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Prospective Study of Measles in Hospitalized, Human Immunodeficiency Virus (HIV)—Infected and HIV—Uninfected Children in Zambia

  1. William J. Moss1,2⇓,
  2. Mwaka Monze4,
  3. Judith J. Ryon1,
  4. Thomas C. Quinn3,
  5. Diane E. Griffin1, and
  6. Felicity Cutts5
  1. 1W. Harry Feinstone Department of Molecular Microbiology and Immunology, Bloomberg School of Public Health, Bethesda, Maryland
  2. 2Department of International Health, Bloomberg School of Public Health, Bethesda, Maryland
  3. 3Division of Infectious Diseases, School of Medicine, Johns Hopkins University, Baltimore, and National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland
  4. 4Virology Laboratory, University Teaching Hospital, Lusaka, Zambia
  5. 5Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom
  1. Reprints or correspondence: Dr. William J. Moss, W. Harry Feinstone Dept. of Molecular Microbiology and Immunology, Bloomberg School of Public Health, Johns Hopkins University, 615 North Wolfe St., Baltimore, MD 21205-2179 (wmoss{at}jhsph.edu).
 
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Abstract

Measles in persons coinfected with human immunodeficiency virus (HIV) has been reported to be unusual in its presentation and frequently fatal. To determine the effect of HIV coinfection on the clinical features and outcome of measles, a prospective study of hospitalized children with measles was conducted between January 1998 and October 2000 in Lusaka, Zambia. One-sixth (17%) of 546 children hospitalized with laboratory-confirmed measles were coinfected with HIV. One-third of the HIV-infected children hospitalized with confirmed measles were <9 months old, compared with 23% of HIV-uninfected children (P = .03). Few differences in clinical manifestations, complications, or mortality were found between HIV-infected and HIV-uninfected children with measles. HIV-infected children constitute a significant proportion of children hospitalized with measles in countries with high HIV prevalence and are more likely to be younger than the age for routine measles immunization.

Measles continues to be a major cause of child morbidity and mortality, particularly in countries in sub-Saharan Africa [1]. In central and eastern Africa, many countries have both a high prevalence of HIV infection and a high incidence of measles. Measles in persons coinfected with HIV has been reported to be unusual in its presentation and frequently fatal [2–9]. Nine of the 19 HIV-infected children with measles reported from the United States had no rash or a rash uncharacteristic of measles, and almost one-third died during the acute illness, most commonly of giant cell pneumonia [10]. The published literature on the clinical features of measles in HIV-infected children and adults residing in industrialized countries, however, consists largely of case reports and case series that may be biased toward severe and atypical presentations.

Few studies have investigated measles morbidity and mortality in HIV-infected children in sub-Saharan Africa, where both infections are endemic. In Zaire (now the Democratic Republic of Congo), the case-fatality rates among HIV-seropositive and HIV-seronegative children hospitalized with measles were similar (31% vs. 28%) [11]. In Zambia, the measles case-fatality rate among HIV-seropositive children aged 9–59 months was significantly higher (28%) than among HIV-seronegative children (8.3%) [12]. These studies did not distinguish HIV-infected from HIV-seropositive children and did not assess the clinical manifestations of measles. We describe the clinical features and outcome of measles in hospitalized HIV-infected and HIV-uninfected children in Zambia.

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Methods

Subjects. Children hospitalized with the clinical diagnosis of measles at the University Teaching Hospital, Lusaka, Zambia, between January 1998 and October 2000 were prospectively enrolled. The University Teaching Hospital is the largest public hospital in Lusaka, and most children who receive a diagnosis of measles in Lusaka are referred to this hospital. Children were usually enrolled on the day after admission to the measles ward. Those who were severely ill or who died within hours of admission were unlikely to be enrolled. Written informed consent was obtained from the parents or guardians of the children studied. The research was done in accordance with the ethical standards of the institutional review boards at the Johns Hopkins University School of Public Health (Baltimore, Maryland), the London School of Hygiene and Tropical Medicine (United Kingdom), and the University Teaching Hospital (Lusaka, Zambia).

