The crude estimated 18-month cumulative incidence of LTFU was significantly higher in children <24 months at baseline compared with that in older children (P < 0.01, Fig. 1) and in children with CD4 percentage ≥20% or unknown percentage at baseline, compared with those with CD4 percentage <20% (P < 0.01, Fig. 2). In the adjusted statistical analysis, a number of patient-level and site-specific factors were identified as independent predictors of higher LTFU hazards adjusted for the competing risk of death (Table 3; see Table, Supplemental Digital Content 2, http://links.lww.com/QAI/A371): age <12 months versus 10–15 years (asHR 1.6; CI: 1.4 to 2.0, P < 0.01), having received a first-line PI-based ART (asHR 1.4; CI: 1.2 to 1.7, P < 0.01); or another regimen (asHR 1.7; CI: 1.3 to 2.1, P < 0.01) versus an NNRTI-based regimen; having clinical AIDS or stage-4 disease (asHR 1.4; CI: 1.2 to 1.6, P < 0.01), or unknown AIDS staging (asHR 1.7; CI: 1.5 to 2.0, P < 0.01) versus non-AIDS stage, having started ART in 2005–2007 (asHR 2.4; CI: 2.0 to 2.8, P < 0.01), or having started ART after 2007 (asHR 3.4; CI: 2.9 to 4.1, P < 0.01) versus having initiated therapy before 2005, receiving care in a nonurban clinic (asHR 1.7; CI: 1.4 to 1.9, P < 0.01) versus being treated at an urban clinic; having to pay for laboratory tests (asHR 2.6, 95% CI: 1.9 to 3.5, P < 0.01) versus receiving free access to laboratory tests and having to pay for first-line antiretrovirals (asHR 5.0, 95% CI: 3.4 to 7.3, P < 0.01) versus having access to free ART, being a member of a larger cohort (ie, 1 with 500–800 children; asHR 1.8, 95% CI: 1.5 to 2.3, P < 00.1) versus a smaller cohort (<250 children), and receiving care in East Africa (asHR 3.5, CI: 2.6 to 4.7, P < 0.01), or in West Africa (asHR 3.1, CI: 2.2 to 4.3, P < 0.01) versus Asia the region with the lowest rates of LTFU (see Table 5, Supplemental Digital Content 1, http://links.lww.com/QAI/A371).
Predictors of a less frequent LTFU were as follows: having CD4% (10%–20%, asHR 0.8; CI: 0.7 to 1.0, P = 0.03) versus ≥20%, receiving care in a private clinic (asHR 0.2 CI: 0.1 to 0.3, P < 0.01) rather than in a public clinic, and cohort size (250–500, asHR 0.8 CI: 0.6 to 0.9, P < 0.01).
As HIV treatment is rapidly scaled up toward universal access in the first decade of the 21st century, the IeDEA multiregional pediatric collaboration provides a unique opportunity to monitor, analyze, and compare children’s outcomes taking into account patient and program-level factors while accounting for regional heterogeneity in these factors, in large-scale care and treatment programs in low- and middle-income countries. This analysis included 13,611 children contributing with 20,417 child-years of follow-up in a large number of pediatric cohorts. The overall cumulative mortality was measured at 5.7%, whereas LTFU rate was 12.3% after 18 months on ART, with marked differences of these estimates between the 4 regions studied: Asia, East Africa, West Africa, and Southern Africa.
There are important observations gleaned from our study. First, the 18-month mortality in children on ART is much lower than the reported mortality estimates among untreated children before the ART era,24,25 arguing for a clear benefit of ART as a pediatric HIV intervention. Our mortality estimates are consistent with those of previous reports of studies conducted among HIV-infected children on ART in resource-constrained countries with reported mortality rates, ranging from 6.3% to 11.5%, usually obtained in small-size cohorts and in the early periods of the ART scale-up.5,7,9–14,26 Despite heterogeneity between regions, our findings consistently reflect the impact of overall delayed ART initiation in children when adjusting for individual, programmatic, and regional factors. Indeed, independent individual predictors of residual mortality on ART (advanced clinical stage of HIV disease, and severe immunosuppression) reflect late access to ART. In addition, most (71%) deaths in this data set occurred within the first 6 months after ART initiation, advocating for earlier and increased access to ART initiation in the pediatric population. These findings are consistent with those reported in previous studies5,7,9–14 and in individual IeDEA regions.8,26–28 A number of site-specific variables also explained part of the observed mortality: A greater cohort size increased mortality risk, possibly reflecting the impact of skilled health care staff shortages or work overload, receiving care in Western Africa independently increased the mortality by 40% compared with in East Africa. Although delayed ART initiation is common in all regions, there were significant differences in site-level factors such as having lower access to free HIV services in Western Africa compared with other regions (laboratory tests, OI prophylaxis, first-line, and second-line ART).
