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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">HIV-Exposed Uninfected Infants in Zimbabwe: Insights into Health Outcomes in the Pre-Antiretroviral Therapy Era</title><author><name sortKey="Evans, Ceri" sort="Evans, Ceri" uniqKey="Evans C" first="Ceri" last="Evans">Ceri Evans</name><affiliation><nlm:aff id="aff1"><institution>Zvitambo Institute for Maternal and Child Health Research</institution>,<addr-line>Harare</addr-line>,<country>Zimbabwe</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff2"><institution>Blizard Institute, Queen Mary University of London</institution>,<addr-line>London</addr-line>,<country>UK</country></nlm:aff></affiliation></author><author><name sortKey="Humphrey, Jean H" sort="Humphrey, Jean H" uniqKey="Humphrey J" first="Jean H." last="Humphrey">Jean H. Humphrey</name><affiliation><nlm:aff id="aff1"><institution>Zvitambo Institute for Maternal and Child Health Research</institution>,<addr-line>Harare</addr-line>,<country>Zimbabwe</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff3"><institution>Department of International Health, Johns Hopkins Bloomberg School of Public Health</institution>,<addr-line>Baltimore, MD</addr-line>,<country>USA</country></nlm:aff></affiliation></author><author><name sortKey="Ntozini, Robert" sort="Ntozini, Robert" uniqKey="Ntozini R" first="Robert" last="Ntozini">Robert Ntozini</name><affiliation><nlm:aff id="aff1"><institution>Zvitambo Institute for Maternal and Child Health Research</institution>,<addr-line>Harare</addr-line>,<country>Zimbabwe</country></nlm:aff></affiliation></author><author><name sortKey="Prendergast, Andrew J" sort="Prendergast, Andrew J" uniqKey="Prendergast A" first="Andrew J." last="Prendergast">Andrew J. Prendergast</name><affiliation><nlm:aff id="aff1"><institution>Zvitambo Institute for Maternal and Child Health Research</institution>,<addr-line>Harare</addr-line>,<country>Zimbabwe</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff2"><institution>Blizard Institute, Queen Mary University of London</institution>,<addr-line>London</addr-line>,<country>UK</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff3"><institution>Department of International Health, Johns Hopkins Bloomberg School of Public Health</institution>,<addr-line>Baltimore, MD</addr-line>,<country>USA</country></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">27375613</idno><idno type="pmc">4893498</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4893498</idno><idno type="RBID">PMC:4893498</idno><idno type="doi">10.3389/fimmu.2016.00190</idno><date when="2016">2016</date><idno type="wicri:Area/Pmc/Corpus">000351</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000351</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">HIV-Exposed Uninfected Infants in Zimbabwe: Insights into Health Outcomes in the Pre-Antiretroviral Therapy Era</title><author><name sortKey="Evans, Ceri" sort="Evans, Ceri" uniqKey="Evans C" first="Ceri" last="Evans">Ceri Evans</name><affiliation><nlm:aff id="aff1"><institution>Zvitambo Institute for Maternal and Child Health Research</institution>,<addr-line>Harare</addr-line>,<country>Zimbabwe</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff2"><institution>Blizard Institute, Queen Mary University of London</institution>,<addr-line>London</addr-line>,<country>UK</country></nlm:aff></affiliation></author><author><name sortKey="Humphrey, Jean H" sort="Humphrey, Jean H" uniqKey="Humphrey J" first="Jean H." last="Humphrey">Jean H. Humphrey</name><affiliation><nlm:aff id="aff1"><institution>Zvitambo Institute for Maternal and Child Health Research</institution>,<addr-line>Harare</addr-line>,<country>Zimbabwe</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff3"><institution>Department of International Health, Johns Hopkins Bloomberg School of Public Health</institution>,<addr-line>Baltimore, MD</addr-line>,<country>USA</country></nlm:aff></affiliation></author><author><name sortKey="Ntozini, Robert" sort="Ntozini, Robert" uniqKey="Ntozini R" first="Robert" last="Ntozini">Robert Ntozini</name><affiliation><nlm:aff id="aff1"><institution>Zvitambo Institute for Maternal and Child Health Research</institution>,<addr-line>Harare</addr-line>,<country>Zimbabwe</country></nlm:aff></affiliation></author><author><name sortKey="Prendergast, Andrew J" sort="Prendergast, Andrew J" uniqKey="Prendergast A" first="Andrew J." last="Prendergast">Andrew J. Prendergast</name><affiliation><nlm:aff id="aff1"><institution>Zvitambo Institute for Maternal and Child Health Research</institution>,<addr-line>Harare</addr-line>,<country>Zimbabwe</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff2"><institution>Blizard Institute, Queen Mary University of London</institution>,<addr-line>London</addr-line>,<country>UK</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff3"><institution>Department of International Health, Johns Hopkins Bloomberg School of Public Health</institution>,<addr-line>Baltimore, MD</addr-line>,<country>USA</country></nlm:aff></affiliation></author></analytic><series><title level="j">Frontiers in Immunology</title><idno type="eISSN">1664-3224</idno><imprint><date when="2016">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>The ZVITAMBO trial recruited 14,110 mother–infant pairs to a randomized controlled trial of vitamin A between 1997 and 2000, before the availability of antiretroviral therapy for HIV prophylaxis or treatment in Zimbabwe. The HIV status of mothers and infants was well characterized through 1–2 years of follow-up, leading to the largest cohort to date of HIV-exposed uninfected (HEU) infants (<italic>n</italic> = 3135), with a suitable comparison group of HIV-unexposed infants (<italic>n</italic> = 9510). Here, we draw on 10 years of published findings from the ZVITAMBO trial. HEU infants had increased morbidity compared to HIV-unexposed infants, with 50% more hospitalizations in the neonatal period and 30% more sick clinic visits during infancy, particularly for skin infections, lower respiratory tract infections, and oral thrush. HEU children had 3.9-fold and 2.0-fold higher mortality than HIV-unexposed children during the first and second years of life, respectively, most commonly due to acute respiratory infections, diarrhea/dysentery, malnutrition, sepsis, and meningitis. Infant morbidity and mortality were strongly related to maternal HIV disease severity, and increased morbidity remained until maternal CD4 counts were >800 cells/μL. HEU infants were more likely to be premature and small-for-gestational age than HIV-unexposed infants, and had more postnatal growth failure. Here, we propose a conceptual framework to explain the increased risk of infectious morbidity, mortality, and growth failure among HEU infants, hypothesizing that immune activation and inflammation are key drivers of both infection susceptibility and growth failure. Future studies should further dissect the causes of infection susceptibility and growth failure and determine the impact of ART and cotrimoxazole on outcomes of this vulnerable group of infants in the current era.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Humphrey, Jh" uniqKey="Humphrey J">JH Humphrey</name></author><author><name sortKey="Iliff, Pj" uniqKey="Iliff P">PJ Iliff</name></author><author><name sortKey="Marinda, Et" uniqKey="Marinda E">ET Marinda</name></author><author><name sortKey="Mutasa, K" uniqKey="Mutasa K">K Mutasa</name></author><author><name sortKey="Moulton, Lh" uniqKey="Moulton L">LH Moulton</name></author><author><name sortKey="Chidawanyika, H" uniqKey="Chidawanyika H">H Chidawanyika</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Marinda, E" uniqKey="Marinda E">E Marinda</name></author><author><name sortKey="Humphrey, Jh" uniqKey="Humphrey J">JH 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Front Immunol</journal-id><journal-id journal-id-type="iso-abbrev">Front Immunol</journal-id><journal-id journal-id-type="publisher-id">Front. Immunol.</journal-id><journal-title-group><journal-title>Frontiers in Immunology</journal-title></journal-title-group><issn pub-type="epub">1664-3224</issn><publisher><publisher-name>Frontiers Media S.A.</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">27375613</article-id><article-id pub-id-type="pmc">4893498</article-id><article-id pub-id-type="doi">10.3389/fimmu.2016.00190</article-id><article-categories><subj-group subj-group-type="heading"><subject>Immunology</subject><subj-group><subject>Hypothesis and Theory</subject></subj-group></subj-group></article-categories><title-group><article-title>HIV-Exposed Uninfected Infants in Zimbabwe: Insights into Health Outcomes in the Pre-Antiretroviral Therapy Era</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Evans</surname><given-names>Ceri</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff2"><sup>2</sup></xref><xref ref-type="corresp" rid="cor1">*</xref><uri xlink:type="simple" xlink:href="http://frontiersin.org/people/u/277984"></uri></contrib><contrib contrib-type="author"><name><surname>Humphrey</surname><given-names>Jean H.