Original Article
Postnatal Transmission of Human Immunodeficiency Virus Type 1 from Mother to Infant — A Prospective Cohort Study in Kigali, Rwanda
N Engl J Med 1991; 325:593-598August 29, 1991
- Abstract
- Abstract
Background.
Although transmission of human immunodeficiency virus type 1 (HIV-1 ) from mother to infant has been well documented during pregnancy and delivery, little is known about the possible transmission of HIV-1 during the postnatal period.
Methods.
We conducted a prospective cohort study in Kigali, Rwanda, of 212 mother—infant pairs who were seronegative for HIV-1 at delivery. All the infants were breast-fed. The subjects were followed at three-month intervals, with Western blot assays for antibodies to HIV-1 and testing of mononuclear cells by a double polymerase chain reaction (PCR) using three sets of primers. To evaluate potential risk factors, each mother who seroconverted was matched with three seronegative control women.
Results.
After a mean follow-up of 16.6 months, 16 of the 212 mothers became seropositive for HIV-1. Of their 16 infants, 9 became seropositive. One infant was excluded from the analysis because of a positive test by PCR on the blood sample obtained at birth. Postnatal seroconversion to HIV-1 occurred in four of the five infants born to the mothers who seroconverted during the first 3 months post partum, and in four infants of the 10 mothers who seroconverted between month 4 and month 21. In all cases, the infant seroconverted during the same three-month period as the mother. The main risk factor for maternal seroconversion was being single.
Conclusions.
HIV-1 infection can be transmitted from mothers to infants during the postnatal period. Colostrum and breast milk may be efficient routes for the transmission of HIV-1 from recently infected mothers to their infants. (N Engl J Med 1991; 325:593–8.)
Article Activity
- Article
IT is generally thought that mother-to-infant transmission of human immunodeficiency virus type 1 (HIV-1) takes place during pregnancy or delivery. Several studies performed in Africa and in the Western world have confirmed this hypothesis and have estimated that the rate of such transmission ranges from 10 to 52 percent.1 Case reports suggest the existence of postnatal mother-to-infant transmission of HIV-1, probably through breast-feeding.2 Nevertheless, this mode of transmission is generally regarded as extremely rare, associated with unusual circumstances involving contamination of the mother, such as the transfusion of infected blood during or after delivery. We report the results of an ongoing prospective cohort study in Kigali, Rwanda, in which we evaluated the frequency of and risk factors for maternal postpartum HIV-1 seroconversion and postnatal transmission of the virus from mothers to their infants.
Methods
Selection of Subjects and Follow-up
Since November 1988, a prospective cohort study of the perinatal transmission of HIV-1 has been under way in Kigali, the capital city of Rwanda. All women delivering at the maternity ward of the Centre Hospitalier de Kigali were informed by social workers of the objectives, constraints, and advantages of the study. The mothers and their newborns were eligible for the study if they fulfilled the following criteria for inclusion: residence for at least six months in a district less than 10 km from the Centre Hospitalier de Kigali, delivery of one or more live newborns, and verbal informed consent to be enrolled in the cohort.
Each newborn of an enrolled HIV-1—seropositive mother was matched with a newborn of an HIV-1—seronegative mother of the same age (within a range of two years) and parity (with one more pregnancy or one fewer) who delivered during the same period. Details of the enrollment procedures are given elsewhere.3 We focus here on the results among the mother—infant pairs who were initially seronegative.
After the mother's delivery, each enrolled family was visited every two weeks by a social worker who collected information on the children's health status by means of a standardized questionnaire. The children and their mothers were examined systematically by a physician every three months, and their clinical status was evaluated according to the World Health Organization (WHO) clinical case definition of the acquired immunodeficiency syndrome (AIDS) in adults and children.4 When necessary, children were seen in the outpatient department or hospitalized in the department of pediatrics of the Centre Hospitalier de Kigali, and were treated free of charge. All medical injections were performed under conditions of strict asepsis, with single-use needles and syringes. The physicians and social workers involved in the follow-up were blinded to the HIV-1 serologic status of the mothers and infants. Since the results of the serologic tests and the polymerase chain reaction (PCR) were available only at the end of the follow-up period, no counseling about feeding practices could be given during the study to the seroconverting mothers.
