Sensitivity analyses of predictors of virological suppression
Restricted to the complete case analysis, the same factors (age at cART initiation, baseline CD4+% and viral load) remained significantly associated with faster virological suppression (Interval) (Supplementary Table 1, http://links.lww.com/QAD/B452). Regression spline analysis further revealed a linear relationship of significant predictors with the outcome (Supplementary Fig. 2, http://links.lww.com/QAD/B452). Results from multivariable analyses of time to virological suppression (Midpoint) and (Observed) were similar, both with and without multiple imputation (Supplementary Tables 1 and 2, http://links.lww.com/QAD/B452). In some sensitivity analyses, initial cART regimen and/or geographical region were found to violate the proportional hazards assumption (i.e. interact with analysis time) hence, corresponding interaction terms were included in the relevant final multivariable models to account for this effect. Additional univariable and multivariable analyses using Cox proportional hazards models and interval-censored parametric survival models with Weibull distribution further confirmed the main findings (data not shown).
To our knowledge, this is the largest study reported to date exploring predictors of faster virological response in infants with perinatal HIV initiating cART within 6 months of life. Most infants achieved virological suppression within 12 months of starting cART. This is the first study to show that even amongst infants initiating therapy within 6 months of life, earlier cART initiation predicted faster virological suppression. Higher baseline CD4+% and lower log10 viral load were also independent predictors of faster virological suppression.
Our findings are consistent with the general conclusions from smaller studies that have identified early treatment as a determinant of faster virological suppression. The European EIC study reported faster suppression in infants starting cART earlier (<3 months of age) compared with later treated infants . In another study (n = 128) investigating older ART naïve African children aged 1.7–13.5 years, children younger than 8 years had increased probability of attaining virological suppression compared with older children . Other studies conducted in the United States/Puerto Rico (n = 52), Italy (n = 133) and South Africa (n = 1748; total of five cohorts), revealed that early therapy was a significant predictor of long-term viral suppression in children starting cART at less than 3 months (versus ≥3 months of age)  and less than 6 months (versus ≥6 months of age) [16,18]. Although determining the onset of infection in adults is problematic, recent studies specifically designed to capture this information, have also identified early ART during primary infection as a key factor for faster viral suppression in adults .
The estimated cumulative probability of achieving virological suppression (Interval), (Midpoint) and (Observed) was 89, 84 and 77%, respectively. This is consistent with previous findings despite the variability in definitions of suppression. In the CHER trial (n = 377) conducted in South Africa, the proportion of infants with viral load less than 400 copies/ml by 12 months post-cART initiation was 77% . Similar findings were reported by the EIC study among 139 infants starting cART before 3 months of age . In two studies conducted in Kenya (n = 121) and Mozambique (n = 119), the proportion of children suppressed to less than 1000 copies/ml was 75%  and 77% , respectively, by 12 months after cART start. Similarly, in a Ugandan study (n = 91), the probability of suppression to less than 400 copies/ml was 83.1% in infants starting cART less than 12 months of age . Further evidence that with early intervention high levels of suppression can be achieved comes from a pilot trial of infants randomised to receive immediate or deferred four-drug (three-class) antiretroviral therapy (n = 63)  at a median age of 28 days (intrauterine-infected) and 55 days (intrapartum-infected). The proportions attaining virological suppression to less than 400 copies/ml and less than 50 copies/ml were higher at 100% and 94%, respectively, 12 months post-cART.
The reasons for the critical timing of cART initiation on virological suppression are unclear. The relationship with lower baseline viral load has been observed before in various settings and at different ages [17,19,21,22,34]. There are sound virological and immunological reasons why an individual with lower levels of circulating virus would suppress more rapidly. The viral decay following initiation of ART occurs in phases. Firstly, the initial decline signifies early loss of short-lived virally productive cells. This is followed by the slower loss of longer lived but productive cells. Finally, there is the much slower loss of latently infected cells . In the context of our findings, the implication would be that earlier treatment may target the short-lived cells, which could have important implications for limiting viral reservoirs. This in turn may also provide optimal opportunities for adjunctive therapies as part of the cure agenda .
