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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Social and immunological differences among uninfected Brazilians exposed
or unexposed to human immunodeficiency virus-infected partners</title><author><name sortKey="Silva, Maria Luiza" sort="Silva, Maria Luiza" uniqKey="Silva M" first="Maria Luiza" last="Silva">Maria Luiza Silva</name><affiliation><nlm:aff id="aff1"> Laboratório Central, Hospital das Clínicas, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte, MG,<country>Brasil</country></nlm:aff></affiliation></author><author><name sortKey="Melo, Victor Hugo" sort="Melo, Victor Hugo" uniqKey="Melo V" first="Victor Hugo" last="Melo">Victor Hugo Melo</name><affiliation><nlm:aff id="aff2"> Departamento de Ginecologia e Obstetrícia, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte, MG,<country>Brasil</country></nlm:aff></affiliation></author><author><name sortKey="Aleixo, Agdemir Waleria" sort="Aleixo, Agdemir Waleria" uniqKey="Aleixo A" first="Agdemir Waléria" last="Aleixo">Agdemir Waléria Aleixo</name><affiliation><nlm:aff id="aff3"> Laboratório de Doenças Infecciosas e Parasitárias, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte, MG,<country>Brasil</country></nlm:aff></affiliation></author><author><name sortKey="Aleixo, Lucia Fernandes" sort="Aleixo, Lucia Fernandes" uniqKey="Aleixo L" first="Lúcia Fernandes" last="Aleixo">Lúcia Fernandes Aleixo</name><affiliation><nlm:aff id="aff3"> Laboratório de Doenças Infecciosas e Parasitárias, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte, MG,<country>Brasil</country></nlm:aff></affiliation></author><author><name sortKey="Pascoal Xavier, Marcelo Antonio" sort="Pascoal Xavier, Marcelo Antonio" uniqKey="Pascoal Xavier M" first="Marcelo Antônio" last="Pascoal-Xavier">Marcelo Antônio Pascoal-Xavier</name><affiliation><nlm:aff id="aff4"> Departamento de Anatomia Patológica e Medicina Legal, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte, MG,<country>Brasil</country></nlm:aff></affiliation></author><author><name sortKey="Silva, Rafaela Oliveira" sort="Silva, Rafaela Oliveira" uniqKey="Silva R" first="Rafaela Oliveira" last="Silva">Rafaela Oliveira Silva</name><affiliation><nlm:aff id="aff3"> Laboratório de Doenças Infecciosas e Parasitárias, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte, MG,<country>Brasil</country></nlm:aff></affiliation></author><author><name sortKey="Ferreira, Lais Alves" sort="Ferreira, Lais Alves" uniqKey="Ferreira L" first="Laís Alves" last="Ferreira">Laís Alves Ferreira</name><affiliation><nlm:aff id="aff3"> Laboratório de Doenças Infecciosas e Parasitárias, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte, MG,<country>Brasil</country></nlm:aff></affiliation></author><author><name sortKey="Domingos, Willian Cunha" sort="Domingos, Willian Cunha" uniqKey="Domingos W" first="Willian Cunha" last="Domingos">Willian Cunha Domingos</name><affiliation><nlm:aff id="aff3"> Laboratório de Doenças Infecciosas e Parasitárias, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte, MG,<country>Brasil</country></nlm:aff></affiliation></author><author><name sortKey="Greco, Dirceu Bartolomeu" sort="Greco, Dirceu Bartolomeu" uniqKey="Greco D" first="Dirceu Bartolomeu" last="Greco">Dirceu Bartolomeu Greco</name><affiliation><nlm:aff id="aff5"> Departamento de Clínica Médica, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte, MG,<country>Brasil</country></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">25317705</idno><idno type="pmc">4238770</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4238770</idno><idno type="RBID">PMC:4238770</idno><idno type="doi">10.1590/0074-0276140140</idno><date when="2014">2014</date><idno type="wicri:Area/Pmc/Corpus">002790</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">002790</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Social and immunological differences among uninfected Brazilians exposed
or unexposed to human immunodeficiency virus-infected partners</title><author><name sortKey="Silva, Maria Luiza" sort="Silva, Maria Luiza" uniqKey="Silva M" first="Maria Luiza" last="Silva">Maria Luiza Silva</name><affiliation><nlm:aff id="aff1"> Laboratório Central, Hospital das Clínicas, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte, MG,<country>Brasil</country></nlm:aff></affiliation></author><author><name sortKey="Melo, Victor Hugo" sort="Melo, Victor Hugo" uniqKey="Melo V" first="Victor Hugo" last="Melo">Victor Hugo Melo</name><affiliation><nlm:aff id="aff2"> Departamento de Ginecologia e Obstetrícia, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte, MG,<country>Brasil</country></nlm:aff></affiliation></author><author><name sortKey="Aleixo, Agdemir Waleria" sort="Aleixo, Agdemir Waleria" uniqKey="Aleixo A" first="Agdemir Waléria" last="Aleixo">Agdemir Waléria Aleixo</name><affiliation><nlm:aff id="aff3"> Laboratório de Doenças Infecciosas e Parasitárias, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte, MG,<country>Brasil</country></nlm:aff></affiliation></author><author><name sortKey="Aleixo, Lucia Fernandes" sort="Aleixo, Lucia Fernandes" uniqKey="Aleixo L" first="Lúcia Fernandes" last="Aleixo">Lúcia Fernandes Aleixo</name><affiliation><nlm:aff id="aff3"> Laboratório de Doenças Infecciosas e Parasitárias, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte, MG,<country>Brasil</country></nlm:aff></affiliation></author><author><name sortKey="Pascoal Xavier, Marcelo Antonio" sort="Pascoal Xavier, Marcelo Antonio" uniqKey="Pascoal Xavier M" first="Marcelo Antônio" last="Pascoal-Xavier">Marcelo Antônio Pascoal-Xavier</name><affiliation><nlm:aff id="aff4"> Departamento de Anatomia Patológica e Medicina Legal, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte, MG,<country>Brasil</country></nlm:aff></affiliation></author><author><name sortKey="Silva, Rafaela Oliveira" sort="Silva, Rafaela Oliveira" uniqKey="Silva R" first="Rafaela Oliveira" last="Silva">Rafaela Oliveira Silva</name><affiliation><nlm:aff id="aff3"> Laboratório de Doenças Infecciosas e Parasitárias, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte, MG,<country>Brasil</country></nlm:aff></affiliation></author><author><name sortKey="Ferreira, Lais Alves" sort="Ferreira, Lais Alves" uniqKey="Ferreira L" first="Laís Alves" last="Ferreira">Laís Alves Ferreira</name><affiliation><nlm:aff id="aff3"> Laboratório de Doenças Infecciosas e Parasitárias, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte, MG,<country>Brasil</country></nlm:aff></affiliation></author><author><name sortKey="Domingos, Willian Cunha" sort="Domingos, Willian Cunha" uniqKey="Domingos W" first="Willian Cunha" last="Domingos">Willian Cunha Domingos</name><affiliation><nlm:aff id="aff3"> Laboratório de Doenças Infecciosas e Parasitárias, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte, MG,<country>Brasil</country></nlm:aff></affiliation></author><author><name sortKey="Greco, Dirceu Bartolomeu" sort="Greco, Dirceu Bartolomeu" uniqKey="Greco D" first="Dirceu Bartolomeu" last="Greco">Dirceu Bartolomeu Greco</name><affiliation><nlm:aff id="aff5"> Departamento de Clínica Médica, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte, MG,<country>Brasil</country></nlm:aff></affiliation></author></analytic><series><title level="j">Memórias do Instituto Oswaldo Cruz</title><idno type="ISSN">0074-0276</idno><idno type="eISSN">1678-8060</idno><imprint><date when="2014">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Understanding the social conditions and immunological characteristics that allow some