Selection of Subjects for the Nested Case–Control Study
Three repeatedly seronegative mothers were matched for age (within a range of two years) and parity (with one more pregnancy or one fewer) to each mother who seroconverted during the follow-up period. A standardized questionnaire was administered blindly to the women who seroconverted and the controls to identify potential risk factors for seroconversion in the mothers and for the postnatal acquisition of HIV-1 in their infants.
Serologic and Immunologic Methods
At delivery, 10 ml of blood was obtained from the mother and from the umbilical cord for the detection of HIV-1 antibodies. All serum samples were screened by a commercial enzyme immunoassay (Vironostika, Organon Teknika, Boxtel, the Netherlands). When serum samples were positive on enzyme immunoassay, the findings were confirmed by a commercial Western blot technique (Du Pont de Nemours, Wilmington, Del.) in which a reaction was defined as positive when it showed at least three bands, one from each gene-product group: gag, pol, and env. 5 At each three-month visit to the hospital, 5 ml of blood was obtained from the mothers and the infants for HIV-1 enzyme immunoassay. In the event of seroconversion, Western blotting was performed retrospectively on all stored samples from the mother and the infant and prospectively on every sample, regardless of the results on the next enzyme immunoassay. A blood sample was obtained from the mother two weeks after delivery. Mononuclear-cell subpopulations were quantified with an indirect immunofluorescence technique and monoclonal antibodies: OKT4 for helper—inducer T cells (T4) and OKT8 for suppressor—cytotoxic T cells (T8) (Ortho Diagnostic Systems, Raritan, N.J.). A T4/T8 ratio of less than 1 was considered to be the criterion for impaired cellular immunity.6
PCR
Five to 10 ml of cord blood and, when possible, blood obtained from infants at each three-month visit was collected into EDTA (10 percent). Peripheral-blood mononuclear cells were separated over a 5.6 percent Ficoll gradient and 9.6 percent metrizoate sodium (Lymphoprep, Nycomed AS, Oslo, Norway). The cells were washed twice in Coons solution containing 1 percent serum bovine albumin, and the cell pellets were stored at — 70°C. DNA from the pellets was extracted in lysis buffer (10 mM TRIS, 5 M sodium chloride, and 0.5 M EDTA) containing 0.5 percent sarcosyl and 0.2 mg of proteinase K per milliliter, followed by extraction with phenol (twice) and chloroform (once) before precipitation in absolute ethanol and direct collection of DNA with a Pasteur pipette. After resuspension in distilled water, DNA was quantified by 260-nm light absorption and used for PCR.
