Article Text

HIV testing: getting the message across—a survey of knowledge, attitudes and practice among non-HIV specialist physicians
1. Ewan Hunter1,
2. Meghan Perry2,
3. Clifford Leen2,
4. Nikhil Premchand1
1. 1Department of Infectious Diseases and Tropical Medicine, Newcastle Upon Tyne Hospitals NHS Foundation Trust, Newcastle Upon Tyne, UK
2. 2Regional Infectious Diseases Unit, NHS Lothian University Hospital Trust, Edinburgh, UK
1. Correspondence to Dr Ewan Hunter, Department of Infectious Diseases and Tropical Medicine, Royal Victoria Infirmary, Newcastle Upon Tyne NE1 4LP, UK; ewan.hunter{at}nuth.nhs.uk

## Abstract

Introduction 26% of people living with HIV in the UK remain undiagnosed and over 50% of adults with HIV are significantly immunocompromised at the time of diagnosis. Current guidelines recommend routine testing in all patients presenting with a range of conditions in low prevalence areas (<2/1000).

Methods The authors conducted an online survey of the knowledge, attitudes and practice of non-HIV specialist physicians with regard to HIV testing in two areas of the UK with a lower prevalence of HIV. Key outcomes included recognition of recommended clinical indications for HIV testing and perceived barriers to performing HIV tests more routinely. All responses were collected in July 2009.

Results Recommended indications for HIV testing were identified by 0–43.7% of 119 respondents. 47.9% cited a low prevalence of HIV as a barrier to routine testing. 88% of 60 consultant physicians were unaware of current guidelines on testing for HIV.

Conclusion The authors found a low awareness of current guidance on testing for HIV and a high level of perceived barriers to testing. Reducing the high number of late diagnoses is a clinical and public health priority. To achieve this, the authors recommend improved policy dispersal coupled with education that targets perceived barriers to testing.

• HIV
• diagnosis
• health knowledge
• attitudes
• practice
• practice guidelines as topic
• general medicine (see internal medicine)
• protocols, guidelines
• AIDS
• public health
• medical education, training
• infectious diseases
• epidemiology
• tropical medicine
• tuberculosis
• internal medicine
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## Introduction

The human immunodeficiency virus (HIV) is unique as a disease-causing virus that has been identified, described and its control essentially stabilised within 20 years of its name being coined; a time period that is incorporated within the length of most physicians' careers. Testing strategies, diagnosis, management and prognosis, however, have all changed dramatically during this time. When HIV testing was first introduced it was recommended to be performed only following extensive counselling,1 was generally prompted only by a high degree of clinical suspicion, and was accompanied by the prospect of arriving at a diagnosis which carried a palliative prognosis at best. Routine screening was discouraged.2 The advent of highly active anti-retroviral therapy has brightened this gloomy picture dramatically and patients can now be offered lifelong treatment that confers a similar life expectancy to that of the general population.3 The prognosis is further improved with early detection of HIV, before the onset of significant immunocompromise.4 In addition to any immediate patient benefits, the availability of HIV testing has itself been shown to decrease high-risk sexual behaviour, bringing the added benefit to public health of reduced onward transmission.5

In this context, screening tests for HIV are now offered routinely in various settings, for example, antenatal assessments and genitourinary medicine clinics.6 7 Screening in these settings alone, however, is not enough to detect all early cases of HIV. Data published by the Health Protection Agency suggest that of the estimated 86 500 people living with HIV in the UK in 2009, approximately a quarter (26%, 22 200) remain unaware of their diagnosis,8 a figure that has not changed in recent years.9 10 Of the 6630 adults (aged 15 years and over) newly diagnosed with HIV in 2009, an estimated 52% were diagnosed late (ie, with a CD4 cell count <350 per mm3 within 3 months of diagnosis), with the risk of late diagnosis being increased in patients over the age of 50 years.11 Furthermore, it has previously been shown that up to 17% of patients newly diagnosed with HIV in the UK may have had contact with health services with a HIV-related issue in the year prior to diagnosis, representing missed opportunities for earlier diagnosis.5 Practice needs to change.

