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August 10, 1994, Vol 272, No. 6 >
ARTICLE | August 10, 1994

Features of HIV-1 That Could Influence Maternal-Child Transmission FREE

Srisakul C. Kliks, PhD; Diane W. Wara, MD; Daniel V. Landers, MD; Jay A. Levy, MD
[+] Author Affiliations

Reprints not available.


JAMA. 1994;272(6):467-474. doi:10.1001/jama.1994.03520060067034
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Article
References

Objective.  —To evaluate the biological and serological properties of the human immunodeficiency virus type 1 (HIV-1) for factors potentially involved in the mother-to-child transmission of HIV-1.

Design.  —Isolates of HIV-1 were recovered from the blood of 12 of 44 nontransmitting mothers and six of eight transmitting mothers and their corresponding infants. These 24 HIV-1 isolates were compared for their biological and immunologic properties to discern any parameters that correlate with vertical transmission of HIV-1.

Main Outcome Measures.  —Replication capabilities of the above-mentioned HIV-1 isolates in human peripheral blood mononuclear cells (PBMCs), human macrophages, and various T-cell lines and the susceptibilities of the viruses to neutralization or enhancement by anti-HIV-1 antibodies in autologous serum samples from mothers and infants.

Setting.  —San Francisco Bay Area, California.

Participants.  —A cohort of 52 HIV-1—infected women and their infants in a prospective study on perinatal HIV transmission by the Bay Area Perinatal AIDS Center.

Results.  —The viral isolates from the transmitting mothers and their infants differed from the isolates from the nontransmitting mothers in their efficient replication in human PBMCs and in their ability to infect one or more human T-lymphocytic cell lines. All the HIV-1 isolates were able to infect human macrophages with only low-level replication and were unable to form syncytia in the MT-2—lymphocytic cells. No correlation between transmission and reactivity of maternal serum samples to the peptide corresponding to the principal neutralization domain of the third hypervariable region of the viral envelope was observed. However, the majority (9/12) of maternal isolates from the nontransmitters were neutralized by their autologous serum samples compared with only two among six in the transmitter group (P<.07). Moreover, five infant isolates were resistant to neutralization by their respective mothers' serum samples, and one was sensitive to infection enhancement by the mother's serum. Another infant isolate was enhanced by his autologous serum.

Conclusions.  —Viral factors that appeared to correlate with mother-to-child transmission of HIV-1 observed in a small cohort included rapid or high-titered replication in human PBMCs, T-cell line tropism, and resistance to neutralization or a sensitivity to enhancement of infection by the maternal serum.(JAMA. 1994;272:467-474)

