Cervical cancer is the most common malignancy affecting South African women aged 15–44 years, with a higher prevalence among women living with HIV (WLWH). Despite recommendations for a screening target of 70%, the reported rate of cervical cancer screening in South Africa is 19.3%.
To investigate the adherence of healthcare workers to cervical cancer screening guidelines in a tertiary-level HIV clinic.
A retrospective cross-sectional record audit of women attending the Charlotte Maxeke Johannesburg Academic Hospital HIV Clinic over a 1-month period.
Out of 403 WLWH who attended the clinic, 180 (44.7%) were screened for cervical cancer in the 3 years prior to the index consultation. Only 115 (51.6%) of those women with no record of prior screening were subsequently referred for screening. Women who had undergone screening in the previous 3 years were significantly older (47 years vs 44 years,
The rate of cervical cancer screening in our institution is below that recommended by the World Health Organization and the South African National Department of Health.
Despite being a preventable disease, cervical cancer is the second most common malignancy affecting South African women, second only to breast cancer, and is the most common malignancy in women aged between 15 and 45 years. Approximately 11 000 women are diagnosed with and 5900 women die from cervical cancer annually in South Africa.
Southern Africa has the highest incidence of HIV worldwide, with the overall prevalence in South Africa being 13.9%. However, this percentage is considerably higher in South Africa’s female population with current statistics showing that 24.1% of women of childbearing age are living with HIV.
Women living with HIV (WLWH) are six times more likely to develop cervical cancer compared to HIV-negative women, and the malignancy is classified as an AIDS-defining illness.
Data from the Charlotte Maxeke Johannesburg Academic Hospital (CMJAH) postnatal clinic showed that 47% of WLWH who had a Papanicolaou (Pap) smear done in the postnatal period had an abnormal smear.
The World Health Organization (WHO) has estimated that to prevent 62 million deaths from cervical cancer over the next 100 years, and effectively eliminate the disease, a cervical cancer screening target of 70% needs to be met by 2030 (in addition to HPV vaccination and treatment targets of 90%).
The South African Society of Obstetricians and Gynaecologists (SASOG) currently recommends that in WLWH cervical cancer screening should start at the time of HIV diagnosis and continue three-yearly in low-resource settings, or annually in high-resource settings, and continue throughout the woman’s lifetime. The South African national guidelines recommend three-yearly screening from the time of HIV diagnosis.
Considering the association between HIV and cervical cancer we aimed to investigate the adherence of healthcare workers to nationally recommended cervical cancer screening guidelines in a tertiary-level HIV clinic.
We conducted a retrospective cross-sectional record audit of all female adult patients attending the CMJAH HIV Clinic from 01 October 2020 to 31 October 2020. The CMJAH HIV Clinic is a large tertiary-level HIV clinic that acts as a referral centre for people living with HIV from urban Johannesburg and surrounds. Approximately 10 000 patients are seen per year, 60% of whom are women. A minimum of 214 files needed to be audited to achieve a 95% confidence level with a 5% of margin error. Male patients were excluded from the study as were female patients under the age of 18, and those who had undergone a total hysterectomy.
Data, including demographic data, date of last cervical screening, result of previous cervical screening, record of referral for cervical screening, time since HIV diagnosis, most recent CD4 count, HIV viral load (VL) within the previous year and record of any previously abnormal cervical screening or previous hysterectomy, were captured directly from patient files using Google Forms (Google LLC, Mountain View, California, United States) and subsequently exported into Microsoft Excel 16.67 (Microsoft Corporation, Redmond, Washington, United States) for analysis. Data were not retrieved from the NHLS as the study was an audit of the clinic record. No patient identifying data were collected; however, files were marked once analysed to avoid duplicate data entry.