In the autumn of 2007 all consultant physicians in England and Scotland were sent a letter by the Chief Medical Officer (CMO) encouraging increased levels of HIV testing. A year later, in 2008, the British HIV Association (BHIVA) in collaboration with the British Association for Sexual Health and HIV (BASHH) and the British Infection Society (BIS) published new testing guidelines.12 These guidelines recommend blanket testing of medical admissions in areas where the prevalence of HIV in the general population exceeds 2 per 1000. The guidelines also state that in areas with a lower prevalence of HIV, physicians should still routinely test for HIV when they encounter specific ‘clinical indicator diseases’ that may represent adult HIV infection (table 1).

Table 1

Clinical indicator diseases for adult HIV infection12

While original research, editorials and news items relating to HIV testing have appeared in generalist journals such as BMJ and The Lancet, detailed guidance on HIV testing intended specifically for a general readership has been more limited.13

With this in mind, we sought to assess the awareness of recommended changes to HIV testing policy among non-HIV specialist physicians working in university teaching hospitals in two low prevalence areas: South East Scotland (SES) and North East England (NEE). More specifically, we aimed to assess knowledge of those aspects of the current HIV testing guidelines that bear particular relevance to the practice of physicians working in a variety of non-HIV specialities. The results of this survey of knowledge, attitudes and practice with regard to HIV testing should be used to help direct educational efforts and plan additional services with the aims of improving HIV testing rates and reducing the number of late diagnoses in low prevalence areas.

## Methods

### Study sites and target population

The study was conducted among non-HIV specialist hospital physicians working in two university teaching hospital trusts in SES and NEE. We targeted consultants, specialist registrars and senior grade doctors in six specialties: haematology, oncology, neurology, gastroenterology/hepatology, dermatology and respiratory medicine. These specialities were chosen as they regularly see patients presenting with diagnoses that appear in the list of clinical indicator diseases in the BHIVA/BASHH/BIS guidelines (table 1). The estimated prevalence of HIV among those aged 15–59 years in 2009 was <1 per 1000 in NEE, and between 1 and 2 per 1000 in SES.8

### Questionnaire design

An electronic 10-item questionnaire was designed to assess knowledge, attitudes and practice among non-HIV specialist physicians with regard to HIV testing (table 2). We aimed to assess awareness of current specific guidance (BHIVA/BASSH guidelines and CMO letter) and knowledge of the extended list of indications for routine testing. Attitudes were assessed by asking respondents to indicate any perceived barriers to testing, with space for free-text comments, and current practice was assessed by asking respondents to quantify the number of HIV tests they had requested in the year prior to the study. The questionnaire was designed with brevity in mind, in a bid to maximise the response rate.

Table 2

Survey questionnaire

### Delivery of survey

Prior to the main survey, a small pilot study was performed to assess acceptability and feasibility. In order to avoid biasing responses to the main survey, only diabetologists were included in the pilot study. These doctors were excluded from the main survey as none of the indicator conditions for testing given in the current HIV guidelines would routinely present or be referred to this specialty. No major problems were identified during the pilot study.

For the main survey, the names and email addresses of physicians currently working within the six target specialties were obtained from local directories with the permission of the directorates of the trusts involved. A short email was sent in July 2009 to the relevant addresses containing a brief explanation for the rationale of the survey, along with reassurance that the survey was anonymous and thanking physicians for their participation. This email also contained a link to the survey questionnaire which was administered using a web engine (http://www.surveymonkey.com). No prize money or other incentive was offered for completion of the survey and all responses were anonymous. One email reminder was sent 2 weeks following the initial email.

### Ethical considerations

No patients or patient-identifiable information were involved, all included responses were fully anonymous, and there were no experimental changes to clinical practice. Formal ethical approval was therefore not considered necessary, although the study was conducted with the approval of the local NHS trusts that were involved.

### Data analysis

All survey data were exported to Microsoft Excel and statistical analyses were performed using the Minitab 15 software package. The primary outcomes were the overall frequency of responses to nominal categories within the survey. The secondary outcomes were the differences between groups of respondents (according to site, specialty and grade). When comparing groups of respondents, 95% CIs were calculated around differences between proportions.