human immunodeficiency virus (HIV)-exposed patients to remain uninfected represents
an on-going challenge. In this study, the socio-demographic and sexual behaviour
characteristics and immune activation profiles of uninfected individuals exposed to
HIV-infected partners were investigated. A confidential and detailed questionnaire
was administered and venous blood was tested using HIV-1/enzyme immunoassays, plasma
HIV-1 RNA levels/bDNA and immunophenotyping/flow cytometry to determine the
frequencies of CD4 and CD8 T cells expressing activation markers. The data analysis
showed significant differences (p < 0.05) for immune parameters in individuals who
were uninfected, albeit exposed to HIV-infected partners, compared with unexposed
individuals. In particular, the exposed, uninfected individuals had a higher
frequency (median, minimum-maximum) of CD4<sup>+</sup>HLA-DR<sup>+ </sup>(4.2,
1.8-6.1), CD8<sup>+</sup>HLA-DR<sup>+</sup> (4.6, 0.9-13.7),
CD4<sup>+</sup>CD45RO<sup>+ </sup>(27.5, 14.2-46.6),
CD4<sup>+</sup>CD45RO<sup>+</sup>CD62L<sup>+</sup> (46.7, 33.9-67.1),
CD8<sup>+</sup>CD45RA<sup>+</sup>HLA-DR<sup>+</sup> (12.1, 3.4-35.8) and
CD8<sup>+</sup>CD45RO<sup>+</sup>HLA-DR<sup>+</sup> (9.0, 3.2-14.8) cells, a
decreased percentage of CD8<sup>+</sup>CD28<sup>+</sup> cells (11.7, 4.5-24.0) and a
lower cell-surface expression of Fcγ-R/CD16 on monocytes (56.5, 22.0-130.0). The
plasma HIV-1 RNA levels demonstrated detectable RNA virus loads in 57% of the
HIV-1<sup>+</sup> female partners. These findings demonstrate an activation
profile in both CD4 and CD8 peripheral T cells from HIV-1 exposed seronegative
individuals of serodiscordant couples from a referral centre in Belo Horizonte, state
of Minas Gerais.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Begaud, E" uniqKey="Begaud E">E Bégaud</name></author><author><name sortKey="Chartier, L" uniqKey="Chartier L">L Chartier</name></author><author><name sortKey="Marechal, V" uniqKey="Marechal V">V Marechal</name></author><author><name sortKey="Ipero, J" uniqKey="Ipero J">J Ipero</name></author><author><name sortKey="Leal, J" uniqKey="Leal J">J Léal</name></author><author><name sortKey="Versmisse, P" uniqKey="Versmisse P">P Versmisse</name></author><author><name sortKey="Breton, G" uniqKey="Breton G">G Breton</name></author><author><name sortKey="Fontanet, A" uniqKey="Fontanet A">A Fontanet</name></author><author><name sortKey="Capoulade Metay, C" uniqKey="Capoulade Metay C">C Capoulade-Metay</name></author><author><name sortKey="Fleury, H" uniqKey="Fleury H">H Fleury</name></author><author><name sortKey="Barre Sinoussi, F" uniqKey="Barre Sinoussi F">F 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Mem Inst Oswaldo Cruz</journal-id><journal-id journal-id-type="iso-abbrev">Mem. Inst. Oswaldo Cruz</journal-id><journal-title-group><journal-title>Memórias do Instituto Oswaldo Cruz</journal-title></journal-title-group><issn pub-type="ppub">0074-0276</issn><issn pub-type="epub">1678-8060</issn><publisher><publisher-name>Instituto Oswaldo Cruz, Ministério da Saúde</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">25317705</article-id><article-id pub-id-type="pmc">4238770</article-id><article-id pub-id-type="doi">10.1590/0074-0276140140</article-id><article-categories><subj-group subj-group-type="heading"><subject>Articles</subject></subj-group></article-categories><title-group><article-title>Social and immunological differences among uninfected Brazilians exposed
or unexposed to human immunodeficiency virus-infected partners</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Silva</surname><given-names>Maria Luiza</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="corresp" rid="c01"><sup>+</sup></xref></contrib><contrib contrib-type="author"><name><surname>Melo</surname><given-names>Victor Hugo</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Aleixo</surname><given-names>Agdemir Waléria</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Aleixo</surname><given-names>Lúcia Fernandes</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Pascoal-Xavier</surname><given-names>Marcelo Antônio</given-names></name><xref ref-type="aff" rid="aff4"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Silva</surname><given-names>Rafaela Oliveira</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Ferreira</surname><given-names>Laís Alves</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Domingos</surname><given-names>Willian Cunha</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Greco</surname><given-names>Dirceu Bartolomeu</given-names></name><xref ref-type="aff" rid="aff5"><sup>5</sup></xref></contrib></contrib-group><aff id="aff1"><label>1</label> Laboratório Central, Hospital das Clínicas, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte, MG,<country>Brasil</country></aff><aff id="aff2"><label>2</label> Departamento de Ginecologia e Obstetrícia, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte, MG,<country>Brasil</country></aff><aff id="aff3"><label>3</label> Laboratório de Doenças Infecciosas e Parasitárias, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte, MG,<country>Brasil</country></aff><aff id="aff4"><label>4</label> Departamento de Anatomia Patológica e Medicina Legal, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte, MG,<country>Brasil</country></aff><aff id="aff5"><label>5</label> Departamento de Clínica Médica, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte, MG,<country>Brasil</country></aff><author-notes><corresp id="c01"><label>+</label> Corresponding author: <email>mariasil@hc.ufmg.br</email></corresp></author-notes><pub-date pub-type="epub-ppub"><month>9</month><year>2014</year></pub-date><pmc-comment>Fake ppub date generated by PMC from publisher
pub-date/@pub-type='epub-ppub' </pmc-comment>
<pub-date pub-type="ppub"><month>9</month><year>2014</year></pub-date><volume>109</volume><issue>6</issue><fpage>775</fpage><lpage>781</lpage><history><date date-type="received"><day>24</day><month>4</month><year>2014</year></date><date date-type="accepted"><day>7</day><month>7</month><year>2014</year></date></history><permissions><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by-nc/3.0/"><license-p>This is an Open Access article distributed under the terms of the Creative
Commons Attribution Non-Commercial License, which permits unrestricted
non-commercial use, distribution, and reproduction in any medium, provided the
original work is properly cited.</license-p></license></permissions><abstract><p>Understanding the social conditions and immunological characteristics that allow some