A double PCR7 was performed with three pairs of HIV-1—specific oligonucleotide primers (Eurogentec, Liege, Belgium). The amplified sequences were located in the gag, pol, and env regions of the HIV-1 genome (Table 1Table 1
Sequences and Locations of Oligonucleotide Primers in the HIV-1 Genome.*). All PCR tests were done in duplicate in Rwanda and confirmed at the University of Liege, Belgium. In the first amplification, 1 μg of target DNA was mixed with 50 μl of reaction buffer (100 mM TRIS–hydrochloric acid [pH 8.3], 500 mM potassium chloride, and 1.5 mM magnesium chloride), 200 μM of each of the deoxynucleoside triphosphates (ATP, CTP, TTP, and GTP), 2 U of Taq polymerase (Perkin—Elmer Cetus, Norwalk, Conn.) per 50 μ, and 1 μM of primers. Amplification of target DNA was carried out by 40 cycles in a Cetus DNA thermal cycler (Perkin—Elmer Cetus). In this procedure, DNA samples were heated to 94°C for 36 seconds (for denaturation of DNA), cooled to 50°C for 42 seconds (for annealing to primers), and incubated for 3 minutes at 68°C (for amplification). For each primer used, the buffer concentration of magnesium chloride had to be optimized. In the second amplification, 1 μg of the primary amplified DNA was amplified in 20 μl of the reaction mixture, and the same program as described above was carried out with a second pair of primers located within the region amplified initially. Five to 10 μl of the second PCR mixture was analyzed by electrophoresis on a 4 percent low-melting-point agarose gel (SeaKem GTG, 1 percent, and Nu-Sieve GTG, 3 percent) containing ethidium bromide. Amplified DNA was visualized by ultraviolet fluorescence and fixed on instant photographs. A PCR test was considered positive when there was a detectable signal for at least two of the three primer pairs.Definition of Postnatal HIV-1 Infection
In an infant or child with HIV-l seroconversion after an earlier negative PCR result, postnatal HIV-1 infection was considered possible if seroconversion occurred in the first three months of life and proved if seroconversion occurred after that time.
Statistical Analysis
The chi-square test, the two-tailed Fisher's exact test, the Mann—Whitney U test, and the Kruskal—Wallis test were used for comparisons with a significance level of 0.05. Odds ratios were computed to measure the strength of the association when appropriate, and their 95 percent confidence intervals were computed according to the Cornfield method. Exact confidence limits of rates were also calculated when necessary.
Results
HIV-1 Seroconversion in the Mothers
Two hundred nineteen infants born to 217 HIV-1—seronegative mothers were enrolled. During the first three months, one mother and four infants (five pairs) died of non-HIV-related causes, and two mother—infant pairs were lost to follow-up. The mean follow-up period for the remaining 212 mother—infant pairs was 16.6 months, for a total of 3639 months of observation (range, 3 to 24 months per pair). Postpartum HIV-1 seroconversion was demonstrated in 16 of 210 mothers. The timing of these seroconversions is shown in Table 2Table 2
Incidence of HIV-1 Seroconversion, According to Time from Delivery or Birth, in 212 Pairs of Mothers and Infants Studied in Kigali, Rwanda, 1988 to 1990.. The incidence of seroconversion in the mothers was 3.4 percent in the first six months post partum (95 percent confidence interval, 0.9 to 5.9 percent), 2.6 percent in the second six months (95 percent confidence interval, 0.3 to 4.9 percent), and 2.6 percent in the third six months (95 percent confidence interval, 0.1 to 5.1 percent), respectively. Blood counts of the subpopulations of circulating mononuclear cells 15 days post partum were available for 15 of the 16 mothers who seroconverted. The OKT4/OKT8 ratio was reversed in three of them, in each instance because of a relative increase in the CD8 + subpopulation. At the most recent check-up whose results were available for study, 9 of the 16 mothers who seroconverted were completely asymptomatic, 4 had generalized lymphadenopathy, 2 had generalized lymphadenopathy and chronic dermatitis, and 1 had generalized lymphadenopathy and oral candidiasis.Table 3Table 3
Potential Risk Factors for HIV-1 Infection in Mothers Who Seroconverted (Cases) and Controls, Kigali, Rwanda, 1988 to 1990.* shows the results of the investigation of potential risk factors for HIV-1 seroconversion in the 16 seroconverting mothers and the 48 age- and parity-matched controls. The women who seroconverted were less likely than the controls to be legally married or involved in common-law unions (9 of 16 vs. 45 of 48; P = 0.001 by two-tailed Fisher's exact test). They also remained sexually abstinent longer after delivery (median, 7 vs. 2 weeks; P = 0.005 by the Mann—Whitney U test). In contrast, the 16 women who seroconverted did not differ significantly from the controls in having a history of genital infections or potential parenteral contact with HIV-1—contaminated blood (Table 3).HIV-1 Infection in Infants
HIV-1 seroconversion was observed in 9 of the 16 infants (8 male and 1 female) of the mothers who seroconverted. No infant had HIV-1 seroconversion unaccompanied by seroconversion of the mother. All the infants seroconverted during the same three-month period in which their mothers were observed to have seroconverted.