REFERENCES

1 +
Chu SY, Buchler JW, Oxtoby MJ, Kilbourne BW.  Impact of the human immunodeficiency virus epidemic on mortality in children, United States. Pediatrics . 1991;;87:806-810.
2 +
Chin J.  Current and future dimensions of the HIV/AIDS pandemic in women and children. Lancet . 1990;;336:221-224.
3 +
Gwinn M, Pappaioanou M, George JR, et al.  Prevalence of HIV infection in childbearing women in the United States: surveillance using newborn blood samples. JAMA . 1991;;265:1704-1708.
4 +
Ryder RW, Nsa W, Hassig SE, et al.  Perinatal transmission of the human immunodeficiency virus type 1 to infants of seropositive women in Zaire. N Engl J Med . 1989;;320:1637-1642.
5 +
Mok JYQ, Hague RA, Yap PL, et al.  Vertical transmission of HIV: a prospective study. Arch Dis Child . 1989;;64:1140-1145.
6 +
European Collaborative Study.  Children born to women with HIV-1 infection: natural history and risk of transmission. Lancet . 1991;;337:253-260.
7 +
Lyman MD, Kress Y, Kure K, Rashbaum WK, Rubinstein A, Soeiro R.  Detection of HIV in fetal central nervous system tissue. AIDS . 1990;;4:917-920.
8 +
Courgnaud V, Laure F, Brossard A, et al.  Frequent and early in utero HIV-1 infection. AIDS Res Hum Retroviruses . 1991;;7:337-341.
9 +
Goedert JJ, Duliege A-M, Amos CI, Felton S, Biggar RJ.  International registry of HIV-exposed twins. Lancet . 1991;;338:1471-1475.
10 +
European Collaborative Study.  Risk factors for mother-to-child transmission of HIV-1. Lancet . 1992;; 339:1007-1012.
11 +
Ziegler JB, Cooper DA, Johnson RO, Gold J.  Postnatal transmission of AIDS—associated retrovirus from mother to infant. Lancet . 1985;;1:896-898.
12 +
Stiehm ER, Vink P.  Transmission of human immunodeficiency virus infection by breast feeding. J Pediatr . 1991;;118:410-412.
13 +
Rossi P.  Report of a Consensus Workshop, Siena, Italy, 1992: maternal factors involved in mother-to-child transmission of HIV-1. J Acquir Immune Defic Syndr . 1992;;5:1169-1178.
14 +
Goedert JJ, Drummond JE, Minkoff HL, et al.  Mother-to-infant transmission of human immunodeficiency virus type 1: association with prematurity or low anti-gp 120. Lancet . 1989;;2:1351-1354.
15 +
Rossi P, Moschese V, Broliden PA, et al.  Presence of maternal antibodies to human immunodeficiency virus type 1 envelope glycoprotein gp 120 epitopes correlates with the uninfected status of children born to seropositive mothers. Proc Natl Acad Sci U S A . 1989;;86:8055-8058.
16 +
Ugen KE, Goedert JJ, Boyer J, et al.  Vertical transmission of human immunodeficiency virus (HIV) infection. J Clin Invest . 1992;;89:1923-1930.
17 +
Williams-Herman D, Wara D, Levy JA, et al. Risk factors for perinatal HIV-1 transmission. Proceedings of the Ninth International Conference on AIDS; June 6-11,1993; Berlin, Germany;1:313. Abstract PO-B05-1064.
18 +
Centers for Disease Control.  Classification system for human immunodeficiency virus (HIV) in children under 13 years of age. MMWR Morb Mortal Wkly Rep . 1987;;36:225-230.
19 +
Centers for Disease Control.  Revision of the CDC surveillance case definition for acquired immunodeficiency syndrome. MMWR Morb Mortal Wkly Rep . 1987;;36:35-155.
20 +
Castro BA, Weiss CD, Wiviott LD, Levy JA.  Optimal conditions for recovery of the human immunodeficiency virus from peripheral blood mononuclear cells. J Clin Microbiol . 1988;;26:2371-2376.
21 +
Hoffman AD, Banapour B, Levy JA.  Characterization of the AIDS-associated retrovirus reverse transcriptase and optimal conditions for its detection in virions. Virology . 1985;;147:326-335.
22 +
McDougal JS, Cort SP, Kennedy MS.  Immunoassay for the detection and quantitation of infectious human retrovirus, lymphadenopathy-associated virus (LAV). J Immunol Methods . 1985;;76: 171-183.
23 +
Levy JA, Hoffman AD, Kramer SM, Landis JA, Shimabukuro JM, Oshiro LS.  Isolation of lymphocytopathic retroviruses from San Francisco patients with AIDS. Science . 1984;;225:840-842.
24 +
Tateno M, Levy JA.  MT-4 plaque formation can distinguish cytopathic subtypes of the human immunodeficiency virus (HIV). Virology . 1988;;167:209-301.
25 +
Cheng-Mayer C, Weiss CD, Seto D, Levy JA.  Isolates of human immunodeficiency virus type 1 from the brain may constitute a special group of the AIDS virus. Proc Natl Acad Sci U S A . 1989;;80: 8575-8579.
26 +
Homsy J, Tateno M, Levy JA.  Antibody-dependent enhancement of HIV infection. Lancet . 1988;; 1:1285-1286.
27 +
Koot M, Vos AHV, Keet RPM, et al.  HIV-1 biological phenotype in long-term infected individuals evaluated with an MT-2 cocultivation assay. AIDS . 1992;;6:49-54.
28 +
Pan L-Z, Cheng-Mayer C, Levy JA.  Patterns of antibody response in individuals infected with the human immunodeficiency virus. J Infect Dis . 1987;; 155:626-632.
29 +