Second, the 18-month LTFU rates were unacceptably high and differed substantially across regions, with significant 3.5-fold and 3.1-fold increased hazards in East Africa and West Africa compared with the risk in Asia. Multiple sources of between-region heterogeneity could explain these higher LTFU rates including variations in (1) operational definitions of LTFU and patient tracing systems, (2) lack of access to free HIV services (laboratory tests, antiretroviral drugs, and OI prophylaxis) in West Africa compared with other regions, (3) failure to accurately capture patient transfers as documented transfer-out rates differed significantly between regions, as very few transfers (<1%) were recorded in East and West Africa compared with 16% in Southern Africa, (4) levels of decentralization of HIV pediatric care out of urban hospitals, and (5) reliability of drug supply chain management for non-NNRTI–based regimens, which are less affordable and accessible in East and West Africa compared with that in Southern Africa. Requiring the patients’ families to shoulder the fees for HIV care and clinical services was associated with higher LTFU rates as has previously been reported in adults.29
In addition to patient-level and site-specific factors, our analysis illustrated the substantial impact of the large-scale ART rollout in lower-income countries over the past decade. Initiation of ART after 2005 and site cohorts with (500–800) children were associated with increased hazard of LTFU, whereas cohorts with <500 children had lower LTFU rates. As antiretroviral treatment decreases mortality, we hypothesize that the number of HIV-infected children treated will continue to increase over time, particularly in regions where transfer-out rates are low, such as in East Africa and West Africa. This substantial increase in the number of HIV-infected children followed in individual health facilities and the associated increased workload may further negatively impact the standard of care. Finally, the political instability and violence crisis could have also increased the rates of LTFU in East and West Africa, as this was recently investigated in Kenya.30
We observed the seemingly contradictory finding that treatment at private clinics (where presumably care is not free) were associated with higher rates of death but lower rates of LTFU compared with being cared at public clinics (more frequently free of charge). Although not explicitly measurable with these data, we suspect that this dichotomy may reflect that record-keeping practices may be better in private settings with a significantly higher mortality rates documented and lower LTFU rates compared with public settings, with a substantial proportion of excess LTFU being unreported mortality.
Limitations must be acknowledged in our study. The mortality rate we observed at 18 months is likely to be underestimated because of the high rates of LTFU, with a proportion of those lost more likely to die soon after defaulting from the program. Indeed, mortality has been commonly underreported in African adult ART programs due to limited access to care and the frequent occurrence of death at home.16 The same finding was recently observed in children in East Africa where mortality and disclosure issues, including fear of family or community discrimination, were the most important reasons why children became lost to follow-up.31 Thus, it would be valuable to further ascertain outcomes at least in a sample of those children lost to follow-up in pediatric programs to correct the mortality rates as proposed in adults.32 Even though this information was available in a small number of cohorts in this study, this was not attempted here so our estimates are likely underestimating overall mortality rates, particularly in regions with high rates of LTFU. This means that pediatric outcomes may be much worse than reported, particularly in regions, such as East and West Africa, with both high mortality and LTFU rates.
When the cohort size is large, as in this case, statistical significance testing of baseline variables may produce highly significant statistical differences, even when they may have little clinical or programmatic implication. For example differences in gender between the regions was <5% (absolute) but was still highly statistically significant.
Data quality is another concern when analyzing such large collaborative data sets is. Lack of data completeness and substantial interstudy heterogeneity may reduce the accuracy of our results compared with studies coming from more homogeneous settings. Also, data on factors related to ART adherence or other social issues such as disclosure and orphan status, which were not generally available in our data, would help to better explain clinical outcomes in HIV-infected children. Smaller studies where these issues were documented have reported that disclosure is associated with ART adherence and needs to be monitored in programs.33 In addition, substantial rates of missing data on a number of target outcomes and their predictors and record-keeping practices have been varied over time and between regions. In the adjusted regression analyses, when missing variables were included as a separate category within variables, this may introduce bias in the effect estimates,34 and this was the reason why we did not included variables if missing data were >70%.
