A study investigating barriers in HIV testing of oncology patients was performed among oncology physicians and patients. Barriers to testing appear to be physician-led, because patient acceptance of testing offered was very high.
Keywords: HIV testing, AIDS-defining cancer, Non-AIDS-defining cancer, Barriers in HIV testing, Opt-out
Abstract
Background.
Although the prevalence of non-AIDS-defining cancers (non-ADCs) among people living with HIV is rising, we observed HIV testing rates below 5% at our oncology center, against a regional HIV prevalence of 0.2%–0.4%. We performed the Investigating Barriers in HIV-Testing Oncology Patients (IBITOP) study among oncology physicians and patients.
Methods.
Between July 1 and October 31, 2013, patients of unknown HIV status newly diagnosed with solid-organ non-ADCs referred to Lausanne University Hospital Oncology Service, Switzerland, were offered free HIV testing as part of their oncology work-up. The primary endpoints were (a) physician willingness to offer and patient acceptance of HIV testing and (b) physicians’ reasons for not offering testing.
Results.
Of 239 patients of unknown HIV status with a new non-ADC diagnosis, 43 (18%) were offered HIV testing, of whom 4 declined (acceptance rate: 39 of 43; 91%). Except for 21 patients tested prior to oncology consultation, 175 patients (of 239; 73%) were not offered testing. Testing rate declined among patients who were >70 years old (12% versus 30%; p = .04); no non-European patients were tested. Physicians gave reasons for not testing in 16% of cases, the main reason being patient follow-up elsewhere (10 patients; 5.7%). HIV testing during the IBITOP study increased the HIV testing rate to 18%.
Conclusion.
Although the IBITOP study increased HIV testing rates, most patients were not tested. Testing was low or nonexistent among individuals at risk of late HIV presentation (older patients and migrants). Barriers to testing appear to be physician-led, because patient acceptance of testing offered was very high (91%). In November 2013, the Swiss HIV testing recommendations were updated to propose testing in cancer patients. Phase II of the IBITOP study is examining the effect of these recommendations on HIV testing rates and focusing on physician-led testing barriers.
Implications for Practice:
Patients of unknown HIV status newly diagnosed with solid-organ non-AIDS-defining cancers were offered free HIV testing. Physician and patient barriers to HIV testing were examined. Most patients (82%) were not offered testing, and testing of individuals at risk of late HIV presentation (older patients and migrants) was low or nonexistent. Conversely, patient acceptance of testing offered was very high (91%), suggesting that testing barriers in this setting are physician-led. Since this study, the Swiss HIV testing recommendations now advise testing cancer patients before chemotherapy. Phase II of the Investigating Barriers in HIV-Testing Oncology Patients study is examining the effect of these recommendations on testing rates and physician barriers.
Introduction
The availability of highly active antiretroviral therapy (HAART) has not only reduced morbidity and mortality among people living with HIV (PLWH) but has changed the epidemiology of HIV infection [1, 2]. Since the advent of HAART in 1996, the population of PLWH has expanded, with particular growth in the group of patients ≥40 years old [3]. Through record linkage of AIDS registries and cancer registries, it has been possible to identify associations between HIV infection and certain cancers and the change in these associations with time post-HAART [3]. Growth and aging of the population of PLWH in developed countries has resulted in a decrease in AIDS-defining cancers (ADCs) and an increase in non-ADCs [2–5], to the extent that non-ADCs are now the leading cause of non-AIDS death [6]. HIV-associated non-ADCs, which occur at a later age than do ADCs, relate to one or a combination of immunosuppression [4], coinfection with oncogenic viruses [4], and risk behavior including smoking [7, 8].
In parallel to the aging of people living with known HIV infection, there is an emerging trend of new HIV infections among older adults [9]. Smith and coauthors described a 3.5-fold increase in adults accessing HIV care between 2000 and 2007 in England, Wales, and Northern Ireland and estimated that 48% of older adults had acquired their infection at the age of 50 years and older. Almost half of older adults were late presenters, and late presentation in this group was associated with a 14-fold greater risk of dying during the first year postdiagnosis in comparison with older adults not presenting late [9]. In Switzerland and elsewhere in Europe, older age is a factor associated with late presentation to HIV diagnosis [10, 11].