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff3"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Ntozini</surname><given-names>Robert</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><uri xlink:type="simple" xlink:href="http://frontiersin.org/people/u/345850"></uri></contrib><contrib contrib-type="author"><name><surname>Prendergast</surname><given-names>Andrew J.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff2"><sup>2</sup></xref><xref ref-type="aff" rid="aff3"><sup>3</sup></xref><uri xlink:type="simple" xlink:href="http://frontiersin.org/people/u/279315"></uri></contrib></contrib-group><aff id="aff1"><sup>1</sup><institution>Zvitambo Institute for Maternal and Child Health Research</institution>,<addr-line>Harare</addr-line>,<country>Zimbabwe</country></aff><aff id="aff2"><sup>2</sup><institution>Blizard Institute, Queen Mary University of London</institution>,<addr-line>London</addr-line>,<country>UK</country></aff><aff id="aff3"><sup>3</sup><institution>Department of International Health, Johns Hopkins Bloomberg School of Public Health</institution>,<addr-line>Baltimore, MD</addr-line>,<country>USA</country></aff><author-notes><fn fn-type="edited-by"><p>Edited by: Tobias R. Kollmann, University of British Columbia, Canada</p></fn><fn fn-type="edited-by"><p>Reviewed by: Amy Louise Slogrove, University of Cape Town, South Africa; Fatima Kakkar, University of Montreal, Canada</p></fn><corresp content-type="corresp" id="cor1">*Correspondence: Ceri Evans, <email>ceri.evans@qmul.ac.uk</email></corresp><fn fn-type="other" id="fn001"><p>Specialty section: This article was submitted to HIV and AIDS, a section of the journal Frontiers in Immunology</p></fn></author-notes><pub-date pub-type="epub"><day>06</day><month>6</month><year>2016</year></pub-date><pub-date pub-type="collection"><year>2016</year></pub-date><volume>7</volume><elocation-id>190</elocation-id><history><date date-type="received"><day>15</day><month>2</month><year>2016</year></date><date date-type="accepted"><day>02</day><month>5</month><year>2016</year></date></history><permissions><copyright-statement>Copyright © 2016 Evans, Humphrey, Ntozini and Prendergast.</copyright-statement><copyright-year>2016</copyright-year><copyright-holder>Evans, Humphrey, Ntozini and Prendergast</copyright-holder><license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</license-p></license></permissions><abstract><p>The ZVITAMBO trial recruited 14,110 mother–infant pairs to a randomized controlled trial of vitamin A between 1997 and 2000, before the availability of antiretroviral therapy for HIV prophylaxis or treatment in Zimbabwe. The HIV status of mothers and infants was well characterized through 1–2 years of follow-up, leading to the largest cohort to date of HIV-exposed uninfected (HEU) infants (<italic>n</italic> = 3135), with a suitable comparison group of HIV-unexposed infants (<italic>n</italic> = 9510). Here, we draw on 10 years of published findings from the ZVITAMBO trial. HEU infants had increased morbidity compared to HIV-unexposed infants, with 50% more hospitalizations in the neonatal period and 30% more sick clinic visits during infancy, particularly for skin infections, lower respiratory tract infections, and oral thrush. HEU children had 3.9-fold and 2.0-fold higher mortality than HIV-unexposed children during the first and second years of life, respectively, most commonly due to acute respiratory infections, diarrhea/dysentery, malnutrition, sepsis, and meningitis. Infant morbidity and mortality were strongly related to maternal HIV disease severity, and increased morbidity remained until maternal CD4 counts were >800 cells/μL. HEU infants were more likely to be premature and small-for-gestational age than HIV-unexposed infants, and had more postnatal growth failure. Here, we propose a conceptual framework to explain the increased risk of infectious morbidity, mortality, and growth failure among HEU infants, hypothesizing that immune activation and inflammation are key drivers of both infection susceptibility and growth failure. Future studies should further dissect the causes of infection susceptibility and growth failure and determine the impact of ART and cotrimoxazole on outcomes of this vulnerable group of infants in the current era.</p></abstract><kwd-group><kwd>HIV exposure</kwd><kwd>infant</kwd><kwd>Zimbabwe</kwd><kwd>Africa</kwd><kwd>inflammation</kwd><kwd>immune activation</kwd><kwd>breast-feeding</kwd></kwd-group><funding-group><award-group><funding-source id="cn01">Wellcome Trust<named-content content-type="fundref-id">10.13039/100004440</named-content></funding-source><award-id rid="cn01">108065/Z/15/Z</award-id></award-group><award-group><funding-source id="cn02">United States Agency for International Development<named-content content-type="fundref-id">10.13039/100000200</named-content></funding-source><award-id rid="cn02">Cooperative agreement number HRN-A-00-97-00015-00 between Johns Hopkins University and the Office of Health and Nutrition – USAID</award-id></award-group><award-group><funding-source id="cn03">Bill and Melinda Gates Foundation<named-content content-type="fundref-id">10.13039/100000865</named-content></funding-source></award-group><award-group><funding-source id="cn04">Rockefeller Foundation<named-content content-type="fundref-id">10.13039/100000877</named-content></funding-source></award-group><award-group><funding-source id="cn05">BASF<named-content content-type="fundref-id">10.13039/100004349</named-content></funding-source></award-group><award-group><funding-source id="cn06">National Institute for Health Research<named-content content-type="fundref-id">10.13039/501100000272</named-content></funding-source></award-group></funding-group><counts><fig-count count="1"></fig-count><table-count count="2"></table-count><equation-count count="0"></equation-count><ref-count count="118"></ref-count><page-count count="12"></page-count><word-count count="10980"></word-count></counts></article-meta></front><body><sec sec-type="introduction" id="S1"><title>Introduction</title><p>Before the availability of antiretroviral therapy (ART), around a quarter of infants born to HIV-infected women in Zimbabwe acquired the infection (<xref rid="B1" ref-type="bibr">1</xref>) and almost two-thirds of perinatally infected children died before their second birthday (<xref rid="B2" ref-type="bibr">2</xref>). Coverage of effective interventions for prevention of mother-to-child transmission (PMTCT) is increasing faster than antenatal HIV prevalence is declining, meaning that fewer HIV-infected infants are born annually, but a population of HIV-exposed uninfected (HEU) infants is emerging (<xref rid="B3" ref-type="bibr">3</xref>). Data from several settings over the past decade suggest that HEU children have poorer health outcomes than HIV-unexposed children. However, many studies have not fully characterized maternal and infant HIV status, or have included control groups of HIV-unexposed infants who differ significantly in socioeconomic status or breast-feeding pattern, which may lead to confounding. Furthermore, modern studies are complicated by exposure to maternal and infant ART for PMTCT or cotrimoxazole prophylaxis, making the natural history of HIV exposure difficult to determine. Findings from historical cohorts with comparable control populations are necessary to understand the health outcomes of HEU infants.</p><p>Between 1997 and 2000, 14,110 mother–infant pairs were recruited to a randomized controlled trial of maternal and infant vitamin A in Zimbabwe. The Zimbabwe Vitamin A for Mothers and Babies (ZVITAMBO) trial (<xref rid="B1" ref-type="bibr">1</xref>) took place before the availability of ART for prophylaxis or treatment in Zimbabwe, or the recommendation to provide cotrimoxazole to HIV-exposed infants. The HIV status of mothers and infants was well characterized through 1–2 years of follow-up, leading to the largest cohort to date of HEU infants (<italic>n</italic> = 3135), with a suitable comparison group of HIV-unexposed infants (<italic>n</italic> = 9510). This Review draws on 10 years of published data from this birth cohort, which has provided some of the strongest evidence to date of the poor health outcomes of HEU infants. First, we discuss the morbidity and mortality of HEU infants and the relationship between maternal characteristics and HEU infant outcomes. Second, we discuss growth outcomes, and set these findings within the wider context of other studies that have shown heterogeneous results. Third, we discuss the need for appropriate feeding strategies in HIV-exposed infants to ensure HIV-free survival and to reduce all-cause morbidity and mortality.</p><p>We propose a conceptual framework for poor outcomes in HEU infants and discuss the potential mechanisms underlying our key findings of infection susceptibility and growth failure, drawing also on other published data.