Finally, our study may not be representative of all children on ART in these regions as most of the data were gathered from urban sites, in which the standard of care may be higher than in rural areas. Thus, we hypothesize that the programmatic deficiencies identified here could be worse in less structured clinical settings or at lower levels of the health care system. Nevertheless, we are confident of our main findings, which raise significant operational concerns regarding the impact of both delayed ART start as measured by the high rates of advanced disease at the time of care initiation in our cohort, and the importance of long-term retention to care once enrolled into a program.
Despite the possibly superior level of care in our facilities, and concerns with missing data or quality of data collection, our mortality outcomes confirm that there is still a gap in achieving the standard of implementation of early ART in all HIV-infected children <2 years old as recommended in the 2010 WHO guidelines.35 Increasing early access to ART would decrease early on-ART mortality as demonstrated in the CHER trial.36 This is one of the primary operational challenges in pediatric care in these settings, pointing to the need for earlier identification of HIV-infected children, as soon as possible after birth, followed by expedited linkages from testing to ART initiation.
Retention in HIV care is one of the most important challenges faced by health care workers and HIV-implementing partners as the coverage of HIV care and ART have improved for children in low-income countries.37 In this study, high LTFU rates were associated with rapid scale-up, suggesting problems of adaptation of the health care organization and/or staff shortages. Evolving to smaller decentralized clinics rather than to expanding large single programs and task shifting could result in increased access to ART services and good program outcomes as recently reported in Malawi.38,39 Finally, LTFU was strongly associated with fees for ART services. This predictable finding, already reported in adults29 underscores the urgent need for universal free access to all ART services for children too.
Future research should assess whether health systems are meeting the challenges of providing care linkages between all points on the HIV care continuum from early infant diagnosis, to ART initiation and long-term retention of patients. It is also crucial to better document the causes of loss to program and to propose sustainable approaches to increase retention in HIV pediatric programs in lower-income countries.
With this aim, access to treatment through a family-centered approach should be considered. In this model, primary caregivers on treatment can be sources of continuity, knowledge, and strength for pediatric patients and other HIV-infected family members.40,41
Although data quality of such international data sets should be improved and documentation of clinical outcomes could have been more complete, this multiregional collaborative study offered a unique opportunity to improve our understanding of the rapidly expanding pediatric ART services taking into account both patient-level and site-specific factors. Such analyses should be repeated to explore secular trends in the second decade of wide ART use in these settings. Large-scale ART for children in resource-limited settings is feasible, but innovative and sustainable approaches are urgently required to improve early ART initiation, and retain children in ART programs in lower-income countries.
The authors acknowledge all the children and their families followed up in the participating pediatric centers. They also thank the staff from all participating pediatric centers. They warmly thank all the investigators and pediatric coordinators from the Pediatric IeDEA Regions contributing to the project: Asia (Annette Sohn), East Africa (Kara Wools-Kaloustian), Southern Africa (Mary-Ann Davies), Western Africa (Alain Azondekon), and the IeDEA Pediatric Working Group: Melanie Bacon, Rosemary McKaig, Robin Huebner, and Lori Schwarze. They also thank Denis Nash (Columbia University, Mailman School of Public Health) for helping with the regional site survey and Andrea Ciaranello for her helpful comments on earlier draft. Special thanks to Alioum Ahmadou (ISPED) for his statistical advice.
This study was led by the IeDEA West-Africa Group (principal investigators: François Dabis, Emmanuel Bissagnéné); Bordeaux staff: Eric Balestre, Didier K. Ekouévi, Charlotte Lewden, Valériane Leroy, Karen Malateste, Elodie Rabourdin, Rodolphe Thiebaut. Abidjan staff: Gérard Allou, Jean-Claude Azani, Patrick Coffie, Hughes Djétouan, and Bertin Kouadio.
The International Epidemiological Databases to Evaluate AIDS in West Africa (IeDEA West Africa) is supported by the National Cancer Institute, the Eunice Kennedy Shriver National Institute of Child Health and Human Development, and the National Institute of Allergy and Infectious Diseases as part of the International Epidemiologic Databases to Evaluate AIDS (IeDEA; grant no. 5U01AI069919-01 to 04). The content of this publication is solely the responsibility of the authors and does not necessarily represent the official views of any of the institutions mentioned above. No funding bodies had any role in study design, data collection and analysis, decision to publish, or preparation of the article.