Although many studies have demonstrated associations between HIV infection and cancer [3, 4, 8, 12], there are very few studies examining HIV prevalence among cancer patients of unknown HIV status [13–16]. Furthermore, in studies in which HIV prevalence was calculated by taking HIV-negative patients who were tested and those of unknown status (untested) as the denominator, rather than those proven to be HIV-negative through testing, the true HIV prevalence has probably been underestimated [13]. Among patients with cervical or anal cancer/dysplasia, the HIV Indicator Diseases Across Europe Study I demonstrated an HIV prevalence of >0.1%, a level determined to be cost effective for HIV testing [17]. Because HIV is now associated with a wide range of non-ADCs, and because non-ADCs tend to affect older age groups than do ADCs and most systemic cancer treatments result in a relative immunosuppression, there is a strong argument for HIV-testing all patients newly diagnosed with cancer [12].
This argument has been embraced by the Federal Office of Public Health (FOPH) in Switzerland, where HIV prevalence is 0.2%–0.4% [18, 19] and 25%–30% of PLWH are diagnosed with advanced disease [10, 20]. The FOPH HIV testing recommendations, proposing physician-initiated counseling and testing that are diagnostic, targeted, and opt-in, were first published in 2007 [21] and updated in 2010 [22]. The recommendations were further updated in November 2013 to include cancer patients as a group in whom HIV testing should be proposed [23]. Prior to 2013, we had reported HIV testing rates of below 5% among cancer outpatients at our center in Lausanne, in southwest Switzerland [24], and although patients with Kaposi’s sarcoma were screened universally, the testing rates in cervical cancer and Hodgkin or non-Hodgkin lymphoma (ADCs) were 11%–60% [25]. We began the Investigating Barriers in HIV-Testing Oncology Patients (IBITOP) study to examine barriers among oncology physicians and patients. Here, we present the findings of Phase I of this study, completed prior to the publication of the 2013 FOPH recommendations.
Methods
Ethics Statement
The IBITOP study was approved by the Ethical Committee on Human Research of the Canton of Vaud, Switzerland (protocol number 262/11). Both physicians and patients received a detailed information sheet and provided written consent prior to participating in the study. The patients’ consent forms included consent to HIV testing.
Study Setting and Participants
The IBITOP study Phase I was conducted prospectively at the Oncology Service of Lausanne University Hospital (LUHOS), Lausanne, Switzerland, between July 1 and October 31, 2013. To examine HIV testing practices that would occur out of the context of a clinical study, the IBITOP study used the existing set-up of physicians and specialist nurses, without additional staff. In view of this, a two-month pilot study was conducted prior to IBITOP to ensure feasibility [26].
All oncology physicians at the LUHOS who agreed to participate were eligible. Adult patients of unknown HIV status referred to the LUHOS with a new diagnosis of solid-organ neoplasia were eligible. Patients referred with an ADC, those with recurrent neoplastic disease, and those unable to provide informed consent were excluded. Patients of known positive HIV status referred with a new non-ADC were included in the secondary analysis (see below). Phase I of the IBITOP study ended in November 2013, when the updated FOPH HIV testing recommendations were published [23].
Study Design
The primary aims were (a) to examine willingness to offer and acceptance of HIV testing among oncology physicians and patients, respectively, as part of the initial oncology work-up and (b) to identify reasons among oncology physicians for not offering testing in this setting. The secondary aim was to determine HIV prevalence in this patient population.
Participating oncology physicians mentioned the IBITOP study to each new patient during the first or second consultation, depending on patient complexity and clinical workload. Mention of the study included the offer of a free HIV test, which was performed on a serum sample obtained as part of the oncology work-up to avoid additional blood tests. Physicians were invited to complete a short questionnaire for each new patient seen, indicating whether they had offered HIV testing, and to specify reasons, when applicable, for not offering testing in the form of free texting. Patient acceptance or refusal was also documented with reasons for refusal, when applicable, from a list of options (no time, not at risk, fear of result, recent test and “other,” with a free-text option). Patients who accepted HIV testing were informed of the result by the oncology physician who had offered the test. A positive HIV test was defined as the detection of anti-HIV-1/2 antibodies or the HIV-1 p24 antigen using a fourth-generation assay (Cobas Elecsys HIV combi PT, Roche, Rotkreuz, Switzerland, https://usdiagnostics.roche.com/en/index.html). The study protocol dictated that in the event of a positive test, the physician would be accompanied by a specialist from the HIV outpatient clinic. Prior to the study, two interactive training sessions were provided to the LUHOS team of physicians and nurses by an HIV specialist (M.C., K.E.A.D.). These sessions covered the impact of HIV infection on cancer care, the 2010 FOPH HIV testing recommendations (which list indications for HIV testing but make no specific mention of cancer patients [22]), the practice of HIV testing, and the study protocol. The sessions were typical of the teaching seminars organized at the LUHOS as part of continued postgraduate training. The presentation slides and the study protocol were made available via the hospital Intranet system throughout the study period.