As well as baseline viral load, faster virological suppression was also associated with a higher baseline CD4+% (also CD4+ cell count). This association has been seen in multiple studies [19,20,34] in infants, children, pregnant women and adults. Although it is tempting to link the lower viral load with the higher CD4+%, they were actually independent predictors of viral suppression, indicating an immunological basis for this finding. Our previous work has shown how critical early treatment is for preserving CD4+ cell counts . In the CHER study, even though early treatment arrested CD4+ decline, it did not fully restore levels to those seen in HIV-uninfected children . When therapy was stopped as part of planned treatment interruption, there was a rapid decline in CD4+ T-cells, which on retreatment returned to levels observed before interruption. This indicates that baseline CD4+ levels provides insight into CD4+ cell homeostasis, with individuals with higher CD4+ having a greater proportion of recent thymic emigrants, which are relatively resistant to HIV infection . The combination of early treatment, low viral load and high baseline CD4+ cells is therefore desirable for many reasons including faster immune reconstitution , limiting viral reservoir seeding, preserving age appropriate CD4+ cell homeostasis and providing opportunities for ‘HIV cure’ . Infants with these characteristics may represent the target population in which to investigate therapeutic vaccines, with the ultimate goal of achieving ART-free HIV remission. Therapeutic vaccines are an integral part of the HIV cure agenda and an increasing global health priority .
Apart from age at cART initiation, baseline CD4+% and viral load, none of the remaining factors examined predicted faster virological suppression in our final multivariable analysis. A few other studies in Europe have, however, reported significant associations with initial cART regimen  and calendar year  in older children starting cART less than 18 years of age. On the other hand, in an Ugandan study, none of the baseline factors investigated (age, sex, CD4+%, WHO stage, cART regimen, weight-for-age or height-for-age z-scores) were found to predict virological suppression to viral load less than 400 copies/ml . Although there was no significant effect of infant and maternal PMTCT prophylaxis on time to virological suppression, the potential effect of PMTCT on suppression has recently been demonstrated .
Our study had limitations. It was a subgroup analysis of pooled observational cohort data, hence potential effects of selection bias and unmeasured confounders cannot be ruled out. Data on exact timing of HIV infection and antiviral treatment adherence were not available and could not be investigated. Although year of cART initiation was not associated with time to virological suppression, our data date back to 1998. Given the changes in treatment guidelines over time across countries, all analyses were adjusted for initial cART regimen and geographical region despite their lack of association with the outcome. Longitudinal investigation of long-term viral suppression in early treated infants is also of interest, but was outside the scope of this article. Finally, although our study supports the earliest feasible cART initiation in infants, there are still challenges that need to be addressed before infants can indeed benefit from very early therapy. These challenges relate to difficulties in scaling up birth testing in low and middle income countries with the highest burden [40–42].
In conclusion, we showed that effective treatment response was achieved in the majority of infants initiating cART within 6 months of life across Europe and Thailand. We identified the conditions needed to attain faster virological suppression in these infants. We demonstrated that even amongst early treated infants, earlier cART initiation, higher baseline CD4+% and lower baseline viral load independently predicted faster virological suppression. These results provide additional support for earlier cART initiation in infants with perinatal HIV and indicate that early treatment influences key virological and immunological parameters that could have important consequences for long-term health.
We thank all the patients for their participation in these cohorts, and the staff members who cared for them.
Writing Group Consisting of Project Team first (ordered alphabetically by name except for the first and last authors for each study team), and also other Writing Group members (ordered alphabetically by cohort name):
EPPICC/EPIICAL Project Team: Man K. Chan (EPIICAL statistician), Ruth Goodall (EPPICC senior statistician), Ali Judd (EPPICC colead), Nigel Klein [Collaborative HIV Paediatric Study (CHIPS), UK and Ireland], Elena Chiappini (Italian Register for HIV Infection in Children, Italy), Thomas Klimkait (Swiss Mother and Child HIV Cohort Study, Switzerland), Nicole Ngo-Giang-Huong [Thailand Program for HIV Prevention and Treatment (PHPT), Thailand], Paolo Palma (EPIICAL colead), Paolo Rossi (EPIICAL scientific coordinator), Claire Thorne (EPPICC colead), Anna Turkova [Paediatric European Network for the Treatment of AIDS (PENTA), Italy], Paola Zangari (EPIICAL scientific coordination), Pablo Rojo (EPIICAL colead), Abdel G. A. Babiker (EPIICAL senior statistician).
