PEDIATRICS Vol. 119 No. 3 March 2007, pp. e666-e671 (doi:10.1542/peds.2006-2107)
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
ARTICLE |
Transmission of West Nile Virus Through Human Breast Milk Seems to Be Rare
Arboviral Diseases Branch, Division of Vector-Borne Infectious Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, US Public Health Service, Department of Health and Human Services, Fort Collins, Colorado
 |
ABSTRACT |
|---|
 TOP ABSTRACT METHODSRESULTSDISCUSSIONREFERENCES |
|---|
INTRODUCTION.In September 2002, possible transmission of West Nile virus via human milk was reported for the first time.
METHODS.Since 2003, the Centers for Disease Control and Prevention collected reports of maternal or infant West Nile virus illness during the breastfeeding period. All of the reported instances were reviewed. In addition, milk samples from women infected during pregnancy were tested for West Nile virus RNA and West Nile virus–specific antibodies.
RESULTS.Six infants were reported to have breastfed from mothers with West Nile virus fever. Five of the 6 infants had no illness or detectable antibodies to West Nile virus in serum after onset of maternal illness. One infant who was not tested and developed a rash was otherwise well 1 week after onset of maternal illness. In addition, 2 infants were reported to have developed West Nile virus illness while breastfeeding; preceding maternal illness was not documented. Two breastfed infants whose mothers acquired West Nile virus fever in the last week of pregnancy developed West Nile virus–specific antibodies; both infant infections could have been congenitally acquired. Of 45 milk samples from women infected with West Nile virus during pregnancy, 2 had West Nile virus RNA, and 14 had immunoglobin M antibodies to West Nile virus.
CONCLUSIONS.Of 10 reported instances since 2003 of maternal or infant West Nile virus illness while breastfeeding, transmission of West Nile virus through human milk could neither be ruled out nor confirmed for 5 cases; in 5 others, serologic tests indicated no vertical transmission. Transmission of West Nile virus through breastfeeding seems to be rare, but more information is needed.
Key Words: West Nile virus • breastfeeding • milk • pregnancy • flavivirus • perinatal transmission • epidemiology
Abbreviations: WNV—West Nile virus • CDC—Centers for Disease Control and Prevention • Ig—immunoglobulin • ELISA—enzyme-linked immunosorbent assay • SLEV—St Louis Encephalitis virus • CSF—cerebrospinal fluid • PCR—polymerase chain reaction
West Nile virus (WNV) has become a major public health threat in the United States, causing 
8000 cases of human neuroinvasive disease since its detection in New York in 1999. WNV is a flavivirus transmitted to humans by infected mosquitoes. In 2002, it was discovered that WNV could be transmitted through blood transfusion, organ transplantation, and transplacentally.1 In September 2002, the first case of possible WNV transmission via human milk was reported.2 Because the majority (
80%) of persons infected by WNV are asymptomatic, cases where transmission occurs via breastfeeding may go unrecognized.3
Other arthropod-borne flaviviruses can be transmitted to humans and animals through ingestion of milk or milk products. In humans, infection with and illness because of tick-borne encephalitis virus has occurred after consumption of raw sheep, goat, and cow's milk and sour-milk products made of infected milk.4–6 In animals, louping-ill and Powassan viruses have been transmitted from lactating goats to suckling kids.7,8 In 1 study, transmission of louping-ill virus through breast milk resulted in infection and clinical illness of 5 of 13 milk-exposed goat kids.7
The first possible transmission of WNV via human milk was reported to the Centers for Disease Control and Prevention (CDC) in September 2002.2,9 In this case, a 40-year-old woman was transfused immediately postpartum with blood that was subsequently found to contain WNV nucleic acid. She began to breastfeed on the day of delivery and continued through day 16 postdelivery, her second day of hospitalization for WNV encephalitis. A sample of undiluted mother's milk from day 16 postdelivery tested positive for the presence of WNV nucleic acid and WNV-specific immunoglobin M (IgM) and IgG antibodies. Viral culture of the milk was negative for WNV. A second sample of undiluted milk collected 24 days after delivery was negative for WNV nucleic acid. This sample was positive for WNV-specific IgM antibodies when tested at a 1:400 dilution. At 25 days of age, serum from the breastfed infant tested WNV-specific IgM positive, although the child remained healthy. The mother reported that the infant had been kept primarily indoors, with no obvious exposures to mosquitoes.2,9 Below we summarize available surveillance data regarding other cases of possible WNV infection via breastfeeding.