Sakamoto D, Baenzinger J, Sinangil F, Lee D, Turck C, Steimer K.  An improved method for assessing antibody responses to the principal neutralizing determinant (PND) of HIV-1 gp 120. J Cell Biochem Suppl . 1993;;17E:85.
30 +
La Rosa GJ, Davide JP, Weinhold K, et al.  Conserved sequence and structural elements in the HIV-1 principal determinant. Science . 1990;;249:932-935.
31 +
Devash Y, Calvelli TA, Wood DG, Regan KJ, Rubinstein A.  Vertical transmission of human immunodeficiency virus is correlated with the absence of high-affinity/avidity maternal antibodies to the gp 120 principal neutralizing maternal antibodies to the gp 120 principal neutralizing domain. Proc Natl Acad Sci U S A . 1990;;87:3445-3449.
32 +
Homsy J, Meyer M, Levy JA.  Serum enhancement of human immunodeficiency virus (HIV) infection correlates with disease in HIV-infected individuals. J Virol . 1990;;64:1437-1440.
33 +
Evans LA, McHugh TM, Stites DP, Levy JA.  Differential ability of human immunodeficiency virus isolates to productively infect human cells. J Immunol . 1987;;138:3415-3418.
34 +
Lewis SH, Reynolds-Kohler C, Fox HE, Nelson JA.  HIV-1 in trophoblastic and villous Hofbauer cells, and haematological precursors in eight-week foetuses. Lancet . 1990;;335:565-568.
35 +
Kesson AM, Fear WR, Kazazi F, et al.  Human immunodeficiency virus type 1 infection of human placental macrophages in vitro. J Infect Dis . 1993;; 168:571-579.
36 +
Valentin A, Albert J, Fenyo EM, Asjö B.  HIV-1 infection of normal human macrophage cultures: implication for silent infection. Virology . 1990;;177: 790-794.
37 +
Cheng-Mayer C, Seto D, Tateno M, Levy JA.  Biologic features of HIV that correlate with virulence in the host. Science . 1988;;240:80-82.
38 +
Broliden PA, Moschese V, Ljunggren K, et al.  Diagnostic implication of specific immunoglobulin G patterns of children born to HIV-infected mothers. AIDS . 1989;;3:577-582.
39 +
Cheng-Mayer C, Homsy J, Evans LA, Levy JA.  Identification of HIV subtypes with distinct patterns of sensitivity to serum neutralization. Proc Natl Acad Sci U S A . 1988;;85:2815-2819.
40 +
Scarlatti G, Hodara V, Rossi P, et al.  Transmission of human immunodeficiency virus type 1 (HIV-1) from mother to child correlates with viral phenotype. Virology . 1993;;197:624-629.
41 +
Asjö B, Albert J, Karlsson A, et al.  Replicative properties of human immunodeficiency virus from patients with varying severity of HIV infection. Lancet . 1986;;2:660-662.
42 +
Tersmette M, Lange JMA, De Goede REY, et al.  Association between biological properties of human immunodeficiency virus variants and risk for AIDS and AIDS mortality. Lancet . 1989;;1:983-985.
43 +
Parekh BS, Shaffer N, Pau C-P, et al.  Lack of correlation between maternal antibodies to V3 loop peptides of gp 120 and perinatal HIV-1 transmission. AIDS . 1991;;5:1179-1184.
44 +
Halsey NA, Markham R, Wahren B, Boulos R, Rossi P, Wigzell H.  Lack of association between antibodies to V3 loop peptides and maternal-infant HIV-1 transmission. J Acquir Immune Defic Syndr . 1992;;5:153-157.
45 +
Scarlatti G, Leitner T, Halapi E, et al.  Comparisons of variable region 3 sequences of human immunodeficiency virus type 1 from infected children with the RNA and DNA sequences of the virus populations of their mothers. Proc Natl Acad Sci U S A . 1993;;90:1721-1725.
46 +
Kliks SC, Shioda T, Haigwood NL, Levy JA.  V3 variability can influence the ability of an antibody to neutralize or enhance infection by diverse HIV-1 strains. Proc Natl Acad Sci U S A . 1993;; 90:11518-11522.
47 +
Gorny MK, Conley AJ, Karwowska S, et al.  Neutralization of diverse human immunodeficiency virus type 1 variants by an anti-V3 human monoclonal antibody. J Virol . 1992;;66:7538-7542.
48 +
Moore J.  The reactivities of HIV-1+ human sera with solid phase V3 loop peptides can be poor predictor of their reactivities with V3 loop on native gp 120 molecules. AIDS Res Hum Retroviruses . 1993;;9:209-219.
49 +
Shioda T, Levy JA, Cheng-Mayer C.  Macrophage and T cell line tropisms of HIV-1 are determined by specific regions of the envelope gp 120 gene. Nature . 1991;;349:167-169.
50 +
Tuofu Z, Mo H, Wang N, et al.  Genotypic and phenotypic characterization of HIV-1 in patients with primary infection. Science . 1993;;261:1179-1181.
51 +
Wolinsky SM, Wike CM, Korber BTM, et al.  Selective transmission of human immunodeficiency virus type 1 variants from mothers to infants. Science . 1992;;255:1134-1137.
52 +
Markham RB, Coberly J, Ruff AJ, et al.  Maternal IgG1 and IgA antibody to V3 loop consensus sequence and maternal-infant HIV-1 transmission. Lancet . 1994;;343:390-391.
53 +
Lallemant M, Baillou A, Lallemant-Le Coeur S, et al.  Maternal antibody response at delivery and perinatal transmission of human immunodeficiency viri type 1 in African women. Lancet . 1994;;343: 1001-1005.