Other Writing Group members: Pieter L. Fraaij, Dasja Pajkrt (ATHENA paediatric cohort, Netherlands); Laura Marques (Centro Hospitalar do Porto, Portugal); Intira J. Collins, Diana M. Gibb [Collaborative HIV Paediatric Study (CHIPS), UK & Ireland]; Maria I. González-Tome, Jose T. Ramos, María L. Navarro (Madrid and CoRISPE cohort, Spain); Antoni Noguera-Julian (CoRISPE-cat cohort, Spain); Josiane Warszawski (French Perinatal Cohort Study, France); Christoph Königs (German Pediatric and Adolescent HIV cohort, Germany); Vana Spoulou (Greece Cohort, Greece); Filipa Prata (Hospital de Santa Maria/CHLN, Lisbon, Portugal); Tessa Goetghebuer (Hospital St Pierre paediatric cohort, Belgium); Luisa Galli (Italian Register for HIV infection in children, Italy); Lars Naver (Karolinska Institutet and University Hospital, Stockholm, Sweden); Carlo Giaquinto [Paediatric European Network for the Treatment of AIDS (PENTA), Italy]; Magdalena Marczynska (Polish paediatric cohort, Poland); Liubov Okhonskaia (Republican Hospital of Infectious Diseases, St Petersburg, Russia); Ruslan Malyuta, Alla Volokha (Ukraine Paediatric HIV Cohort Study, Odessa, Ukraine); Luminita Ene (‘Victor Babes’ Hospital Cohort, Romania).
The EPIICAL Consortium study team: Nigel Klein, Diana Gibb, Sarah Watters, Man Chan, Laura McCoy, Abdel Babiker (University College London, UK); Anne-Genevieve Marcelin, Vincent Calvez (Université Pierre et Marie Curie, France); Maria Angeles Munoz (Servicio Madrileño de Salud-Hospital General Universitario Gregorio Marañon, Spain); Britta Wahren (Karolinska Institutet, Sweden); Caroline Foster (Imperial College Healthcare NHS Trust, London, UK); Mark Cotton (Stellenbosch University-Faculty of Medicine and Health Sciences, South Africa); Merlin Robb, Jintanat Ananworanich (The Henry M. Jackson Foundation for the Advancement of Military Medicine, Maryland); Polly Claiden (HIV i-Base, UK); Deenan Pillay (University of KwaZulu-Natal Africa Center, South Africa); Deborah Persaud (Johns Hopkins University); Rob J De Boer, Juliane Schröter, Anet J.N. Anelone (University of Utrecht, Netherlands); Thanyawee Puthanakit (Thai Red Cross AIDS-Research Centre, Thailand); Adriana Ceci, Viviana Giannuzzi (Consorzio per Valutazioni Biologiche e Farmacologiche, Italy); Kathrine Luzuriaga (University of Massachusetts Medical School, Worcester, Massachusetts); Nicolas Chomont (Centre de Recherche du Centre Hospitalier de l’Universitè de Montreal-University of Montreal, Canada); Mark Cameron (Case Western Reserve University, Cleveland, Ohio); Caterina Cancrini (Università degli Studi di Roma Tor Vergata, Italy); Andrew Yates, Louise Kuhn (Columbia University, New York); Avy Violari, Kennedy Otwombe (University of the Witwatersrand, Johannesburg [PHRU] South Africa); Ilaria Pepponi, Francesca Rocchi (Children's Hospital “Bambino Gesu”, Rome, Italy); Stefano Rinaldi (University of Miami, Miller School of Medicine, Florida); Alfredo Tagarro (Hospital 12 de Octubre, Universidad Complutense, Madrid, Spain); Maria Grazia Lain, Paula Vaz (Fundação Ariel Glaser contra o SIDA Pediátrico, Mozambique); Elisa Lopez, Tacita Nhampossa (Fundação Manhiça, Mozambique).
Author contributions: M.C. and R.G. performed the statistical analyses and drafted the article. A.B., A.J., D.G. and P.R. conceptualized and designed the study and, were involved in the preparation and review of the final article. All coauthors participated in discussions about interpretation of findings, were involved in the preparation and critical review of the final article. All participating cohorts within EPPICC were involved in the collection of data and interpretation of the findings.