Data Management and Statistical Analysis
Patient demographic data, cancer diagnosis, and IBITOP questionnaire responses were entered into an anonymized database by the study investigators (S.Z., L.M.). Patients were categorized by cancer primary site for analysis, with categories based on patient number or relevance to HIV infection according to peer-reviewed literature available at the time of the study.
Data are presented as mean ± SD, median ± interquartile ratio, and percentages. Proportions were compared using the chi-square test, or Fisher’s exact test when appropriate, and means were compared using Student’s t test. The statistical analysis was conducted using Microsoft Excel 2008 (Microsoft Corporation, Redmond, WA, https://www.microsoft.com).
Results
Patients
During the study period, 251 new oncology patients were seen, of whom eight were excluded because of having ADCs. Four patients presenting with non-ADCs (two with nonliver gastrointestinal cancer and two with ear, nose, and throat cancer) were of known HIV-positive status and were included in the secondary analysis only. The demographic details and cancer diagnoses of the remaining 239 patients are shown in Table 1. Mean age was slightly lower in brain cancer patients than in those with other cancers (49 ± 13 versus 62 ± 11 years; p = .08) and age distribution (patients >60 years old) was significantly different (p = .005; Table 1). There were no other significant demographic differences between the cancer groups.
Table 1.
Demographic details of study patients and HIV testing rates prior to and during the Investigating Barriers in HIV-Testing Oncology Patients study, presented by cancer diagnosis
Oncology Physician and Patient Acceptance of HIV Testing
Prior to their initial oncology consultation (pre-IBITOP), 21 patients (8.8%) had already been tested for HIV (median time: 4.7 weeks pre-IBITOP; range: 1.3 to 44.9 weeks). During the IBITOP study, oncology physicians offered HIV testing to an additional 43 patients, of whom 39 (91%) agreed to be tested (Table 2). There was a trend overall toward testing being offered to younger patients (mean age of patients offered testing was 59 years ± 11 versus 63 years ± 11 for patients not offered testing; p = .1) and a significantly lower testing rate among patients older than 70 years in comparison with those age 70 years and younger (p = .04; Table 2). Conversely, the lower median age among brain cancer patients was not associated with higher HIV testing rates in this group (Table 1). Although there was no difference in testing practice with sex, origin (Swiss or non-Swiss), or civil status, no non-European patient was offered testing either prior to or during the IBITOP study (Table 2).
Table 2.
HIV testing by patient age, sex, origin, and civil status
Of the 43 patients offered HIV testing during the IBITOP study, 4 declined, giving the reasons of not considering themselves at risk (3 patients) or not being interested (1 patient). Table 1 shows the HIV testing rates by cancer type prior to the initial oncology consultation (pre-IBITOP) and the increment in testing as a result of the IBITOP study. As a group, lung cancer patients experienced the greatest increase in HIV testing with IBITOP (Table 1).
Oncology Physician Reasons for Not Offering HIV Testing
Of 239 patients, 64 were offered HIV testing, either pre-IBITOP (21 patients) or during the IBITOP study (43 patients), leaving 175 patients of unknown HIV status who were not offered testing (Table 3). Most physicians who did not offer testing did not provide a reason; of the reasons given, the top three were as follows: patient follow-up at another center (10 patients), cognitive difficulties (5 patients), and lack of time (4 patients) (Table 3). There were no significant changes in testing practice or questionnaire completion between the start of the study and later on (Table 3).
Table 3.
Oncologist testing practice and questionnaire completion during the first and second halves of the Investigating Barriers in HIV-Testing Oncology Patients study
HIV Prevalence
No patient in whom an HIV test was performed, either pre-IBITOP or during the IBITOP study, had a reactive test. By excluding from the primary analyses the 4 patients of known HIV-positive status, we found the HIV prevalence in this patient population to be 1.6% (4 of 243).
