Treatment guidelines are developed to assist clinicians in optimizing patient care. The US Department of Health and Human Services (DHHS) first developed Guidelines for the Use of Antiretroviral Agents in HIV-1–Infected Adults and Adolescents (the guidelines) in 1998.1 They offer guidance for the use of antiretroviral therapy (ART) and are updated when significant developments in HIV treatment occur. The guidelines have become increasingly evidence based, particularly regarding the initiation of ART. At its February 2005 meeting, the Australian Health Minister's National Advisory Committee on HIV/AIDS and Related Communicable Diseases decided to adopt the DHHS guidelines and requested the Australasian Society of HIV Medicine devise a commentary to the guidelines to ensure they were appropriate to the Australasian setting.2 The main differences are the inclusion of nevirapine as a “preferred” treatment option for initial ART and, in the 2011 Australian commentary, that ART initiation commence when the CD4+ lymphocyte count is <350 cells per microliter (rather than <500 cells/μL).
It is unknown how closely HIV treatment guidelines have been followed in Australians initiating ART, what predicts adherence to treatment guidelines, and what changes in management might improve patient care and outcomes. Such needs analyses are usually undertaken via a clinical audit.3–5 Previous published ART guidelines audits have significant limitations. Many involved nonconsecutive patient samples and considered only a limited number of guideline recommendations.6–14 Also, the most comprehensive audit only examined patients initiating ART up to 2004.6 Since 2004, the guidelines have expanded to include numerous complex recommendations for baseline assessments, patient counseling and clinical and laboratory monitoring, including for comorbidities such as cardiovascular disease (CVD) and non–AIDS-defining cancer. No ART guideline audit has been performed in Australia, and no audit has reviewed adherence to guidelines-recommended comorbid disease assessments.
The objectives of this audit were to determine the degree of adherence to recommendations of the DHHS guidelines with Australian Commentary for patients initiating ART and to identify factors associated with greater adherence.
Site Characteristics and Study Population
The audit was conducted in 4 high HIV-caseload sites (1 primary care and 1 hospital clinic each in Sydney and in Melbourne). High HIV-caseload clinics manage several 100 HIV patients, and each selected clinic manages more than 1000 patients. All adults at each site commencing their first ART regimen were identified using clinical databases, clinical trial lists, and pharmacy records. Patient case notes were retrospectively examined for 125 consecutive HIV-1–infected adults who initiated ART (from December 2008 backwards) at each site. Data collection commenced in June 2009, to ensure at least 6 months of follow-up for each patient.
The audit involved a retrospective review of article and electronic medical records, pathology results, pharmacy records, and databases. Trained auditors with HIV clinical experience entered de-identified data into a purpose-built, web-based, data collection form. To maximize data consistency, only 1 auditor reviewed and entered all data at each site where possible. Only data explicitly stated in the medical records were abstracted, that is, if assessments or tests were not recorded in case notes, they were assumed to not have been performed.
Information regarding patient history, demographics, physical examination, laboratory investigations, initial ART, follow-up schedule, concomitant medications, and assessment of drug toxicities and clinical outcomes were collected, so as to encompass each recommendation from the guidelines. Data on HIV management experience of treating physicians involved in the initiation of ART were recorded.
The guidelines dated November 2008 (with Australian commentary)15 were utilized for assessment, being the current guidelines at the time of audit development. In addition, we also compared data against the guidelines current at the time of ART initiation (ie, applied to ART initiated at least 1 month after release of latest guidelines) (seeTable, Supplemental Digital Content 1, http://links.lww.com/QAI/A266).
The entered data were systematically checked and any uncertain data returned to site staff for clarification. Completed data from the first 5 patients at each site were monitored for consistency with all entries source verified. There was a single central monitor of the audit data to ensure consistency and reliability across all sites.
Study approval was obtained from each site's Human Research Ethics Committee.