human immunodeficiency virus (HIV)-exposed patients to remain uninfected represents
an on-going challenge. In this study, the socio-demographic and sexual behaviour
characteristics and immune activation profiles of uninfected individuals exposed to
HIV-infected partners were investigated. A confidential and detailed questionnaire
was administered and venous blood was tested using HIV-1/enzyme immunoassays, plasma
HIV-1 RNA levels/bDNA and immunophenotyping/flow cytometry to determine the
frequencies of CD4 and CD8 T cells expressing activation markers. The data analysis
showed significant differences (p < 0.05) for immune parameters in individuals who
were uninfected, albeit exposed to HIV-infected partners, compared with unexposed
individuals. In particular, the exposed, uninfected individuals had a higher
frequency (median, minimum-maximum) of CD4<sup>+</sup>HLA-DR<sup>+ </sup>(4.2,
1.8-6.1), CD8<sup>+</sup>HLA-DR<sup>+</sup> (4.6, 0.9-13.7),
CD4<sup>+</sup>CD45RO<sup>+ </sup>(27.5, 14.2-46.6),
CD4<sup>+</sup>CD45RO<sup>+</sup>CD62L<sup>+</sup> (46.7, 33.9-67.1),
CD8<sup>+</sup>CD45RA<sup>+</sup>HLA-DR<sup>+</sup> (12.1, 3.4-35.8) and
CD8<sup>+</sup>CD45RO<sup>+</sup>HLA-DR<sup>+</sup> (9.0, 3.2-14.8) cells, a
decreased percentage of CD8<sup>+</sup>CD28<sup>+</sup> cells (11.7, 4.5-24.0) and a
lower cell-surface expression of Fcγ-R/CD16 on monocytes (56.5, 22.0-130.0). The
plasma HIV-1 RNA levels demonstrated detectable RNA virus loads in 57% of the
HIV-1<sup>+</sup> female partners. These findings demonstrate an activation
profile in both CD4 and CD8 peripheral T cells from HIV-1 exposed seronegative
individuals of serodiscordant couples from a referral centre in Belo Horizonte, state
of Minas Gerais.</p></abstract><kwd-group><kwd>HIV-1 discordant couples</kwd><kwd>flow cytometry</kwd><kwd>immune activation</kwd><kwd>immunophenotyping</kwd></kwd-group><counts><fig-count count="3"></fig-count><table-count count="2"></table-count><ref-count count="34"></ref-count><page-count count="7"></page-count></counts></article-meta></front><body><p>Heterosexual intercourse is currently the main route of human immunodeficiency virus type 1
(HIV-1) acquisition worldwide and the rate of transmission in this manner is increasing
throughout Africa, Asia, Latin America and many industrialised countries (<xref rid="B25" ref-type="bibr">Piot et al. 2001</xref>, <xref rid="B34" ref-type="bibr">Yang
et al. 2005</xref>)).</p><p>The risk of transmission has been associated with a wide variety of behaviours, such as the
frequency and type of sexual contact (<xref rid="B26" ref-type="bibr">Quinn et al.
2000</xref>, <xref rid="B14" ref-type="bibr">Kaur & Mehra 2009</xref>)) and the use
or non-use of condoms, as well as types of interindividual variability, including genetic
predisposition, intrinsic cellular defence mechanisms and mucosal and systemic
HIV-1-specific cellular and humoral responses (<xref rid="B29" ref-type="bibr">Soriano et
al. 2002 </xref>, <xref rid="B11" ref-type="bibr">Kaslow et al. 2005)</xref>). These
variations in immunity can also impact natural killer (NK) cell activity, HIV-specific
immunoglobulin A levels and HIV-specific T cells (<xref rid="B20" ref-type="bibr">Mazzoli
et al. 1997 </xref>, <xref rid="B12" ref-type="bibr">Kaul et al. 2001a</xref>, <xref rid="B17" ref-type="bibr">Lo Caputo et al. 2003 </xref>, <xref rid="B18" ref-type="bibr">Makedonas et al. 2005)</xref>). In addition, virus characteristics and levels of plasma
viral load (PVL) have been implicated in resistance to infection (<xref rid="B23" ref-type="bibr">Operskalski et al. 1997)</xref>).</p><p>It has been reported that some individuals remain HIV seronegative despite being exposed to
HIV, in some cases repeatedly and over long periods of time. These individuals are called
HIV-exposed seronegatives (HESN). Although host factors are involved in the production of
this resistance to HIV acquisition, there is no clear explanation for such a low
susceptibility to infection (<xref rid="B28" ref-type="bibr">Rowland-Jones & McMichael
1995</xref>, <xref rid="B27" ref-type="bibr">Restrepo et al. 2011)</xref>). Immune
activation has been suggested to be critical in the susceptibility to HIV-1 transmission.
In vitro, HIV-1 requires activated T cells for a productive infection (<xref rid="B14" ref-type="bibr">Kaur & Mehra 2009)</xref>) and subjects with an activated
immune system show increased in vitro susceptibility to HIV and higher in vivo replication
(<xref rid="B16" ref-type="bibr">Lawn et al. 2001)</xref>).</p><p>HIV-1 replicates preferentially in CD45RO<sup>+</sup> memory T lymphocytes rather than
immature and immunologically quiescent naïve CD45RA<sup>+</sup> lymphocytes (<xref rid="B30" ref-type="bibr">Spina et al. 1997</xref>, <xref rid="B33" ref-type="bibr">Woods et al. 1997</xref>)). Additionally, the upregulation of adhesion molecules during
inflammatory processes may further promote virus-induced cell-cell fusion, thereby
facilitating the direct spread of the virus between cells (<xref rid="B9" ref-type="bibr">Hildreth & Orentas 1989</xref>, <xref rid="B16" ref-type="bibr">Lawn et al.
2001)</xref>).</p><p>As highly active antiretroviral therapy has greatly improved the quality of life of
HIV-positive patients, the number of discordant couples (in which the male is HIV positive
and the female is negative or <italic>vice versa</italic>) who are interested in pregnancy
is increasing (<xref rid="B32" ref-type="bibr">Vernazza et al. 2000</xref>)).</p><p>A better understanding of the genetic and immunologic bases of natural resistance to HIV-1
infection could be important for the development of preventive and therapeutic modalities.
In this study, we investigated the socio-demographics, sexual behaviour and immune
activation and memory status of peripheral blood leukocytes from uninfected individuals
exposed to HIV-1-infected partners and compared these results with the results of unexposed
individuals using flow cytometry. The aim was to characterise immunophenotyping features
that might facilitate an understanding of the immunological features of Brazilian HIV-1
serodiscordant couples.</p><sec><title>SUBJECTS, MATERIALS AND METHODS</title><p><italic>Study groups</italic> - Fourteen individuals who were uninfected yet exposed to
HIV-infected partners (HESN) as part of a group of HIV-1 discordant heterosexual couples
who visited the Clinics Hospital of Federal University of Minas Gerais (UFMG) were
invited to participate in the study. The inclusion criteria were an HIV-seronegative
male partner and an HIV-1 infected female partner, a stable relationship and a history
of penetrative sexual intercourse without condom use within the six months prior to the
study. Ten volunteer, HIV-1-negative males (10 low-risk laboratory personnel unexposed
to HIV-infected partners) who reported no sexual intercourse with an HIV-1-positive
partner were recruited to form the negative, HVI-1-unexposed seronegative group (HUSN).
