Replacement-Fed Infants Born to HIV-Infected Mothers in India Have a High Early Postpartum Rate of Hospitalization -- Phadke et al. 133 (10): 3153 -- Journal of Nutrition
QUICK SEARCH:
[advanced]
Author:
Keyword(s):
Year:
Vol:
Page:
This Article
Abstract
Full Text (PDF)
Alert me when this article is cited
Alert me if a correction is posted
Services
Similar articles in this journal
Similar articles in PubMed
Alert me to new issues of the journal
Download to citation manager
Cited by other online articles
Google Scholar
Articles by Phadke, M. A.
Articles by Bollinger, R. C.
Articles citing this Article
PubMed
PubMed Citation
Articles by Phadke, M. A.
Articles by Bollinger, R. C.
© 2003 The American Society for Nutritional Sciences J. Nutr. 133:3153-3157, October 2003
Community and International Nutrition
Replacement-Fed Infants Born to HIV-Infected Mothers in India Have a High Early Postpartum Rate of Hospitalization 1 , 2 Mridula A. Phadke * , Bhaghyashree Gadgil , Kapila E. Bharucha , Aparna N. Shrotri , Jayagowri Sastry ** , Nikhil A. Gupte ** , Ronald Brookmeyer ** , Ramesh S. Paranjape , Pandurang M. Bulakh , Hemalata Pisal ** , Nishi Suryavanshi ** , Anita V. Shankar ** , Lidia Propper ** , P. L. Joshi and Robert C. Bollinger ** ,3
* Department of Medical Education and Research, Government of Maharashtra, Mumbai, India; Byramjee JeeJeebhoy Medical College/Sassoon Hospital, Pune, India; ** Johns Hopkins University, Baltimore, Maryland 21205; National AIDS Research Institute, Pune, India; and National AIDS Control Organization, New Delhi, India
3 To whom correspondence should be addressed. E-mail: rcb{at}jhmi.edu
ABSTRACT
TOP
ABSTRACT
METHODS
RESULTS
DISCUSSION
LITERATURE CITED
Access to safe breast-feeding alternatives for HIV-infected mothers and their infants in many settings is limited. We compared the rates of early postpartum hospitalization of infants born to HIV-infected mothers using different infant-feeding practices in a large government hospital in Pune, India. From March 1, 2000 to November 30, 2001, infants born to HIV-infected mothers were followed in a postpartum clinic. All mothers had received a standard short course of antenatal zidovudine. Infant-feeding practices were assessed within 3 d of delivery, prior to postpartum hospital discharge. Sixty-two of 148 mothers (42%) were breast-feeding their infants. Eighty-six of the mothers (58%) were providing replacement feeding, primarily diluted cow, goat or buffalo milk (top feeding). Twenty-one of the 148 participating infants (14.2%) born during the study period required hospitalization within the 1st 6 mo of life and 6 infants required repeat hospitalization. All hospitalized infants were receiving replacement feeding with a rate of 0.093 hospitalizations per 100 person-days (95% CI, 0.062 to 0.136). The reasons for hospitalization included acute gastroenteritis (48.1%), pneumonia (18.5%), septicemia (11.1%) and jaundice (11.1%). A high risk for early postpartum hospitalization was seen in replacement-fed infants born to HIV-infected mothers in Pune, India. In settings such as India, where access to safe replacement feeding is limited, interventions making exclusive breast-feeding safer for HIV-infected mothers and infants are needed. Such interventions would be valuable additions to the very effective national prevention programs that currently rely on the provision of short-course zidovudine and nevirapine.
KEY WORDS: • HIV • replacement feeding • breast-feeding
Since the demonstration that HIV type 1 (HIV-1) 3 can be transmitted by breast-feeding, HIV-infected mothers, their clinicians and public health practitioners in resource-poor settings have struggled with the uncertainty of whether breast-feeding or replacement feeding is preferred. Although formula feeding has been shown to reduce the risk of HIV transmission from mother to child ( 1 ), the use of alternatives to breast-feeding in resource-poor settings has been known to increase infant mortality and morbidity ( 2 ). In this uncertain context, WHO, the Joint United Nations Program on HIV/AIDS (UNAIDS) and the United Nations Children’s Fund recommend that HIV-infected women be fully informed of the risks and benefits of the available infant-feeding options and that they be supported in their decision ( 3 ). These recommendations have proven difficult to implement because the relative risk-benefit ratio of infant-feeding options may vary considerably in resource-poor settings and there are limited data that can guide HIV-infected mothers and their caregivers. This has led some to recommend that resource-limited communities should assess the relative risks and benefits of various feeding options in their particular situation ( 2 , 4 ).