Assessment of Adherence to Guidelines
ART initiation is a process, and the guidelines relating to ART initiation were deemed to have been adhered to if recommended procedures and assessments were performed at consultations within 1 year before ART initiation. Adherence to ART initiation guidelines focused on 3 key questions: “when to start”, “what to start”, and comorbid disease assessment. Meeting the “when to start” guideline depended upon the CD4+ lymphocyte count, plasma HIV RNA and relevant clinical features at the time of ART initiation. The DHHS guidelines have strongly (level A) recommended ART initiation at CD4 count <200 cells per microliter during periods 1 and 2 of the study (2004–2007), with a strong recommendation at CD4 count <350 cells per microliter from December 1, 2007. If CD4+ counts were above the threshold, and other criteria were not met, for example, symptomatic HIV or VL >100,000, ART initiation was considered to be outside the guidelines. “What to start” was classified as initiation of a “preferred” regimen (met guidelines criteria for regimen with the highest efficacy, tolerability, and simplicity) or an “alternative” regimen (determined by guidelines as similar to “preferred” but having 1 or more limitations).
Meeting comorbid disease assessment recommended before ART initiation included adherence to AIII (highly recommended based on expert advice): complete blood count (white blood cell count), liver transaminases (alanine aminotransferase), creatinine, urinalysis, fasting lipids (high-density lipoprotein cholesterol), fasting glucose, hepatitis serology (hepatitis A IgG, hepatitis B surface antigen, hepatitis C antibody, syphilis serology, and toxoplasma serology (toxoplasma IgG) If hepatitis serology or vaccination results were in records more than 1 year before initiation, and indicating no need to repeat, then these were recorded as “done”). Adherence to chest radiography (recommended in the Australian Commentary) was also included as a key comorbid disease assessment. Tuberculosis (TB) testing was included in adherence to AIII guideline-recommended comorbid disease assessments but excluded from analysis of predictors of adherence because of the use of Australian Commentary-mandated chest radiograph recommendation, as was Pap smear testing because of the low number of female patients (4.1%) included in the audit (PAP smears were performed in 38.8% of female patients). Anal pap testing is not routinely performed in Australia and not recommended by the DHHS guidelines.
Additionally comorbidities were clustered as coinfection (syphilis serology, hepatitis B surface antigen, hepatitis C antibody, toxoplasma serology, and chest radiograph), renal (urinalysis, creatinine), hepatic (alanine aminotransferase, bilirubin), and CVD risk (smoking, blood pressure, total cholesterol, fasting high-density lipoprotein cholesterol, fasting glucose); adherence to each cluster was determined if all components were assessed. Multivariable predictors of adherence were assessed using logistic regression.
Adherence to guidelines was measured for all participants, and comparisons made between primary care and hospital sites, Sydney and Melbourne sites, and those patients who initiated ART via a clinical trial and those who did not.
To assess comparisons in adherence to guidelines over time, ART initiation dates was categorized in tertiles (and covering 1 month postpublication of guidelines): tertile or period 1 (2004 to November 9, 2006) included ART initiation before November 10, 2006, that is, guidelines issued on March 23, 2004; October 29, 2004; April 7, 2005; October 6, 2005;and May 4, 2006; tertile or period 2 (November 10, 2006, to December 31, 2007) included guidelines issued on October 10, 2006; and tertile or period 3 includes ART initiation from January 1, 2008, onwards that is, guidelines issued on December 1, 2007; February 1, 2008, and November 3, 2008.
All analysis was performed using SAS version 9.2 (SAS Institute Inc, Cary, NC). Comparisons of proportions were performed using χ2 tests for equal proportions (or Fisher exact tests where numbers were small) and reported as percentages. Continuous normally distributed variables were compared using student t tests or analysis of variance and reported as means (standard deviations), whereas nonnormally distributed data were compared using Wilcoxon rank sum tests or Kruskal Wallis tests and reported as medians [interquartile range (IQR)].
Univariable predictors of adherence to guidelines for “when to start”, “what to start”, and comorbidity assessment before ART were performed analyzing demographic and relevant guidelines adherence variables. Univariable linear regression was used to determine the relationship between adherence to comorbid disease assessment and all other variables in the dataset. Multivariable models were developed using logistic regression for adherence to guidelines on ART initiation and linear regression for adherence to comorbid disease assessment. All multivariable models were developed using both stepwise selection and backwards elimination procedures before undergoing a final assessment for clinical and biological plausibility. Although all variables with univariable P values <0.10 were considered for inclusion into the models, to reduce the chance of type I errors and increase the robustness of the prediction models, only variables with a multivariable P value <0.01 were included in final models.