</p></sec><sec id="S2"><title>The ZVITAMBO Trial</title><p>The ZVITAMBO trial was a randomized placebo-controlled trial of maternal and/or neonatal vitamin A to reduce HIV transmission and improve child mortality (<xref rid="B1" ref-type="bibr">1</xref>, <xref rid="B4" ref-type="bibr">4</xref>). In brief, 14,110 postpartum mothers and their infants were enrolled within 96 h of delivery between November 1997 and January 2000 in Harare. Mothers and infants were eligible if neither had an acutely life-threatening condition; the infant was a singleton with birth weight ≥1500 g, and the mother planned to stay in Harare after delivery. A single large dose of vitamin A was given in a factorial design either to mother and infant, mother only, infant only, or neither. All but four infants started breast-feeding; at 6 months, 93% of infants were mixed breast-fed. The HIV status of mothers and infants was well characterized: at baseline, 9562 (67.8%) mothers were HIV-negative and 4495 (31.9%) HIV-positive; the remaining 53 mothers were HIV indeterminate. Of infants born to HIV-positive mothers, 381, 508, and 258 were infected <italic>in utero</italic>, intrapartum, and postnatally, respectively; 189 infants became HIV-infected, but the timing was uncertain; and 24 infants did not undergo PCR testing at any time, leaving 3135 live born infants who never had a PCR-positive test and were classified as HEU. Trial participants provided written informed consent for storage and use of data and samples for future, related studies. Overall, the trial found no effect of vitamin A on child mortality (<xref rid="B1" ref-type="bibr">1</xref>, <xref rid="B4" ref-type="bibr">4</xref>) or on HIV transmission among HIV-exposed infants (<xref rid="B1" ref-type="bibr">1</xref>).</p><p>The ZVITAMBO trial offered a unique opportunity to study HEU infants for several key reasons: first, maternal and infant HIV status was well characterized throughout follow-up (see below); second, the HIV-unexposed comparison group was similar and contemporaneous; third, the majority of infants in each group had similar feeding patterns (mixed breast-feeding); and, fourth, all infants had access to a free “sick clinic,” allowing similar assessment of morbidity status between groups.</p></sec><sec id="S3"><title>Methods for Identifying HIV Infection</title><p>Studies investigating the outcomes of HEU infants need to ensure regular HIV testing of mothers and infants. Without repeat testing of mothers, those seroconverting during follow-up will be unidentified, meaning HIV-unexposed infant groups may be contaminated with HEU or HIV-infected infants; without repeat testing of infants, HEU infant groups may be contaminated with postnatally infected infants. In the ZVITAMBO trial, mothers were first tested for HIV at baseline; those testing HIV negative were retested at every subsequent blood draw to detect seroconversion. Infants born to mothers who remained HIV uninfected throughout follow-up were classified as HIV unexposed. Children born to HIV-positive mothers had samples stored at −70°C. At the end of the follow-up period, the last available sample from each child was tested for HIV; if this was negative, the child was classified as HEU. Various methods were used to ensure that the HEU group was not contaminated with postnatally infected infants, including censoring infants at the last negative HIV test if further testing was not conducted before the end of follow-up or infant death (as described below) (<xref rid="B2" ref-type="bibr">2</xref>, <xref rid="B5" ref-type="bibr">5</xref>).</p></sec><sec id="S4"><title>Morbidity and Mortality of HEU Infants</title><sec id="S4-1"><title>Morbidity</title><p>HIV-exposed uninfected infants in the ZVITAMBO trial had clear evidence of increased infectious morbidity compared to HIV-unexposed infants (<xref rid="B5" ref-type="bibr">5</xref>). HEU infants had 30% more sick clinic visits in the first year of life, peaking between 1 and 3 months of age, and 50% more hospitalizations within the first 28 days of life.</p><sec id="S4-1-1"><title>Sick Clinic Visits</title><p>The incidence of sick clinic visits among HEU infants was highest in the first 3 months of life, and remained significantly higher than for HIV-unexposed infants throughout infancy. The incidence rate ratios (IRR) for sick clinic visits were 1.2 (95% CI 1.1–1.4), 1.4 (1.3–1.5), 1.1 (1.1–1.2), and 1.1 (1.1–1.2) for 0–28, 29–91, 92–182, and 182–365 days, respectively. The most common illnesses among HEU infants were skin infections, lower respiratory tract infections, and oral thrush. Lower respiratory tract infections were particularly common in the first 3 months of life, with IRR of 1.6 (95% CI 1.1–2.3) and 1.5 (1.2–1.8) for 0–28 and 29–91 days, respectively (<xref rid="B5" ref-type="bibr">5</xref>).</p></sec><sec id="S4-1-2"><title>Hospitalization</title><p>All-cause hospitalization was significantly higher in the first 28 days of life (IRR 1.5, 95% CI 1.2–2.0) among HEU compared to HIV-unexposed infants, with a trend toward increased all-cause hospitalization through 6 months of age. Hospitalization for malnutrition or diarrhea was common overall, but was not increased in HEU compared to HIV-unexposed infants, which may be due to the similar breast-feeding rates between groups. Increased risk of hospitalization for lower respiratory tract infections was particularly high in the first 28 days of life (IRR 2.7, 95% CI 1.6–4.7) (<xref rid="B5" ref-type="bibr">5</xref>).</p></sec></sec><sec id="S4-2"><title>Mortality</title><p>HIV-exposed uninfected children had higher mortality than HIV-unexposed children through 2 years of age (<xref rid="B2" ref-type="bibr">2</xref>). The mortality difference between groups was twice as high during the first year (3.9-fold) compared to the second year of life (2.0-fold), highlighting infancy as a period of particularly high mortality, and suggesting an attenuation of mortality risk over time. The proportion of HEU infants who died by 30 days, 6 months, 1 and 2 years of age was 1.9% (95% CI 1.4–2.5), 6.0% (5.2–7.0), 7.4% (6.5–8.4) and 9.2% (8.1–10.5), respectively, compared to 0.7% (0.6–0.9), 1.6% (1.3–1.8), 1.9% (1.7–2.2) and 2.9% (2.5–3.5) of HIV-unexposed infants. Notably, the difference in mortality between groups was greater than the difference in morbidity; this may indicate greater severity of infections in HEU infants, as recently demonstrated in respiratory syncytial virus-associated lower respiratory tract infections in South Africa (<xref rid="B6" ref-type="bibr">6</xref>). The most common causes of death in HEU infants were acute respiratory infections (57.7%), diarrheal illness/dysentery (16.1%), malnutrition (13.3%), sepsis (6.0%), and meningitis (4.8%). Overall, the causes of death were similar between HIV-unexposed, HEU and HIV-infected infants.</p></sec><sec id="S4-3"><title>Sensitivity Analyses</title><p>Because of the possibility that the HEU infant group was contaminated with postnatally infected infants who died prior to testing HIV-positive, several sensitivity analyses were conducted. For morbidity, HEU infants were censored 42 days before their last HIV test (taking into account the window period for the test). The original analysis may in fact have underestimated morbidity among HEU infants, because the risk of hospitalization increased in sensitivity analyses, thereby adding confidence to the initial findings (<xref rid="B5" ref-type="bibr">5</xref>). For mortality, the sensitivity analyses included only those infants with at least one negative HIV test after 8 weeks of age; despite this, mortality remained 2.5-fold and 2.0-fold higher among HEU compared to HIV-unexposed infants by 12 and 24 months, respectively (<xref rid="B2" ref-type="bibr">2</xref>).</p></sec><sec id="S4-4"><title>Why Are HEU Infants at Risk of Infection and Death?</title><p>Here, we evaluate the potential underlying causes of morbidity and mortality in HEU infants, drawing on available evidence and plausible mechanisms from animal models and <italic>in vitro</italic> studies. In Figure <xref ref-type="fig" rid="F1">1</xref>, we propose a conceptual framework to explain infection susceptibility in HEU infants.</p><fig id="F1" position="float"><label>Figure 1</label><caption><p><bold>Conceptual framework for poor clinical outcomes of HEU infants</bold>. A combination of <italic>in utero</italic> and postnatal exposures may contribute to inflammation and immune activation in HEU infants. Immunodeficiency may be related directly to HIV exposure or may occur indirectly through reduced transplacental transfer of antibodies. Coinfections before and after birth (such as CMV and malaria) may also contribute to immune activation. Postnatally, exposure to HIV in breast milk may disrupt the intestinal barrier and lead to an enteropathy and microbial translocation. In non-breast-feeding infants, enteropathy may still be present secondary to abnormal assembly of the infant gut microbiota.