The only randomized clinical trial of feeding practices in infants born to HIV-1–infected mothers was recently completed in Kenya, demonstrating that within the 1st 2 y of life, formula-fed infants had mortality and morbidity rates similar to those of breast-fed infants ( 5 ). This same study demonstrated a higher HIV-1–free survival rate in formula-fed than in breast-fed infants. The authors concluded that formula feeding can be a safe alternative to breast-feeding for infants of HIV-1–infected mothers in resource-poor settings. However, they acknowledged that access to formula and clean water is not universally available in all settings in which HIV-infected mothers must make this choice.
India has the greatest occurrence of HIV-1 infection in Asia, with more than four million people currently infected ( 6 ). In some urban areas of western and southern India, >4% of pregnant women are HIV-infected ( 6 ). Data about the risks and benefits of infant-feeding options from other resource-limited settings may not be directly relevant to India. In India, infant formula is not affordable for most mothers. In addition, the conditions for safe preparation of replacement feeding are not widely available. Finally, the potential for social stigma associated with replacement feeding is a potential concern. In order to provide the first estimates of the risks and benefits of various feeding practices for infants born to HIV-infected mothers in India, early postpartum infant hospitalization data were analyzed from one of the centers participating in the Indian Government National AIDS Control Organization (NACO) study of antenatal zidovudine (ZDV) administration for the prevention of mother-to-child HIV-1 transmission ( 7 ).
METHODS
TOP
ABSTRACT
METHODS
RESULTS
DISCUSSION
LITERATURE CITED
Subjects.
This study was conducted at Byramjee JeeJeebhoy Medical College, in Pune, India, one of the 11 centers participating in a feasibility study of short-course ZDV use for the prevention of mother-to-infant HIV transmission, directed by NACO ( 7 ). Informed consent was obtained from all participating mothers. This study was reviewed and approved by independent ethical committees in India and in the United States.
Study procedures and data collection.
In the antenatal clinic, counselors and physicians provided mothers with information about the risks and benefits of various forms of infant feeding according to UNAIDS guidelines ( 3 ) and were subsequently offered full support for their infant-feeding choice. After informed consent was obtained, HIV-infected mothers and their newborn infants were enrolled in a prospective follow-up study. As part of the NACO study, enrolled mothers received zidovudine at no cost beginning at 36-wk gestation until the onset of labor (300 mg orally twice a day) and until delivery (300 mg orally every 3 h).
Available data on infant feeding included in these analyses were limited to an assessment of reported infant-feeding practices collected within 3 d of birth from consenting mothers prior to postpartum discharge from the hospital. Mothers and newborn infants were subsequently followed in the postpartum clinic with routine scheduled visits at 48 h, 2, 3 and 4 mo postpartum. At each scheduled follow-up visit, mothers were asked to report any history of clinical symptoms or hospitalizations of their infants. In addition, postpartum hospitalizations of participating mothers and infants were detected by the study staff reviewing the admission records of the Sassoon General Hospital on a daily basis. All hospitalization events included in these analyses were inpatient admissions identified by review of the hospital admissions records.
Analysis.
Hospitalization rates were calculated as the number of hospitalizations divided by the total person-time of follow-up ( 8 ). Each hospitalization episode was counted as an independent event. Although 6 infants accounted for more than one event, each admission was felt to be due to an independent clinical episode requiring hospitalization. Hospitalization rates were calculated separately for breast-fed and replacement-fed infants. CI and comparison of rates were based on person-time analyses using Poisson data methods. A Kaplan-Meier analysis was performed comparing the proportion of breast-fed infants without hospitalization to that of replacement-fed infants ( 9 ).