For all the infants of seroconverting mothers, a double PCR was performed with the mononuclear cells obtained before seroconversion. One of the infants (Subject 6) had a PCR test at birth that was positive for all three HIV-1 primer pairs and positive results on two other sequential samples (Fig. 1Figure 1
Detection of HIV-1 Sequences by Two-Stage PCR in Cord Blood and Peripheral-Blood Mononuclear Cells of Infants. and 2Figure 2
Sequential Results of HIV Serologic Tests and PCR in 16 Infants Born to Mothers Who Seroconverted.). At 21 months of age, this infant had pulmonary tuberculosis, delayed psychomotor development, and generalized lymphadenopathy. He was then excluded from the analysis of postnatal transmission. The other 15 babies tested had a negative PCR at birth, just before seroconversion, or both (Fig. 2). Therefore, it was concluded that four infants who seroconverted during the first three months of life had possibly acquired their HIV-1 infections postnatally from their seroconverting mothers (Subjects 1,2,3, and 5) and that four infants who seroconverted between months 4 and 21 (Subjects 7, 10, 15, and 16) had proved postnatally acquired infections. Double PCR also confirmed HIV-1 infection in five infants (13 samples) for whom mononuclear cells were available for analysis after the appearance of HIV-1 antibodies. By contrast, 17 samples from seven infants who did not seroconvert remained PCR-negative.Table 2 shows the timing of HIV-1 seroconversion in the eight infants with postnatal seroconversion. Postnatal HIV-1 seroconversion occurred in 4 of the 5 infants of mothers who seroconverted during the first postpartum trimester, as compared with 4 of the 10 who seroconverted later (P = 0.28 by two-tailed Fisher's exact test).
As compared with the uninfected infants born to mothers who seroconverted, the infants who seroconverted did not differ in birth weight, gestational age, or nutritional status at the time of the mother's seroconversion. At the end of follow-up, 7 of 8 infected infants had at least one sign or symptom from the WHO clinical case definition of pediatric AIDS, as compared with 2 of 7 uninfected infants born to mothers who seroconverted and 12 of 45 seronegative controls born of mothers who did not seroconvert (chi-square = 11.19, 2 df; P = 0.003). One of the seroconverting infants (Subject 3) died at 12 months of age with signs and symptoms fulfilling the criteria of the WHO clinical definition of pediatric AIDS and severe cerebral malaria.
Table 4Table 4
Potential Risk Factors for Postnatal Transmission of HIV-1 from Mother to Infant, According to Infant's Infection Status and Mother's Seroconversion Status. shows the potential risk factors for postnatal mother-to-infant transmission of HIV-1 during the case–control study. All subjects except one (who did not seroconvert) and all controls were breast-fed during the entire follow-up period. There was no difference between the three groups with respect to potential exposure to contaminated blood from injections. There was neither reported exposure to blood given in transfusion nor evidence of swallowing of infected blood from breast sores or abscesses. Reversed OKT4/OKT8 ratios at 15 days post partum were present in 3 of the 7 seroconverting mothers with infected infants, in none of the 7 tested mothers who seroconverted and had uninfected infants, and in 6 of the 45 seronegative controls (P not significant).Discussion
The incidence of HIV-1 seroconversion during the first postpartum year was 6.3 percent in the 210 mothers enrolled in this study (95 percent confidence interval, 2.8 to 9.8 percent) (data not shown). This rate is comparable to the annual incidence of 4.7 percent determined in Kigali during the same period in a cohort of 808 women with or without a recent pregnancy.8 In our cohort, the risk factors for seroconversion were separated, single, or widowed status and a long period of sexual abstinence post partum. In Rwanda, the traditional practice is to name a newborn eight days after birth, after which the parents generally resume regular sexual activity. The longer period of abstinence among the women who seroconverted probably reflected unstable sexual partnerships characterized by the absence of the father from the home at irregular intervals.