There were 500 patients included in the study, and each site contributed 125 patients. Three sites initiated 125 patients each in the period from 2006 to 2008. The fourth site recruited less than 125 patients in this period, so the period of review was extended back to 2004 to achieve their quota of 125 patients.
Patients were predominantly male (95.2%) with mean age at ART initiation of 40.2 years, median CD4 count of 270 (IQR: 174, 360) cells per microliter and plasma HIV RNA of 67,300 (IQR: 19,400–212,900) copies per milliliter (Table 1). There were a mean 3.1 years from diagnosis of HIV infection to ART initiation. Forty-six patients (9.2%) initiated ART in hospital, and 102 (20.4%) initiated ART via a clinical trial.
There were 364 patients who initiated therapy within 1 year of entering care. The remaining 136 patients commenced ART a median 2.6 years (IQR: 1.7–4.2 yrs) after entering care, and their initial CD4 count was median (IQR) 466 (381–595) cells per microliter in comparison with those patients initiating therapy ≤1 year of entering care [273 (156–371) cells/μL, P < 0.0001]. Of the patients commencing ART >1 year after entering care, 5 had CD4 count <200 at the initial visit.
The 54 physicians who initiated ART (and 60 involved in follow-up visits) had a median 13.5 (IQR: 8–19.5) years of experience in treating HIV (Table 2). Each physician initiated ART in a median of 5 (IQR: 2.5–10.5) patients in the audit. ART was initiated in 25% patients by the most experienced quartile of physicians and in 27% patients by the least experienced quartile of physicians.
Adherence to Guidelines
“When to Start”
“When to start” guidelines at the time of ART initiation were followed for 438 (87.6%) patients (Table 2). Adherence to this guideline was similar in primary care and hospital sites but significantly higher in Melbourne versus Sydney (92.8% vs. 82.4%, respectively; P = 0.0004), mainly driven by higher levels of initiation via clinical trial in the latter city (4.8% vs. 36.0%, respectively; P < 0.0001). Adherence increased over time with adherence rates in periods 1, 2, and 3 being 83.2%, 93.0%, and 86.5%, respectively (P = 0.019 for trend) (Fig. 1).
During period 3 (ie, 2008), when initiating ART at CD4 200–350 cells per cubic millimeter became a strongly recommended guideline (level A), 173 patients commenced ART. After exclusion of 7 patients (including 2 with primary HIV infection) whose CD4+ count rebounded and remained above 350 cells per microliter on retesting, there were 41 patients at the 4 sites who had a CD4 count <350 cells per microliter who did not commence ART. Of these, 14 were lost to follow-up, 11 declined ART despite physician recommendation, 5 commenced ART within 6 months (in early 2009), 10 commenced ART in 2009, 6–12 months after CD4 <350 cells per cubic millimeter, and 1 patient died without commencing ART. Adherence to “when to start” ART reduced adherence to guidelines to 67% when the 41 patients were included in period 3.
Univariable predictors for greater adherence to “when to start” guidelines included variables associated with illness or more advanced HIV disease, including CDC category C, category B, Mycobacterium avium complex testing, lower CD4 count, inpatient ART initiation, lower weight, and older age. Predictors for nonadherence included clinical trial variables such as use of investigational agents, use of raltegravir, having HIV resistance testing and urinalysis. Additionally, nonsmokers, those receiving no concomitant medication, and patient preference as a reason for initiation of ART were each significantly associated with nonadherence.
In multivariable analysis, adherence to “when to start” was less likely in those who initiated ART in a clinical trial and who had previously received short-term nontherapeutic ART (via HIV postexposure prophylaxis or a 2-week pharmacokinetic study) (Table 3).