Clinical data collection. At enrollment, a study nurse or clinical officer administered a questionnaire and performed a physical examination. The questionnaire allowed for µ1 type of rash to be recorded per child. Clinical findings were recorded again at discharge from the hospital, and parents or guardians were requested to bring the child to the hospital for follow-up 1 month after discharge. Active tracing of children who failed to return after discharge was not done. Measles vaccine is routinely administered at 9 months of age in Zambia, and standard practice was to administer vitamin A to all children with measles.

Specimen collection and laboratory assays. Blood specimens were collected in EDTA tubes and transported to the laboratory. Aliquots of whole blood were removed for performance of WBC counts and monoclonal antibody staining for flow cytometry. WBC counts and differential WBC counts were done manually. Plasma was separated and stored in aliquots at ‒70°C for later measurement of antibodies to measles and HIV and for determination of levels of HIV RNA in plasma.

Measles virus infection was confirmed by detection of measles virus—specific IgM in plasma by EIA (Wampole Laboratories). Children were classified as having confirmed measles if measles virus—specific IgM was detected at any time point (i.e., at study entry, at hospital discharge, or at 1-month follow-up). Measles virus infection was excluded if measles virus—specific IgM was not detected in plasma obtained at ⩾2 time points. Children in whom measles was neither confirmed nor excluded were classified as having unconfirmed measles. Plasma was tested for antibody to HIV by EIA (Organon Teknika). Plasma samples positive for antibody to HIV by EIA were assayed for HIV RNA. Plasma levels of HIV RNA were quantified by use of a reverse-transcriptase—PCR assay (Amplicor HIV-1 Monitor version 1.5; Roche Molecular Systems). Children were classified as being HIV-infected if HIV RNA was detected in any plasma sample.

Whole blood was stained with directly labeled monoclonal antibodies to CD3, CD4, and CD8 antigens. After RBC lysis, flow cytometry was done on a FACScan flow cytometer with use of Cell Quest software (Becton Dickinson).

Weight-for-height and height-for-age Z scores were determined by use of Epi-Info 2000 software, version 1.0 (Centers for Disease Control and Prevention [CDC]), on the basis of growth reference curves recommended by the World Health Organization and developed by the National Center for Health Statistics and the CDC. “Wasting” was defined as a weight-for-height score ⩾2 SD less than the normal value, and “stunting” was defined as a height-for-age score ⩾2 SD less than the normal value.

Statistical analysis. Categorical variables were compared by the χ2 test. Logistic regression was used to assess interaction and to control for potential confounders. We were interested a priori in examining interactions between sex and HIV infection status [12] and between sex and measles vaccination [13]. We therefore included interaction terms for these variables, although, for some of the outcomes, the interaction was not statistically significant (i.e., P µ .05). Continuous variables were compared by the nonparametric Kruskal-Wallis test. No formal adjustment was made for multiple testing. Statistical analyses were done with Stata statistical software, release 6 (Stata).

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Results

Measles and HIV infection status. From January 1998 through October 2000, 655 hospitalized children with clinically diagnosed measles were enrolled, who comprised 27% of all children hospitalized with clinically diagnosed measles at the University Teaching Hospital. Measles virus infection was confirmed or excluded for 590 children, 552 (94%) of whom had detectable measles virus—specific IgM antibodies. The remaining 65 children lacked sufficient information to confirm or exclude measles virus infection. HIV infection status was determined for 546 children with confirmed measles, 93 (17%) of whom were coinfected with measles virus and HIV. Thirty-eight children tested negative for IgM antibody to measles virus on 2 occasions; 3 of these children were infected with HIV.

