Date of study period: April 12 May 7, 2010 and August September, 2010

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1 Classification of antiretroviral therapy failure using immunologic and clinical versus virologic monitoring in HIV-infected children and adolescents in Cambodia Date of study period: April 12 May 7, 2010 and August September, 2010 Location/Foreign Institution: Angkor Hospital for Children (AHC), Siem Reap, Kingdom of Cambodia. AHC is a pediatric teaching hospital funded by Friends without a Border, a New York based non-governmental organization (NGO) founded by Kenro Izu in 1996 whose sole initial aim was to build a pediatric hospital in Siem Reap, Cambodia. Construction was completed in 1999 and over 650,000 children have been treated in the subsequent decade of operation. The AHC Medical Education Center, a joint project, formally trains over 1,000 local doctors and nurses annually. Staffing is provided by full-time Cambodian directors of nursing, surgery, and pediatrics, with administrative leadership from ex-pat stakeholders. The hospital complex provides 24 hour emergency care, outpatient and inpatient clinical services, as well as basic surgical and dental services. Outpatient services include pediatric TB and HIV clinics, the latter currently servicing approximately 800 children. Since its inception, AHC has been closely associated with Hasbro Children s Hospital and Brown University through partnerships initiated by Dr. David Pugatch and continued by Dr. Randall Rockney. The currently available Brown Medical School elective BioMed 467 Pediatrics in a Developing Country: Cambodia is highly desired, and pediatric residents at Hasbro are encouraged to spend a month rotation at AHC during their training. Rotating medical students and residents are further encouraged to undertake educational, research, or community-based projects during their stay under the leadership of local faculty including Dr. Soeung Seitaboth who directs the pediatric HIV program and is a prior trainee of the Fogarty AIDS Training and Research Program at Brown University. Hospital rounds and clinical records are recorded in the English language. Information from patient files, including admission and follow-up data, is routinely entered into an HIV-specific database that can be accessed to provide de-identified information for use in quality improvement projects and chart reviews. Mentor: Mentorship will be provided by Dr. Rami Kantor. Dr. Kantor is an Assistant Professor of Medicine in the Division of Infectious Diseases at the Alpert School of Medicine at Brown University and an expert in the area of HIV drug resistance, with numerous prior publications in this area conducted in partnership with overseas institutions. He recently completed a study in western Kenya on treatment failure misclassification based on immunologic criteria, published in Clinical Infectious Diseases (Clin Infect Dis, 2009; 49:454-62). Dr. Kantor will serve as primary mentor for this project, advising on study design, data collection, and statistical analysis. Additional mentorship will be provided by Dr. Elizabeth Dufort. Dr. Dufort is an Assistant Professor of Pediatrics in the Division of Pediatric Infectious Diseases at the Alpert School of Medicine at Brown University, and an expert in the care of children and adolescents with HIV. She has extensive experience working in resource-limited settings, and has recently completed work on a study of antiretroviral therapy failure from