Discussion
In this prospective single-center study, the offer of HIV testing to new oncology outpatients resulted in a testing rate of 16% (39 of 239), more than 3-fold higher than that previously observed [24]. Testing rates were significantly lower in patients of more than 70 years of age and absent among patients of non-European origin. Patient acceptance of testing offered was high (91%), and most patients who declined did so through self-perception of not being at risk. The majority of oncology physicians who did not offer testing failed to give a reason. Although there were no new HIV diagnoses made, overall HIV prevalence in this patient population was 1.6%.
Our results suggest that offering HIV testing routinely to new oncology patients is acceptable to patients and increases the HIV testing rate. Some patients in this study had been tested for HIV prior to IBITOP (8.8%). Because this occurred before IBITOP inclusion, it is not possible to determine the rationale for HIV testing. However, by examining the breakdown of oncology diagnoses in Table 1, it is possible that testing had been introduced as policy by some subspecialties. All breast cancer patients tested pre-IBITOP, for example, were at moderate to high risk of relapse and were planning for chemotherapy that was either significantly immunosuppressant or of long duration. Because each cancer type has a designated oncology team, it is difficult to speculate as to whether increases in HIV testing were driven by the pre-IBITOP training seminars, and so awareness of the association between HIV infection and certain cancers, or by the attitudes of the head of each team. Although none of the authors participated directly in the study, one author (S.P.) led the thoracic cancer team, which treats lung cancer.
The distribution of testing, notably the reduced and absent testing rates in older and non-European patients, respectively, goes against emerging knowledge of populations to target for testing. In Europe, older patients [9–11] and migrants [11, 27], especially those of sub-Saharan African origin [10], are at higher risk of presenting late with HIV infection. The absence of testing in non-European patients in this study, including patients of sub-Saharan African origin, also goes against the FOPH HIV testing recommendations published at the time of IBITOP, which proposed testing in individuals from countries with high HIV prevalence [22]. In a large retrospective study of HIV testing in patients with both ADCs and non-ADCs attending an oncology center in Texas, USA, Hwang et al. described lower testing rates among black patients than among white patients, and yet HIV prevalence was higher among black patients [16]. The overall testing rate in this study was 18.6%, but among 14,972 solid-organ non-ADC patients, the rate was 3.4%. It is likely that our higher rate among non-ADC patients of 18% during IBITOP was influenced by the prestudy training sessions and the prospective nature of our study.
The high patient acceptance we observed has been described in other studies. In our center, we have reported acceptance, in principle, of routine (nontargeted) testing among 81% of surgical patients [28] and 72% of patients presenting to the emergency department (ED) [29]. The reason of not wishing to be tested through perceived low risk has also been described in patients presenting to the ED, both in our center (De Rossi, Dattner, Cavassini, et al., manuscript submitted for publication, 2016) and elsewhere [30]. Confidentiality concerns, described in other medical settings [31], were not cited during IBITOP, nor was anxiety related to HIV testing or fear of a positive result.
Although we obtained reasons among patients for declining HIV testing, one of the primary aims of this study was to identify barriers to HIV testing among oncology physicians. Although 175 physicians did not offer testing, only 16% of these gave reasons. Physician barriers to HIV testing have been classified into three categories: policy based (consent process, reimbursement), logistical (including time and result provision), and educational (knowledge of or training in HIV testing) [31]. Policy-based and educational barriers were addressed by the study protocol and the prestudy training sessions, so it is likely that physician-led barriers were logistical. The reason given by most physicians, that patient follow-up was being done at another center, is a logistical barrier that represents a missed opportunity for HIV testing: If each center assumes that the patient has been tested for HIV elsewhere, testing will not be performed. If this reason is a proxy for concern of follow-up in terms of HIV result provision, this could be circumvented by the use of rapid HIV testing for which the result is available before the end of the consultation. This would also circumvent the barrier of “no time,” cited by four physicians. The reason of “forgetting” could be addressed by using pop-up reminders in the patients’ electronic medical records for the team to test for HIV at diagnosis or before commencing immunosuppressive treatment [32]. Opt-out testing, in which testing is performed routinely unless the patient expressly refuses, would also address the barrier of forgetting, because HIV would be part of the baseline patient work-up.