All of the subjects were interviewed to ascertain their socio-demographic
characteristics {i.e., educational level, family income, religion and sexual behaviour
[age at 1st intercourse, frequency of intercourse, practice of oral and/or anal sex
during the previous 6 months, reported sexually transmitted diseases (STDs) and duration
of relationship]}.</p><p><italic>Blood samples</italic> - Peripheral blood samples (5 and 7 mL) were collected by
a trained professional at the Central Laboratory of the Clinics Hospital and placed into
Vacutainer<sup>TM</sup> tubes containing ethylenediamine tetraacetic acid (EDTA) as
an anticoagulant, a clot activator and gel for serum separation (both purchased from
Becton Dickinson, USA). Serologic tests for HIV-1 were used to detect anti-HIV
antibodies using microparticle enzyme immunoassays (MEIA) for HIV-1 and HIV-2 (Abbott
Laboratories, USA) and were performed at the Central Laboratory. Plasma HIV-1 RNA levels
(VLs) were quantified using VERSANT HIV-1 RNA 3.0 Assay (bDNA) (Siemens Healthcare
Diagnostics). A flow cytometric analysis of unstimulated whole blood was performed as
recommended by Becton Dickinson with the following modifications. First, 50-µL aliquots
of EDTA-anticoagulated blood were dispensed into 5-mL polystyrene tubes
(Falcon<sup>®</sup>, BD Pharmingen, USA). The samples were then individually stained
for specific cell-surface markers using three or four-colour immunocytometric assays
with the following anti-human cell surface marker monoclonal antibodies conjugated to
fluorescein isothiocyanate (FITC), phycoerythrin (PE), peridinin-chlorophyll protein
(PerCP), R-PE or cyanine dye Cy5 (PE Cy5.0) and allophycocyanin (APC): anti-CD4 FITC
(RPA-T4), anti-CD8 PerCP (RPA-T8), anti-CD3 FITC (UCHT1), anti-CD3 PerCP (SP34-2),
anti-CD14 FITC (M5E2), anti-CD16 PE Cy5.0 (3G8), anti-CD18 PE (6.7), anti-CD28 PE
(CD28.2), anti-CD38 PE (HIT2), anti-CD45RA PE (HI100), anti-CD45RO PE (UCHL1), anti-CD56
PE (B159), anti-CD62L APC (DREG-56), anti-HLA-DR PE (G46-6), anti-HLA-DR APC (MøP9) and
anti-CCR5 APC (2D7/CCR5). These antibodies were purchased from BD Pharmingen.</p><p>The samples were gently treated with vortex homogenisation and incubated in the dark for
30 min at room temperature (RT). Following incubation, the erythrocytes were lysed using
0.45 mL of fluorescence-activated cell sorter (FACS) lysing solution (Becton Dickinson)
and re-incubated for an additional 15 min at RT in the dark. After incubation, the cells
were washed twice with 2 mL of phosphate-buffered saline (PBS) containing 0.01% sodium
azide (NaN3). After erythrocyte lysis was complete, the samples were centrifuged at 600
<italic>g</italic> for 7 min at RT. The supernatants were discarded and the cell
pellets were washed twice with 2 mL of PBS containing 0.01% NaN3 and stored at 4ºC in
the dark prior to flow cytometry analysis. FACS data were acquired within 4 h after
staining.</p><p><italic>Flow cytometry acquisition and analysis</italic> - In total, 3,000 events/tube
were acquired within the lymphocyte gate using a FACSCalibur<sup>®</sup> flow cytometer
(Becton Dickinson) that was properly set up to measure forward (FSC) and side (SSC)
light scatters, FITC (FL-1), PE (FL-2), PerCP or PE Cy5.0 (FL-3) and APC (FL4). The
CELLQuest<sup>TM</sup> software (Franklin Lakes, USA), which was provided by the
manufacturer, was used for the data acquisition and analysis and the data were prepared
using the FlowJo software (Tree Star, USA). The selective analysis of lymphocytes was
carried out by first placing an electronic gate on the FSC vs. SSC dot plot to select
small blood lymphocytes based on their morphometric features. The gated lymphocyte
population was further characterised based on its relative fluorescent properties to
quantify the percentage of fluorescent-positive subpopulations. The selective analysis
of NK and NKT cells was initially performed using the lymphocyte scatter gate, created
according to the FSC vs. SSC dot plots, followed by immunophenotyping using anti-CD3
FITC, anti-CD16 PE Cy5.0 and anti-CD56 PE to determine the subpopulation of interest.
The analysis of monocytes was performed by immunophenotyping using SSC vs.
FL-1/anti-CD14-FITC dot plots to select SSC<sup>Low</sup>CD14<sup>High</sup> monocytes,
followed by immunophenotyping using anti-CD16 PE Cy5 and HLA-DR PE. The results were
expressed as the percentage of positive cells within the selected gates. Cell-surface
markers presenting a bimodal distribution and/or single-colour histograms were used to
evaluate the density or expression of cell-surface markers presenting a unimodal
distribution, which was expressed as the mean fluorescence intensity, within the gated
lymphocytes or monocytes.</p><p><italic>Statistical analysis</italic> - The statistical analysis was performed using the
non-parametric Mann-Whitney <italic>U</italic> test to compare the mean rates obtained
from the HESN and HUSN groups using GraphPad Prism software, v.5.0 (USA). Significant
differences were considered at p ≤ 0.05.</p><p><italic>Ethics</italic> - All of the subjects signed an informed consent form that was
approved by the Ethical Committee of UFMG (UFMG-ETIC 261/2009), Belo Horizonte, state of
Minas Gerais, Brazil.</p></sec><sec sec-type="results"><title>RESULTS</title><p>The socio-demographic and sexual behaviour characteristics of the individuals enrolled
in this study are shown in <xref ref-type="table" rid="t01">Table I</xref>. The age
range of the HESN and HUSN individuals varied from 28-56 and 20-38 years, respectively.
The median age for first reported sexual intercourse was 10-15 years among the HESN
group and 14-18 years among the HUSN group. Among the HESN individuals, the median
duration of cohabitation was 8.5 years (range from 5-10 years) and the median number of
sexual acts per week was three times; oral and anal sex in the past six months were
reported by 57.1% and 28.6% of the subjects, respectively. Among the HESN subjects,
14.3% reported a previous history of any STD and a minority (42.9%) reported regular
condom use. For the HUSN group, the median duration of cohabitation was seven years and
the median number of sexual acts per week was three. Oral sex in the past six months was
reported by 40% individuals and all of the subjects denied practicing anal sex. Of the
HUSN subjects, 50% reported a previous history of an STD and a majority (55.6%) reported
the regular use of condoms. The majority of HESN subjects reported practicing a religion
(92.9%). In contrast, half of the HUSN group said they did not practice any religion.