RESULTS
TOP
ABSTRACT
METHODS
RESULTS
DISCUSSION
LITERATURE CITED
From March 1, 2000 to November 30, 2001, 161 mothers were enrolled in the NACO study. By the end of the observation period for these analyses, 149 infants were born to HIV-infected mothers receiving short-course ZDV. One infant died at birth and was not included in these analyses. When asked within 3 d of birth, 77 of 148 mothers (52%) reported that they were replacement feeding their infants. In this setting, replacement feeding usually consists of top feeding, which is typically the use of cow, goat or buffalo milk diluted with water. Supplemental vitamins are not commonly used in top feeding in India because of the cost. Only 2 mothers (1.3%) reported formula feeding. Sixty-two of the mothers (41.9%) reported exclusive breast-feeding and 7 (4.7%) mothers reported mixed feeding. For the purposes of subsequent analyses, infant feeding practices were classified as breast-fed ( n = 62) or replacement fed ( n = 86).
The infants were followed for a mean of 19.5 wk from birth (median 13.4 wk). The mean follow-up period of breast-fed infants was somewhat less than that of replacement-fed infants (15.8 and 21.5 wk, respectively). However, this difference was not significant ( P = 0.07, unpaired t test). Twenty-one of the 148 participating infants (14.2%) were hospitalized and 6 were hospitalized twice for a total of 27 events yielding an overall postpartum infant hospitalization rate of 0.061 per 100 person-days (95% CI, 0.040 to 0.087). Estimates of postpartum infant hospitalization rates for a number of maternal and infant factors were determined ( Table 1 ). None of these factors were associated with a significant difference in infant hospitalization rates, except infant feeding ( P < 0.0001). None of the breast-fed infants were hospitalized over 15,170 person-days of follow-up. For replacement-fed infants, 28,919 person-days of follow-up showed a rate of 0.093 hospitalizations per 100 person-days (95% CI, 0.062 to 0.136; P < 0.0001 compared with breast-fed infants’ hospitalization rate). The hospitalization rate for replacement-fed infants was higher in the 1st 30 d postpartum (0.5029 per 100 person-days; 95% CI, 0.2681 to 0.8616) than in the 2nd and 3rd months of life (0.2101 per 100 person-days; 95% CI, 0.1068 to 0.3761). A Kaplan-Meier analysis was performed comparing the proportion of breast-fed infants without hospitalization to that of replacement-fed infants, demonstrating a high risk of early postpartum hospitalization for replacement-fed infants ( Fig. 1 ).
View this table:
[in this window]
[in a new window]
TABLE 1 Postpartum hospitalization rate of infants born to HIV-infected mothers in Pune, India
View larger version (14K):
[in this window]
[in a new window]
FIGURE 1 Kaplan-Meier estimate of the time to first hospitalization by infant-feeding practice for infants born to HIV-infected mothers in Pune, India. These data demonstrate the proportion without hospitalization in breast-fed ( n = 62) and replacement-fed infants ( n = 86). All mothers received short-course prenatal zidovudine. Infant-feeding practices were assessed within 72 h of birth, prior to postpartum hospital discharge. Hospitalizations were defined as overnight infant admissions to the hospital for clinical care and were identified by daily screening of hospital admission records.
To investigate whether maternal or peripartum factors could have impacted the risk of subsequent postpartum infant hospitalization, available maternal demographics and delivery details were compared between breast-fed and replacement-fed infants ( Table 2 ). There was no significant difference in parity ( P = 0.11) or maternal hemoglobin level ( P = 0.35). There were also no significant differences in the gestational age ( P = 0.826) at delivery, type of delivery ( P = 0.59), birth weight ( P = 0.17) or recorded delivery complications ( P = 0.50). Only 1 mother reported a history of smoking or alcohol use during pregnancy and 1 mother had hypertension. Breast-fed infants were more likely to be male and to have somewhat higher Apgar scores, although the clinical relevance of this is unclear.