</p></caption><graphic xlink:href="fimmu-07-00190-g001"></graphic></fig><p>A growing body of evidence indicates that HEU infants have immunological abnormalities. First, studies show low concentrations of maternally derived antibody at birth (<xref rid="B7" ref-type="bibr">7</xref>–<xref rid="B12" ref-type="bibr">12</xref>). As newborns rely heavily on passive immunity before maturation of their own adaptive responses, this paucity of antibody may leave HEU infants at particular risk of infection. Second, there are numerous T-cell abnormalities: low CD4 count (<xref rid="B13" ref-type="bibr">13</xref>), high frequency of “double-negative” (CD4<sup>–</sup>/CD8<sup>–</sup>) T-cells (<xref rid="B14" ref-type="bibr">14</xref>, <xref rid="B15" ref-type="bibr">15</xref>), and activated T-cell phenotypes (<xref rid="B13" ref-type="bibr">13</xref>, <xref rid="B14" ref-type="bibr">14</xref>, <xref rid="B16" ref-type="bibr">16</xref>–<xref rid="B19" ref-type="bibr">19</xref>) have all been well described. As T-cells are the primary target for HIV, it is perhaps unsurprising that they appear disproportionately affected in infants exposed to the virus. Third, HEU infants have elevated markers of immune activation and systemic inflammation (<xref rid="B13" ref-type="bibr">13</xref>, <xref rid="B14" ref-type="bibr">14</xref>, <xref rid="B16" ref-type="bibr">16</xref>–<xref rid="B24" ref-type="bibr">24</xref>).</p><p>Immune activation is an important cause of immune dysfunction in HIV-infected individuals, and its severity may be a better prognostic marker than HIV viral load (<xref rid="B25" ref-type="bibr">25</xref>). Animal models demonstrate the importance of chronic immune activation in growth failure and infection susceptibility. Transgenic mice that constitutively expressed CD70, leading to chronic T-cell stimulation, developed progressive naive T-cell depletion, weight loss, and premature death from <italic>Pneumocystis jirovecii</italic> pneumonia (<xref rid="B26" ref-type="bibr">26</xref>). Chronic immune activation in HEU infants may lead to infection susceptibility, and the resulting inflammation may further supress immune function. The causes of immune activation in HEU infants have not been well established; here, we speculate on plausible underlying causes (Figure <xref ref-type="fig" rid="F1">1</xref>).</p><sec id="S4-4-1"><title>Direct Exposure to the HIV Virus <italic>In Utero</italic> and the Influence of Maternal HIV Disease Severity</title><p>Fetal immune activation may result from direct exposure to HIV <italic>in utero</italic>; notably, HEU infants have evidence of HIV-specific T-cell responses (<xref rid="B27" ref-type="bibr">27</xref>, <xref rid="B28" ref-type="bibr">28</xref>), suggestive of <italic>in utero</italic> sensitization. These responses are greater in infants born to mothers with high compared to low viral loads (<xref rid="B29" ref-type="bibr">29</xref>). Direct exposure to HIV or its components at a critical time of T-cell development <italic>in utero</italic> may contribute to the T-cell abnormalities described. HIV genomic material has been found in macrophages of the chorionic villus and in trophoblasts (<xref rid="B30" ref-type="bibr">30</xref>, <xref rid="B31" ref-type="bibr">31</xref>). Components of HIV such as Nef have complex effects on the immune system, including CD4 depletion, activation, and apoptosis (<xref rid="B32" ref-type="bibr">32</xref>, <xref rid="B33" ref-type="bibr">33</xref>). Furthermore, in a rodent model, Nef breaches placental barrier function and may enable HIV, other viral proteins and microbial products (see below) to cross the placenta (<xref rid="B34" ref-type="bibr">34</xref>), potentially exacerbating effects on the fetal immune system.</p><p>HIV-exposed uninfected infant morbidity and mortality outcomes in the ZVITAMBO trial were strongly influenced by maternal factors (Table <xref ref-type="table" rid="T1">1</xref>) (<xref rid="B2" ref-type="bibr">2</xref>, <xref rid="B5" ref-type="bibr">5</xref>). Infants born to mothers with more severe HIV disease (as assessed by maternal CD4 count) had higher rates of morbidity and mortality than those born to mothers with less severe HIV disease. Compared to HEU infants born to mothers with CD4 counts >400 cells/μL, those born to mothers with CD4 counts <200 cells/μL had 2.6-fold increased mortality by 2 years of age (95% CI 1.8–3.8). Increased morbidity risk remained until maternal CD4 counts were above 800 cells/μL. Oral candidiasis, an important indicator of immune function in the context of HIV, was particularly associated with maternal disease severity; compared to HIV-unexposed infants, HEU infants born to mothers with CD4 counts <200 cells/μL had an incidence rate ratio of oral thrush of 3.91 (95% CI 2.29–6.66), whereas those born to mothers with CD4 counts >800 cells/μL had an IRR of 1.91 (95% CI 1.02–3.58). The difference between these two HEU groups was statistically significant (<italic>P</italic> < 0.05).</p><table-wrap id="T1" position="float"><label>Table 1</label><caption><p><bold>Associations between maternal factors and HEU morbidity and mortality in the ZVITAMBO cohort</bold>.</p></caption><table frame="hsides" rules="groups"><thead><tr><th valign="middle" align="left" rowspan="1" colspan="1">Maternal factor</th><th valign="middle" align="left" rowspan="1" colspan="1">Comparison group</th><th valign="middle" align="left" rowspan="1" colspan="1">Reference group</th><th valign="top" align="left" rowspan="1" colspan="1">Outcome (95% confidence interval)</th></tr></thead><tbody><tr><td align="left" valign="top" colspan="4" rowspan="1"><bold>Maternal disease severity and 2-year mortality of HEU infants (<xref rid="B2" ref-type="bibr">2</xref>)</bold></td></tr><tr><td align="left" valign="top" rowspan="2" colspan="1">Maternal CD4 count (cells/μL)</td><td align="left" valign="middle" rowspan="1" colspan="1"><200</td><td align="left" valign="middle" rowspan="1" colspan="1">≥400</td><td align="left" valign="middle" rowspan="1" colspan="1">HR 2.62 (1.8–3.8)<xref ref-type="table-fn" rid="tfn1"><sup>a</sup></xref></td></tr><tr><td align="left" valign="middle" rowspan="1" colspan="1">200–400</td><td align="left" valign="middle" rowspan="1" colspan="1">≥400</td><td align="left" valign="middle" rowspan="1" colspan="1">HR 1.26 (0.9–1.5)</td></tr><tr><td align="left" valign="middle" rowspan="1" colspan="1">Hemoglobin (g/L)</td><td align="left" valign="middle" rowspan="1" colspan="1"><70</td><td align="left" valign="middle" rowspan="1" colspan="1">≥70</td><td align="left" valign="middle" rowspan="1" colspan="1">HR 3.79 (2.06–6.97)<xref ref-type="table-fn" rid="tfn1"><sup>a</sup></xref></td></tr><tr><td align="left" valign="middle" rowspan="1" colspan="1">Maternal survival (at 12 months after delivery)</td><td align="left" valign="middle" rowspan="1" colspan="1">Died</td><td align="left" valign="middle" rowspan="1" colspan="1">Survived</td><td align="left" valign="middle" rowspan="1" colspan="1">HR 2.68 (1.86–3.87)<xref ref-type="table-fn" rid="tfn1"><sup>a</sup></xref></td></tr><tr><td align="left" valign="top" colspan="4" rowspan="1"><bold>Maternal social status and 2-year mortality of HEU infants (<xref rid="B2" ref-type="bibr">2</xref>)</bold></td></tr><tr><td align="left" valign="top" rowspan="2" colspan="1">Marital status</td><td align="left" valign="middle" rowspan="1" colspan="1">Single</td><td align="left" valign="middle" rowspan="1" colspan="1">Married/cohabiting</td><td align="left" valign="middle" rowspan="1" colspan="1">HR 2.55 (1.29–5.06)<xref ref-type="table-fn" rid="tfn1"><sup>a</sup></xref></td></tr><tr><td align="left" valign="middle" rowspan="1" colspan="1">Widowed</td><td align="left" valign="middle" rowspan="1" colspan="1">Married/cohabiting</td><td align="left" valign="middle" rowspan="1" colspan="1">HR 1.97 (1.25–3.12)<xref ref-type="table-fn" rid="tfn1"><sup>a</sup></xref></td></tr><tr><td align="left" valign="top" rowspan="2" colspan="1">Household income (US $)</td><td align="left" valign="middle" rowspan="1" colspan="1"><1.20</td><td align="left" valign="middle" rowspan="1" colspan="1">≥2.40</td><td align="left" valign="middle" rowspan="1" colspan="1">HR 1.87 (1.28–2.73)<xref ref-type="table-fn" rid="tfn1"><sup>a</sup></xref></td></tr><tr><td align="left" valign="middle" rowspan="1" colspan="1">1.20–2.40</td><td align="left" valign="middle" rowspan="1" colspan="1">≥2.40</td><td align="left" valign="middle" rowspan="1" colspan="1">HR 1.30 (0.91–1.84)</td></tr><tr><td align="left" valign="top" colspan="4" rowspan="1"><bold>Maternal disease severity and 2-year sick clinic visit in HEU infants, compared to HUU infants (<xref rid="B5" ref-type="bibr">5</xref>)</bold></td></tr><tr><td align="left" valign="top" rowspan="4" colspan="1">Maternal CD4 count (cells/μL)</td><td align="left" valign="middle" rowspan="1" colspan="1"><200</td><td align="left" valign="middle" rowspan="1" colspan="1">HUU infants</td><td align="left" valign="middle" rowspan="1" colspan="1">IRR 1.33 (1.17–1.50)<sup>b,c</sup></td></tr><tr><td align="left" valign="middle" rowspan="1" colspan="1">200–499</td><td align="left" valign="middle" rowspan="1" colspan="1">HUU infants</td><td align="left" valign="middle" rowspan="1" colspan="1">IRR 1.24 (1.17–1.32)<sup>b,c</sup></td></tr><tr><td align="left" valign="middle" rowspan="1" colspan="1">500–799</td><td align="left" valign="middle" rowspan="1" colspan="1">HUU infants</td><td align="left" valign="middle" rowspan="1" colspan="1">IRR 1.11 (1.08–1.27)<xref ref-type="table-fn" rid="tfn2"><sup>b</sup></xref></td></tr><tr><td align="left" valign="middle" rowspan="1" colspan="1">≥800</td><td align="left" valign="middle" rowspan="1" colspan="1">HUU infants</td><td align="left" valign="middle" rowspan="1" colspan="1">IRR 1.02 (0.89–1.16)</td></tr></tbody></table><table-wrap-foot><p><italic>Based on data presented in Marinda et al. (<xref rid="B2" ref-type="bibr">2</xref>) and Koyanagi et al. (<xref rid="B5" ref-type="bibr">5</xref>)</italic>.