An option to leave free-text responses were made available to allow participants to expand on or clarify their responses as well as to glean additional relevant information that might inform discussion of the results. All free-text responses were reviewed and discussed by three of the authors (EH, MP and NP). The main objective of the study was to provide quantitative descriptive results, and no formal qualitative analysis of the free-text responses was attempted.

## Results

### Responses

A total of 283 emails were initially sent out, with 119 physicians (42%) ultimately completing the survey. The response rates from the two centres were broadly similar (63 from Edinburgh and 56 from Newcastle). In terms of specialties, oncology and respiratory medicine accounted for almost half of the responses between them. One respondent gave their specialty as acute medicine, which was in addition to the six specialties originally targeted (figure 1). Of the 119 respondents, 60 (50%) were consultants, 50 (42%) were specialist registrars or specialty trainees and 9 (8%) described themselves as staff grade or associate specialists.

Figure 1

Responses by specialty.

### Knowledge and practice

Of the 60 consultants that responded, 49 (82%) did not recall having received the CMO's letter in autumn 2007 recommending increased uptake of HIV testing, and 53 (88%) were unaware of the BHIVA/BASHH/BIS guidelines for HIV testing published in September 2008. Eighty-five respondents (71%) had requested <5 HIV tests in the year preceding the survey. Seven (13%) physicians from NEE had requested more than 10 HIV tests during the preceding year compared with three (5%) from SES (difference in proportions 0.08; 95% CI −0.02 to 0.18). A total of 43 respondents (36%) believed that a HIV test requires pre-test counselling from a specialist, with 27 respondents (46%) from SES expressing this view compared with 14 (25%) from NEE (difference in proportions 0.21; 95% CI 0.04 to 0.38). A total of 36 respondents (30%) believed that ever having had a HIV test may potentially affect life or health insurance policies. This view was held by 22 respondents (35%) from SES compared with 14 (25%) from NEE (difference in proportions 0.10; 95% CI −0.06 to 0.26).

The most frequently identified conditions for testing were fever of unknown origin, chosen by 52 respondents (44%), weight loss of unknown cause, chosen by 50 respondents (42%) and viral hepatitis, chosen by 44 respondents (37%) (figure 2). The conditions least frequently identified for testing were psoriasis and bacterial pneumonia (not selected by any respondent), lung cancer and salmonella diarrhoea, each chosen by two respondents (2%), and seborrhoeic dermatitis, each chosen by three respondents (3%). Of all 119 respondents, 40 (34%) selected ‘none of the above’ and only one respondent selected ‘all of the above’. While the pattern of responses was broadly similar across the two sites, some apparent inconsistencies were observed—the conditions in which physicians stated they would test for HIV and the number of HIV tests they reported to have performed in the last year; for example, a hepatologist who had requested <5 HIV tests in the last year also stated that they tested for HIV when managing viral hepatitis.

Figure 2

Proportions of respondents who would consider HIV testing (according to the indicator disease).

### Attitudes

The three greatest perceived barriers to HIV testing identified were ‘low risk population’, chosen by 57 respondents (48%), ‘lack of patient acceptance’, chosen by 42 respondents (35%) and ‘consent process/pre-test counselling’, chosen by 39 respondents (33%) (figure 3).

Figure 3

Perceived barriers to HIV testing in routine practice (proportion of all respondents for each barrier).

Twenty-eight respondents provided additional free-text comments related to perceived barriers to testing, and 28 left additional comments in the final open-ended free-text item. There was a general impression that HIV should be tested for only in unusual presentations, or that it may be considered in the ‘second round of investigations’. While doubts were expressed about the need for testing when there is an otherwise definable cause for a clinical indicator disease, there were also expressions of a general need for increased knowledge of local policies.

## Discussion

As far as we are aware, this is the first study since the present guidelines were published to address the opinions of non-HIV specialist physicians working in areas with a low prevalence of HIV with regard to HIV testing. Our results indicate a low awareness of current guidelines advocating a lower clinical threshold for carrying out HIV tests.