View this table:
[in this window]
[in a new window]
TABLE 2 Maternal and delivery details of breast-fed and replacement-fed infants born to HIV-infected mothers in Pune, India 1
A specific admission diagnosis was documented for 25 of the 27 hospitalizations of replacement-fed infants. Dehydration with acute gastroenteritis in 13 infants (48.1%) was the most common admission diagnosis. Sepsis with acute respiratory infection was reported in 5 of the admitted replacement-fed infants (18.5%). Three infants were admitted with jaundice and 3 were admitted with sepsis. One infant was admitted with a severe dermatitis.
There were 4 deaths among the 148 infants during the follow-up period. Thus, the crude infant mortality rate in children born to HIV-infected mothers was 27.03 per 1000 live births. The 4 infants died at 7, 13, 26 and 40 wk of age, with 2 diagnoses of pneumonia and 2 of gastroenteritis with sepsis. All 4 infants who died were replacement-fed, resulting in a crude infant mortality rate of 46.51 per 1000 live births for replacement-fed infants. A Fisher’s exact test comparing the 4 deaths out of 77 exclusively replacement-fed and the 0 deaths out of 62 exclusively breast-fed infants yielded a two-tailed P value of 0.13.
Overall national estimates of vertical HIV-1 transmission rates from the NACO study are 8.4% at birth and 10.2% at 2 mo, among infants whose mothers received ZDV ( 7 ). Although site-specific HIV-1 transmission rates for infants born to participating mothers in Pune were unavailable, HIV-1 PCR results performed at 48-h postpartum and at 2-mo postpartum were available on a subset of the 148 infants. Among the 62 breast-fed infants, available results showed that 1 of 39 infants tested at 48 h of age was HIV-1 PCR positive. Two additional breast-fed infants, who were HIV-1 PCR negative at birth, were HIV-1 PCR positive at 2 mo of age. One additional breast-fed infant was HIV-1 PCR positive at 2 mo of age; however, the 48-h PCR results were unavailable. Among the remaining 86 replacement-fed infants, 4 of 82 tested were HIV-1 PCR positive at 48 h. Three additional replacement-fed infants of 48 tested, who were HIV-1 PCR negative at 48 h, were HIV-1 PCR positive at 2 mo of age. Of the 20 replacement-fed infants who were hospitalized and had HIV-1 PCR results available at 48 h, 3 (15%) were HIV-1 PCR positive. An additional 2 hospitalized infants became HIV-1 PCR positive at 2 mo of age. Of the 4 infants who died, HIV-1 PCR results were negative at 48 h for all and were repeatedly HIV-1 PCR negative for 2 infants at 2 mo of age.
DISCUSSION
TOP
ABSTRACT
METHODS
RESULTS
DISCUSSION
LITERATURE CITED
This study demonstrates an increased risk of hospitalization, resulting from increased risk of morbidity, for replacement-fed Indian infants who are born to HIV-infected mothers, compared with breast-fed infants. These results are of importance because all of the mothers received prenatal ZDV therapy for prevention of mother-to-infant HIV transmission. Although this observational study with limited follow-up did not demonstrate a significant difference in mortality ( P = 0.13), it is also worth noting that none of the 4 infants who died were breast-fed. In addition, none of infants who died were HIV-1 PCR positive at 48 h or 2 mo postpartum.
These data from India appear to be consistent with other studies demonstrating an increased risk of infant morbidity and mortality associated with replacement feeding ( 2 , 10 – 16 ). However, these data are not consistent with a recent well-designed randomized clinical trial comparing breast-feeding to formula feeding in Kenya ( 1 ). In contrast to the Kenyan study, ours was an observational study of the current local clinical standard of care in Pune, where access to affordable and safe infant formula is very limited. There are no other data available on the benefits and risks of cow, buffalo and goat milk (top feeding) as an alternative replacement for breast milk for infants born to either HIV-infected or uninfected mothers. However, top feeding is a widespread practice in South Asia. Although breast-feeding is nearly universal in India, exclusive breast-feeding is not. Recent data from the 1998–99 Indian National Family Health Survey-2 ( 17 ) show that only 16% of infants began breast-feeding within 1 h of birth and only 37% began breast-feeding within 1 d. In addition, early introduction of supplemental feeding is common in India, with only 55% of children under 4 mo of age receiving exclusive breast-feeding.
