30th July 2010, Volume 123 Number 1319

Jasmin Grewal, Michele Lowe, Hilary Gerrard, Rebecca Henley, Nicky Perkins, Simon Briggs

Women with HIV infection have an increased risk of cervical cytologic abnormalities1and cervical cancer2,3 compared to women without HIV infection. An American study containing almost 20,000 women with HIV infection found a standardised incidence ratio for cervical cancer (observed incidence of cervical cancer in women with HIV infection divided by expected incidence of cervical cancer based on population rates) of 2.9 (95%CI 1.9–4.2).2

The current New Zealand and American recommendations are that women with HIV infection receive cervical screening when their HIV infection is diagnosed, 6 months later if the initial screen is normal and then yearly if the second screen is normal.4,5

The Infectious Diseases and Sexual Health Services at Auckland City Hospital provide secondary level care for all women with HIV infection in the Auckland and Northland regions.

We aimed to review our current cohort of women with HIV infection in the Auckland and Northland regions to document the number of women who had received a yearly cervical smear since their diagnosis of HIV infection and the number of women who were likely to have had undiagnosed HIV infection at the time of their first abnormal cervical smear.

Method

This audit was a retrospective review of the cervical smear history of all adult women (≥16 years) with HIV infection who were under active follow up by the Infectious Diseases and Sexual Health Services at Auckland City Hospital on 31 December 2007.
We excluded women younger than 20 or older than 69 years of age on 31 December 2007 as routine cervical screening is not recommended for women of these ages by the National Cervical Screening Unit.4
Data including demographics, date of diagnosis of HIV infection, duration of follow-up, and whether the need for a yearly cervical smear was documented in one of the first two clinic letters sent to the woman’s general practitioner (GP) were collected from clinical records at Auckland City Hospital.
The cervical smear history, results and the person(s) performing the cervical smear(s) for each woman were obtained from the National Cervical Screening Unit.
Cervical smears were defined as being taken yearly if the following criteria were met. The number of cervical smears performed divided by the number of years since the diagnosis of HIV infection was ≥0.8 and there were no gaps between cervical smears of ≥2 years, i.e. 4 cervical smears performed in a 5-year period without a gap of ≥2 years would meet our definition of a yearly cervical smear. For those women who were diagnosed with HIV infection before their arrival in New Zealand, we used the number of years they had resided in New Zealand instead of the number of years since the diagnosis of HIV infection.
This audit received approval from the Northern X Regional Ethics Committee.
The two-tailed Fisher’s exact test was used to calculate univariate p values. The two-tailed Mann-Whitney test was used to calculate p values for age, time since diagnosis and duration of follow-up.

Results

At 31 December 2007, 128 adult women with HIV infection were under active follow-up by the Infectious Diseases or Sexual Health Services at Auckland City Hospital. Five women were excluded as they were younger than 20 or older than 69 years of age. The remaining 123 women form the basis of this audit.

113 of these women were under the care of the Infectious Diseases Service, 8 were under the care of the Sexual Health Service and 2 had been transferred from the care of the Sexual Health Service to the Infectious Diseases Service. The median age was 38 (range 22 to 59) years.

The self-reported ethnicity was recorded as sub-Saharan African (n=69), Asian/South-East Asian (n=19), New Zealand European (n=18), European (n=9), Pacific Island Person (n=4), Māori (n=3) and other (n=1). Twenty-five women required an interpreter when they were seen in clinic.

These women had been diagnosed with HIV infection for a median of 5 (range 0 to 22) years. They had been under the care of the Infectious Diseases or Sexual Health Services at Auckland City Hospital for a median of 4 (range 0 to 16) years. The median CD4 count at diagnosis (available for 112 women) was 310 (range 3 to 877) cells/mm3. The median CD4 count from the most recent test prior to 31 December 2007 (available for all women) was 448 (range 100 to 1341) cells/mm3. Eighty-three (67%) women were receiving antiretroviral treatment on 31 December 2007. These women had been on antiretroviral treatment for a median of 3 (range 0 to 18) years. Sixty-seven of the 83 (81%) women receiving antiretroviral treatment had an undetectable viral load on the most recent test prior to 31 December 2007.

120 (98%) women had had at least one cervical smear since 1991. Sixty-nine (56%) women met the definition for yearly cervical smears. Table 1 shows a number of parameters for women who did or did not meet the definition of a yearly cervical smear. The proportion of women who received a cervical smear for each yearly period from 2003 to 2007 is shown in Table 2.