</p><p><italic>HR, hazard ratio; IRR, incidence rate ratio; HEU, HIV-exposed uninfected; HUU, HIV-unexposed uninfected</italic>.</p><p><italic>Hazard ratios (HR) calculated using Cox proportional hazard models</italic>.</p><p><italic>Incident rate ratios (IRR) calculated using negative binomial with the HUU infants as the reference group</italic>.</p><fn id="tfn1"><p><italic><sup>a</sup>Significant difference between comparison groups (HEU vs. HEU)</italic>.</p></fn><fn id="tfn2"><p><italic><sup>b</sup>Significant difference between comparison groups (HEU vs. HUU)</italic>.</p></fn><fn id="tfn3"><p><italic><sup>c</sup>Significant difference between that group and HEU infants born to mothers with CD4 count ≥800 cells/μL (HEU vs. HEU)</italic>.</p></fn></table-wrap-foot></table-wrap><p>The relative influences of maternal viremia (as assessed by viral load) and maternal immune suppression (as assessed by CD4 count) on HEU outcomes should be determined in future studies; this may help to establish the drivers of infection susceptibility, particularly in the current ART era.</p></sec><sec id="S4-4-2"><title>Increased Exposure to Coinfections</title><p>Coinfections such as cytomegalovirus (CMV) are more prevalent in HIV-infected compared to HIV-uninfected pregnant women (<xref rid="B35" ref-type="bibr">35</xref>, <xref rid="B36" ref-type="bibr">36</xref>), and could contribute to immune activation in their offspring both before (<xref rid="B37" ref-type="bibr">37</xref>) and after (<xref rid="B38" ref-type="bibr">38</xref>–<xref rid="B40" ref-type="bibr">40</xref>) birth. Infants born to HIV-infected mothers have a very high frequency of congenital CMV infection (11–29%) (<xref rid="B36" ref-type="bibr">36</xref>, <xref rid="B41" ref-type="bibr">41</xref>, <xref rid="B42" ref-type="bibr">42</xref>), and postnatal infection is almost ubiquitous during infancy in sub-Saharan Africa. There is an overlap between the effects of CMV infection and HIV exposure in infancy, including growth failure (<xref rid="B43" ref-type="bibr">43</xref>) and mortality (<xref rid="B43" ref-type="bibr">43</xref>, <xref rid="B44" ref-type="bibr">44</xref>). For example, HIV-exposed infants with pneumonia in South Africa had 4.3-fold higher frequency of CMV viremia compared to asymptomatic HIV-exposed infants after adjusting for infant HIV infection (95% CI 2.6–7.0) (<xref rid="B45" ref-type="bibr">45</xref>).</p><p>There are plausible reasons why CMV acquisition may lead to immune dysfunction. First, in order to evade the immune system and promote latency, CMV has evolved multiple immunomodulatory properties to downregulate the human immune system (<xref rid="B46" ref-type="bibr">46</xref>, <xref rid="B47" ref-type="bibr">47</xref>). Therefore, CMV infection in early life could be associated with increased susceptibility to other childhood infections. Second, evidence from humans and from murine models suggests that CMV causes immune activation. Studies report associations between primary and latent CMV infection and immune activation in adults; (<xref rid="B48" ref-type="bibr">48</xref>) a bias toward pro-inflammatory and Th17-polarized cytokines in the placenta and amniotic fluid during maternal CMV infection; (<xref rid="B49" ref-type="bibr">49</xref>) a lower regulatory T-cell (Treg)/Th17 ratio in CMV-infected children; and an impact of CMV coinfection on immune activation in HIV-infected individuals (<xref rid="B50" ref-type="bibr">50</xref>). Th17-polarized cytokines are associated with increased inflammation in response to viral infections, and it has been suggested that this may increase mortality (<xref rid="B51" ref-type="bibr">51</xref>). Furthermore, inflammation associated with CMV carrier status may affect responses to vaccinations (<xref rid="B52" ref-type="bibr">52</xref>). Third, CMV is acquired either <italic>in utero</italic> or early in infancy in sub-Saharan Africa and typically induces large magnitude immune responses. Infants with congenital CMV infection have evidence of considerable expansions in γδ T-cells (<xref rid="B53" ref-type="bibr">53</xref>), NK cells (<xref rid="B54" ref-type="bibr">54</xref>), and conventional αβ T-cells with a highly differentiated phenotype (<xref rid="B55" ref-type="bibr">55</xref>). Whether primary CMV infection at a critical time of immune development causes immunomodulation in HEU infants, and whether this alters infection susceptibility or mortality, has not been well addressed to date. We hypothesize that primary CMV infection in HEU infants results in inflammation and distortion of the immune system, leading to increased infection susceptibility, but further studies are required.</p><p>Pharmacological interventions to prevent CMV transmission to HEU infants have been considered a potentially important intervention but have so far reported unfavorable results. A Kenyan trial, in which women were randomized to 12 months of valaciclovir or placebo from 34 gestational weeks, did not reduce CMV transmission to HEU infants (<xref rid="B56" ref-type="bibr">56</xref>), and maternal nelfinavir for at least the last 4 weeks of pregnancy did not reduce congenital CMV in HEU infants in the USA (<xref rid="B57" ref-type="bibr">57</xref>). Formula feeding of HEU infants was associated with a lower incidence of CMV infection by 1 year of age in Kenya (<xref rid="B58" ref-type="bibr">58</xref>), highlighting breast-feeding as a major route of CMV transmission. However, the risks of formula feeding make it an impractical intervention to reduce CMV in developing countries.</p></sec><sec id="S4-4-3"><title>Maternal Microbial Translocation</title><p>Microbial translocation causes immune activation in HIV infection (<xref rid="B59" ref-type="bibr">59</xref>), and is a key distinction between HIV infection in humans and non-pathogenic simian immunodeficiency virus (SIV) infection in sooty mangabeys (<xref rid="B60" ref-type="bibr">60</xref>). Lipopolysaccharide (LPS) and other bacterial components from intestinal microbes are able to cross a leaky gut barrier as a direct result of HIV exposure, activating immune cells in the systemic circulation; increased LPS, as a marker of translocation, has been directly associated with innate and adaptive immune activation in HIV infection (<xref rid="B59" ref-type="bibr">59</xref>). HIV-infected pregnant women have higher levels of circulating soluble CD14 (sCD14) and LPS-binding protein than HIV-uninfected women, suggesting that microbial translocation occurs throughout pregnancy; first trimester sCD14 levels were independently associated with preterm birth (<xref rid="B61" ref-type="bibr">61</xref>) in multivariate analyses. In an animal model (<xref rid="B62" ref-type="bibr">62</xref>), subclinical infection with murine gammaherpesvirus 68 sensitizes pregnant mice to a greater cytokine response to LPS, suggesting that viral infections have potential to amplify the impact of LPS exposure during pregnancy. Maternal microbial translocation in HIV-affected pregnancies may plausibly contribute to immune activation in HEU infants: LPS can cross the placental barrier in mice (<xref rid="B63" ref-type="bibr">63</xref>), meaning that translocated maternal LPS could potentially activate fetal immune cells, particularly in the context of Nef-mediated placental barrier dysfunction (<xref rid="B34" ref-type="bibr">34</xref>). Whether LPS or other microbial products cross the placental barrier in HEU infants and contribute to immune activation has yet to be confirmed.</p><p>Notably, microbial translocation, and its associated immune activation, often persists in HIV-infected individuals despite ART (<xref rid="B64" ref-type="bibr">64</xref>–<xref rid="B67" ref-type="bibr">67</xref>). If this mechanism is related to immune activation in HEU infants, HEU infants may continue to be at risk of infection susceptibility despite maternal viral suppression throughout pregnancy.