Age, sex, and measles vaccination status. The median age of HIV-infected children with measles was 10 months, compared with 15 months for HIV-uninfected children (P = .04). The proportion of HIV-infected children <9 months of age was 33%, compared with 23% of HIV-uninfected children (P = .03); the proportions of children <6 months of age in these 2 groups were 7.8% and 4%, respectively (P = .12) (table 1). Boys constituted 58% of HIV-infected children and 51% of HIV-uninfected children with measles (P = .24). Information on measles vaccination status was available for 89% of 372 children ⩾9 months old. The proportion with a reported or documented history of measles vaccination was higher among HIV-infected (60%) than HIV-uninfected (48%) children (P = .10).

Table 1
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Table 1

Clinical and demographic characteristics and reported clinical history before hospitalization for children in prospective study of measles in Zambia.

Clinical presentation of measles. HIV-infected children had a slightly longer duration of illness (median, 7 days) before hospitalization than did HIV-uninfected children (median, 6 days; P = .03). No significant differences were observed in the proportions of HIV-infected and HIV-uninfected children who had been treated before hospitalization with antibiotics (47% and 42%, respectively; P = .20) or vitamin A (17% and 19%, respectively; P = .95). The presence of at least 1 other concurrent case of measles in the patient's household was reported more frequently among households of HIV-uninfected children (20%) than among those of HIV-infected children (11%; P = .08).

Reported signs and symptoms of measles did not differ in frequency between HIV-infected and HIV-uninfected children at the time of hospitalization (table 1). However, fewer HIV-infected children had a history of conjunctivitis (P = .06) or diarrhea (P = .01), although these symptoms were reported in the majority of HIV-infected children. History of conjunctivitis (OR, 0.33; 95% CI, 0.11–0.95) and diarrhea (OR, 0.47; 95% CI, 0.26–0.83) remained inversely correlated with HIV infection after adjusting for age, sex, and measles vaccination status. On physical examination, conjunctivitis was observed at study entry in an equal proportion of HIV-infected and HIV-uninfected children (table 2).

Table 2
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Table 2

Clinical characteristics, complications, and outcome of measles during hospitalization in children in a prospective study of measles in Zambia.

Stunting was noted in almost one-half of all children (48%), but stunting was noted in a greater proportion of HIV-infected children than HIV-uninfected children (61% vs. 44%, P = .01) (table 2). Wasting was noted in 20% of HIV-infected children, compared with 10% of HIV-uninfected children (P = .005). The signs and symptoms of measles did not differ significantly between children in whom stunting or wasting was noted and children without these conditions, except that children with stunting were more likely to have had a desquamating than morbilliform rash at study entry (P = .02).

Complications of measles. HIV-infected children with measles were significantly more likely to have thrush but were no more likely than HIV-uninfected children to have diarrhea or pneumonia during hospitalization for measles (table 3). These findings changed little after adjusting for age, sex, and measles vaccination status, and there was no significant interaction between HIV infection and sex for these outcomes. Children not vaccinated against measles were more likely to have thrush, diarrhea, and/or pneumonia during acute measles than were vaccinated children, even after age, sex, and HIV infection status were adjusted for (table 3). The difference between unvaccinated and vaccinated children was significant for thrush, among boys; for diarrhea, among girls; and for pneumonia, among patients of both sexes.

Table 3
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Table 3

Factors that affected complications and outcome of measles among 546 hospitalized children with confirmed measles in Zambia.

The duration of hospitalization was longer for HIV-infected children (median, 3 days; interquartile range [IQR], 2–6 days) than for HIV-uninfected children (median, 3 days; IQR, 2–4 days; P = .0004), and the difference remained significant after adjusting for age, sex, and measles vaccination status (P < .0001; data not tabulated).