With regard to education, at least 64% of the individuals from the HESN group reported
seven years of school; the majority (100%) of the individuals in the HUSN group reported
completing high school or beyond. Concerning income, 57.1% of the HESN group declared a
family monthly income of less than US$ 800, whereas the majority (60%) of the HUSN group
reported a family income above US$ 800.</p><p><table-wrap id="t01" orientation="portrait" position="float"><label>TABLE I</label><caption><title>Socio-demographic and sexual behaviour characteristics of 14 human
immunodeficiency virus type 1 (HIV-1) exposed seronegative (HESN) and 10
unexposed seronegative (HUSN) heterosexual men</title></caption><table frame="hsides" rules="groups"><colgroup span="1"><col width="80%" span="1"></col><col width="10%" span="1"></col><col width="10%" span="1"></col></colgroup><thead><tr><th align="left" style="font-weight:normal" rowspan="1" colspan="1">Characteristics</th><th style="font-weight:normal" rowspan="1" colspan="1">HESN</th><th style="font-weight:normal" rowspan="1" colspan="1">HUSN</th></tr></thead><tbody><tr><td rowspan="1" colspan="1">Age (years) (mean)</td><td align="center" rowspan="1" colspan="1">39.1</td><td align="center" rowspan="1" colspan="1">26.6</td></tr><tr><td rowspan="1" colspan="1">Age at first sex (years)(mean)</td><td align="center" rowspan="1" colspan="1">15.5</td><td align="center" rowspan="1" colspan="1">18</td></tr><tr><td rowspan="1" colspan="1">Average of sexual acts/week</td><td align="center" rowspan="1" colspan="1">3.0</td><td align="center" rowspan="1" colspan="1">3.0</td></tr><tr><td rowspan="1" colspan="1">Reported oral sex in the past six months
(%)</td><td align="center" rowspan="1" colspan="1">57.1</td><td align="center" rowspan="1" colspan="1">40</td></tr><tr><td rowspan="1" colspan="1">Reported anal intercourse in the past six months
(%)</td><td align="center" rowspan="1" colspan="1">28.6</td><td align="center" rowspan="1" colspan="1">0</td></tr><tr><td rowspan="1" colspan="1">Self reported sexually transmitted disease
(%)</td><td align="center" rowspan="1" colspan="1">14.3</td><td align="center" rowspan="1" colspan="1">50</td></tr><tr><td rowspan="1" colspan="1">Self reported regular condom use (%)</td><td align="center" rowspan="1" colspan="1">42.9</td><td align="center" rowspan="1" colspan="1">55.6</td></tr><tr><td rowspan="1" colspan="1">Duration of union (years)(mean)</td><td align="center" rowspan="1" colspan="1">8.5</td><td align="center" rowspan="1" colspan="1">7</td></tr><tr><td rowspan="1" colspan="1">Number of children(mean)</td><td align="center" rowspan="1" colspan="1">1</td><td align="center" rowspan="1" colspan="1">< 1</td></tr><tr><td rowspan="1" colspan="1">Religiousness (%)</td><td align="center" rowspan="1" colspan="1">92.8</td><td align="center" rowspan="1" colspan="1">50</td></tr><tr><td rowspan="1" colspan="1">Catholic (%)</td><td align="center" rowspan="1" colspan="1">35.7</td><td align="center" rowspan="1" colspan="1">30</td></tr><tr><td rowspan="1" colspan="1">Protestant (%)</td><td align="center" rowspan="1" colspan="1">57.1</td><td align="center" rowspan="1" colspan="1">10</td></tr><tr><td rowspan="1" colspan="1">Education (years)(mean)</td><td align="center" rowspan="1" colspan="1">6.4</td><td align="center" rowspan="1" colspan="1">12.6</td></tr><tr><td rowspan="1" colspan="1">Income (< US$800/month) (%)</td><td align="center" rowspan="1" colspan="1">57.1</td><td align="center" rowspan="1" colspan="1">40</td></tr></tbody></table></table-wrap></p><p>Regarding laboratory characteristics, all of the HESN and HUNS individuals were HIV-1
seronegative (as tested by MEIA). The plasma HIV-1 RNA levels (VL) demonstrated
detectable RNA virus loads (detection threshold 50 copies/mL) in eight out of 14 (57%)
of the HIV-1<sup>+</sup> female partners. The median of RNA virus loads in copies/mL and
minimum-maximum (min-max) was 4,691 and 228-26,302 and in log<sub>10</sub> and min-max
was 3,269 and 2,358-4,420 (<xref ref-type="table" rid="t02">Table II</xref>). CD4 counts
were determined for all of the subjects and the median CD4 counts observed in the HESN
and HUSN groups were 931 (529-2,000) and 760 (573-1,326) cells/µL, respectively (<xref ref-type="table" rid="t02">Table II</xref>). No differences were observed when the
HESN and HUNS data were compared.</p><p><table-wrap id="t02" orientation="portrait" position="float"><label>TABLE II</label><caption><title>Laboratory characterisation of 14 exposed seronegative heterosexual men and
their partners</title></caption><table frame="hsides" rules="groups"><colgroup width="14%" span="1"><col span="1"></col><col span="1"></col><col span="1"></col><col span="1"></col><col span="1"></col><col span="1"></col><col span="1"></col></colgroup><thead><tr><th colspan="3" style="font-weight:normal" rowspan="1">Exposed seronegative
men</th><th colspan="4" style="font-weight:normal" rowspan="1">Human
immunodeficiency virus type 1 (HIV-1)-infected women</th></tr><tr><th colspan="7" style="font-weight:normal" rowspan="1"><hr></hr> </th></tr><tr><th style="font-weight:normal" rowspan="1" colspan="1">ID</th><th style="font-weight:normal" rowspan="1" colspan="1">CD4 (cells/µL)</th><th style="font-weight:normal" rowspan="1" colspan="1">CD8 (cells/µL)</th><th style="font-weight:normal" rowspan="1" colspan="1">ID</th><th style="font-weight:normal" rowspan="1" colspan="1">HIV-1 RNA