</p></sec><sec id="S4-4-4"><title>Postnatal Exposure to HIV</title><p>Postnatal contact between HIV and the gut epithelium during breast-feeding may damage the mucosal barrier, enabling infant microbial translocation (<xref rid="B68" ref-type="bibr">68</xref>), although we recently showed that plasma levels of intestinal fatty acid binding protein, one marker of small intestinal villous damage, were similar between HIV-exposed and HIV-unexposed infants in the ZVITAMBO trial, and between HIV-exposed infants who did and did not acquire postnatal HIV infection through breast milk.<xref ref-type="fn" rid="fn1"><sup>1</sup></xref> In South Africa, greater exclusivity of breast-feeding was associated with less gut inflammation; (<xref rid="B69" ref-type="bibr">69</xref>) among infants recruited to the BAN trial, plasma LPS, a marker of microbial translocation, was higher after compared to before weaning (<xref rid="B70" ref-type="bibr">70</xref>).</p></sec><sec id="S4-4-5"><title>Socioeconomic Factors</title><p>Social and economic factors are also likely to be important in infection susceptibility among HEU infants, including parental health and parental care-taking capacities; socioeconomic status; and pathogen exposure in the home environment, although a detailed discussion of these remains outside the scope of this Review. In the ZVITAMBO trial, morbidity and mortality outcomes were associated with family social factors, including parental relationship stability and household income (Table <xref ref-type="table" rid="T1">1</xref>).</p></sec><sec id="S4-4-6"><title>Postnatal Vitamin A</title><p>Vitamin A supplementation had no effect on HIV transmission in the ZVITAMBO trial, whether it was given to mothers, infants, or both. Furthermore, maternal and/or infant vitamin A had no overall effect on child mortality. However, in subgroup analyses, it was found that vitamin A had heterogeneous effects. Maternal or neonatal vitamin A had no effect on infants who acquired HIV <italic>in utero</italic>, but neonatal vitamin A did reduce mortality in those infected around the time of birth. In infants who were uninfected at 6 weeks of age (a group that included HEU and infants who later became postnatally infected), vitamin A was associated with higher 24-month mortality compared to placebo (Table <xref ref-type="table" rid="T2">2</xref>). On sensitivity analysis, it appeared that the majority of those who died were HIV-infected before death. It is plausible therefore that vitamin A prior to HIV infection hastened disease progression when infants were subsequently infected through breast milk transmission of HIV (<xref rid="B1" ref-type="bibr">1</xref>).</p><table-wrap id="T2" position="float"><label>Table 2</label><caption><p><bold>Associations between maternal and infant vitamin A exposure and 24-month mortality in HIV-exposed infants remaining HIV PCR negative at 6 weeks (<italic>n</italic> = 2876) in ZVITAMBO</bold>.</p></caption><table frame="border" rules="all"><thead><tr><th valign="middle" align="left" rowspan="2" colspan="2"></th><th valign="middle" align="center" colspan="2" rowspan="1">Infant randomization</th></tr><tr><th valign="middle" align="center" rowspan="1" colspan="1">Vitamin A</th><th valign="middle" align="center" rowspan="1" colspan="1">Placebo</th></tr></thead><tbody><tr><td align="left" valign="middle" rowspan="2" colspan="1">Mother randomization</td><td align="center" valign="middle" rowspan="1" colspan="1">Vitamin A</td><td align="center" valign="middle" rowspan="1" colspan="1">2.05 (1.14–3.67)<break></break><italic>P</italic> = 0.02</td><td align="center" valign="middle" rowspan="1" colspan="1">1.82 (0.99–3.31)<break></break><italic>P</italic> = 0.05</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Placebo</td><td align="center" valign="middle" rowspan="1" colspan="1">1.89 (1.05–3.40)<break></break><italic>P</italic> = 0.03</td><td align="center" valign="middle" rowspan="1" colspan="1">1.00</td></tr><tr><td valign="middle" align="left" rowspan="2" colspan="2"></td><td valign="middle" align="center" colspan="2" rowspan="1"><bold>Infant randomization</bold></td></tr><tr><td valign="middle" align="center" rowspan="1" colspan="1"><bold>Vitamin A</bold></td><td valign="middle" align="center" rowspan="1" colspan="1"><bold>Placebo</bold></td></tr><tr><td align="left" valign="middle" rowspan="2" colspan="1">Mother randomization</td><td align="center" valign="middle" rowspan="1" colspan="1">Vitamin A</td><td align="center" valign="middle" rowspan="2" colspan="1">1.41 (0.97–2.05)<break></break><italic>P</italic> = 0.07</td><td align="center" valign="bottom" rowspan="2" colspan="1">1.00</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Placebo</td></tr><tr><td valign="middle" align="left" rowspan="2" colspan="2"></td><td valign="middle" align="center" colspan="2" rowspan="1"><bold>Infant randomization</bold></td></tr><tr><td valign="middle" align="center" rowspan="1" colspan="1"><bold>Vitamin A</bold></td><td valign="middle" align="center" rowspan="1" colspan="1"><bold>Placebso</bold></td></tr><tr><td align="left" valign="middle" rowspan="2" colspan="1">Mother randomization</td><td align="center" valign="middle" rowspan="1" colspan="1">Vitamin A</td><td align="center" valign="middle" colspan="2" rowspan="1">1.33 (0.92–1.92)<break></break><italic>P</italic> = 0.14</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Placebo</td><td align="center" valign="middle" colspan="2" rowspan="1">1.00</td></tr></tbody></table><table-wrap-foot><p><italic>Based on data presented in Humphrey et al. (<xref rid="B1" ref-type="bibr">1</xref>)</italic>.</p><p><italic>Adjusted hazard ratios (95% confidence intervals) calculated by Cox proportional hazard models with the following covariates – maternal mid-upper arm circumference, maternal death, maternal CD4 count, maternal hemoglobin, and maternal marital status</italic>.</p></table-wrap-foot></table-wrap></sec><sec id="S4-4-7"><title>Future Studies</title><p>Future studies should focus on better characterizing the nature and drivers of immunodeficiency in HEU infants and the relationship between immune ontogeny and clinical outcomes in this group. Whether immune dysfunction among HEU infants can be prevented or ameliorated with use of maternal ART or with other interventions remains unclear. However, immune activation in HIV-infected adults persists despite ART (<xref rid="B64" ref-type="bibr">64</xref>–<xref rid="B67" ref-type="bibr">67</xref>), and there is some evidence that ART exposure may actually worsen immune activation in HEU infants: in South Africa, T-cell activation at birth was unexpectedly higher among HEU infants exposed to antenatal and postnatal nevirapine compared to those unexposed to ART, perhaps due to an activating effect of nevirapine either on HIV-infected or bystander cells (<xref rid="B71" ref-type="bibr">71</xref>).</p><p>Studies of prospective cohorts are needed to evaluate the relationship between markers of immune dysfunction, such as immune activation, and infection susceptibility in HEU infants. Furthermore, studies comparing infection susceptibility and mortality outcomes in HEU and HIV-unexposed infants in context of suppressive maternal ART are required, in order to determine if the differences seen in the ZVITAMBO trial remain modern era. Although studies have been undertaken in the era of short periods of ART for PMTCT, there have so far been no studies undertaken in the setting of fully suppressive maternal ART throughout pregnancy, which is now the standard of care.</p></sec></sec></sec><sec id="S5"><title>Growth of HEU Infants in the ZVITAMBO Trial</title><p>Growth failure is common in sub-Saharan Africa and is associated with childhood mortality (<xref rid="B72" ref-type="bibr">72</xref>). Poor growth has been well described in HIV-infected infants and children, but the effect of maternal HIV on the growth of HEU infants is less clear. Although the majority of cohorts across sub-Saharan Africa have shown trends toward poorer growth among HEU infants, many results do not reach statistical significance, potentially due to small numbers of children (<xref rid="B3" ref-type="bibr">3</xref>). We recently showed in the ZVITAMBO trial that HEU infants were more likely to be born premature and small-for-gestational age (SGA) than HIV-unexposed infants. HEU infants had evidence of growth failure at birth (<xref rid="B2" ref-type="bibr">2</xref>), and mean length-for-age and weight-for-age <italic>Z</italic>-scores remained lower among HEU compared to HIV-unexposed infants throughout 2 years of follow-up. The differences in growth between HEU and HIV-unexposed infants peaked at 6 weeks of age, when HEU infants were 25% more likely to be stunted, 55% more likely to be underweight, and 58% more likely to be wasted; these differences in stunting, underweight, and wasting persisted until 1 year of age.