There are other potential explanations for the differences in hospitalization rates seen in breast-fed and replacement-fed infants in our study. In most populations, morbidity and mortality are higher in males than in females. However, in India, female mortality is higher than male mortality in many age groups. Therefore, a higher percentage of male infants could potentially result in an underestimation of the relative hospitalization rate in the breast-fed infants. However, recent data from India suggests that although overall child mortality is higher for females, this difference is not seen within the 1st y of life ( 17 ). In fact, female mortality in India is 14% lower than male mortality during the neonatal period.
During the observation period for this study, an additional 110 infants were born to HIV-infected mothers that were not included in these analyses. These were infants whose mothers were not enrolled in the NACO study. Available data on these women are limited. Many of these mothers presented in labor, without an opportunity to initiate the antenatal ZDV NACO regimen. A number of them had complicated pregnancies that made them ineligible for the NACO study. Therefore, an additional limitation to our analyses was that our selected population of infants born to mothers enrolled in the NACO study, who all received short-course antenatal ZDV, may not be representative of all HIV-infected mothers and their infants in Pune.
Although the mean follow-up periods of the 2 groups were not significantly different ( P = 0.07), the replacement-fed infants were followed 6 wk longer than the breast-fed infants. The reasons for this difference are unclear. Although it is possible that the shorter follow-up of breast-fed infants could have failed to detect hospitalizations, all but 2 of the 27 hospitalizations in replacement-fed infants occurred within 16 wk postpartum, the mean follow-up for the breast-fed infants.
It is possible that early postpartum maternal reports of infant-feeding practices are not entirely accurate, resulting in misclassification of infants’ feeding. In our analyses, we classified 62 infants as breast-fed because their mothers reported exclusive breast-feeding in the postpartum ward of the hospital. As has been previously stated, exclusive breast-feeding is not common in India. In addition, the other 86 infants classified as replacement fed included 77 infants reported as exclusively fed with buffalo, cow or goat milk (top feeding), 7 reported mixed feeding and 2 reported exclusive formula feeding. All but 1 of the 27 hospitalization events occurred in the infants reported as exclusively receiving top feeding. In addition, it is possible that the infant-feeding practices in these groups could have changed following postpartum hospital discharge. This would also result in misclassification. Data available on extended infant-feeding practices from the NACO study were limited. However, the fact that none of the observed hospitalizations occurred in the infants reported as exclusively breast-fed prior to postpartum hospital discharge is striking, despite the potential for misclassification.
Finally, it is possible that this difference in early postpartum hospitalization rates was not due to differences in infant-feeding practices. This difference could also be the result of breast-fed infants being less likely to be brought to the hospital when ill or mothers who breast-fed being more experienced and knowledgeable about infant care behaviors. The available data for our analyses were a limited number of factors (Table 2) , showing no significant differences in maternal hemoglobin ( P = 0.35), parity ( P = 0.11) or infant birth weight ( P = 0.17). This suggests that prenatal maternal risk factors, care behaviors and economic factors may be similar in both groups, but antenatal data were limited and we have no postpartum data available on economic resources or care behaviors to completely rule out such confounders in our analyses.
In the absence of morbidity and mortality data from infants born to HIV-infected mothers in India, mothers and their physicians are relying on data from other settings and a high percentage of mothers are electing not to breast-feed their infants. Few of these women have access to safe affordable infant formula. Although the use of prenatal ZDV or nevirapine can effectively reduce the risk of mother-to-infant HIV-1 transmission, this study suggests that the risks associated with commonly utilized alternative infant feedings, i.e., other than exclusive breast milk, may be high for infants born to HIV-infected mothers in India.
These results support the recommendation that each community needs to assess the relative risks and benefits of their own available feeding options for infants born to HIV-infected mothers ( 4 ). In settings such as India, where access to affordable safe infant formula is limited and where social stigmatization of nonbreast-feeding mothers is a concern, new interventions that make exclusive breast-feeding safer for both mother and infant are needed. These data suggest that interventions to specifically prevent HIV transmission by breast milk, while preserving the benefits of breast-feeding, may be particularly important for India. Such interventions would be valuable additions to the very effective short-course zidovudine and/or nevirapine prevention programs currently in use.