2 a large cohort of children in Western Kenya. She will provide assistance in analysis of collected data with a focus on factors relevant to care of HIV-infected children in these settings. Additional on-site guidance and support will be provided by Dr. Soeung Seitaboth, Director, Pediatric HIV Services, Angkor Hospital for Children. Finally, support is also being provided by Dr. Herb Harwell, Associate Professor, Division of Infectious Diseases, Brown University. Dr. Harwell is an experienced pediatric and adult infections diseases clinician, currently a consultant for the Clinton Foundation and based in Southeast Asia. He has been collaborating with researchers in Cambodia since Background and Significance: Globally, an estimated 2 million children under the age of 15 years are living with HIV/AIDS. While the majority resides in sub-saharan Africa, South and Southeast Asia account for up to 140,000 of these cases. Cambodia has the second-highest HIV prevalence in Southeast Asia, currently estimated at 67,000-84,000 total cases and accounting for 0.8% of the population. Among antenatal clinic (ANC) attendees, HIV prevalence was last estimated at 1.4-5% in % of HIV-infected pregnant women have access to antiretroviral (ARV) medications for the prevention of mother-to-child transmission (PMTCT), and only 9.8% of ANC clinics offer HIV counseling and testing. As a result, an estimated 4,400 children under the age of 15 are currently living with HIV/AIDS. Combination antiretroviral therapy (ART) became available in 2003 and by the end of 2007, 2,541 children were receiving ART (1). In resource-rich settings, HIV-infected children receiving ART are monitored with routine CD4 and HIV viral load (VL) testing at each visit. This allows for the detection of treatment failure manifesting as persistently elevated VL despite good adherence to the prescribed medication regimen, typically defined as >6 months of elevated VL (2). In resource-limited areas where VL assays are not available, clinical and immunologic monitoring may be the only available means for detection of ART failure. Current WHO guidelines suggest that VL measurement is not recommended for decision-making on initiation or regular monitoring of ART in resource-limited settings, but rather be reserved for scenarios of discordance in clinical or immunologic parameters (3). The rationale for this recommendation is that a precise threshold of virologic replication predicting clinical failure in children is not known, and that resources should be reserved when possible. Instead, failure of an ART regimen is identified by immunologic and clinical monitoring in most resource-limited settings. WHO guidelines define immunologic treatment failure as: 1) development of age-related severe immunodeficiency (as determined by age-related CD4 value) after a period of initial recovery, 2) new progressive age-related severe immunodeficiency, or 3) rapid decline of CD4 value below the threshold of age-related severe immunodeficiency. WHO guideline definitions of clinical treatment failure include any new WHO clinical stage 3 or 4 events in a child receiving ART. Both definitions require >24 weeks of consistent therapy with ensured adherence and adequate treatment of malnutrition and intercurrent opportunistic infections or immune reconstitution inflammatory syndrome events (3). Concern has been raised that clinical and immunologic parameters may not be sufficiently sensitive to detect virologic failure in adults receiving ART, and that delay in recognition may result in increased acquisition of drug resistant mutations as well as increased morbidity and mortality (4-5). Conversely, patients categorized as failing ART by clinical and immunologic criteria may in fact be fully suppressed and therefore

3 switched to 2 nd line regimens inappropriately (6-8). Whether the same is true in HIVinfected children is not clear. Preliminary data from our group has shown that among a cohort of 117 Kenyan children aged 0 18 years who were assessed by on-site clinicians as failing ART, 25% actually had undetectable HIV viral loads and would likely have been inappropriately switched to second-line ARV regimens had virologic monitoring not been performed (9). Similar rates of misclassification may also be occurring in other resource-limited settings outside of sub-saharan Africa. Data from the Kenyan cohort did not allow assessment of virologic failure in children without clinical or immunologic failure since VL monitoring was not routinely performed. Whether misclassification can be predicted based on additional parameters, such as patient demographics, ARV regimen, age, or comorbidity is also unknown. Additional insight into these issues may impact future recommendations for treatment monitoring of HIV-infected children receiving ART in resource-limited settings. The AHC site offers an excellent opportunity for investigation of these questions, as viral loads are determined at 6 month intervals for all children receiving ART. Objectives and Specific Aims: 1) To identify the frequency of misclassification of virologic failure in children receiving ART at the HIV clinic based at Angkor Hospital for Children in Siem Reap, Cambodia. a. To determine the proportion of children that are incorrectly identified as failing ART by clinical and immunologic criteria when in fact the HIV viral load has remained undetectable. b. To determine the proportion of children that are incorrectly identified as NOT failing ART by clinical and immunologic criteria when in fact the viral load has remained persistently detectable. 2) To describe the characteristics of children who are misclassified by immunologic and clinical criteria. a. To identify factors that may predict misclassification, which will therefore allow prioritization of viral load monitoring in those children at highest risk of misclassification. b. To describe the antiretroviral resistance patterns of children misclassified by current WHO criteria. Methods/Data Collection Procedures: This study will be a retrospective observational study of de-identified data from the AHC HIV clinic cohort. All HIV-infected pediatric patients aged 6m to 18y receiving combination ART for 6 months who had HIV viral load determined while on therapy between 1 January 2007 and 1 January 2010 will be included. Patients will be excluded if no viral load assay was performed after receipt of 6 months of a stable regimen. Data from clinical charts will be collected on age, gender, death, and most recent encounter date. In children defined by WHO guidelines as failing ART by either immunologic or clinical critera, or in whom the plasma VL is not fully suppressed, data