Our study shows that HIV-1 infection can be acquired postnatally by infants from seroconverting mothers. When the rate of this transmission is measured, an important factor should be taken into account: the difficulty of discriminating between late in utero or intrapartum transmission from postnatal transmission. Indeed, recent studies suggest that PCR performed with cord blood or the blood of an infant less than two months of age lacks sensitivity, because of the small number of viral copies present in peripheral blood early in life and the sequestration of virus in tissue macrophages and other sanctuaries.9 In an analysis of published studies in which the results for 173 infants of HIV-1—seropositive mothers were pooled, PCR performed before the age of one month identified only 55 percent of the truly infected infants.10 However, the nested PCR technique used in our study has already been shown to be particularly suitable for the diagnosis of HIV-1 infection in infants and to increase its sensitivity considerably. Using this technique, Williams and coworkers were able to diagnose correctly all infections among the infants in a cohort study of 55 infants born to HIV-1—seropositive mothers in Scotland.7 Supporting the idea of late in utero or intrapartum transmission of HIV-1 in our four early seroconverting infants is the fact that two of their mothers had reversed OKT4/OKT8 ratios 15 days post partum, suggesting infection at an earlier date. In summary, postnatal transmission of HIV-1 was ruled out in one infant (Subject 6), could be questioned in four (Subjects 1, 2, 3, and 5), but was proved in four (Subjects 7, 10, 15, and 16). Two extreme estimates of the rate of postnatal transmission of HIV-1 can be calculated from these observations. First, if one considers that all 4 infants with HIV-1 seroconversion during the first three months of life were infected either in late gestation or during the birthing process, the rate of postnatal transmission would be 4 of 11 (36 percent; 95 percent confidence interval, 10 to 72 percent). Second, if one considers that all 4 infants were infected postnatally, the rate of transmission would be 8 of 15 (53 percent; 95 percent confidence interval, 28 to 78 percent).
It should be emphasized that in all cases the infants acquired their postnatal HIV-1 infections during the same three months in which the mothers seroconverted. This suggests that the peak viremia associated with early HIV-1 infection11 enhances the risk of postnatal mother-to-infant transmission of HIV-1 or could even be a necessary condition for it. Thus, it is certainly not possible to extrapolate our estimate of the risk of such transmission of HIV-1 to situations in which the mothers had been infected before pregnancy.
The virtually simultaneous acquisition of HIV-1 by the mother and the infant could also be explained theoretically by infant-to-mother transmission of the virus. Such a possibility has already been suggested in a mother who apparently acquired HIV infection after long-term contact with blood and other body fluids from her child with AIDS.12 This explanation seems unlikely in our study, however, since the infected infants had no risk factors for HIV-1 infection other than being born to mothers seroconverting for HIV-1 and since none of the mothers were in regular contact with contaminated body fluids from severely ill infants. Also, in a nosocomial outbreak of HIV-1 infection involving 152 children and 12 mothers in Elista, Rostov-on-Don, and Volgograd, U.S.S.R., the only risk factor for infant-to-mother transmission of HIV-1 was the simultaneous presence of ulcerations in the infants' mouths and cracked nipples in the mothers.13 In our study, neither of these lesions was observed.