|
METHODS |
|---|
|
TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Since 2003, data on WNV disease in humans, including demographic and clinical information on women or children who became ill while breastfeeding, have been routinely reported to the CDC by 54 state and local health departments through ArboNET, a national arboviral disease surveillance system.10 Also in 2003, CDC and state health departments organized a surveillance registry to assess pregnancy and infant health outcomes for women infected with WNV during pregnancy.11 This enhanced surveillance system was designed to collect maternal and infant health information and diagnostic samples, including human colostrum or mature human milk samples. Breast milk and serum specimens collected from case subjects were tested at a 1:400 dilution for WNV-specific IgA (breast milk only), IgM, and IgG antibodies by an enzyme-linked immunosorbent assay (ELISA).12,13 Positive ELISA results were confirmed by plaque-reduction neutralization tests for neutralizing antibodies to WNV, St Louis Encephalitis virus (SLEV), and other closely related flaviviruses.13 To indicate specificity to WNV, only samples with neutralizing antibody titers
10 and 4 times higher than corresponding titers to St Louis Encephalitis virus were considered positive. Whenever possible, undiluted cerebrospinal fluid (CSF) was tested using these same techniques. Breast milk and CSF were also tested for the presence of WNV nucleic acid by polymerase chain reaction (PCR).14 These activities were defined by the National Center for Infectious Diseases as public health practice, thus institutional review board regulations do not apply, and informed consent was not required. |
RESULTS |
|---|
|
TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Mothers Who Were Breastfeeding at Time of Maternal WNV Illness
In August of 2003, 4 mothers who developed WNV fever while breastfeeding were reported to the CDC. All 4 of the mothers had IgM to WNV detected in serum shortly after illness onset. In the first instance, a breastfed infant developed a rash and no other symptoms 11 days after onset of WNV illness in the mother. No infant serum or maternal breast milk samples were collected; therefore, the possibility of transmission of WNV by breastfeeding could not be further evaluated. In the second instance, a breast milk sample obtained 12 days after the onset of maternal WNV illness tested positive for WNV-specific IgA antibodies; negative for WNV-specific IgM, IgG, and neutralizing antibodies; and negative for the presence of WNV RNA. The 4-month-old infant remained healthy and had no detectable antibodies to WNV in serum collected 13 days after the onset of maternal illness. In the third instance, a breast milk sample collected 46 days after the onset of maternal WNV illness tested negative for IgA, IgM, IgG, and neutralizing antibodies and negative for the presence of WNV RNA. The 2-month-old infant remained healthy and had no detectable WNV antibodies in serum collected nearly 7 weeks after maternal illness. In the last instance, a breast milk sample obtained
5 months (192 days) after the onset of maternal WNV illness tested negative for WNV-specific IgA, IgM, IgG, and neutralizing antibodies and negative for the presence of WNV RNA. The newborn infant remained healthy and had no detectable WNV-specific antibodies in serum collected 11 days after the mother's breast milk sample was collected. No similar reports were received during 2004, but in 2005, 2 more mothers who developed WNV fever while breastfeeding were reported to the CDC. Again, both mothers developed IgM to WNV shortly after illness onset. Breast milk samples were obtained from the first mother at 44, 45, 47, and 48 days after the onset of WNV illness. All of these samples tested negative for WNV-specific IgA, IgM, and neutralizing antibodies, as well as for WNV RNA. This woman's 7-month-old infant remained healthy and had no detectable antibodies to WNV in serum collected at 48 days after the onset of maternal illness. Breast milk samples collected from the second mother at 28, 29, 31, 32, and 35 days after the onset of WNV illness were also negative for WNV RNA but were not tested for WNV-specific antibodies. This woman's 12-month-old infant remained healthy and had no detectable antibodies to WNV in serum collected at 36 days after the onset of maternal illness. Information pertaining to these mothers who were breastfeeding at time of maternal WNV illness is summarized in Table 1.