“What to Start”
Three hundred and forty-five patients (69%) initiated ART with drugs that were included in the guidelines-“preferred” category, and 85.8% of drugs used were classified as either “preferred” and/or “alternative”, increasing to 88.7% after exclusion of patients initiating ART via a clinical trial. Seventy-one patients (14.2%) initiated ART containing at least 1 nonpreferred/alternative drug. One hundred and twenty (93%) of the nonpreferred/alternative drugs were used before later inclusion in the guidelines, whereas 9 (7%) drugs were no longer recommended in the guidelines at the time of ART initiation. Contraindicated or not recommended ART was initiated in 19 (3.8%) patients, most commonly nevirapine in men and women with CD4+ counts >400 and >250 cells per microliter, respectively (13 patients), and atazanavir in patients also receiving a proton pump inhibitor or H2 antagonist (6 patients). No patient-initiated monotherapy or dualtherapy ART, contraindicated combinations of ART, efavirenz during pregnancy, a protease inhibitor although taking simvastatin, abacavir when HLA-B*5701 positive, or ART without lamivudine, emtricitabine, or tenofovir when hepatitis B surface antigen positive.
The changing pattern of ART regimens over time (seeFigure, Supplemental Digital Content 2, http://links.lww.com/QAI/A267) largely reflects the changes in guideline recommendations (Table 3). Dual nucleoside analogue reverse transcriptase inhibitor backbones remain the predominant choice for ART initiation. Coformulated zidovudine–lamivudine use significantly declined over time (P < 0.0001), coformulated abacavir–lamivudine use declined more recently (P < 0.0001), whereas use of coformulated tenofovir–emtricitabine significantly increased (P < 0.0001). Nonnucleoside analogue reverse transcriptase inhibitor use as the third ART drug significantly increased (P = 0.03), due mainly to an increase in efavirenz use. Protease inhibitor use correspondingly declined (P < 0.0001) and, whereas atazanavir use increased, coformulated lopinavir–ritonavir use diminished (P < 0.0001).
Hospital sites were more likely than primary care sites to use “preferred” ART regimens (76.8% vs. 62.2%, P = 0.0002), mainly due to the preference for coformulated abacavir–lamivudine in primary care sites (24.8% vs. 16.0%, P = 0.015). Adherence to “preferred” ART regimens increased significantly in the most recent tertile period with adherence to “preferred ART” of 63.6%, 61.6%, and 83.2% during periods 1, 2, and 3, respectively, (P < 0.0001) (Fig. 1).
Univariable predictors for adherence to “what to start” guidelines-“preferred” drugs included variables consistent with more recent ART initiation date, parameters of more advanced disease such as initiating ART after an AIDS diagnosis, Mycobacterium avium complex testing, lower hemoglobin and lower CD4 percentage. Initiation of ART adherent to “what to start” guidelines was more likely to occur in patients comanaged between Primary Care and Hospital sites, patients assessed for injecting drug use, patients in whom blood pressure, fasting glucose, creatinine, and chest radiograph were performed, and patients with hepatitis B coinfection, but were less likely to have had diet and lifestyle counseling or negative chlamydia and/or gonorrhoea testing. Predictors of nonadherence to “what-to-start” guidelines included HLA B*5701 testing, use of lamivudine in ART initiation (reflecting use of lamivudine with abacavir), and white race (higher in primary care sites).
Adherence to “what to start” using guidelines-preferred drugs on multivariable analysis (Table 3) was more likely with recent initiation of ART and less likely at the Melbourne primary care site.
Adherence to Comorbid Disease Assessment
Comorbid disease assessment guidelines (level AIII) were adhered to variably ranging from 0.8% for TB testing by TB skin test or interferon gamma release assay to 99.2% for full blood count (as measured by white cell count) (Table 2).
Primary care sites were more likely to assess fasting lipids (48.8% vs. 35.6%, P = 0.014), glucose (52.4% vs. 42.4%, P = 0.015), syphilis serology (74.8% vs. 65.6%, P = 0.025), and Pap smears in women (83.3% vs. 30.4%, P < 0.0001). Hospital clinics were more to test for creatinine (94.4% vs. 82.4%, P < 0.0001), toxoplasma serology (64.0% vs. 36.8%, P < 0.0001), and hepatitis B serology (81.2% vs. 45.6%, P < 0.0001). Testing for comorbid diseases was more likely to occur in Sydney than in Melbourne, perhaps reflecting the higher testing rates in patients initiating ART via a clinical trial (Table 2).