This work was funded by the Early-treated Perinatally HIV-infected Individuals: Improving Children's Actual Life with Novel Immunotherapeutic Strategies (EPIICAL) consortium (http://www.epiical.org), supported by Paediatric European Network for Treatment of AIDS (PENTA) Foundation, funded through an independent grant by ViiV Healthcare UK. This work was also funded by Medical Research Council programme grant MC_UU_12023/26 awarded to the MRC Clinical Trials Unit and a pilot award to P.P. obtained by Children's Hospital Bambino Gesú (Ricerca corrente 2017 and 2018), and Associazione Volontari Bambino Gesù.
Group authorship: Man K. Chana, Ruth Goodalla, Ali Judda, Nigel Kleinb, Elena Chiappinic, Thomas Klimkaitd, Nicole Ngo-Giang-Huonge, Paolo Palmaf, Paolo Rossif, Claire Thorneb, Anna Turkovaa, Paola Zangarif, Pieter L. Fraaijg,h, Dasja Pajkrti, Laura Marquesj, Intira J. Collinsa, Diana M. Gibba, Maria I. Gonzalez-Tomek, Maria L. Navarrol, Jose T. Ramosm, Antoni Noguera-Juliann, Josiane Warszawskio, Christoph Königsp, Vana Spoulouq, Filipa Pratar, Tessa Goetghebuers, Luisa Gallit, Lars Naveru, Carlo Giaquintov, Magdalena Marczynskaw, Liubov Okhonskaiax, Ruslan Malyutay, Alla Volokhaz, Luminita Eneaa, Pablo Rojok and Abdel G.A. Babikera
Group authorship affiliations:aMRC Clinical Trials Unit at UCL, Institute of Clinical Trials & Methodology, University College London (UCL), bUCL Great Ormond Street Institute of Child Health, London, UK, cUniversity of Florence, Florence, Italy, dUniversity of Basel, Basel, Switzerland, eMI 174 PHPT/Faculty of Medical Sciences, Chiang Mai University, Chiang Mai, Thailand, fResearch Unit in Congenital and Perinatal Infection, Academic Department of Pediatrics (DPUO), Children's Hospital Bambino Gesu‘, Rome, Italy, gDepartment of Viroscience, Erasmus Medical Centre, hSubdivision of Infectious Diseases and Immunology, Department of Pediatrics, Erasmus Medical Centre – Sophia, Rotterdam, iDepartment of Pediatric Infectious Diseases, Emma Children's Hospital, Amsterdam UMC, University of Amsterdam, Amsterdam, The Netherlands, jPaediatric Infectious Diseases and Immunodeficiencies Unit, Pediatric Department, Porto Central Hospital, Porto, Portugal, kPeadiatric HIV and Infectious Diseases Department, Hospital Doce de Octubre, lPediatrics Infectious Diseases Unit, Hospital Universitario Gregorio, mPaediatrics Department, Hospital Clínico Universitario San Carlos, Madrid, nUnitat d’Infectologia, Servei de Pediatria, Hospital Sant Joan de Deu, Universitat de Barcelona, Barcelona, Spain, oInstitut National de la Santé et de la Recherche (INSERM), Paris, France, pDepartment of Paediatrics, University Hospital Frankfurt, Goethe University, Frankfurt, Germany, qDepartment of Infectious Diseases, University of Athens, Athens, Greece, rHospital de Santa Maria, Lisbon, Portugal, sHopital St Pierre, Brussels, Belgium, tUniversita Degli Studi Firenze, Firenze, Italy, uKarolinska Institutet and University Hospital, Stockholm, Sweden, vPaediatric European Network for the Treatment of AIDS (PENTA), Padova, Italy, wMedical University of Warsaw, Hospital of Infectious Diseases, Warsaw, Poland, xRepublican Hospital of Infectious Diseases, St Petersburg, Russia, yPerinatal Prevention of AIDS Initiative, Odessa, zShupyk National Medical Academy of Postgraduate Education, Kiev, Ukraine, and aaVictor Babes Hospital, Bucharest, Romania.
Conflicts of interest
There are no conflicts of interest.
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* Please see Acknowledgements section for list of group authorship authors.
early combination antiretroviral therapy; infants; perinatal HIV; predictors; virological suppression
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