Data were analysed using Microsoft Excel 16.67 (Microsoft Corporation, Redmond, Washington, United States) and Prism 8.4 (GraphPad Software Inc., La Jolla, California, United States). Non-parametric statistical tests were used as data were non-normally distributed using the Shapiro-Wilk Normality test. Categorical variables, such as the number of women who had undergone a cervical smear, are presented as percentages and frequencies, and Pearson’s chi-square test was used to analyse differences in categorical data between groups. Continuous variables such as age, CD4 and HIV VL are presented as medians with interquartile ranges (IQRs), and the Mann-Whitney test was used to compare continuous variables between two groups. A
Permission to conduct the study was granted by the Research Committee and Head of Internal Medicine at CMJAH. Ethical clearance was obtained from the University of the Witwatersrand Human Research Ethics Committee (Medical) with clearance certificate M2011107. The study was also registered on the National Health Research Database.
During the period under audit, 430 WLWH were seen at the clinic. Twenty-six women had undergone a previous total hysterectomy and one was under the age of 18 years, resulting in a final cohort of 403 women. The median age of this cohort was 46 years (IQR: 39–52 years). The median time from diagnosis to the index consultation was 132 months (IQR: 84–176 months). Two hundred and thirty women (57%) had a known month and year of HIV diagnosis and the remainder, 173 (43%), only a known year of diagnosis. In the case of woman without a known month of diagnosis the month of diagnosis was assumed to be January for calculation purposes.
A CD4 count was available for 389 women. The median CD4 count for those with available data was 523 cells/mm3 (IQR: 345 cells/mm3 – 722 cells/mm3) and 36 women (8.9%) had a CD4 count of less than 200 cells/mm3 at the index consultation. HIV VL data was available for 402 women (99.8%) and most women (
Concerningly, only 180 women (44.7%) were noted to have undergone cervical cancer screening in the 3 years prior to the index consultation and 223 (55.3%) had no record of screening in the same period. Among women who had undergone cervical cancer screening in the preceding 3 years, 96 smears (53.3%) were reported as negative for intraepithelial malignancy (NILM), 16 (8.9%) as low-grade squamous intraepithelial lesion (LSIL), 6 (3.3%) as high-grade intraepithelial squamous lesion (HSIL) and 4 (2.2%) had lesions recorded as ‘other’. Fifty-eight (32.2%) women did not have a smear result recorded in their clinic file despite having undergone screening.
The differences between screened and unscreened women are described in
Comparison of women who were and were not screened for cervical cancer in the 3 years prior to the index consultation.
| Variable | Total cohort ( |
Screened ( |
Not screened ( |
|||||||
|---|---|---|---|---|---|---|---|---|---|---|
| % | IQR | % | IQR | % | IQR | |||||
| Age (years) | 46 | - | 39–52 | 47 | - | 41–52 | 44 | - | 38–52 | 0.046** |
| Time since HIV diagnosis (months) | 132 | - | 84–176 | 144 | - | 98–181 | 126 | - | 72–170 | 0.0011** |
| CD4 count, cells/mm3 | 523 |
- | 345–722 | 529 |
- | 358–729 | 521 |
- | 306–714 | 0.247** |
| HIV viral load < 50 copies/mL | 343 | 85.3 | - | 155 | 86.1 | - | 188 | 84.3 | - | 0.674* |
| HIV viral load > 50 copies/mL | 59 | 14.7 | - | 25 | 13.9 | - | 34 | 15.4 | - | - |
Note:
IQR, interquartile range.
, Total cohort out of
, Screened out of
, not screened out of
In the 223 women who had no record of previous cervical cancer screening only 115 (51.6%) women were noted to have been subsequently referred for screening, as shown in
Comparison of women who had not been screened for cervical cancer in the 3 years prior to the index consultation and who were or were not referred for screening.
| Variable | Total ( |
Referred ( |
Not referred ( |
|||||||
|---|---|---|---|---|---|---|---|---|---|---|
| % | IQR | % | IQR | % | IQR | |||||
| Age, years | 44 | - | 38–52 | 45 | - | 39–52 | 44 | - | 37–51 | 0.496** |
| Time since HIV diagnosis, months | 125 | - | 65–168 | 132 | - | 92–170 | 118 | - | 48–158 | 0.021** |
| CD4 count, cells/mm3 | 521 |
- | 306–714 | 530 |
- | 344–718 | 519 |
- | 264–720 | 0.900** |
| Viral load < 50 copies/mL | 188 | 84.6 | - | 103 | 89.6 | - | 85 | 79.4 | - | 0.041* |
| Viral load > 50 copies/mL | 34 | 15.4 | - | 12 | 10.4 | - | 22 | 20.6 | - | - |
Note:
IQR, interquartile range.