Mean adherence to assessment of the 11 AIII comorbid disease parameters (excluding TB testing and Pap smear) was 58.6%. Adherence to each of the 11 comorbid disease parameters that comprised this score ranged from 25.6% (urinalysis) to 99.2% (white blood count). Only 1.6% of patients received all 11 nominated assessments for comorbid diseases.
Seven variables were independently associated with adherence to comorbid disease assessment (Table 3). Significantly greater comorbid assessment was performed in patients who initiated ART in a clinical trial or after an AIDS diagnosis, patients referred to allied health practitioners for diet and lifestyle advice, and patients provided with treatment education although significantly less comorbid disease assessment occurred in primary care sites and patients in whom a smoking history was not collected. Finally, adherence to comorbid disease assessment significantly improved over time (individual comorbid assessments over time can be seen in Supplemental Digital Content 3, http://links.lww.com/QAI/A268).
Adherence to comorbid clusters increased over time but was low for coinfections, renal and CVD risk (Table 2 and Fig. 2). Multivariable predictors for cluster comorbidities (Table 3) showed association of coinfection assessment at hospital sites and in Melbourne and renal and CVD risk assessment in Sydney.
This study is the most comprehensive audit of adherence to DHHS guidelines on initiation of ART and the largest audit of more recent guidelines. Between 2004 and 2008, there was a high level of adherence in the 4 primary care and hospital-based sites in Sydney and Melbourne to the guidelines on “when to start” and “what to start”, and to key guidelines that were strongly recommended and supported by clinical trial evidence. There was more variable adherence to comorbid disease assessment and other recommended guidelines that were based on expert opinion or not categorized.
The adherence to guidelines compares favorably with audits conducted in the United States6,7 and United Kingdom.8–14 An audit in 2001–2002 involving 113 UK sites and 942 patients revealed 89.6% adherence to United Kingdom recommendations for initiating ART.13 However, small numbers of patients were studied at each site, and were unlikely to have been recruited consecutively, and thus may have been a biased sample. A more thorough study of 217 women initiating ART in multiple clinics from 1998 to 2004 was conducted by the WIHS consortium in the United States as follows: 54% of patients met “when to start” criteria whilst 53% met “what to start – preferred or alternative regimen” and a high rate of 17% were initiated on ART that was “not recommended”.6 The WIHS study covers an earlier period of ART initiation than our study, but does contrast with the rates in the Australian sites of 86% meeting “preferred or alternative” ART and 4% meeting “not recommended” therapy.
The high adherence we observed may reflect the geographical and therapeutic concentration of HIV patients in Australia. Most of the 20,000 cases and the approximately 1000 annual new diagnoses are in men who have sex with men living in inner city Sydney and Melbourne.16 Their HIV treatment is managed by high caseload primary care practices and hospital clinics. A key component to achieving high adherence to guidelines has been the restriction of ART prescribing to registered prescribers who participate in ongoing training and education and dispensing of ART by specified hospital outpatient pharmacies. The higher adherence may also be due to the relatively low proportion of patients who actively inject drugs (specific substance not collected) or have socioeconomic disadvantage (not collected in this audit), the universal access to health care and ART, and a relatively high level of HIV experience of treating physicians and restricted prescriber status in Australia. Adherence to guidelines on “what to start” in our study is an underestimate. The overwhelming majority of patients initiating nonrecommended ART did so in clinical trials and received regimens that were subsequently recommended.