There were 23 deaths during hospitalization among the 546 children in the study who had confirmed measles and a known HIV infection status, corresponding to a case-fatality rate of 4.2%. The case-fatality rate for all children admitted to the hospital with clinically diagnosed measles during the study period, regardless of whether they were enrolled in the study, was 5.2%. Five HIV-infected children (5.4%) and 18 HIV-uninfected children (4.0%) died (P = .45) (table 2). In a logistic regression model that included interaction terms for sex and HIV infection status (P = .3) and sex and measles vaccination status (P = .04), the OR for death among HIV-infected children compared with death among HIV-uninfected children was 0.8 for girls and 3.2 for boys, but neither of these ORs was significantly different from unity (table 3). The risk of death was higher for girls than for boys; most of the difference was due to deaths of unvaccinated children, regardless of their HIV infection status (table 3). The risk of death was not higher for children in households with ⩾1 concurrent case of measles (data not shown).

Characteristics at follow-up. Two hundred twelve children with measles (39%), of whom 39 (18%) were HIV-infected, returned for follow-up a median of 39 days after onset of rash. Similar proportions of HIV-infected and HIV-uninfected children returned for follow-up (42% and 38%, respectively; P = .50). The median number of days from the onset of rash to follow-up was slightly greater for HIV-infected than HIV-uninfected children (40 and 38 days, respectively; P = .004). Reported history of signs and symptoms of intercurrent illness did not differ between the 2 groups of children, except that HIV-infected children were more likely to have a history of cough after hospital discharge (62% vs. 45%; P = .06) and to be given the diagnosis of pneumonia at the follow-up visit (10% vs. 3%; P = .04). The proportion of households reporting incident measles cases since hospital discharge of the study child did not differ between HIV-infected and HIV-uninfected children with measles (13% vs. 16%; P = .60).

Laboratory findings. CD4+ T lymphocyte counts and percentages were determined at enrollment for 50 HIV-infected and 278 HIV-uninfected children with measles (table 4). As expected, the median CD4+ T lymphocyte percentage was lower for HIV-infected children, and a greater proportion of HIV-infected children had a CD4+ T lymphocyte percentage of <25%. The CD4+ T lymphocyte percentages for 2 HIV-infected children with confirmed measles who died were 7% and 13%; the median CD4+ T lymphocyte percentage for 11 HIV-uninfected children with measles who died was 17.5% (range, 15%–59%).

Table 4
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Table 4

CD4+ T lymphocyte counts and percentages in HIV-infected and HIV-uninfected children with measles in Zambia.

Several differences between HIV-infected and HIV-uninfected children persisted or were more apparent after controlling for CD4+ T lymphocyte percentage (table 5). Among children with CD4+ T lymphocyte percentages of <25%, HIV-infected children were less likely to have a history of red eyes or diarrhea or to have conjunctivitis on physical examination. Almost all deaths occurred among children with CD4+ T lymphocyte percentages of <25%.

Table 5
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Table 5

Clinical characteristics, complications, and outcome of measles, stratified by CD4+ T lymphocyte percentage and HIV infection status, for a cohort of children in Zambia.

Analysis of all children hospitalized with clinically diagnosed measles. A higher proportion of HIV-infected children than of HIV-uninfected children had unconfirmed measles (18% vs. 6%; P = .0001). Overall, 33 (5%) of the 655 children enrolled in the study died, 11 of whom were HIV-infected. When all children with clinically diagnosed measles were included in the analysis (table 2), HIV-infected children had a higher fatality rate (9.4%) than did HIV-uninfected children (4.0%; P = .02). The 6 HIV-infected children with unconfirmed measles virus infection who died had undetectable levels of IgM antibody to measles virus in the single specimen available for testing, which was obtained a median of 3 days after the onset of rash (range, 2–4 days). CD4+ T lymphocyte counts at study entry for 2 of these 6 HIV-infected children were 45 and 152 cells/mm3. Only 3 of the children with unconfirmed measles who died were HIV-uninfected. These 3 children also had undetectable levels of IgM antibody to measles virus in a single specimen, and the CD4+ T lymphocyte counts for 2 of these 3 children were 323 and 464 cells/mm3. Differences between HIV-infected and HIV-uninfected children with respect to the clinical manifestations and complications of measles did not change substantially after inclusion of all children with clinically diagnosed measles, except with respect to the outcome “death” (tables 1 and 2).