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The IeDEA West Africa Working Group is organized as follows: Primary Investigators: Pr François Dabis* (INSERM U897, ISPED, Bordeaux, France), Pr Emmanuel Bissagnene* (SMIT, CHU de Treichville, Abidjan, Côte d’Ivoire). Clinical Investigators by country and alphabetical order (*Member of the IeDEA West Africa Technical Committee): Jocelyn Akakpo, Alain Azondékon, Jules Bashi, Sagbo Gratien, Sikiratou Koumakpaï, Marcel D. Zannou* (Benin); Ye Diarra, Eric-Arnaud Diendere, Joseph Drabo,* Fla Koueta (Burkina Faso); Edmond Aka-Addi, Clarisse Amani-Bosse, Franck-Olivier Ba-Gomis, François Eboua-Tanoh, Serge-Paul Eholie,* Calixte Guehi, Kouakou Kouadio, Serge-Olivier Koulé, Eugène Messou, Albert Minga, Aristophane Tanon, Marguerite Timité-Konan, Pety Touré (Côte d’Ivoire); Kevin Peterson* (Gambia); Bamenla Goka, Lorna Renner* (Ghana); Hadizatou Coulibaly, Fatoumata Dicko, Moussa Maiga,* Daouda Minta, Mariam Sylla, Hamar Alassane Traoré; Man Charurat* (Man Charurat); Bernard Diop, Fatou Ly Ndiaye, Papa Salif Sow, Haby Signaté Sy,* Judicaël Tine (Senegal). Epidemiology and Statistical Unit (INSERM U897, ISPED, Université Victor Segalen, Bordeaux, France): Eric Balestre, Didier K. Ekouévi,* Antoine Jaquet,* Valériane Leroy,* Charlotte Lewden,* Karen Malateste, Annie Sasco, Rodolphe Thiebaut. Data Management Unit (PACCI, CHU Treichville, Abidjan, Côte d’Ivoire): Gérard Allou, Jean Claude Azani, Patrick Coffie. Pediatric clinical centers by city and country: Abidjan, Côte d’Ivoire: ACONDA-CEPREF, ACONDA-MTCT-Plus, CHU de Yopougon, Centre Intégré de Recherche Bioclinique d’Abidjan (CIRBA). Accra, Ghana: Korle Bu Teaching Hospital, Bamako, Mali: Hôpital Gabriel Touré. Cotonou, Benin: Centre National Hospitalo-Universitaire Hubert Maga, Hôpital d’Instruction des Armées. Dakar, Senegal: Hôpital d’Enfants Albert-Royer. Fajara, Gambia: Medical Research Council. Ouagadougou, Burkina-Faso: Centre Hospitalier Charles de Gaulle. Administration: Alexandra Doring and Elodie Rabourdin (ISPED), Hughes Djétouan, Bertin Kouadio, and Adrienne Kouakou (PACCI).
The IeDEA Southern Africa Steering Group is organized as follows: Member Sites (sites denoted with an asterisk contributed data to this analysis): *Cleophas Chimbetete, Newlands Clinic, Harare, Zimbabwe; Anna Coutsoudis, PMTCT Plus, Cato Manor, Durban; Diana Dickinson, Gaborone Independent Hospital, Gaborone, Botswana; *Brian Eley, Red Cross Children’s Hospital, Cape Town, South Africa; Lara Fairall, Free State Provincial ART Program, South Africa; Christiane Fritz, SolidarMed Zimbabwe, Zimbabwe;*Daniella Garone, Khayelitsha ART Program and Médecins Sans Frontières, Cape Town, South Africa; *Janet Giddy, McCord Hospital, Durban, South Africa; Christopher Hoffmann, Aurum Institute for Health Research, South Africa; Timothy Meade, CorpMed Clinic, Lusaka, Zambia; Patrick MacPhail, Themba Lethu Clinic, Helen Joseph Hospital, Johannesburg, South Africa; Lerato Mohapi, Perinatal HIV Research Unit, Johannesburg, South Africa; *Harry Moultrie, Wits Institute for Sexual Reproductive Health, HIV and Related Diseases, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, and Harriet Shezi Children’s Clinic, Chris Hani Baragwanath Hospital, Soweto, South Africa; James Ndirangu, Hlabisa HIV Treatment and Care Program, South Africa; Sabrina Pestilli, SolidarMed Mozambique, Mozambique; *Sam Phiri, Lighthouse Clinic, Lilongwe, Malawi; *Hans Prozesky, Tygerberg Academic Hospital, Stellenbosch, South Africa; Jeff Stringer, Center for Infectious Disease Research in Zambia, Zambia; *Karl Technau, Empilweni Service and Research Unit, Rahima Moosa Mother and Child Hospital, University of the Witwatersrand, Johannesburg, South Africa; *Paula Vaz, Paediatric Day Hospital, Maputo, Mozambique; *Robin Wood, Gugulethu and Masiphumelele ART Programs and Desmond Tutu HIV Centre, Cape Town, South Africa. Central Team: Matthias Egger, Claire Graber, Fritz Kaeser, Olivia Keiser, Institute of Social and Preventive Medicine, University of Bern, Bern, Switzerland; Andrew Boulle, Morna Cornell, Mary-Ann Davies, Nicola Maxwell, School of Public Health and Family Medicine, University of Cape Town, Cape Town, South Africa.