Table 1. Parameters for women who did or did not meet the definition of a yearly cervical smear
Variables
Yearly cervical smear
P value
Yes (n=69)
No (n=54)
Age (years)
Median (range)
38 (22–59)
39 (24–56)
0.31
Ethnicity
Sub-Saharan African
36
33
0.36
Asian/South-East Asian
12
7
0.62
New Zealand European
11
7
0.80
European
5
4
1
Pacific Island Person
2
2
1
Māori
2
1
1
Other
1
0
1
Required interpreter

15
10
0.82
Time since diagnosis (years)
Median (range)
4 (0–18)
7 (0–22)
0.01
Duration of follow up (years)
Median (range)
3 (0–15)
5 (0–16)
0.02
Those prescribed antiretroviral treatment

46 (67%)
37 (69%)
0.85
Those where one of the first two clinic letters discussed the need for a yearly cervical smear

15
10
0.82
Cervical smears performed by
GP
13
20
0.04
HIV nurse specialist
13
11
1
Gynaecology Service
8
0
0.009
Sexual Health Service
3
0
0.26
Mangere Refugee Centre
0
1
0.44
Combination including Gynaecology Service
22
9
0.06
Other combination
8
7
1
Unknown
2
3
0.65
Those with at least one abnormal cervical smear

41
12
0.0001

The need for yearly cervical smears was documented in one of the first two clinic letters of 25 (20%) women.

The cervical smears were performed by a GP (n=33), an HIV nurse specialist (n=24), the Gynaecology Service (n=8), the Sexual Health Service (n=3), the Mangere Refugee Centre (n=1), a combination including the Gynaecology Service (n=31), another combination (n=15) and an unidentified clinician (n=5).

Fifty-three (43%) women had one or more abnormal cervical smears. The most abnormal cervical smear for each woman was abnormal squamous cells of undetermined significance (ASCUS) (n=4), cervical intraepithelial neoplasia (CIN) I (n=27), CIN II (n=6), CIN II/III (n=9) and CIN III (n=7). One patient with a cervical smear that showed CINII/III was found to have a poorly differentiated squamous cell carcinoma requiring chemo/radiotherapy.

Table 2. The proportion of women who received a cervical smear for each yearly period from 2003 to 2007
Year
Number of women diagnosed with HIV infection at the beginning of each year
Number of women who received a cervical smear
Proportion of women who received a cervical smear (%)
P value (using 2003 as the comparator)
2003
2004
2005
2006
2007
60
70
82
98
113
30
45
58
61
73
50
64
71
62
65

0.11
0.01
0.14
0.07

Eleven (9%) women had one or more abnormal cervical smears before they were diagnosed with HIV infection. Their details are shown in Table 3. Not all these women would have had HIV infection at the time of their first abnormal cervical smear.

Taking into account the women’s CD4 count at the time of the diagnosis of their HIV infection it is very likely that seven women (patients 4 to 9 and 11) had undiagnosed HIV infection at the time of their first abnormal cervical smear. It is likely that two women (patients 1 and 2) had HIV infection at the time of their first abnormal cervical smear.

It is unlikely that one woman (patient 3) had HIV infection at the time of her first abnormal cervical smear and one woman (patient 10) is known to have contracted HIV infection just after her first abnormal cervical smear.

The median time between the first abnormal cervical smear and the diagnosis of HIV infection for the women who were very likely to have had undiagnosed HIV infection at the time of their first abnormal cervical smear was 24 (range 3 to 44) months. The self-reported ethnicity of these women was recorded as sub-Saharan African (n=5), New Zealand European (n=1) and South-East Asian (n=1).

Table 3. Women who had one or more abnormal cervical smears before they were diagnosed with HIV infection.
Patient
Ethnicity
Age at time of abnormal cervical smear (years)
Date of abnormal cervical smear (abnormality)
Date of HIV diagnosis
CD4 count at time of HIV diagnosis (cells/mm3)
Time between abnormal cervical smear and diagnosis of HIV infection (months)
1
Māori
19
1997 (CIN I)
2006
22
108
2
NZE
42
1998 (ASCUS)
2006
4
96



2005 (CIN I)


14
3
NZE
28
1988 (CIN II)
1993
818
60
4
South-East Asian
38
2002 (ASCUS)
2006
203
44
5
Sub-Saharan African
30
2004 (ASCUS)
2007
113
30
6
NZE
34
1993 (ASCUS)
1995
251
30
7
Sub-Saharan African
24
2004 (ASCUS)
2006
221
24



2005 (ASCUS)


16



2005 (CIN II/III)


14
8
Sub-Saharan African
37
2004 (ASCUS)
2006
477
18



2005 (ASCUS)


9
9
Sub-Saharan African
34
2004 (CIN I)
2004
102
7
10
Sub-Saharan African
47
2005 (ASCUS)
2005
722
4
11
Sub-Saharan African
24
2005 (CIN I)
2005
155
3
Note: NZE: New Zealand European, ASCUS: abnormal squamous cells of undetermined significance, CIN: cervical intraepithelial neoplasia.