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Discussion

One-sixth of children hospitalized with confirmed measles at the University Teaching Hospital, Lusaka, Zambia, were coinfected with HIV. This proportion is higher than expected for the general population of children in Lusaka (given an HIV seroprevalence of 25% among pregnant women and a maternal-infant transmission rate of 30%, a maximum prevalence of 7.5% would be expected, even if differential infant mortality is ignored), and this high proportion suggests that HIV-infected children are more likely than uninfected children to acquire severe measles and/or to require hospitalization for measles.

One-third of the HIV-infected children hospitalized with measles were <9 months of age (the age at which measles vaccine is routinely administered in Zambia), compared with 23% of HIV-uninfected children. This finding is consistent with the observation that placental transfer of maternal antibodies may be lower for HIV-infected women and that children born to HIV-infected women may be at greater risk of acquiring measles before they are 9 months of age [14–17]. The World Health Organization recommends that HIV-infected children receive 2 doses of measles vaccine at 6 and 9 months of age [18], although this recommendation has not, to our knowledge, been implemented in any country.

HIV-infected children are reported to have high rates of primary and secondary measles vaccine failure [10]. A higher proportion of HIV-infected children with measles had a history of measles vaccination, although the difference was not significant. We lack the information on vaccine coverage rates according to HIV status in the general population that is needed to estimate the effectiveness of the vaccine [19]; however, we would not expect a higher rate of vaccine coverage among HIV-infected than HIV-uninfected children in the general population, and our results, therefore, suggest an increased rate of vaccine failure among HIV-infected children.

Both the duration of illness before hospitalization and the duration of hospitalization were longer for HIV-infected children than for HIV-uninfected children, which suggests that disease is generally more severe in the former group, although specific complications such as diarrhea and pneumonia were not noted more frequently among HIV-infected children. However, our cohort consisted of children with signs that led to a clinical diagnosis of measles, which likely explains our failure to find major differences in clinical signs and symptoms between HIV-infected and HIV-uninfected children with measles. The distinguishing clinical features of measles, in particular the morbilliform rash, are manifestations of the host's cellular immune response to measles virus [20], and persons with impaired cellular immunity may lack the characteristic clinical signs of measles [8, 21–23]. The HIV-infected children with measles in our study, apparently, had levels of cellular immunity sufficient to manifest a morbilliform rash. When HIV-infected and HIV-uninfected children were stratified according to whether they had a CD4+ T lymphocyte percentage of <25%, several differences became apparent or more marked. These findings suggest that the clinical characteristics of measles are altered in the presence of more severe suppression of cellular immunity.

We were less likely to enroll critically ill children and children who died within hours of hospital admission than other hospitalized children with measles. The lower case-fatality rate among the study children, compared with all children admitted because of clinically diagnosed measles, suggests that the study cohort was biased toward children with less-severe illness. Despite the small number of deaths, the ratio of deaths among HIV-infected and deaths among HIV-uninfected children was similar to that in the previous study undertaken at the same hospital [12], which suggests that enrollment bias reduced the apparent severity of measles in both HIV-infected and HIV-uninfected children.

Six HIV-infected children died with a measles-like illness but had undetectable levels of IgM antibody to measles virus in a single plasma sample obtained at study entry. In the 2 children for whom data were available, CD4+ T lymphocyte counts were extremely low. These HIV-infected children may have had immunologic capacity sufficient to manifest signs and symptoms of measles but not sufficient to generate an early IgM antibody response or to prevent fatal infection. If HIV infection impairs antibody responses, then this standard diagnostic test for measles may lack sufficient sensitivity to be useful for efforts to control measles in regions of high HIV prevalence.