|
Infants Who Were Breastfeeding at Time of Infant WNV Illness
In 2003, the CDC received reports of 2 infants who were breastfeeding at the time of their WNV illness. The first was a girl who developed fever and rash at 8 months of age. Serum obtained 1 week after the onset was negative for WNV-specific IgM antibodies, but a convalescent serum obtained
2 weeks after onset was positive for WNV-specific IgM antibodies. The mother reported no illness until nearly a month after onset of infant illness, and maternal serum was subsequently positive for IgM antibodies to WNV. Because the incubation period for symptomatic WNV infections is thought to be shorter than 15 days,15 and this mother's illness followed the onset of her child's illness by nearly a month, it seems unlikely that transmission through breastfeeding occurred unless the mother was asymptomatically infected with WNV while the child was breastfeeding, and her subsequent symptomatic illness was of different etiology. The second breastfed infant developed a fever and rash that progressed to encephalitis at 9 months of age. Serum and CSF specimens were positive for WNV-specific IgM antibodies. The mother did not report illness before the infant's illness; asymptomatic WNV infection of the mother could not be evaluated, because no maternal specimens were collected.
Breastfeeding Infants With Mothers Infected Before Delivery
Two previously reported women who had been enrolled in the CDC's WNV pregnancy registry in 2003 gave birth to infants who breastfed and subsequently tested positive for WNV IgM antibodies, indicating WNV infection of the infants.11 However, maternal infection occurred close to parturition, making it difficult to know whether transmission occurred before or after delivery. The first mother became acutely ill with WNV fever and rash 5 days before delivery in August 2003. Her serum was positive for WNV-specific IgM antibodies 7 days after her illness onset. Her male child was born afebrile with a transient maculopapular rash that resolved at 36 hours of life, coarctation of the aorta, and a bicuspid aortic valve. Cord blood, infant serum, and colostrum were not obtained at birth. Infant serum collected 2 months after birth was positive for WNV-specific IgM and neutralizing antibodies. A second infant serum sample collected at 8 months of age was positive for IgM and IgG to WNV, and the neutralizing antibody titer to WNV was fourfold higher than the titer in the previous sample. The child remained otherwise healthy. The mother's breast milk sample obtained 20 days after delivery was negative for the presence of WNV RNA and for IgA, IgM, and IgG antibodies to WNV but was positive for neutralizing antibodies. Another breast milk sample collected 2 months after delivery was negative for all of the WNV-specific antibodies. Because of the late identification of infant WNV infection relative to birth, neither congenital transmission nor transmission by mosquito exposure can be excluded.
The second mother had onset of WNV illness and rash in September 2003, 6 days before delivery. A maternal serum sample collected 12 days after illness onset tested positive for WNV-specific IgM, IgG, and neutralizing antibodies and was negative for WNV RNA. A cord blood sample collected at delivery, 6 days after the onset of symptoms, tested negative for WNV-specific IgM, IgG, and neutralizing antibodies. At 10 days of age, the infant girl developed neonatal meningitis, and her CSF and serum were both positive for WNV-specific IgM antibodies. Breast milk obtained 37 days after onset of the mother's illness tested positive for WNV-specific IgM antibodies (testing for IgA was not performed) and neutralizing antibodies and negative for WNV RNA.