(copies/mL)</th><th style="font-weight:normal" rowspan="1" colspan="1">CD4 (cells/µL)</th><th style="font-weight:normal" rowspan="1" colspan="1">CD8 (cells/µL)</th></tr></thead><tbody><tr><td align="center" rowspan="1" colspan="1">M-001</td><td align="center" rowspan="1" colspan="1">1,160</td><td align="center" rowspan="1" colspan="1">209</td><td align="center" rowspan="1" colspan="1">F-001</td><td align="center" rowspan="1" colspan="1">746</td><td align="center" rowspan="1" colspan="1">389</td><td align="center" rowspan="1" colspan="1">468</td></tr><tr><td align="center" rowspan="1" colspan="1">M-002</td><td align="center" rowspan="1" colspan="1">600</td><td align="center" rowspan="1" colspan="1">378</td><td align="center" rowspan="1" colspan="1">F-002</td><td align="center" rowspan="1" colspan="1">5,975</td><td align="center" rowspan="1" colspan="1">550</td><td align="center" rowspan="1" colspan="1">1,162</td></tr><tr><td align="center" rowspan="1" colspan="1">M-003</td><td align="center" rowspan="1" colspan="1">931</td><td align="center" rowspan="1" colspan="1">537</td><td align="center" rowspan="1" colspan="1">F-003</td><td align="center" rowspan="1" colspan="1">< 50</td><td align="center" rowspan="1" colspan="1">259</td><td align="center" rowspan="1" colspan="1">433</td></tr><tr><td align="center" rowspan="1" colspan="1">M-004</td><td align="center" rowspan="1" colspan="1">685</td><td align="center" rowspan="1" colspan="1">465</td><td align="center" rowspan="1" colspan="1">F-004</td><td align="center" rowspan="1" colspan="1">883</td><td align="center" rowspan="1" colspan="1">299</td><td align="center" rowspan="1" colspan="1">1,227</td></tr><tr><td align="center" rowspan="1" colspan="1">M-005</td><td align="center" rowspan="1" colspan="1">769</td><td align="center" rowspan="1" colspan="1">356</td><td align="center" rowspan="1" colspan="1">F-005</td><td align="center" rowspan="1" colspan="1">10,111</td><td align="center" rowspan="1" colspan="1">449</td><td align="center" rowspan="1" colspan="1">2,617</td></tr><tr><td align="center" rowspan="1" colspan="1">M-006</td><td align="center" rowspan="1" colspan="1">969</td><td align="center" rowspan="1" colspan="1">916</td><td align="center" rowspan="1" colspan="1">F-006</td><td align="center" rowspan="1" colspan="1">< 50</td><td align="center" rowspan="1" colspan="1">877</td><td align="center" rowspan="1" colspan="1">1,182</td></tr><tr><td align="center" rowspan="1" colspan="1">M-007</td><td align="center" rowspan="1" colspan="1">804</td><td align="center" rowspan="1" colspan="1">2,117</td><td align="center" rowspan="1" colspan="1">F-007</td><td align="center" rowspan="1" colspan="1">26,302</td><td align="center" rowspan="1" colspan="1">374</td><td align="center" rowspan="1" colspan="1">983</td></tr><tr><td align="center" rowspan="1" colspan="1">M-008</td><td align="center" rowspan="1" colspan="1">1,147</td><td align="center" rowspan="1" colspan="1">626</td><td align="center" rowspan="1" colspan="1">F-008</td><td align="center" rowspan="1" colspan="1">12,456</td><td align="center" rowspan="1" colspan="1">338</td><td align="center" rowspan="1" colspan="1">309</td></tr><tr><td align="center" rowspan="1" colspan="1">M-010</td><td align="center" rowspan="1" colspan="1">1,634</td><td align="center" rowspan="1" colspan="1">778</td><td align="center" rowspan="1" colspan="1">F-010</td><td align="center" rowspan="1" colspan="1">< 50</td><td align="center" rowspan="1" colspan="1">651</td><td align="center" rowspan="1" colspan="1">756</td></tr><tr><td align="center" rowspan="1" colspan="1">M-011</td><td align="center" rowspan="1" colspan="1">954</td><td align="center" rowspan="1" colspan="1">813</td><td align="center" rowspan="1" colspan="1">F-011</td><td align="center" rowspan="1" colspan="1">3,407</td><td align="center" rowspan="1" colspan="1">439</td><td align="center" rowspan="1" colspan="1">854</td></tr><tr><td align="center" rowspan="1" colspan="1">M-012</td><td align="center" rowspan="1" colspan="1">2,000</td><td align="center" rowspan="1" colspan="1">553</td><td align="center" rowspan="1" colspan="1">F-012</td><td align="center" rowspan="1" colspan="1">228</td><td align="center" rowspan="1" colspan="1">1,317</td><td align="center" rowspan="1" colspan="1">705</td></tr><tr><td align="center" rowspan="1" colspan="1">M-013</td><td align="center" rowspan="1" colspan="1">742</td><td align="center" rowspan="1" colspan="1">672</td><td align="center" rowspan="1" colspan="1">F-013</td><td align="center" rowspan="1" colspan="1">< 50</td><td align="center" rowspan="1" colspan="1">977</td><td align="center" rowspan="1" colspan="1">590</td></tr><tr><td align="center" rowspan="1" colspan="1">M-014</td><td align="center" rowspan="1" colspan="1">529</td><td align="center" rowspan="1" colspan="1">487</td><td align="center" rowspan="1" colspan="1">F-014</td><td align="center" rowspan="1" colspan="1">< 50</td><td align="center" rowspan="1" colspan="1">499</td><td align="center" rowspan="1" colspan="1">832</td></tr><tr><td align="center" rowspan="1" colspan="1">M-015</td><td align="center" rowspan="1" colspan="1">1,096</td><td align="center" rowspan="1" colspan="1">555</td><td align="center" rowspan="1" colspan="1">F-015</td><td align="center" rowspan="1" colspan="1">< 50</td><td align="center" rowspan="1" colspan="1">1,228</td><td align="center" rowspan="1" colspan="1">1,287</td></tr></tbody></table><table-wrap-foot><fn id="TFN01t02"><p>data are expressed as cells/µL for CD4 and CD8 T cells and copies/mL for
HIV-1 RNA levels. F: females; M: males.</p></fn></table-wrap-foot></table-wrap></p><p>An ex vivo analysis of leukocyte subsets (frequency, activation status and C-C chemokine
receptor type 5 expression) present in the peripheral blood was performed using
four-colour flow cytometry assays (<xref ref-type="fig" rid="f01">Figs 1</xref>-<xref ref-type="fig" rid="f03">3</xref>). The results of the HESN group were compared to
the results of the HUSN group.</p><p><fig id="f01" orientation="portrait" position="float"><label>Fig. 1</label><caption><title>: frequency of T cell activation and adhesion molecule expression in the
whole blood samples of the human immunodeficiency virus type 1 (HIV-1)-exposed
seronegatives (HESN) (n = 14) or HVI-1-unexposed seronegative group (HUSN)
individuals (n = 10). The results are expressed in a box plot format for the
frequency of CD28, CD38, CD62L, HLA-DR, CCR5 and the mean fluorescence
intensity (MFI) of CD18 in CD4 and CD8 T cells. The box stretches from the
lower hinge (defined as the 25th percentile) to the upper hinge (the 75th
percentile) and, therefore, contains the middle half of the score in the
distribution. The median is shown as a line across the box. Therefore, ¼ of the
distribution is between this line and the bottom or the top. Significant
differences (p < 0.05) are indicated with an asterisk.</title></caption><graphic xlink:href="0074-0276-mioc-109-6-0775-gf01"></graphic></fig></p><p><fig id="f02" orientation="portrait" position="float"><label>Fig. 2</label><caption><title>: status of naïve and memory T cells in the unstimulated peripheral blood