In countries with high HIV prevalence, HIV-infected children constitute a significant proportion of children hospitalized with measles. In contrast to the cases reported in the published literature, we found that many HIV-infected children develop the characteristic clinical features of measles, and most recover sufficiently from the acute illness to be discharged from the hospital. Because HIV-infected children with measles clear measles virus more slowly than do HIV-uninfected children [24], they may be important transmitters of measles virus and hinder measles elimination efforts.

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Acknowledgments

We thank N. P. Luo, L. Munkonkange, E. M. Chomba, Evans Mpabalwani, Gina Mulundu, and Francis Kasolo, for facilitating research at the Virology Laboratory and University Teaching Hospital in Zambia; laboratory and nursing staff in Zambia, for work with patient recruitment and sample processing; and the Japan International Cooperation Agency, for generously allowing the use of laboratory facilities.

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Footnotes

  • Financial support: National Institutes of Health (grant AI-23047); World Health Organization; Infectious Diseases Society of America (Wyeth-Lederle Vaccines and Pediatrics Young Investigator Award in Vaccine Development to W.J.M.).

  • Received October 23, 2001.
  • Revision received February 25, 2002.
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References

  1. ↵
    1. Centers for Disease Control and Prevention
    . Global measles control and regional elimination, 1998–1999. MMWR Morb Mortal Wkly Rep 1999;48:1124-30.
    Medline
  2. ↵
    1. Centers for Disease Control and Prevention
    . Measles in HIV-infected children, United States: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Morb Mortal Wkly Rep 1988;37:183-6.
    Medline
    1. Markowitz LE,
    2. Chandler FW,
    3. Roldan EO,
    4. et al
    . Fatal measles pneumonia without rash in a child with AIDS. J Infect Dis 1988;158:480-3.
    FREE Full Text
    1. Krasinski K,
    2. Borkowsky W
    . Measles and measles immunity in children infected with human immunodeficiency virus. JAMA 1989;261:2512-6.
    Abstract/FREE Full Text
    1. Nadel S,
    2. McGann K,
    3. Hodinka RL,
    4. Rutstein R,
    5. Chatten J
    . Measles giant cell pneumonia in a child with human immunodeficiency virus infection. Pediatr Infect Dis J 1991;10:542-4.
    MedlineWeb of Science
    1. Palumbo P,
    2. Hoyt L,
    3. Demasio K,
    4. Oleske J,
    5. Connor E
    . Population-based study of measles and measles immunization in human immunodeficiency virus-infected children. Pediatr Infect Dis J 1992;11:1008-14.
    MedlineWeb of Science
    1. Rudy BJ,
    2. Rutstein RM,
    3. Pinto-Martin J
    . Response to measles immunization in children infected with human immunodeficiency virus. J Pediatr 1994;125:72-4.
    CrossRefMedlineWeb of Science
  8. ↵
    1. Kaplan LJ,
    2. Daum RS,
    3. Smaron M,
    4. McCarthy CA
    . Severe measles in immunocompromised patients. JAMA 1992;267:1237-41.
    Abstract/FREE Full Text
  9. ↵
    1. Forni AL,
    2. Schluger NW,
    3. Roberts RB
    . Severe measles pneumonitis in adults: evaluation of clinical characteristics and therapy with intravenous ribavirin. Clin Infect Dis 1994;19:454-62.
    Abstract/FREE Full Text
  10. ↵
    1. Moss WJ,
    2. Cutts F,
    3. Griffin DE
    . Implications of the human immunodeficiency virus epidemic for control and eradication of measles. Clin Infect Dis 1999;29:106-12.