Testing for HIV in clinical indicator conditions does not appear to be part of routine practice and there are significant perceived barriers to performing HIV tests. These findings echo those of a previous survey conducted in 2007, prior to publication of the current guidelines, among specialist registrars in admitting specialties in a British teaching hospital serving a population with a prevalence of HIV-seropositivity of 1 in 1000.14 A review of literature on this issue from the USA, also published in 2007, collated the results of surveys looking at attitudes and practice surrounding HIV testing in antenatal care, emergency medicine and other healthcare settings.15 Barriers mutual to all settings were broadly similar to those identified in our survey and included logistical and educational concerns as well as a reluctance to broach a topic that the patient may find difficult or awkward. Financial issues were also significant in the American setting, although these were not found to be a perceived barrier among physicians responding to our survey. The three main perceived barriers to increasing HIV testing identified by our survey were ‘lack of patient acceptance’, the ‘pre-test/counselling process’ and ‘low risk patient population’. These could all be addressed with appropriately targeted education.

A consistent finding from many studies looking at how HIV testing strategies could be improved has been a high level of patient acceptance of having a HIV test, with the barrier often found instead in the perceptions of attending medical healthcare professionals.16 Education and guidance on how best to offer HIV tests to patients and on the information they require should be delivered in hospitals throughout the UK. The perception that HIV tests should not be routinely performed in areas of low prevalence does not take into account the public health benefits of HIV testing and the economic benefits of diagnosing a patient early in the course of their disease.4 Testing for hepatitis B and C is regularly performed in the UK with a low degree of clinical suspicion. We would like HIV testing to become at least as commonplace as testing for these viruses.

A recent editorial in The Lancet entitled ‘The UK's appalling failure to tackle HIV’ stated that ‘hospitals pay little attention to their public health responsibilities of which HIV diagnosis is an important part’.17 Although, the BHIVA/BASHH/BIS guidelines may be available in acute hospital trusts, the free-text comments in our survey indicate that most physicians are not aware of them. Furthermore, our survey shows that the Department of Health initiative of sending a ‘Dear Doctor’ letter was unsuccessful. In September 2009 the CMO wrote again on this issue to the various specialist societies,18 although their responses were disappointing, with the issue of tackling undiagnosed HIV infection remaining relatively low on the agendas of most colleges.19

Mathematical modelling of the cost-effectiveness of expanded screening for HIV in low prevalence populations in the USA have concluded that the incremental cost per quality-adjusted life year would be $113 000 in the general population (background prevalence of undiagnosed HIV 0.1%).20 Another study has shown that this falls to <$50 000 in healthcare populations where the prevalence of undiagnosed HIV exceeded 0.05%.21 These figures refer to screening, and it may be anticipated that the cost per quality-adjusted life year for targeted testing would be significantly lower. Furthermore, as both the above studies allude to, earlier diagnosis of HIV can reduce onward transmission to sexual partners thereby reducing the burden of secondary infection. Making cost-effectiveness estimates for extended testing in UK healthcare populations are beyond the scope of this study, but if comprehensive efforts are to be made to increase adherence to the current UK guidance, such estimates would obviously be of great importance.

Other studies from the UK have either focussed on retrospective collections of data indicating practice, or have reported on pilot projects of new HIV testing strategies.22 Neither of these approaches directly assesses the opinions of physicians in their day-to-day practice. Such studies have been published mainly in specialist journals and therefore non-HIV specialist physicians may only be exposed to their results when they are presented locally, for example, in ‘grand rounds’ or hospital policy meetings.

Although a comparison between sites was not a primary outcome in our survey, our findings do suggest a trend towards heterogeneity between the two sites studied, with lower numbers of HIV tests being accompanied by aberrant perceptions surrounding the implications of offering a HIV test. While only one of these differences achieved statistical significance (the perceived need for specialist pre-test counselling), such factors should be closely examined when targeting any local educational interventions.