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Country-Specific Mortality and Growth Failure in Infancy and Yound Children and Association With Material Stature

Use interactive graphics and maps to view and sort country-specific infant and early dhildhood mortality and growth failure data and their association with maternal

1 +
Chu SY, Buchler JW, Oxtoby MJ, Kilbourne BW.  Impact of the human immunodeficiency virus epidemic on mortality in children, United States. Pediatrics . 1991;;87:806-810.
2 +
Chin J.  Current and future dimensions of the HIV/AIDS pandemic in women and children. Lancet . 1990;;336:221-224.
3 +
Gwinn M, Pappaioanou M, George JR, et al.  Prevalence of HIV infection in childbearing women in the United States: surveillance using newborn blood samples. JAMA . 1991;;265:1704-1708.
4 +
Ryder RW, Nsa W, Hassig SE, et al.  Perinatal transmission of the human immunodeficiency virus type 1 to infants of seropositive women in Zaire. N Engl J Med . 1989;;320:1637-1642.
5 +
Mok JYQ, Hague RA, Yap PL, et al.  Vertical transmission of HIV: a prospective study. Arch Dis Child . 1989;;64:1140-1145.
6 +
European Collaborative Study.  Children born to women with HIV-1 infection: natural history and risk of transmission. Lancet . 1991;;337:253-260.
7 +
Lyman MD, Kress Y, Kure K, Rashbaum WK, Rubinstein A, Soeiro R.  Detection of HIV in fetal central nervous system tissue. AIDS . 1990;;4:917-920.
8 +
Courgnaud V, Laure F, Brossard A, et al.  Frequent and early in utero HIV-1 infection. AIDS Res Hum Retroviruses . 1991;;7:337-341.
9 +
Goedert JJ, Duliege A-M, Amos CI, Felton S, Biggar RJ.  International registry of HIV-exposed twins. Lancet . 1991;;338:1471-1475.
10 +
European Collaborative Study.  Risk factors for mother-to-child transmission of HIV-1. Lancet . 1992;; 339:1007-1012.
11 +
Ziegler JB, Cooper DA, Johnson RO, Gold J.  Postnatal transmission of AIDS—associated retrovirus from mother to infant. Lancet . 1985;;1:896-898.
12 +
Stiehm ER, Vink P.  Transmission of human immunodeficiency virus infection by breast feeding. J Pediatr . 1991;;118:410-412.
13 +
Rossi P.  Report of a Consensus Workshop, Siena, Italy, 1992: maternal factors involved in mother-to-child transmission of HIV-1. J Acquir Immune Defic Syndr . 1992;;5:1169-1178.
14 +
Goedert JJ, Drummond JE, Minkoff HL, et al.  Mother-to-infant transmission of human immunodeficiency virus type 1: association with prematurity or low anti-gp 120. Lancet . 1989;;2:1351-1354.
15 +
Rossi P, Moschese V, Broliden PA, et al.  Presence of maternal antibodies to human immunodeficiency virus type 1 envelope glycoprotein gp 120 epitopes correlates with the uninfected status of children born to seropositive mothers. Proc Natl Acad Sci U S A . 1989;;86:8055-8058.
16 +
Ugen KE, Goedert JJ, Boyer J, et al.  Vertical transmission of human immunodeficiency virus (HIV) infection. J Clin Invest . 1992;;89:1923-1930.
17 +
Williams-Herman D, Wara D, Levy JA, et al. Risk factors for perinatal HIV-1 transmission. Proceedings of the Ninth International Conference on AIDS; June 6-11,1993; Berlin, Germany;1:313. Abstract PO-B05-1064.
18 +
Centers for Disease Control.  Classification system for human immunodeficiency virus (HIV) in children under 13 years of age. MMWR Morb Mortal Wkly Rep . 1987;;36:225-230.
19 +