    Abstract/FREE Full Text
  11. ↵
    1. Sension MG,
    2. Quinn T,
    3. Markowitz LE,
    4. et al
    . Measles in hospitalized children infected with human immunodeficiency virus. Am J Dis Child 1988;142:1271-2.
    Abstract/FREE Full Text
  12. ↵
    1. Oshitani H,
    2. Suzuki H,
    3. Mpabalwani ME,
    4. Mizuta K,
    5. Numazaki Y
    . Measles case fatality by sex, vaccination status, and HIV-1 antibody in Zambian children. Lancet 1996;348:415.
    MedlineWeb of Science
  13. ↵
    1. Aaby P,
    2. Pedersen IR,
    3. Knudsen K,
    4. et al
    . Child mortality related to seroconversion or lack of seroconversion after measles vaccination. Pediatr Infect Dis J 1989;8:197-200.
    MedlineWeb of Science
  14. ↵
    1. Embree JE,
    2. Datta P,
    3. Stackiw W,
    4. et al
    . Increased risk of early measles in infants of human immunodeficiency virus type 1-seropositive mothers. J Infect Dis 1992;165:262-7.
    Abstract/FREE Full Text
    1. De Moraes-Pinto MI,
    2. Farhat CK,
    3. Carbonare SB,
    4. et al
    . Maternally acquired immunity in newborns from women infected by the human immunodeficiency virus. Acta Paediatr 1993;82:1034-8.
    MedlineWeb of Science
    1. De Moraes-Pinto MI,
    2. Almeida ACM,
    3. Kenj G,
    4. et al
    . Placental transfer and maternally acquired neonatal IgG immunity in human immunodeficiency virus infection. J Infect Dis 1996;173:1077-84.
    MedlineWeb of Science
  17. ↵
    1. Lepage P,
    2. Dabis F,
    3. Msellati P,
    4. Mukamabano B,
    5. Van Goethem C,
    6. Van de Perre P
    . Safety and immunogenicity of high-dose Edmonston-Zagreb measles vaccine in children with HIV-1 infection. A cohort study in Kigali, Rwanda. Am J Dis Child 1992;146:550-5.
  18. ↵
    1. global Programme on AIDS and Expanded Programme on Immunization, World Health Organization
    . Joint WHO/UNICEF statement on early immunization for HIV-infected children. Wkly Epidemiol Rec 1989;64:48-9.
  19. ↵
    1. Orenstein WA,
    2. Bernier RH,
    3. Dondero TJ,
    4. et al
    . Field evaluation of vaccine efficacy. Bull World Health Organ 1985;63:1055-68.
    MedlineWeb of Science
  20. ↵
    1. Griffin DE,
    2. Bellini WJ
    . Measles virus. Fields' virology Philadelphia, Lippincott: Raven; 1956:1627-312.
  21. ↵
    1. MacCarthy K,
    2. Mitus A,
    3. Cheatman W,
    4. Peebles T,
    5. Kibrick S
    . Isolation of virus of measles from three fatal cases of giant-cell pneumonia. Am J Dis Child 1956;96:500-1.
    1. Enders JF,
    2. McCarthy K,
    3. Mitus A,
    4. Cheatham WJ
    . Isolation of measles virus at autopsy in cases of giant-cell pneumonia without rash. N Engl J Med 1959;261:875-81.
    MedlineWeb of Science
  23. ↵
    1. de Swart RL,
    2. Wertheim-van Dillen PME,
    3. van Binnendijk RS,
    4. Muller CP,
    5. Frenkel J,
    6. Osterhaus ADME
    . Measles in a Dutch hospital introduced by an immunocompromised infant from Indonesia infected with a new virus genotype. Lancet 2000;355:201-2.
    CrossRefMedlineWeb of Science
  24. ↵
    1. Permar SR,
    2. Moss WJ,
    3. Ryon JJ,
    4. et al
    . Prolonged measles virus shedding in human immunodeficiency virus-infected children, detected by reverse transcriptase-polymerase chain reaction. J Infect Dis 2001;183:532-8.
    Abstract/FREE Full Text
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  1. Clin Infect Dis. (2002) 35 (2): 189-196. doi: 10.1086/341248
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