<xref ref-type="fn" rid="fn2"><sup>2</sup></xref> Compared to HIV-unexposed infants, HEU infants also had poorer head growth in the first year of life,<xref ref-type="fn" rid="fn3"><sup>3</sup></xref> although the influence of such a finding on neurodevelopmental outcomes remains uncertain.</p><p>To ensure robust growth outcome results, HEU infants were censored from analyses at their last negative HIV test.</p><sec id="S5-1"><title>Why Are HEU Infants at Risk of Growth Failure?</title><p>A number of mechanisms may underlie the association between maternal HIV infection and poor infant growth. Maternal immune activation may lead to pro-inflammatory vascular damage resulting in reduced placental blood supply (<xref rid="B73" ref-type="bibr">73</xref>) or increased placental inflammation and chorio-amnionitis; (<xref rid="B74" ref-type="bibr">74</xref>) each may lead to poor fetal growth. The high burden of coinfections in HIV-infected women may also influence growth of their offspring; for example, coinfection with HIV and malaria causes SGA (<xref rid="B75" ref-type="bibr">75</xref>, <xref rid="B76" ref-type="bibr">76</xref>), which may be due to modifications in the placental cytokine environment (<xref rid="B77" ref-type="bibr">77</xref>). Congenital CMV infection causes poor fetal growth (<xref rid="B43" ref-type="bibr">43</xref>), and this effect may be more pronounced in infants of HIV-infected mothers.</p><sec id="S5-1-1"><title>Inflammation</title><p>Inflammation may also be a key driver of growth failure. In a recent sub-study of HIV-unexposed infants from the ZVITAMBO trial, we found linear growth failure was related both to acute illness and to chronic inflammation, with both clinical and subclinical disease associated with suppression of the growth hormone axis (<xref rid="B78" ref-type="bibr">78</xref>, <xref rid="B79" ref-type="bibr">79</xref>). At 6 weeks of age, HEU infants in ZVITAMBO had higher C-reactive protein (CRP) than HIV-unexposed infants<sup>1</sup>; it is therefore plausible that the growth failure seen in HEU infants is related to higher levels of systemic inflammation leading to reduced insulin-like growth factor 1 (<xref rid="B79" ref-type="bibr">79</xref>); however, further data are needed to test this hypothesis.</p></sec><sec id="S5-1-2"><title>Microbiota and Enteropathy</title><p>The intestinal microbiota is emerging as a key contributor to healthy postnatal growth, and a series of recent studies (<xref rid="B80" ref-type="bibr">80</xref>–<xref rid="B82" ref-type="bibr">82</xref>) has established that maturational defects in the composition and function of the microbiota underlie malnutrition in developing countries. An inflammatory pathology of the small intestine, termed environmental enteric dysfunction, is a potentially important cause of stunting among young children in developing countries (<xref rid="B83" ref-type="bibr">83</xref>, <xref rid="B84" ref-type="bibr">84</xref>) and may be related to the configuration and function of the microbiota (<xref rid="B85" ref-type="bibr">85</xref>). The early life infant microbiota is founded following vertical transmission from the mother (<xref rid="B86" ref-type="bibr">86</xref>), so a distorted maternal microbiota in the context of HIV infection (<xref rid="B87" ref-type="bibr">87</xref>, <xref rid="B88" ref-type="bibr">88</xref>) may lead to abnormal assembly of the microbiota in HEU infants, which could plausibly drive growth failure through subclinical intestinal damage and inflammation. However, to our knowledge, this has not been investigated to date. Greater intestinal inflammation and increased microbial translocation could drive systemic inflammation and immune activation in HEU infants, and could therefore contribute to both growth restriction and infection susceptibility. Notably, there are higher rates of stunting in HEU infants affected by diarrhea compared to those without diarrhea (<xref rid="B89" ref-type="bibr">89</xref>). Differences in microbiota composition and small intestinal pathology between HEU and HIV-unexposed infants warrant further exploration, as these processes are potentially amenable to gut-focused therapy.</p></sec><sec id="S5-1-3"><title>Intrauterine Growth Restriction and Preterm Birth</title><p>It has been estimated that around 20% of stunting has fetal origins (<xref rid="B90" ref-type="bibr">90</xref>). In HEU infants born at term in the ZVITAMBO trial, SGA and length-for-age <italic>Z</italic>-score at birth were closely associated with stunting, highlighting intrauterine growth and development as a key contributor to future growth potential of HEU infants. Conversely, preterm birth without associated SGA was not associated with poorer growth trends across the first 12 months of life<sup>2</sup>.</p></sec><sec id="S5-1-4"><title>Maternal Disease Severity</title><p>In contrast to morbidity and mortality, growth among HEU infants in ZVITAMBO was not associated with maternal disease severity (as determined by CD4 count at birth). This is also in contrast to studies from other countries that showed poorer fetal (<xref rid="B91" ref-type="bibr">91</xref>) and postnatal (<xref rid="B92" ref-type="bibr">92</xref>, <xref rid="B93" ref-type="bibr">93</xref>) growth in HEU infants born to mothers with greater HIV disease severity. A recent study from rural Uganda highlights the importance of maternal nutritional status and HEU infant growth; HIV mothers with poor weight gain throughout pregnancy were more likely to have preterm and/or low-birth-weight HEU infants.</p></sec><sec id="S5-1-5"><title>Antiretroviral Therapy</title><p>As infant growth was not associated with maternal disease severity in ZVITAMBO, virological suppression and immune reconstitution on ART may not necessarily improve growth outcomes. A Ugandan study undertaken in the context of maternal ART demonstrated a non-significant trend toward higher rates of stunting among HEU compared to HIV-unexposed infants [12-month adjusted odds ratio (OR) 1.55, 95% CI 0.92–2.61] (<xref rid="B94" ref-type="bibr">94</xref>), but this result may have been limited by a relatively small number of HEU infants included in the study. Differences in ponderal growth have not been found in most studies from the ART era (<xref rid="B15" ref-type="bibr">15</xref>, <xref rid="B94" ref-type="bibr">94</xref>–<xref rid="B98" ref-type="bibr">98</xref>), although one Ugandan study reported an adjusted OR for wasting of 3.29 at median 5.2 months of age (<italic>P</italic> = 0.02) among HEU compared to HIV-unexposed infants (<xref rid="B99" ref-type="bibr">99</xref>). As wasting is often associated with acute illness, it is plausible that ART-related improvements in HEU infant immune function may reduce infection susceptibility and improve weight gain.</p><p>However, exposure to ART itself throughout fetal development, and choice of maternal ART regimen, may influence differences in birth outcomes and growth. It is becoming clear that maternal ART is associated with an elevated risk of adverse birth outcomes (<xref rid="B100" ref-type="bibr">100</xref>). In the Promoting Maternal–Infant Survival Everywhere (PROMISE) trial (<xref rid="B101" ref-type="bibr">101</xref>), women were randomized to lopinavir/ritonavir-based ART or zidovudine alone with intrapartum single-dose nevirapine; although mother-to-child tranmission was significantly lower in the combination ART arm, preterm delivery was significantly higher (20.5 vs. 13.1%). In some (<xref rid="B102" ref-type="bibr">102</xref>) studies, but not others (<xref rid="B103" ref-type="bibr">103</xref>), protease inhibitor-based ART has been particularly associated with risk of preterm birth (<xref rid="B104" ref-type="bibr">104</xref>). In most of sub-Saharan Africa, efavrienz-based ART is the standard regimen used in pregnancy; however, there is still evidence of increased preterm delivery and SGA (<xref rid="B105" ref-type="bibr">105</xref>, <xref rid="B106" ref-type="bibr">106</xref>) following exposure to non-nucleoside reverse transcriptase inhibitor (NNRTI)-based regimens. Growth deficits associated with ART exposure that are evident at birth may persist and contribute to postnatal growth failure. For example, in Botswana, birth LAZ, WAZ, and WLZ were each significantly lower among infants exposed to triple ART compared to zidovudine monotherapy; LAZ remained significantly lower through 6 months of follow-up (<xref rid="B107" ref-type="bibr">107</xref>).</p></sec><sec id="S5-1-6"><title>Socioeconomic Factors</title><p>In the ZVITAMBO trial, wasting and underweight were more frequent in HEU infants born to mothers with primary compared to A level education. Interestingly, this educational difference was apparent despite very high levels of literacy across the study population.</p><p>Taken together, there are several plausible mechanisms that could lead to growth failure in HEU infants (Figure <xref ref-type="fig" rid="F1">1</xref>), although further clinical and laboratory studies are required to dissect these mechanistic pathways further. Notably, data from the ZVITAMBO trial are unable to determine the causal association between morbidity and growth failure; poor growth may result from a higher incidence of infections, or may be itself be a cause of infection susceptibility.