ACKNOWLEDGMENTS
The authors thank the participants and the Research Officers at Byramjee JeeJeebhoy Medical College for their technical assistance with this study.
FOOTNOTES
1 These data were previously presented in part as Abstract Number 0347, Global Strategies Conference on Mother to Child HIV Transmission, Kampala, Uganda, September 2001 [Phadke, M. A., Joshi, P. L., Balpande, D. N., Deshmukh, D., Bharadwaj, R., Sastry, J., Patke, D., Gupte, N., Bulakh, P. M., Karmarkar, A., Bharucha, K. E., Shrotri, A., Pisal, H., Suryawanshi, N., Shankar, A., Propper, L., Brookmeyer, R. & Bollinger, R. C. Early post-partum morbidity of non-breast fed infants born to HIV infected women], and Abstract Number WePeB5926, XIV International AIDS Conference, Barcelona, Spain, July 7–12, 2002 [Phadke, M. A., Bharucha, K. E., Shrotri, A. N., Sastry, J., Gupte, N. A., Brookmeyer, R., Joshi, P. L. & Bollinger, R. C. High post-partum morbidity in replacement fed infants born to HIV-infected women in India, receiving short-course zidovudine].
2 This study was supported by grants from NIH, NIAID (R01AI45462) and the NIH-Fogarty International Center NIH Program of International Training Grants in Epidemiology Related to AIDS (D43-TW0000). This work was also undertaken in collaboration with the National AIDS Control Organization (NACO) and the Byramjee JeeJeebhoy Medical College in India. The views expressed do not represent those of the NIH, NACO or BJMC.
4 Abbreviations used: HIV-1, HIV type-1; NACO, National AIDS Control Organization; UNAIDS, Joint United Nations Programme on HIV/AIDS; ZDV, zidovudine.
Manuscript received 12 April 2003. Initial review completed 9 May 2003. Revision accepted 2 July 2003.
LITERATURE CITED
TOP
ABSTRACT
METHODS
RESULTS
DISCUSSION
LITERATURE CITED
1. Nduati, R., John, G., Mbori-Ngacha, D., Richardson, B., Overbaugh, J., Mwatha, A., Ndinya-Achola, J., Bwayo, J., Onyango, F. E., Hughes, J. & Kreiss, J. (2000) Effect of breastfeeding and formula feeding on transmission of HIV-1: a randomized clinical trial. J. Am. Med. Assoc. 283:1167-1174. [Abstract/ Free Full Text]
2. WHO Collaborative Study Team on the Role of Breastfeeding on the Prevention of Infant Mortality (2000) Effect of breastfeeding on infant and child mortality due to infectious diseases in less developed countries: a pooled analysis. Lancet 355:451-455. [Medline]
3. The World Health Organization (1998) The Joint United Nations Programme on HIV AIDS and The United Nations Children’s Fund. HIV and Infant Feeding: A Guide for Decision-Makers 1998 http://www.unaids.org/publications/documents/mtct/index.html. (Accessed June 12, 2003).
4. Guay, L. A. & Ruff, A. J. (2001) HIV and infant feeding—an ongoing challenge. J. Am. Med. Assoc. 286:2462-2464. [ Free Full Text]
5. Mbori-Ngacha, D., Nduati, R., John, G., Reilly, M., Richardson, B., Mwatha, A., Ndinya-Achola, J., Bwayo, J. & Kreiss, J. (2001) Morbidity and mortality in breastfed and formula-fed infants of HIV-1-infected women. A randomized clinical trial. J. Am. Med. Assoc. 286:2413-2420. [Abstract/ Free Full Text]
6. National AIDS Control Organization and Ministry of Health and Family Welfare, Government of India (2001) Estimation of HIV Infection 2001 2001 http://www.naco.nic.in/indianscene/esthiv.htm. (Accessed June 12, 2003).
7. National AIDS Control Organization (2002) Ministry of Health and Family Welfare Government of India. Feasibility Study of Administering Short-term AZT Intervention Among HIV-infected Mothers to Prevent Mother-to-Child Transmission of HIV in India 2002 http://www.naco.nic.in/nacp/program/pmtct.htm. (Accessed June 12, 2003).