It appears that some infected infants in our study were indeed infected postnatally by their seroconverting mothers, the most plausible explanation being viral transmission through breast-feeding. HIV-1 has already been isolated from the cell-free breast milk of three infected women14 and from the colostrum of an HIV-1 carrier.15 Electron microscopy has demonstrated that HIV-1 is mostly associated with the cell fraction of milk and with histiocytes in particular.16 To date, only eight published case reports strongly indicate transmission of HIV-1 by breast-feeding.2 In seven of these, the transmission was the consequence of a postpartum infection of the mothers as a result of blood transfusion or intravenous drug use. In the remaining report, the virus was transmitted by a wet nurse with symptomatic HIV-1 infection. More recently, Hira and coworkers identified 3 infants with postnatal seroconversion at the age of 18 to 22 months, from a cohort of 1720 subjects followed incompletely (with a 56 percent dropout rate).17
As compared with mature milk, colostrum and early milk are rich in mononuclear cells, mainly macrophages, in concentrations of about 3.5 ×106 cells per milliliter.18 Mature milk contains cell concentrations that are only 1.5 to 2 percent of those found in colostrum.18 19 20 In another model of lentivirus infection — visna—maedi virus, or caprine arthritis encephalitis virus — lambs and kids are infected by the ingestion of infected colostral macrophages.21 In this prototype of lentiviral infection that is very similar to HIV-1, the simple withholding of colostrum can prevent postnatal transmission of the virus from infected sheep or goats.21 , 22 The human T-cell leukemia virus type 1, which is also primarily cell-associated, is transmitted to infants almost exclusively by infected cells during breast-feeding.23 It is highly conceivable that cell-to-cell contact has a crucial role in HIV-1 transmission in humans,24 particularly in neonates whose intestinal mucosa is still fragile or in the presence of achlorhydria. One can then anticipate that infants can acquire HIV-1 by swallowing infected colostral or milk cells in these specific conditions. However, massive ingestion of contaminated milk cells is certainly not a prerequisite for transmission. Indeed, two children (Subjects 15 and 16) acquired their HIV-1 infections from their mothers late in the lactation period — at 15 and 18 months of age, respectively. Our data suggest that HIV-1 can be transmitted by breast-feeding when mothers seroconvert at any time during lactation.
Our results have important public health implications for breast-feeding in the context of AIDS. Seronegative mothers at risk for HIV-1 infection should be counseled about the high risk of transmitting the virus to their children should they seroconvert. Moreover, when a safe alternative to breast-feeding is available, women at risk for seroconversion should refrain from breast-feeding their babies. The implications might be different when there is no safe alternative to breast-feeding, as is the case in many developing countries where feeding with formula is associated with unacceptably high morbidity and mortality due to diarrhea and pulmonary infections.25 , 26 In this context, further intervention studies should urgently evaluate the efficacy and feasibility of alternative nutritional practices, such as wet nursing, in women at risk of acquiring HIV-1 infection in the months after delivery.
Supported by the AIDS Task Force of the European Economic Community.
We are indebted to the Minister of Health of the Rwandan Republic, Dr. F. Nsengumuremyi, for his support in this study; to Dr. A. Bucyendore, director of the National AIDS Control Program, for constant encouragement; to Dr. L. Fransen (AIDS Task Force), Mr. F. Baan, Mr. F. Cardessa, Mr. J. Roman (European Economic Community delegation in Kigali), and Dr. P. Stoffels for their collaboration; to Professor J.P. Butzler, Professor A. Burny, Dr. S. Allen, Dr. J. Homsy, and Dr. E. Fox for advice and criticism; to the paramedical-staff members of the Mother-to-Child Transmission Study for their active collaboration; and to the nurses of the Pediatrics Department of the Centre Hospitalier de Kigali for their devoted and compassionate care of patients with AIDS.
Source Information
From the AIDS Reference Laboratory, National AIDS Control Program (P.V., A.S., E.K.), and the Department of Pediatrics, Centre Hospitalier (D.-G.H., A.B., C.V.G., A.-M.S., P.L.), both in Kigali, Rwanda; INSERM U 330, University of Bordeaux II, France (P.M., F.D.); and the Transfusion Center, University of Liege, Belgium (D.V., D.S.-T.). Address reprint requests to Dr. Van de Perre at the AIDS Reference Laboratory, National AIDS Control Program, BP 780, Kigali, Rwanda.
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