Discussion

In this audit of 123 women with HIV infection followed by our services for a median duration of 4 years, 120 women had at least one cervical smear but only 69 (56%) met our definition for yearly cervical smears.

Sixty-five percent of the women in this audit had a cervical smear in 2007. This is somewhat lower than two cohorts of women with HIV infection from the UK and USA that found that 73 and 77% of women respectively had a cervical smear in the previous year although the American cohort relied on self-reported cervical smear uptake.6,7 In 2002, it was estimated that 73% of all eligible New Zealand women had a cervical smear in the previous 3 years.8

The factors associated with receiving yearly cervical smears were women who had a shorter duration of follow up, women who had received their cervical smears from the Gynaecology Service and women who had at least one abnormal cervical smear. We would expect women with a shorter duration of follow up to have a higher rate of yearly cervical smears compared to those with a longer duration of follow up, as the importance of yearly cervical smears in women with HIV infection has become more widely recognised in recent years.

Women with a shorter duration of follow up will also have had less opportunity to miss one or more scheduled cervical smears. We would also expect that women receiving their cervical smears from the Gynaecology Service would have a high rate of yearly cervical smears given this service’s awareness of the need for yearly cervical smears in women with HIV infection and their effective recall system. This reason could also explain why women who had at least one abnormal cervical smear were more likely to have yearly cervical smears as the majority of women with an abnormal cervical smear were referred to the Gynaecology Service.

The only factor we found that was associated with not receiving yearly cervical smears was women who had received cervical smears from their GP. Not all GPs may have been aware of the need for yearly cervical smears in women with HIV infection. This potential lack of awareness was not helped by two factors. Firstly, clinic letters from our services to the woman’s GP often did not document the need for yearly cervical smears; only 20% of the first two clinic letters for women in this audit documented this issue. Secondly, the comment at the bottom of a normal cervical smear report from the National Cervical Screening Unit states that “the next smear should be taken at the usual screening interval”. It is only if the National Cervical Screening Unit knows that a woman is immunocompromised that the comment “please repeat this smear in 12 months” is included; we expect that most GPs would not have documented that women in this audit had HIV infection on the cervical smear request form.

We have instituted a number of changes in an attempt to increase GPs awareness of the need for yearly cervical smears in women with HIV infection. These include sending a letter documenting this issue to all GPs caring for women with HIV infection seen by our services, documenting this issue in the first clinic letter for women with HIV infection who are newly referred to our services and sending a list of all women with HIV infection seen by our services to the National Cervical Screening Unit stating that these women are immunocompromised. We will continue to send an updated list to the National Cervical Screening Unit once a year.

Another reason why women with HIV infection may not obtain a yearly cervical smear is the potential cost of this examination. While women seen by the Infectious Diseases Service could previously obtain cervical smears free of charge from our HIV nurse specialists, this service is no longer provided due to the increasing workload of our nurse specialists and the lack of an effective recall system. Women seen by the Sexual Health Service continue to be able to obtain cervical smears free of charge from this service.

Women seen by the Infectious Diseases Service may not be aware that a cervical smear can be obtained from Family Planning Clinics at a cost of 5 dollars for women with a community services card or from WONS (previously known as Well Women’s Nursing Services) in Auckland free of charge for Māori and Pacific Island women, women with a community services card and women who have not had a cervical smear within the last 5 years.

We have sent a letter to all women seen by the Infectious Diseases Service informing them of these options for obtaining a cervical smear. Despite the availability of a cervical smear at little or no cost, some women may be reluctant to access these options as this will require them to inform a new healthcare professional of their HIV infection.

Given the retrospective nature of this audit we were unable to explore other reasons why some women with HIV infection did not obtain a yearly cervical smear. We need to ensure that we carefully discuss the need for yearly cervical smears with all women with HIV infection. This is especially important for women who require an interpreter.