8. Breslow, N. E. & Day, N. E. (1987) Statistical Methods in Cancer Research—The Design and Analysis of Cohort Studies II Oxford University Press .
9. Kaplan, E. L. & Meier, P. (1958) Nonparametric estimation from incomplete observations. J. Am. Stat. Assoc. 53:457-481.
10. Cesar, J. A., Victora, C. G., Barros, F. C., Santos, I. S. & Flores, J. A. (1999) Impact of breast feeding on admission for pneumonia during postneonatal period in Brazil: nested case-control study. BMJ 318:1316-1320. [Abstract/ Free Full Text]
11. Victora, C. G., Fuchs, S. C., Kirkwood, B. R., Lombardi, C. & Barros, F. C. (1992) Breast-feeding, nutritional status, and other prognostic factors for dehydration among young children with diarrhoea in Brazil. Bull. World Health Organ. 70:467-475. [Medline]
12. Victora, C. G., Smith, P. G., Barros, F. C., Vaughan, J. P. & Fuchs, S. C. (1989) Risk factors for deaths due to respiratory infections among Brazilian infants. Int. J. Epidemiol. 18:918-925. [Abstract]
13. Victora, C. G., Smith, P. G., Vaughan, J. P., Nobre, L. C., Lombardi, C., Teixeira, A. M., Fuch, S. C., Moreira, L. B., Gigante, L. P. & Barros, F. C. (1989) Infant feeding and deaths due to diarrhea. A case-control study. Am. J. Epidemiol. 129:1032-1041. [Abstract]
14. Victora, C. G., Smith, P. G., Vaughan, J. P., Nobre, L. C., Lombardi, C., Teixeira, A. M., Fuchs, S. M., Moreira, L. B., Gigante, L. P. & Barros, F. C. (1987) Evidence for protection by breast-feeding against infant deaths from infectious diseases in Brazil. Lancet 2:319-322. [Medline]
15. Mahmood, D. A., Feachem, R. G. & Huttly, S. R. (1989) Infant feeding and risk of severe diarrhoea in Basrah city, Iraq: a case-control study. Bull. World Health Organ. 67:701-706. [Medline]
16. Feachem, R. G. & Koblinsky, M. A. (1984) Interventions for the control of diarrhoeal diseases among young children: promotion of breast-feeding. Bull. World Health Organ. 62:271-291. [Medline]
17. International Institute for Populations Sciences (IIPS) and ORC Macro (2002) National Family Health Survey (NFHS-2), India, 1998–1999 2002 http://www.nfhsindia.org/. (Accessed June 12, 2003).
This article has been cited by other articles: ( Search Google Scholar for Other Citing Articles )
P. C Papathakis, N. C Rollins, K. H Brown, M. L Bennish, and M. D Van Loan
Comparison of isotope dilution with bioimpedance spectroscopy and anthropometry for assessment of body composition in asymptomatic HIV-infected and HIV-uninfected breastfeeding mothers
Am. J. Clinical Nutrition, September 1, 2005; 82(3): 538 - 546.
[Abstract] [Full Text] [PDF]
T Duke
Neonatal pneumonia in developing countries
Arch. Dis. Child. Fetal Neonatal Ed., May 1, 2005; 90(3): F211 - f219.
[Abstract] [Full Text] [PDF]
A. V. Shankar, J. Sastry, A. Erande, A. Joshi, N. Suryawanshi, M. A. Phadke, and R. C. Bollinger
Making the Choice: the Translation of Global HIV and Infant Feeding Policy to Local Practice among Mothers in Pune, India
J. Nutr., April 1, 2005; 135(4): 960 - 965.
[Abstract] [Full Text] [PDF]
Recent References
J Hum Lact, February 1, 2004; 20(1): 106 - 112.
[PDF]
This Article
Abstract
Full Text (PDF)
Alert me when this article is cited
Alert me if a correction is posted
Services
Similar articles in this journal
Similar articles in PubMed
Alert me to new issues of the journal
Download to citation manager
Google Scholar
Articles by Phadke, M. A.
Articles by Bollinger, R. C.
Articles citing this Article
PubMed
PubMed Citation
Articles by Phadke, M. A.
Articles by Bollinger, R. C.