The HIV prevalence in our cancer patient sample was at least 1.6%, because many patients were not offered testing, and therefore higher than the HIV prevalence of 0.2%–0.4% of the local population [18, 19] and higher than the 0.1% threshold for cost effectiveness for routine HIV screening [33, 34]. Hwang et al. reported the figure of 1.6% for HIV prevalence in patients with all cancer types, and HIV prevalence was 2% among patients with solid-organ non-ADCs [16].
This study has limitations. Although we maintained a “normal” work setting, without additional staff during the study, we removed educational barriers to testing through the organization of prestudy training sessions. It is likely that the baseline knowledge of HIV epidemiology in cancer patients and awareness of the FOPH HIV testing recommendations are lower among physicians who did not receive this training. We previously observed in the ED setting that 18% of physicians in French-speaking Switzerland were aware of the 2010 FOPH HIV testing recommendations [35]. Our testing rates are therefore not reproducible without first improving physician awareness of the national HIV testing recommendations and the relevance of HIV to their clinical practice. Second, through poor physician questionnaire completion, we have identified only a few physician-led barriers to testing, and it is not possible to determine whether these are representative of all the physicians who participated or indeed of settings outside of the IBITOP study. Against this backdrop, we have reasons for declining testing from the few patients in this group.
In conclusion, the HIV testing rate during the IBITOP study increased more than 3-fold, in comparison with previous rates in this service. However, in light of emerging associations between HIV infection and many non-ADCs, and in the face of high patient acceptance, the offer of testing is unsatisfactorily low. The low testing rates among groups at risk of late presentation, namely, older patients and migrants, are a concern. Because HIV-positive status affects the medical management of cancer patients, and because HIV prevalence in this study sample was above the 0.1% threshold for cost effectiveness, we would recommend an opt-out testing strategy to improve testing rates in this patient population. Since this study, the 2013 FOPH HIV testing recommendations introduced cancer patients as a group in whom HIV testing should be proposed. The IBITOP study Phase II is examining the effect of these recommendations on HIV testing rates in patients with non-ADCs and is focusing on physician-led barriers to HIV testing in this group.
Acknowledgments
We thank all the oncology physicians and patients who took part in this study. This study was partially financed through research support from Gilead Sciences and an unrestricted grant from Roche. The funders had no role in the design of the study nor in the drafting of the manuscript.
Footnotes
For Further Reading: Carolyn A. Brown, Gita Suneja, Neo Tapela et al. Predictors of Timely Access of Oncology Services and Advanced-Stage Cancer in an HIV-Endemic Setting. The Oncologist 2016;21:731–738.
Implications for Practice: The majority (54%) of patients in this large cohort from Botswana presented with advanced-stage cancer despite universal access to free health care. Median time from first symptom to specialized oncology care was 13 months. For HIV-infected patients (51% of total), regular longitudinal contact with the health system, through quarterly doctor visits for HIV management, was not successful in providing faster linkages into oncology care. However, patients who used traditional medicine/healers engaged in cancer care faster, indicating potential for leveraging traditional healers as partners in early cancer detection. New strategies are urgently needed to facilitate diagnosis and timely treatment of cancer in low- and middle-income countries.
Author Contributions
Conception/Design: Solange Peters, Matthias Cavassini, Katherine E.A. Darling
Provision of study material or patients: Stefan Zimmermann, Solange Peters, Matthias Cavassini, Katherine E.A. Darling
Collection and/or assembly of data: Laurent Merz, Stefan Zimmermann
Data analysis and interpretation: Laurent Merz, Stefan Zimmermann, Katherine E.A. Darling
Manuscript writing: Laurent Merz, Katherine E.A. Darling
Final approval of manuscript: Laurent Merz, Stefan Zimmermann, Solange Peters, Matthias Cavassini, Katherine E.A. Darling
Disclosures
Laurent Merz: Gilead (C/A); Stefan Zimmermann: Roche Genentech (C/A); Matthias Cavassini: Gilead, Viiv (RF), Bristol-Myers Squibb, Gilead, Merck Sharpe & Dohme (ET); Katherine E.A. Darling: Gilead Sciences (RF). The other author indicated no financial relationships.
(C/A) Consulting/advisory relationship; (RF) Research funding; (E) Employment; (ET) Expert testimony; (H) Honoraria received; (OI) Ownership interests; (IP) Intellectual property rights/inventor/patent holder; (SAB) Scientific advisory board
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