of the human immunodeficiency virus type 1 (HIV-1)-exposed seronegatives (HESN)
(n = 14) or HVI-1-unexposed seronegative group (HUSN) (n = 10) groups. The
results are expressed in a box plot format for the frequency of naïve T cells
(CD45RA+ or CD45RA+CD62L+) (left panels), memory T cells (CD45RO+) (right
panels), which are classified as central memory T cells (CD45RO+CD62L+) and
effector memory T cells (CD45RO+, CD62L-) (left panels) and naïve or
memory-activated (CD45RA+/CD45RO+ HLA-DR+) T cells (left and right bottom
panels). The box stretches from the lower hinge (defined as the 25th
percentile) to the upper hinge (the 75th percentile) and therefore, contains
the middle half of the scores in the distribution. The median is shown as a
line across the box. Therefore ¼ of the distribution is between this line and
the bottom or the top of the box. Significant differences (p < 0.05) are
identified with an asterisk.</title></caption><graphic xlink:href="0074-0276-mioc-109-6-0775-gf02"></graphic></fig></p><p>No statistically significant difference was observed when comparing the
CCR5<sup>+</sup>CD4<sup>+</sup> and CCR5<sup>+</sup>CD8<sup>+</sup> results between
the HESN and HUSN individuals (<xref ref-type="fig" rid="f01">Fig. 1D</xref>). The
frequency of CCR5 expression in peripheral T cells from the HESN group was 12 (4.9-17.6)
for CD4<sup>+</sup> cells and 14.7 (6.7-32.5) for CD8<sup>+</sup> cells. In the HUSN
group, the frequencies of CD4<sup>+</sup>CCR5<sup>+</sup> and
CD8<sup>+</sup>CCR5<sup>+</sup> T cells were 10.9 (2.6-16.3) and 12.9 (2.8-19.9),
respectively. When the activation status of peripheral T cells was examined, the
activation profile of T cells among the HESN group compared with the HUSN group was
characterised by a lower frequency of CD8<sup>+</sup>CD28<sup>+</sup> cells and a higher
frequency of CD4<sup>+</sup>HLA-DR<sup>+</sup> and CD8<sup>+</sup>HLA-DR<sup>+</sup> T
cells (<xref ref-type="fig" rid="f01">Fig. 1A</xref>, <xref ref-type="fig" rid="f01">B</xref>). An analysis of adhesion molecule expression among circulating T cells
showed no significant differences in CD18 expression on CD4 and CD8 T cells (<xref ref-type="fig" rid="f01">Fig. 1E</xref>) or in the frequency of CD4<sup>+</sup> and
CD8<sup>+</sup>CD62L<sup>+</sup> cells (<xref ref-type="fig" rid="f01">Fig.
1F</xref>).</p><p>To evaluate the patterns and activation status of naïve and memory T cells in peripheral
blood, the frequency of CD45RA, CD45RO, CD62L and HLA-DR expression was investigated
using multicolour flow cytometric assays (<xref ref-type="fig" rid="f02">Fig. 2</xref>).
The analysis of the data demonstrated an increased frequency of naïve, activated CD8 T
cells (CD8<sup>+</sup>CD45RA<sup>+</sup>HLA-DR<sup>+</sup>) in the HESN group (<xref ref-type="fig" rid="f02">Fig. 2C</xref>), though no difference was found in the
frequency of CD62L<sup>+</sup>CD45RA<sup>+</sup> cells among CD4 and CD8 T cells (<xref ref-type="fig" rid="f02">Fig. 2B</xref>). In addition, higher levels of memory cells
were demonstrated in the HESN individuals, which were characterised by increased levels
of CD4<sup>+</sup>CD45RO<sup>+</sup> cells (<xref ref-type="fig" rid="f02">Fig.
2D</xref>), central memory cells (CD4<sup>+</sup>CD45RO<sup>+</sup>CD62L<sup>+</sup>)
(<xref ref-type="fig" rid="f02">Fig. 2E</xref>) and memory-activated cells
(CD4<sup>+</sup> and CD8<sup>+</sup>CD45RO<sup>+</sup>HLA-DR<sup>+</sup>) (<xref ref-type="fig" rid="f02">Fig. 2G</xref>). No significant difference was observed
between the groups in terms of the percentage of effector memory T cells (CD4 and
CD8<sup>+</sup>CD45RO<sup>+</sup>CD62L<sup>-</sup>) (<xref ref-type="fig" rid="f02">Fig. 2F</xref>).</p><p><fig id="f03" orientation="portrait" position="float"><label>Fig. 3</label><caption><title>: analysis of monocytes, natural killer (NK) and NKT lymphocyte subsets in
the whole blood of the human immunodeficiency virus type 1 (HIV-1)-exposed
seronegatives (HESN) (n = 14) or HVI-1-unexposed seronegative group (HUSN) (n =
10) groups. A triple staining immunophenotyping platform was used to identify
the lymphocyte subsets as CD3-CD16+CD56+ NK-cells or CD3+CD16+CD56+ NKT-cells.
The results are expressed in a box plot format. The box stretches from the
lower hinge (defined as the 25th percentile) to the upper hinge (the 75th
percentile) and therefore, contains the middle half of the scores in the
distribution. The median is shown as a line across the box. Therefore, ¼ of the
distribution is between this line and the bottom or the top of the box.
Significant differences (p < 0.05) are identified with an asterisk.</title></caption><graphic xlink:href="0074-0276-mioc-109-6-0775-gf03"></graphic></fig></p><p>The monocyte expression of HLA-DR, CD16 and CCR5 and the frequency of circulating NK
(CD3<sup>-</sup>CD16<sup>+/-</sup>CD56<sup>+/-</sup>) and NKT
(CD3<sup>+</sup>CD16<sup>+/-</sup>CD56<sup>+/</sup>) cells was also analysed (<xref ref-type="fig" rid="f03">Fig. 3</xref>). However, no significant differences were
observed in the expression of HLA-DR or CCR5 by monocytes (<xref ref-type="fig" rid="f03">Fig. 3A</xref>, <xref ref-type="fig" rid="f03">B</xref>) or in the
frequency of circulating NK and NKT cells between the groups (<xref ref-type="fig" rid="f03">Fig. 3C</xref>). In contrast, decreased cell-surface expression of Fcγ-R
(CD16) was observed on the monocytes obtained from the HESN group (<xref ref-type="fig" rid="f03">Fig. 3A</xref>).</p></sec><sec sec-type="discussion"><title>DISCUSSION</title><p>Few studies characterising HIV-1-discordant couples have been conducted in our country
and only a small number of them have been performed as an immunological investigation.
Aiming to characterise the socio-demographic determinants, sexual behaviours and
immunophenotypic patterns of uninfected individuals exposed to HIV-1-infected partners,
this study enrolled 14 heterosexual men from HIV-1-serodiscordant couples who were
assisted in a large referral centre in Belo Horizonte, as well as 10 individuals not
exposed to HIV-1-infected partners.</p><p>The demographic and behavioural characteristics observed in this study reflect the
current state of the HIV/acquired immune deficiency syndrome epidemic in Brazil,
especially with regard to pauperisation (<xref rid="B3" ref-type="bibr">Brito et al.