</p></sec></sec></sec><sec id="S6"><title>Feeding HEU Infants</title><p>Targeting HIV-infected mothers and their exposed children with appropriate clinical and nutritional interventions is critical to improve survival. Until the availability of highly effective ART interventions for HIV-positive mothers and their infants, breast-feeding caused more than 200,000 new cases of pediatric HIV globally each year (<xref rid="B108" ref-type="bibr">108</xref>), but also prevented millions of infant deaths [one Ugandan trial reported that HEU infant mortality was over sixfold lower in infants who breast-fed for longer than 6 months compared to those who breast-fed for a shorter duration (<xref rid="B109" ref-type="bibr">109</xref>)]. Infant feeding therefore became one of the most profound dilemmas of the HIV epidemic.</p><p>The ZVITAMBO trial provided strong evidence for the association between exclusive breast-feeding (EBF) and reduced risk of postnatal HIV transmission (<xref rid="B110" ref-type="bibr">110</xref>). Among HIV-positive mothers, early EBF (feeding only breast milk) was associated with a 75% reduction in breast-feeding-associated HIV transmission by 6 months of age compared with early mixed breast-feeding (feeding both breast milk and non-breast milk liquid or solid foods). Compared to early EBF, early mixed breast-feeding was associated with 4.03-fold (95% CI 0.98–16.61), 3.79-fold (1.40–10.29), and 2.60-fold (1.21–5.55) greater risk of postnatal HIV transmission at 6, 12, and 18 months, respectively (<xref rid="B110" ref-type="bibr">110</xref>). This finding was due to nesting a “natural experiment” within the ZVITAMBO trial: 8 months after the trial was launched, WHO released policy that HIV testing and counseling should be available to all antenatal women, allowing mothers to make informed decisions about infant feeding (<xref rid="B111" ref-type="bibr">111</xref>). Importantly, the policy recommended early EBF and continued breast-feeding for women of unknown HIV status (the majority of women enrolled into the trial chose against learning their HIV status). In response, ZVITAMBO introduced an infant feeding intervention to support known HIV-positive women to make empowered choices about infant feeding, and to promote “safer breast-feeding” among HIV-negative mothers and those unwilling to learn their HIV status (early EBF; safe sex to avoid new HIV infections; prompt treatment of, and optimal techniques to reduce, breast problems) (<xref rid="B112" ref-type="bibr">112</xref>). Contact with this intervention was the strongest predictor of EBF in ZVITAMBO: EBF rates increased and postnatal HIV transmission rates declined with each additional exposure to the intervention (<xref rid="B112" ref-type="bibr">112</xref>).</p><sec id="S6-1"><title>Why Is Exclusive Breast-feeding Associated with Better HIV-exposed Infant Outcomes?</title><p>The underlying reasons for the protective effect of EBF on PMTCT remain uncertain (<xref rid="B113" ref-type="bibr">113</xref>). We hypothesize that early introduction of non-milk fluids and solid food, as is the cultural norm in Zimbabwe (<xref rid="B112" ref-type="bibr">112</xref>), increases intestinal inflammation due to modulation of the microbiota (<xref rid="B114" ref-type="bibr">114</xref>) or introduction of pathogenic bacteria (<xref rid="B115" ref-type="bibr">115</xref>). Intestinal inflammation may impair gut integrity and increase the pool of activated intestinal CD4 cells that are targeted by the virus. In the BAN trial, infants had higher markers of microbial translocation (LPS) after weaning than before, and pre-transmission LPS levels were a predictor of subsequent infection (<xref rid="B70" ref-type="bibr">70</xref>). It has alternatively been proposed that the association between EBF and reduced breast milk transmission is due to reverse causality – that women in better health, who are less likely to transmit HIV, are also more likely to exclusively breast-feed.</p></sec><sec id="S6-2"><title>Breast-feeding Interventions</title><p>Although continued breast-feeding after 6 months is likely to provide the greatest chance of survival for the majority of infants living in developing countries, this policy has proved difficult to implement. However, recent experience in Zimbabwe indicates that interventions targeting specific contextual barriers may be successful in increasing rates of EBF to 6 months (<xref rid="B116" ref-type="bibr">116</xref>–<xref rid="B118" ref-type="bibr">118</xref>). HIV-exposed infants may benefit from targeted EBF promotion; contact with healthcare professionals at birth or during early infant diagnosis at 6 weeks of age could be an opportunity to empower HIV-infected mothers to exclusively breast-feed. As contact with a counseling program was the strongest predictor of EBF in the ZVITAMBO trial (<xref rid="B112" ref-type="bibr">112</xref>), such programs may be paramount to empower women and improve the health of HEU infants.</p></sec></sec><sec id="S7"><title>Summary</title><p>HIV-exposed uninfected infants in the ZVITAMBO trial had poorer health outcomes than HIV-unexposed infants. Hospitalization was 50% more frequent among HEU infants in the first month of life, and mortality rates were higher over the 24-month follow-up period. Morbidity and mortality outcomes were associated with maternal disease severity and social factors, including parental relationship stability and household income (Table <xref ref-type="table" rid="T1">1</xref>). HEU infants were at higher risk of stunting, wasting, and underweight than HIV-unexposed infants, although maternal disease severity was not associated with growth outcomes.</p><p>We propose that immune activation and inflammation and may be key drivers of both infection susceptibility and growth failure in HEU infants. Notably, baseline CRP was higher in HEU compared to HIV-unexposed infants at 6 weeks of age, and was still elevated at 6 months of age. Our conceptual framework highlights a number of key pathways that may drive inflammation and immune activation, including maternal HIV itself (<italic>in utero</italic> and postnatally); coinfections (such as CMV and malaria); and a distorted gut microbiota (which may be acquired from the HIV-infected mother). Future work will aim to elucidate and describe pathways leading to poor health outcomes of HEU infants.</p></sec><sec id="S8"><title>Conclusion</title><p>Infants recruited to the ZVITAMBO trial have contributed to our understanding of the HEU population. Future studies should draw on these and other results in order to determine the causes of infection susceptibility and growth failure, and determine the impact of ART and cotrimoxazole on outcomes of this vulnerable group of infants.</p></sec><sec id="S9"><title>Author Contributions</title><p>CE wrote the first draft of the manuscript, which was critically reviewed and revised by JH, RN, and AP. JH designed and recruited to the original ZVITAMBO trial. RN was a coinvestigator on the original ZVITAMBO trial.</p></sec><sec id="S10"><title>Conflict of Interest Statement</title><p>The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. CE is funded by the National Institute for Health Research. AJP is funded by the Wellcome Trust (108065/Z/15/Z).</p></sec></body><back><fn-group><fn id="fn1"><p><sup>1</sup> Prendergast AJ, Chasekwa B, Rukobo S, Govha M, Mutasa K, Ntozini R, et al. Intestinal damage and immune activation in HIV-exposed and HIV-infected Zimbabwean infants (submitted 2016).</p></fn><fn id="fn2"><p><sup>2</sup>Omoni AO, Ntozini R, Evans C, Prendergast AJ, Moulton LH, Christian PS, et al. Child growth according to maternal and child HIV status in Zimbabwe (submitted 2016).</p></fn><fn id="fn3"><p><sup>3</sup>Evans C, Chasekwa B, Ntozini R, Humphrey JH, Prendergast AJ. Head circumferences of children born to HIV-infected and HIV-uninfected mothers in Zimbabwe during the pre-ART era (submitted 2016).</p></fn></fn-group><sec id="S11"><title>Funding</title><p>The ZVITAMBO trial was supported by the Canadian International Development Agency (CIDA) (R/C Project 690/M3688), United States Agency for International Development (USAID) (cooperative agreement number HRN-A-00-97-00015-00 between Johns Hopkins University and the Office of Health and Nutrition – USAID) and a grant from the Bill and Melinda Gates Foundation, Seattle, WA, USA. Additional funding was received from the SARA Project, which is operated by the Academy for Educational Development, Washington DC and is funded by USAID’s Bureau for Africa, Office of Sustainable Development under the terms of Contract AOT-C-00-99-00237-00, the Rockefeller Foundation (New York, NY), and BASF (Ludwigshafen, Germany). CE is funded by the National Institute for Health Research. 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