The success of ART in suppressing HIV and providing improved prognosis has focused attention on the importance of comorbid diseases in managing patients with HIV.17,18 Our study showed a far lower and more variable adherence to guidelines-recommended comorbid disease assessment than for “what to start” or “when to start”, although there was significant improvement over time. Since the period of ART initiation from 2004 to 2008, awareness of the importance of comorbidities in HIV management has increased and with the greater emphasis on comorbidities such as CVD and renal disease, a greater adherence to monitoring of these conditions is expected. The relatively low level of baseline resistance testing was one of the adverse findings of the audit. HIV resistance in Australia is comparable with other Western countries and given the high use of nonnucleoside reverse transcriptase inhibitors as first-line therapy, this omission will change with the introduction in 2010 of reimbursement for testing in Australia.
One of the limitations of this study is the evaluation of ART initiation at specific high HIV caseload inner city sites where relatively large numbers of HIV patients are treated and may not represent the treatment practices in low caseload and more geographically isolated sites in Australia. In these practices, and in Australia, the majority of patients with HIV are men who have sex with men and have access to healthcare and 63% have some contact with HIV/AIDS organizations.19 Another factor possibly limiting the generalizability of our findings is the greater HIV experience in audit physicians (mean 13.8 years) relative to HIV prescribers (approximately 5 years; unpublished data, Australasian Society of HIV Medicine).
In addition, the characteristics of all patients eligible for treatment, but not initiating ART over the 3 periods, at the study sites was not included, which may bias the results. Inclusion of the 41 patients with CD4 counts <350 cells per microliter, with the 173 patients initiating ART in period 3, reduced the adherence of when to start from 86% to 67%. The Australian HIV Observational Database collected data from 27 Australian clinics on 501 patients initiating ART mainly before 2005,20 and found the median CD4 count in this population was 236 cells per microliter compared with 270 cells per microliter in our audit. It is unknown whether adherence to “what to start” and assessment of comorbid diseases is similar in the Australian HIV Observational Database cohort in comparison to our study.
Experience from this study provides a baseline for further investigation and clarity on the direction of future audits. There were a large number of variables predicting adherence to guidelines, but only a few were related to adherence in multivariable analyses suggesting that these latter variables deserve close attention in any audit, and perhaps in patient care. A more simplified audit is therefore feasible with all sites still focusing on key guidelines but also addressing assessment of comorbid diseases, which have been more variably adhered to in this audit.
Adherence to key treatment guidelines for ART initiation is supported by clinical trial data. A key question remaining, however, is whether adherence to treatment guidelines improves patient outcomes.
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HIV Guidelines Audit Steering Committee: Mark Bloch, Andrew Carr, Nicola Cunningham, Jennifer Hoy, Anna Pierce, Norman Roth, and Jo Watson.
Participating sites, patients. and physicians—Melbourne: The Alfred Hospital: Paul Cameron, Kate Cherry, Suzanne Crowe, Jon Darby, Justin Denholm, Joe Doyle, Julian Elliott, Andrew Fuller, Michelle Giles, Margaret Hellard, Jenny Hoy, Simon Iles, David Iser, Adam Jenney, Stephen Kent, Sharon Lewin, John Mills, Anne Mijch, Orla Morrissey, Jessica Rotty, Joe Sasadeusz, Matthew Skinner, Denis Spelman, Alan Street, Olga Vujovic, Amanda Wade, Steve Wesselingh; Ian Woolley, Edwina Wright, Michelle Yong, Prahran Market Clinic: Drs Mark Choong, Pauline Cundill, Beng Eu, Tek Lim, Mike Porter, Norm Roth, Sven Strecker. Sydney: Holdsworth House Medical Practice: Drs David Austin, Mark Bloch, Andrew Gowers, Hsin Hua Liu, Ercel Ozser, Dick Quan. St Vincent's Hospital: Drs Mark Boyd, Bruce Brew, Andrew Carr, David Cooper, Greg Dore, Anthony Kelleher, Kersten Koelsch, Debbie Marriott, Gail Matthews, Sam Milliken, and Sarah Pett.
Project Manager: N. Cunningham (HHMP).
Site coordinators: S. Agrawal (HHMP), K. Sinn (SVH), H. Lau, and M. Bryant (PMC), C. Rayner, J. Armishaw & A. Pierce (The Alfred).
Statisticians: M. Bailey and N. Andriopoulos.
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