2001</xref>)). Individuals who were uninfected, but exposed to HIV-infected partners
from HIV-1-discordant heterosexual couples demonstrated greater indicators of poverty,
such as a poor education and insufficient income and, consequently, reported a low
adherence to condom use and a large number of children. These characteristics are
similar to those reported in other studies performed in Africa and China in
HIV-1-serodiscordant couples (<xref rid="B10" ref-type="bibr">Isiugo-Abanihe
2006</xref>, <xref rid="B19" ref-type="bibr">Matovu 2010</xref>, <xref rid="B5" ref-type="bibr">Duan et al. 2012</xref>)). Another intriguing result was the great religious
bond of exposed, uninfected partners, mainly those of Protestant religions.
Hypothetically, this link to religious practices could influence sexual behaviour and
promote safe sex (<xref rid="B22" ref-type="bibr">Muñoz-Laboy et al. 2011</xref>));
however, our results showed the opposite trend for uninfected partners, as sexual
practices with a high risk for HIV transmission remained despite the declaration of
religious practice. Unfortunately, we did not ask how long the individuals were
practicing their religious precepts or whether they ascribed to them after learning the
HIV status of their partner.</p><p>The transmission and acquisition of HIV-1 have been associated with VL as well as viral
and host biological characteristics (<xref rid="B23" ref-type="bibr">Operskalski et al.
1997</xref>, <xref rid="B26" ref-type="bibr">Quinn et al. 2000</xref>, <xref rid="B11" ref-type="bibr">Kaslow et al. 2005</xref>)). <xref rid="B7" ref-type="bibr">Gray et al. (2001)</xref>), in an observational study of monogamous,
HIV-1-serodiscordant couples, identified plasma HIV-1 RNA as the strongest predictor of
HIV-1 transmission, with transmission probabilities that increased with genital
ulceration (<xref rid="B7" ref-type="bibr">Gray et al. 2001</xref>)). Our data
demonstrated a detectable RNA virus load in 57% of the infected female partners;
however, the VL was low (< 10,000 copies/mL) in these women. Furthermore, 87.7% of
the HESN group reported no history of any STD. These data together might have
contributed to the HIV-1 seronegative status in this study. Although VL has been
associated with an increased rate of seroconversion, the same trend was not demonstrated
for CD4 cell levels (<xref rid="B24" ref-type="bibr">Pedraza et al. 1999</xref>, <xref rid="B6" ref-type="bibr">Fideli et al. 2001</xref>, , <xref rid="B21" ref-type="bibr">Melo et al. 2008)</xref>). In our study, there were no significant differences in
CD4 counts; however, immune changes characterised by an activation pattern of CD4 and
CD8 T cells in the peripheral blood of the HESN individuals were observed. CD8-activated
lymphocytes in the peripheral circulation play an important role in the host antiviral
response (<xref rid="B16" ref-type="bibr">Lawn et al. 2001)</xref>). It was also
reported that cytotoxic T lymphocytes play a role in resistance to HIV infection, though
this resistance is believed to be dependent on the persistent exposure to HIV (<xref rid="B13" ref-type="bibr">Kaul et al. 2001b</xref>).</p><p>Two hypotheses have been suggested to explain the immunophenotypic changes observed in
the HESN group. The immunophenotypic changes observed in highly HIV-exposed, uninfected
individuals could be a consequence of immunogenic challenge during viral exposure.
Mucosal and systemic immune activation was reported in seronegative women who had
multiple episodes of unprotected heterosexual intercourse with their HIV-1-infected
heterosexual partners, as demonstrated by lower levels of naïve CD4<sup>+</sup> T cells
and a higher level of CD4<sup>+</sup> memory, CD4<sup>+</sup>CD28<sup>-</sup>,
CD8<sup>+</sup>CD28<sup>+</sup> and CD8<sup>+</sup>CD38<sup>+</sup> T cells than in
healthy control subjects (<xref rid="B2" ref-type="bibr">Biasin et al. 2000</xref>)).
<xref rid="B31" ref-type="bibr">Suy et al. (2007)</xref>) observed changes in the
memory and activated T cells of highly HIV-exposed, uninfected partners, including lower
levels of naïve and CD28<sup>+</sup> T cells and higher levels of HLA-DR<sup>+</sup> T
cells, CD4<sup>+</sup> T cells expressing CCR5 and memory CD4<sup>+</sup> T cells,
compared with control subjects. Because immune activation has been suggested to be
critical for HIV-1 transmission susceptibility (<xref rid="B24" ref-type="bibr">Pedraza
et al. 1999</xref>, <xref rid="B4" ref-type="bibr">Camara et al. 2010</xref>)), it is
reasonable to hypothesise that the individuals with lower levels of immune activation
would have a decreased susceptibility to HIV infection. Within this context, some
investigators have found low levels of CD4<sup>+</sup> T cell immune activation and low
T cell responsiveness in studies involving HESN individuals. In a cohort of highly
exposed, but HIV-seronegative men who had sex with men in Amsterdam, higher naïve
(CD45RO<sup>-</sup>CD27<sup>+</sup>) CD4 and CD8 T cell numbers and lower percentages
of activated (HLADR<sup>+</sup>CD38<sup>+</sup>, CD70<sup>+</sup>) CD4 and proliferating
(Ki67) CD4 and CD8 T cells were observed (<xref rid="B15" ref-type="bibr">Koning et al.
2005</xref>)). <xref rid="B1" ref-type="bibr">Bégaud et al. (2006)</xref>) also
reported a lower proportion of activation marker-expressing CD4 T lymphocytes
(HLA-DR<sup>+</sup>CD4 and CCR5<sup>+</sup>CD4 T cells) in highly exposed, uninfected
partners of HIV-1-infected individuals compared to low-risk controls.</p><p>Our data revealed an increased activation pattern in naïve and memory CD4<sup>+</sup>and CD8<sup>+</sup> T cells, as well as an increased frequency of memory cells, in HESN
individuals compared with HUSN individuals. We also found a low VL in 57% of the female
partners of the HESN group, corroborating the first hypothesis. However, our data did
not demonstrate a significant difference in CCR5 expression on CD4<sup>+</sup> T cells,
as previously described (<xref rid="B2" ref-type="bibr">Biasin et al. 2000</xref>, <xref rid="B15" ref-type="bibr">Koning et al. 2005</xref>, <xref rid="B1" ref-type="bibr">Bégaud et al. 2006</xref>)). Decreased monocyte CD16 expression in the HESN group
was observed in our work; FcγRIII (CD16) is normally associated with the activation or
maturation of monocytes and circulating CD14<sup>+</sup>CD16<sup>+</sup> monocytes are
an important cellular target for HIV-1 entry (<xref rid="B8" ref-type="bibr">Han et al.
2009</xref>)).</p><p>Susceptibility to HIV infection varies among individuals; however, the mechanisms
determining HIV transmission are not well understood. Thus, the multiple virological,
immunological and host factors that are likely involved in protecting against HIV-1
infection should be more extensively investigated.</p><p>Our findings demonstrate immunological features (i.e., a higher frequency of activation
markers on CD4 and CD8 naïve and memory T cells) in this study of uninfected Brazilians
exposed to HIV-infected partners. The data presented in this paper represent the
preliminary results of a pilot study involving a small number of individuals and further
investigations are required to obtain a better understanding of these immunological
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