Centers for Disease Control.  Revision of the CDC surveillance case definition for acquired immunodeficiency syndrome. MMWR Morb Mortal Wkly Rep . 1987;;36:35-155.
20 +
Castro BA, Weiss CD, Wiviott LD, Levy JA.  Optimal conditions for recovery of the human immunodeficiency virus from peripheral blood mononuclear cells. J Clin Microbiol . 1988;;26:2371-2376.
21 +
Hoffman AD, Banapour B, Levy JA.  Characterization of the AIDS-associated retrovirus reverse transcriptase and optimal conditions for its detection in virions. Virology . 1985;;147:326-335.
22 +
McDougal JS, Cort SP, Kennedy MS.  Immunoassay for the detection and quantitation of infectious human retrovirus, lymphadenopathy-associated virus (LAV). J Immunol Methods . 1985;;76: 171-183.
23 +
Levy JA, Hoffman AD, Kramer SM, Landis JA, Shimabukuro JM, Oshiro LS.  Isolation of lymphocytopathic retroviruses from San Francisco patients with AIDS. Science . 1984;;225:840-842.
24 +
Tateno M, Levy JA.  MT-4 plaque formation can distinguish cytopathic subtypes of the human immunodeficiency virus (HIV). Virology . 1988;;167:209-301.
25 +
Cheng-Mayer C, Weiss CD, Seto D, Levy JA.  Isolates of human immunodeficiency virus type 1 from the brain may constitute a special group of the AIDS virus. Proc Natl Acad Sci U S A . 1989;;80: 8575-8579.
26 +
Homsy J, Tateno M, Levy JA.  Antibody-dependent enhancement of HIV infection. Lancet . 1988;; 1:1285-1286.
27 +
Koot M, Vos AHV, Keet RPM, et al.  HIV-1 biological phenotype in long-term infected individuals evaluated with an MT-2 cocultivation assay. AIDS . 1992;;6:49-54.
28 +
Pan L-Z, Cheng-Mayer C, Levy JA.  Patterns of antibody response in individuals infected with the human immunodeficiency virus. J Infect Dis . 1987;; 155:626-632.
29 +
Sakamoto D, Baenzinger J, Sinangil F, Lee D, Turck C, Steimer K.  An improved method for assessing antibody responses to the principal neutralizing determinant (PND) of HIV-1 gp 120. J Cell Biochem Suppl . 1993;;17E:85.
30 +
La Rosa GJ, Davide JP, Weinhold K, et al.  Conserved sequence and structural elements in the HIV-1 principal determinant. Science . 1990;;249:932-935.
31 +
Devash Y, Calvelli TA, Wood DG, Regan KJ, Rubinstein A.  Vertical transmission of human immunodeficiency virus is correlated with the absence of high-affinity/avidity maternal antibodies to the gp 120 principal neutralizing maternal antibodies to the gp 120 principal neutralizing domain. Proc Natl Acad Sci U S A . 1990;;87:3445-3449.
32 +
Homsy J, Meyer M, Levy JA.  Serum enhancement of human immunodeficiency virus (HIV) infection correlates with disease in HIV-infected individuals. J Virol . 1990;;64:1437-1440.
33 +
Evans LA, McHugh TM, Stites DP, Levy JA.  Differential ability of human immunodeficiency virus isolates to productively infect human cells. J Immunol . 1987;;138:3415-3418.
34 +
Lewis SH, Reynolds-Kohler C, Fox HE, Nelson JA.  HIV-1 in trophoblastic and villous Hofbauer cells, and haematological precursors in eight-week foetuses. Lancet . 1990;;335:565-568.
35 +
Kesson AM, Fear WR, Kazazi F, et al.  Human immunodeficiency virus type 1 infection of human placental macrophages in vitro. J Infect Dis . 1993;; 168:571-579.
36 +
Valentin A, Albert J, Fenyo EM, Asjö B.  HIV-1 infection of normal human macrophage cultures: implication for silent infection. Virology . 1990;;177: 790-794.