The TREAT Asia Pediatric Network of IeDEA Asia-Pacific is organized as follows: V. Saphonn,* S. Saramony, National Centre for HIV/AIDS Dermatology and STDs, Phnom Penh, Cambodia; U. Vibol,* S. Sophan, National Pediatric Hospital, Phnom Penh, Cambodia; J. Tucker, New Hope for Cambodian Children, Phnom Penh, Cambodia; F.J. Zhang, Beijing Ditan Hospital, Capital Medical University, Beijing, China; N. Kumarasamy,* S. Saghayam, Y.R. Gaitonde Centre for AIDS Research and Education, Chennai, India; N. Kurniati,* D. Muktiarti, Cipto Mangunkusumo General Hospital, Jakarta, Indonesia; SM Fong,* M. Thien, Hospital Likas, Kota Kinabalu, Malaysia; N.K. Nik Yusoff,* L.C. Hai, Hospital Raja Perempuan Zainab II, Kelantan, Malaysia; K.A. Razali,* J.M. Thahira, N.F. Abdul Rahman, Pediatric Institute, Hospital Kuala Lumpur, Kuala Lumpur, Malaysia; R. Nallusamy,* K.C. Chan, Penang Hospital, Penang, Malaysia; V. Sirisanthana,* L. Aurpibul, Chiang Mai University, Chiang Mai, Thailand; R. Hansudewechakul,* P. Taeprasert, Chiangrai Prachanukroh Hospital, Chiang Rai, Thailand; P. Lumbiganon,* P. Kosalaraksa, P. Tharnprisan, Khon Kaen University, Khon Kaen, Thailand; G. Jourdain, Program for HIV Prevention and Treatment, Chiang Mai, Thailand; J. Ananworanich,* C. Phasomsap, T. Suwanlerk, The HIV Netherlands, Australia, Thailand Research Collaboration (HIV-NAT), Bangkok, Thailand; K. Chokephaibulkit,* W. Phongsamart, O. Wittawatmongkol, Siriraj Hospital, Mahidol University, Bangkok, Thailand; H.K. Truong,* D.A.N. Mai, Children’s Hospital 1, Ho Chi Minh City, Vietnam; C.V. Do,* M.T. Ha, Children’s Hospital 2, Ho Chi Minh City, Vietnam; B.V. Huy,* V.L. Nguyen, National Hospital of Pediatrics, Hanoi, Vietnam; N.O. Le, Worldwide Orphans Foundation, Ho Chi Minh City, Vietnam; A.H. Sohn,* N. Durier, J. Pang, TREAT Asia, amfAR—The Foundation for AIDS Research, Bangkok, Thailand; D.A. Cooper, M.G. Law,* A. Kariminia, The Kirby Institute, University of New South Wales, Sydney, Australia (*Steering Committee members).
The IeDEA East Africa Steering Group is organized as follows: Dr. S. Ayaya: the United States Agency for International Development-Academic Model Providing Access To Health Care (USAID-AMPATH) Program; Dr. Lyamuya: Morogoro; Dr. Maruchu: Tumbi; Dr. Bukusi and Dr. Cohen: Family AIDS Care and Education Services; BS. Musick, C.T. Yiannoutsos, and E. Sang: East African Regional Data Center.