, Total out of
, referred out of
, not referred out of
There was no significant difference in the age of women who had and had not been referred for a cervical smear (45 years vs 44 years,
Women living with HIV have a significantly increased risk of cervical cancer. Ongoing population-wide efforts to detect non-invasive disease are recommended across national and international guidelines.
In this audit, we report on 403 WLWH attending a large HIV clinic in a tertiary centre with direct access to Gynaecology services, in Johannesburg. We show that the target of the National Programme for Cervical Cancer Screening was not met. Fewer than half (44.7%) of the women seen during the study period had undergone screening for cervical cancer within the preceding 3 years. In a similar cross-sectional study among WLWH in Uganda, 44% of women had ever been screened for cervical cancer, with 16.1% having been screened in the preceding year.
Women who had undergone screening for cervical cancer were significantly older than those who had not undergone screening. This may reflect adherence to national guidelines for women without HIV (i.e. screening at age 30, 40 and 50 years) and lack of knowledge of the HIV-specific guidelines. While this result is statistically significant it may not be clinically relevant; considering the median age in both groups was greater than 40 years.
We observed that women who had undergone screening were more likely to have been living with HIV for longer, suggesting that women in care for longer are more likely to be aware of the need for cervical cancer screening and may request referral or self-refer for screening. This is similar to a finding in an Ethiopian study where uptake of cervical cancer screening was significantly higher in women who had been living with HIV for 10 years or longer.
It was not possible to assess reasons for lack of referral in this study as a formal assessment through staff interviews has not taken place. However, women requiring cervical screening are referred to their local (primary care) clinic and there is no standard form or referral letter in use for this. This may reflect an extra administrative burden where clinicians are required to write a referral letter for their patients to have cervical screening. Sigfrid and colleagues suggest that integrating HIV care and cervical cancer screening is both ‘feasible as well as acceptable to women living with HIV’.
Finally, we are encouraged by the number of WLWH in our clinic who had a recent VL and by the rate of viral suppression among WLWH in our clinic.
Our study was limited by its retrospective nature in that incomplete patient notes may have limited the amount of information captured from each file – women may have been referred for or undergone cervical cancer screening but not had this noted in their file. Additionally, the NHLS system was not checked when results were not recorded in the patient record, thus several patients may have been screened with the result not recorded in the patient record.
Our study suggests poor adherence to guideline-recommended cervical cancer screening among WLWH in a single specialised centre. The care of people living with HIV is a complex and multifaceted task involving treatment of existing pathology and screening for co-morbid conditions, including cervical cancer. Although this study exhibited promising rates of viral suppression, that is not the only objective of HIV care. Our audit has highlighted substantial gaps in cervical cancer screening as part of the overall management of WLWH at a tertiary-level. This raises concerns for the cervical cancer screening programmes at other tertiary hospitals and, perhaps, more so at lower-level facilities. Furthermore, it highlights the challenges associated with a compartmentalised approach to HIV care with different tasks allocated to different facilities. This ultimately adds further time and financial burdens onto the patient and increases the risk of poor adherence. The reasons for these gaps in care are unclear; however, this audit may serve as a baseline reference to necessitate an intervention and prompt future investigation and quality improvement audits to improve overall care and patient outcomes.
The authors wish to thank the staff of the CMJAH HIV Clinic for their assistance with data collection.
The authors declare that they have no financial or personal relationships that may have inappropriately influenced them in writing this article.
J.Z. and N.I. conceived the study. J.B., A.S., L. Moonsamy and N.A. were responsible for data collection and cleaning. A.S. and J.Z. performed statistical analysis. J.Z., L. Murray, N.I., L. Mbodi and S.S. drafted the initial manuscript and all authors contributed to the final manuscript.
The authors received no financial support for the research, authorship or publication of this article.
The data that support the findings of this study are available from the corresponding author, J.Z., upon reasonable request.
The views expressed in the submitted article are the authors’ own and not an official position of the institution.