Our study had some important limitations. Only the views of physicians in six selected specialties in two low prevalence areas in the UK were represented, with responses coming predominantly from physicians working in respiratory medicine and oncology. Furthermore, the overall response rate was low (42%), which may reflect the method of using an online survey administered without an incentive for response.23 At the time of the study, the 2008 BHIVA/BASSH guidelines were only available on the web. While these are easily accessible via any search engine, the study may have been more valid if it had been conducted after this guidance subsequently appeared in print.13 We acknowledge these limitations, but also argue that the respondents are likely to represent a self-selecting group, and the level of knowledge in relation to HIV testing in those who did not reply may be lower. We hope that the survey can be repeated to include a wider group of both hospital physicians and general practitioners, ideally in association with educational and service interventions.

Since the late 1990s and the advent of highly active anti-retroviral therapy, there has been a call to treat HIV like other infectious diseases and for a change from ‘exceptionalism to normalisation’.24 While this has been partially achieved through routine screening in antenatal and genitourinary medicine settings, it is clear from our findings that perceptions and practice among physicians practicing in non-HIV specialties still need to change. If this can be achieved, a greater readiness to test for HIV will bring public health benefits, and may in turn have the desired knock-on effect on public perceptions of HIV and HIV testing.25

The number of people presently living in the UK with undiagnosed HIV remains unacceptably high, and any effort to decrease this number will also help to decrease the ongoing incidence and subsequent morbidity from this virus. A small study conducted in 1998 showed that British general practitioners at that time would discourage patients perceived as being ‘low risk’ from seeking a HIV test.26 Although things have undoubtedly moved on since then, our survey clearly highlights the continued need for enhanced policy dispersal and education. There is a need for specialist societies to develop HIV testing guidelines in conjunction with infection societies so that more cases of HIV can be diagnosed earlier. Furthermore, if non-HIV specialist physicians disagree with current guidelines as indicated in the free-text comments, a forum for discussion needs to be set up to address these issues.

We hope that the results of this survey will help to raise awareness of the importance to public health of early and widespread HIV testing, and of the existence of expert guidance designed to help clinicians practising across all specialities.

### Main messages

• There is low awareness of specific guidance on HIV testing and conditions which are recommended as indicators for routine HIV testing among non-HIV specialist physicians.

• Non-HIV specialist physicians report a low rate of HIV testing as part of routine clinical practice.

• Perceived barriers to routine HIV-testing among non-HIV specialist physicians reflect low levels of awareness about current guidance and aberrant perceptions of the acceptability of routine testing among the patient population.

### Current research questions

• How can qualitative understanding of attitudinal barriers to routine HIV testing inform educational strategies targeting non-specialist clinicians?

• How can policy dispersal among non-specialist clinicians be improved?

• What are the cost–benefit implications, in terms of quality-adjusted life years, of increased targeted testing in UK patient populations with a low prevalence of undiagnosed HIV infections?

### Key references

• Smith RD, Delpech VC, Brown AE, et al. HIV transmission and high rates of late diagnoses among adults aged 50 years and over. AIDS 2010;24:2109–15.

• BHIVA, BASHH, BIS. UK National Guidelines for HIV Testing. 2008. http://www.bhiva.org/files/file1031097.pdf (accessed 29 Dec 2010).

• Palfreeman A, Fisher M, Ong E. Testing for HIV: concise guidance. Clin Med 2009;9:471–6.

• Krentz HB, Auld MC, Gill MJ. The high cost of medical care for patients who present late (CD4 < 200 cells/microL) with HIV infection. HIV Med 2004;5:93–8.

• Sullivan AK, Curtis H, Sabin CA, et al. Newly diagnosed HIV infections: a review in UK and Ireland. BMJ 2005;330:1301–2.

View Abstract

## Footnotes

• EH and MP contributed equally to the research.

• Competing interests None.

• Ethics approval This is a descriptive study which includes aspects of audit, comparing current practice with published guidelines. No patients or patient-identifiable information were involved, all included responses were fully anonymous and there were no immediate implications for changes to clinical practice. Formal ethical approval was therefore not considered necessary, although the study was conducted with the approval of the local NHS Trusts that were involved.

• Provenance and peer review Not commissioned; externally peer reviewed.

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