It is very likely that seven women in this audit had undiagnosed HIV infection at the time of their first abnormal cervical smear. Assuming that this was the case, the median delay in the diagnosis of these women’s HIV infection was 24 months. Six of these seven women had immigrated to New Zealand from sub-Saharan Africa or South-East Asia; areas with high rates of HIV infection.

The World Health Organization estimates rates of HIV infection in women aged 15 to 49 years of up to 20% in sub-Saharan Africa and 2% in South-East Asia.9 Cervical smear takers should consider offering an HIV test to all women with an abnormal cervical smear who have resided in areas with high rates of HIV infection. It should be acknowledged however that a similar risk based approach was not successful when used for antenatal HIV screening in New Zealand.

The strengths of this audit include the use of the National Cervical Screening Unit’s data and that our services see most women with known HIV infection in the Auckland and Northland regions. Use of the National Cervical Screening Unit’s data enabled us to obtain accurate cervical smear histories for all women. These data will be significantly more robust than studies that use self reported rates of cervical smear uptake.

While it can be argued that our definition of what constituted a yearly cervical smear was somewhat lax, we felt that this definition reflected the real world where there may be a delay between notification of the need for a cervical smear and having this test performed. This audit is limited by its retrospective design and its relatively small size.

The proportion of women with HIV infection in the Auckland and Northland regions who received a yearly cervical smear during the audit period was low. We have put a number of interventions in place that we expect will improve this rate. We have recently audited the proportion of women under active follow up by our services on 31 December 2007 who received a cervical smear in 2008. This showed that the number of women who had received a cervical smear in 2008 had increased to 73% (p=0.003, using 2003 data as the comparator).

We intend to repeat audits of the proportion of women with HIV infection who receive a yearly cervical smear at regular intervals to ensure that this rate continues to increase.

Summary

Women with HIV infection have an increased risk of cervical cancer. It is recommended that women with HIV infection receive yearly cervical smears. Only 56% of women with HIV infection who were seen by the Infectious Diseases and Sexual Health Services at Auckland City Hospital had received a yearly cervical smear. It is very likely that seven women in this audit had undiagnosed HIV infection at the time of their first abnormal cervical smear. Health professionals performing cervical smear tests should consider offering an HIV test to all women with an abnormal cervical smear who have resided in areas with high rates of HIV infection.

Abstract

Aim

We aimed to review our current cohort of women with HIV infection to document the number of women who had received a yearly cervical smear since their diagnosis of HIV infection and the number of women who were likely to have had undiagnosed HIV infection at the time of their first abnormal cervical smear.

Method

This audit was a retrospective review of the cervical smear history of all adult women (≥16 years) with HIV infection who were under active follow-up by the Infectious Diseases and Sexual Health Services at Auckland City Hospital on 31 December 2007.

Results

Sixty-nine of the 123 (56%) women in this audit met the definition for yearly cervical smears. The factor associated with not receiving yearly cervical smears was women who had received cervical smears from their general practitioner (GP). Taking into account the women’s CD4 count at the time of the diagnosis of their HIV infection, it is very likely that seven women had undiagnosed HIV infection at the time of their first abnormal cervical smear.

Conclusion

The proportion of women with HIV infection in the Auckland and Northland regions who received a yearly cervical smear during the audit period was low. We have put a number of interventions in place that we expect will improve this rate. These interventions include informing GPs of the need for yearly cervical smears for women with HIV infection, informing the National Cervical Screening Unit that these women are immunocompromised which will result in a yearly recall comment and informing these women of options for obtaining a cervical smear at little or no cost. Cervical smear takers should consider offering an HIV test to all women with an abnormal cervical smear who have resided in areas with high rates of HIV infection.

Author Information

Jasmin Grewal, Infectious Diseases Registrar, Infectious Diseases; Michele Lowe, HIV Nurse Specialist, Infectious Diseases; Hilary Gerrard, HIV Nurse Specialist, Infectious Diseases; Rebecca Henley, HIV Nurse Specialist, Infectious Diseases; Nicky Perkins, Sexual Health Physician, Sexual Health; Simon Briggs, Infectious Diseases Physician, Infectious Diseases; Auckland City Hospital, Auckland

Acknowledgements

We thank Hadir Elkerdani (Programme Principal, National Cervical Screening Programme, Auckland Region) for her assistance.

Correspondence

Simon Briggs, Infectious Diseases Physician, Infectious Diseases, Auckland City Hospital, Private Bag 92-024, Auckland 1023. Telephone (09) 379 7440, ext 22991, Fax (09) 307 4940

Correspondence Email

sbriggs@adhb.govt.nz

Competing Interests

None known.

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