervical smear, taken 12 months before the clinical diagnosis of cervical cancer was made, was found to contain Trichomonas and numerous pus cells. No malignant cells were seen.
82 S. H . Wilson & J. Johnson The patient was referred for biopsy because the smear taker noted an ‘unhealthy looking cervix’ and stage 1b cervical cancer was diagnosed. She survived 1 month after diagnosis. Case 7
An abnormal smear in 1978 had been followed by six normal smears over a 4-year period. A smear taken in 1983contained no malignant cells, although many pus cells were noted on the report. She had no further smear but in 1987 a biopsy confirmed stage 4 cervical cancer. Despite radical surgery she survived only 9 months. Case 8
A smear was taken in an ante-natal clinic and reported to contain many pus cells but no malignant cells were seen. She received no follow-up and subsequently presented 5 years later with stage 2b cervical cancer and died at the age of 30,14 months after diagnosis. Case 9
A routine smear taken by a general practitioner was reported as containing many pus cells but no malignant cells were seen and the patient was never followed-up. Diagnosis of stage 2 cervical cancer was made 3 years later. Six months after a hysterectomy her smear was normal, but she died 26 months later. There was no record of any other post-hysterectomy smear being taken. DISCUSSION Screening rate
Only nine of the 57 women who died from cervical cancer in 1986 and 1987 had ever participated in the national screening programme. In this district in 1986 the screening rates were 3 5 4 5 % for the 50-64-year age-group and 4 6 5 8 % for the 36-49-year age-group. The screening rate in the group of women who died was low (16%) but is unlikely to reflect the true picture because of the limited access to complete records. The issue of invitations for screening and the emphasis on targets for screening in the new UK general practitioner contract5should improve district screening rates in the future. It is encouraging to report that 65% of unscreened women aged 4 5 4 6 responded to the first phase of the computerized call scheme in this district6. Adequacy of follow-up of abnormal smears
The evidence that some women who had availed themselves of the screening programme had nevertheless developed invasive cervical cancer is a cause for concern. In 1984 Elwood’ reported that only 59% of Nottingham women with abnormal smears received adequate follow-up. Subsequently it was shown that women with an abnormal smear report who were inadequately followed-up had a 29% chance of harbouring CIN 2 or worse’. In our study, case 2 might have received adequate treatment if her abnormal smear had been conscientiously followed-up. As a result of our study the screening laboratory now has a computerized system for the follow-up of abnormal smears and, although follow-up remains
Cervical cancer deaths 83
the responsibility of the smear taker, default in recall automatically generates reminder letters. Delegation of follow-up to the general practitioner of abnormalities detected in hospital clinics has to be notified to the laboratory so that subsequent reminder letters are correctly addressed and responsibility for follow-up made explicit. False negative results
Six women in our review had a negative screening smear within 5 years of the diagnosis of cervical cancer being made. These slides were not available for review. The possibility of false negatives cannot be excluded. Storage space for at least the previous 3 years’ slides is now available and is being expanded to ensure that previous negative smears can be reviewed. Adequacy of smears
There are four cases in our review (cases 6 9 ) where masking by pus and blood cells should have resulted in the smear being rejected as unsatisfactory and a repeat smear requested. The laboratory now has a written policy about adequacy of smears based on the guidelines set out by the British Society for Clinical Cytology. The usefulness of audit
This exercise was valuable in demonstrating significant deficiencies in both the organisational and technical aspects of the screening programme. The results were of interest to both clinicians and managers and led to some important changes in practice. This audit is a good example of cooperation between Health Authority managers, cytology staff and Public Health physicians. ACKNOWLEDGEMENTS We are grateful to the staff at the University and City Hospitals’ Pathology Departments for extracting cytology and histology reports, to the District Cytology Group for its support, and to the secretarial staff in the Department of Public Health Medicine and Epidemiology for preparing the manuscript.
REFERENCES 1 IARC Working Group on Evaluation of cervical
cancer screening programmes. Screening for squarnous cervical cancer: duration of low risk after negative results of cervical cytology and its irnplications for screening policies. Br Med J 1986 293 659-64. 2 Paterson MEL, Peel KR, J o s h CAF. Cervical smear histories of 500 women with invasive cervical cancer in Yorkshire. Br Med J 1984; 289 8 9 6 8 . 3 Mills A. Confidential enquiry into deaths from cervical cancer? Br J Family Planning 1987; 13 1. 4 Wilson S, Fowler P. The social and demographic
5
6
7
8
characteristics of women dying from cervical cancer in Nottingham. Public Health 1990; 104.449-55. General Practice in the National Health Service: The 1990 Contract. London: Health Departments of Great Britain, 1989. Wilson SH, Johnson J. Abnormalities detected in unscreened women invited for cervical cancer screening. Health Trends 1990; 2 1 6 7 7 . Elwood JM, Cotton R, Johnson J et al. Are patients with abnormal cervical smears adequately managed? Br Med J 1984; 289 890-4. Cotton RE, Elwood JM, Jones G. Results of delayed follow-up of abnormal cervical smears. Br MedJ 1986; 292:799-800.