37 +
Cheng-Mayer C, Seto D, Tateno M, Levy JA.  Biologic features of HIV that correlate with virulence in the host. Science . 1988;;240:80-82.
38 +
Broliden PA, Moschese V, Ljunggren K, et al.  Diagnostic implication of specific immunoglobulin G patterns of children born to HIV-infected mothers. AIDS . 1989;;3:577-582.
39 +
Cheng-Mayer C, Homsy J, Evans LA, Levy JA.  Identification of HIV subtypes with distinct patterns of sensitivity to serum neutralization. Proc Natl Acad Sci U S A . 1988;;85:2815-2819.
40 +
Scarlatti G, Hodara V, Rossi P, et al.  Transmission of human immunodeficiency virus type 1 (HIV-1) from mother to child correlates with viral phenotype. Virology . 1993;;197:624-629.
41 +
Asjö B, Albert J, Karlsson A, et al.  Replicative properties of human immunodeficiency virus from patients with varying severity of HIV infection. Lancet . 1986;;2:660-662.
42 +
Tersmette M, Lange JMA, De Goede REY, et al.  Association between biological properties of human immunodeficiency virus variants and risk for AIDS and AIDS mortality. Lancet . 1989;;1:983-985.
43 +
Parekh BS, Shaffer N, Pau C-P, et al.  Lack of correlation between maternal antibodies to V3 loop peptides of gp 120 and perinatal HIV-1 transmission. AIDS . 1991;;5:1179-1184.
44 +
Halsey NA, Markham R, Wahren B, Boulos R, Rossi P, Wigzell H.  Lack of association between antibodies to V3 loop peptides and maternal-infant HIV-1 transmission. J Acquir Immune Defic Syndr . 1992;;5:153-157.
45 +
Scarlatti G, Leitner T, Halapi E, et al.  Comparisons of variable region 3 sequences of human immunodeficiency virus type 1 from infected children with the RNA and DNA sequences of the virus populations of their mothers. Proc Natl Acad Sci U S A . 1993;;90:1721-1725.
46 +
Kliks SC, Shioda T, Haigwood NL, Levy JA.  V3 variability can influence the ability of an antibody to neutralize or enhance infection by diverse HIV-1 strains. Proc Natl Acad Sci U S A . 1993;; 90:11518-11522.
47 +
Gorny MK, Conley AJ, Karwowska S, et al.  Neutralization of diverse human immunodeficiency virus type 1 variants by an anti-V3 human monoclonal antibody. J Virol . 1992;;66:7538-7542.
48 +
Moore J.  The reactivities of HIV-1+ human sera with solid phase V3 loop peptides can be poor predictor of their reactivities with V3 loop on native gp 120 molecules. AIDS Res Hum Retroviruses . 1993;;9:209-219.
49 +
Shioda T, Levy JA, Cheng-Mayer C.  Macrophage and T cell line tropisms of HIV-1 are determined by specific regions of the envelope gp 120 gene. Nature . 1991;;349:167-169.
50 +
Tuofu Z, Mo H, Wang N, et al.  Genotypic and phenotypic characterization of HIV-1 in patients with primary infection. Science . 1993;;261:1179-1181.
51 +
Wolinsky SM, Wike CM, Korber BTM, et al.  Selective transmission of human immunodeficiency virus type 1 variants from mothers to infants. Science . 1992;;255:1134-1137.
52 +
Markham RB, Coberly J, Ruff AJ, et al.  Maternal IgG1 and IgA antibody to V3 loop consensus sequence and maternal-infant HIV-1 transmission. Lancet . 1994;;343:390-391.
53 +
Lallemant M, Baillou A, Lallemant-Le Coeur S, et al.  Maternal antibody response at delivery and perinatal transmission of human immunodeficiency viri type 1 in African women. Lancet . 1994;;343: 1001-1005.

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