4 on WHO stage, ART regimen, CD4 count and percentage, history of treatment with ARVs for PMTCT, and history of treatment for active tuberculosis with a rifampicincontaining regimen while receiving ART will be collected from the time period before, during, and after the determination of ART failure was made up to the time of data collection cutoff on 1 January Antiretroviral resistance raw data and profiles obtained at the time of virologic failure will also be recorded. Virologic failure will be defined as a viral load above the limit of detection of the utilized assay on a single occasion in children receiving ART for >6 months. Virologic suppression will be defined as viral load results below the limit of detection of the utilized assay. During data analysis, additional viral load cutoffs of <1,000 (low) and <5,000 (high) will be analyzed to account for low level virologic replication (blips) that may not represent ongoing virologic failure. Clinical and immunologic failure will be defined as outlined by the WHO guidelines for the antiretroviral therapy of HIV infection in infants and children (3). Misclassification will be defined as a child meeting WHO clinical or immunologic, but not virologic, definition of failure OR a child NOT meeting WHO clinical nor immunologic definition of failure but with a detectable viral load. Institutional Review Board (IRB) approval will be obtained from Brown University and Angkor Hospital for Children prior to the collection of protected health information. Planned dates of travel to Cambodia are 1) April 12 May 7, 2010, and 2) 8 weeks from August September, Data Analysis: Primary outcome will be defined as misclassification of treatment failure as defined by clinical and immunologic, each vs. virologic criteria. Descriptive analysis of the cohort will be performed with analysis of variance methodologies by age group based on WHO age-based criteria for immunologic monitoring as follows: 1) < 5 years, 2) 5 12 years, and 3) years of age. Logistic regression analysis will be used to identify associations between recorded clinical, laboratory and demographic data and likelihood of misclassification of failure. Identified associations will be tested using prediction models to determine whether a subset of children may be reliably identified as high risk for misclassification of treatment failure and therefore constitute a group in whom virologic testing should be recommended. Plan for Dissemination: Findings from this project will be presented in the following manner, in close cooperation with our Cambodian partners. 1) Presentation at a bi-weekly lunch conference at Angkor Hospital for Children. 2) Presentation in Cambodia at a future national HIV conference (not yet scheduled). 3) Presentation at Brown Center for Aids Research (CFAR) Friday afternoon research-in-progress conference. 4) Abstract submission to an international meeting of the IDSA (October, 2010), CROI (February, 2011), or IAS (July, 2011).

5 5) Manuscript submission to a peer-reviewed journal such as Clinical Infectious Diseases, Pediatric Infectious Diseases Journal, or AIDS. Detailed Budget: Airfare: Providence to Siem Reap, Cambodia $2,800 April May and August September, 2010 $1,400 round-trip Accommodation in Siem Reap $1350 $15/day x 90d Biostatistics consultation $500 Communications: Internet access $5/day x 90 days $450 Cellular phone $30/month x3 months $90 TOTAL $5,190 Sources: 1. UNAIDS/WHO Epidemiological Fact Sheets on HIV and AIDS, 2008 Update. Accessed at on 1/23/ Working Group on Antiretroviral Therapy and Medical Management of HIV- Infected Children. Guidelines for the use of antiretroviral agents in pediatric HIV infection. February 23, 2009; p Available at 3. World Health Organization. Antiretroviral Therapy of HIV Infection in Infants and Children: Towards Universal Access, recommendations for a public health approach Meya, D. et al, Development and evaluation of a clinical algorithm to monitor patients on antiretrovirals in resource-limited settings using adherence, clinical, and CD4 cell count criteria. J Int AIDS Soc, 2009; 12:3 5. Chaiwarith, R. et al., Sensitivity and specificity of using CD4+ measurement and clinical evaluation to determine antiretroviral treatment failure in Thailand. Int J Infect Dis, 2007; 11: Kantor R, et al. Misclassification of First-line Antiretroviral Treatment Failure based on Immunological Monitoring of HIV-infection in Resource-Limited Settings. Clin Infect Dis, 2009; 49: Meya, D., et al. Development and evaluation of a clinical algorithm to monitor patients on antiretrovirals in resource-limited settings using adherence, clinical and CD4 cell count criteria. J Int AIDS Soc, : Reynolds, S.J., et.al., Failure of immunologic criteria to appropriately identify antiretroviral treatment failure in Uganda. AIDS, : Dufort E.M., Winstone M. Nyandiko, and Rami Kantor. Unpublished data.

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