WNV RNA and Antibodies in Breast Milk
Thirty-two colostrum and 13 mature human milk samples collected from 45 of 72 women enrolled in the CDC's WNV pregnancy registry during the 2003 and 2004 transmission seasons were tested for WNV RNA by PCR. Two colostrum samples were positive; all of the other samples were negative. One positive sample was collected 50 days after the onset of maternal illness; the other sample was collected 70 days after the onset. Because of the low level of RNA detected in these samples, virus isolation was not attempted. The 2 children exposed to these colostrum samples did not apparently become infected with WNV, as evidenced by the lack of WNV-specific antibodies in blood samples drawn at 291 and 308 days of age, respectively. For both cases where colostrum was positive, WNV RNA was not detected in maternal serum at 2 months after the onset of illness. Of the 43 WNV PCR-negative specimens, 9 were collected <70 days after the onset. The number of milk samples testing positive for the presence of RNA or WNV-specific antibodies is presented in Table 2.
|
Thirty-four colostrum and 13 breast milk samples were tested for WNV-specific IgM antibodies. Eleven colostrum samples (32%) and 3 breast milk samples (23%), collected at 8, 23, and 31 days postpartum, respectively, tested positive. The average time from onset of illness to collection of IgM-positive breast milk and colostrum samples was 81 days (range: 24–153 days). Time from onset of illness to collection of IgM-negative samples was longer, with an average of 184 days (range: 11–293 days; P < .0001, by unpaired t test).
Six (19%) of 31 colostrum samples and 1 (11%) of 9 breast milk samples tested for WNV-specific IgA antibodies were positive. The average time from onset of illness to collection of IgA-positive breast and colostrum samples was 92 days (range: 11–158 days). Time from onset of illness to collection of IgA-negative samples was longer, with an average of 159 days (range: 26–293 days; P = .04).
All 31 colostrum and 11 breast milk samples tested for IgG to WNV by ELISA were negative. However, neutralizing antibodies, which may be IgM, IgG, or IgA, against WNV were found in 26 (84%) of 31 colostrum samples and 6 (55%) of 11 breast milk samples. The average time from onset of illness to collection of samples testing positive for neutralizing antibodies was 118 days (range: 11–281 days) compared with 170 days (range: 37–293 days) for negative samples (P = .07).
|
DISCUSSION |
|---|
|
TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Only 1 likely instance of WNV transmission by breastfeeding has been reported to date, in 2002, when the mother was infected postdelivery by transfusion with blood products containing WNV. Through heightened surveillance, we found no evidence of WNV transmission to infants of 5 breastfeeding mothers with laboratory-documented postpartum WNV illness and were unable to assess possible transmission in a sixth infant. Two other reported infants were breastfeeding at the time of their WNV infection, but preceding maternal WNV infection was not documented in either case. Lastly, 2 other infants became infected while breastfeeding after maternal infection that occurred before delivery. These infants could have acquired their infection congenitally, through breastfeeding, or from infected mosquitoes.
Several differences exist between the mother thought to have transmitted WNV to her infant through breast milk in 2002 and the breastfeeding mothers in subsequent years who were ill but apparently did not transmit the virus. The mother in 2002 acquired infection through blood transfusion and developed WNV encephalitis, whereas the other mothers acquired infection from infected mosquitoes and developed WNV fever. Either a higher virus inoculum from blood transfusion or host factors in the mother at the time of infection, including asymptomatic mastitis or unreported minor areolar lesions,16 might have increased the likelihood of breast milk transmission.17
Immune factors in human breast milk and those in the infant gastrointestinal tract and saliva may interact synergistically to provide protective antiviral benefits.18,19 Antiviral activity against 2 flaviviruses, Japanese B encephalitis virus and Dengue virus, have been observed in the fat fraction of human milk.20,21 Milk lipids provide antiviral activity during digestion, when they are broken down into fatty acids and monoglycerides by both milk-derived bile-salt–stimulated lipase and lipolytic activity in the infant's gut.20,22 In addition, secretory IgA, the predominant immunoglobulin found in human milk, is thought to protect the recipient infant from common enteric and respiratory pathogens.23,24 In addition to the antiviral agents in human milk that were already mentioned, several other components, including lactoferrin, lysozyme, glycoconjugates, and oligosaccharides, may contribute to protection against flavivirus infection.25,26
Infant age may also influence the likelihood of acquiring WNV infection from human breast milk. For example, the intestinal immaturity of the neonate can allow for increased attachment of certain pathogenic organisms to gut epithelial cells.24 Epithelial barriers in the newborn's intestinal tract are stimulated by growth factors in human milk, including epidermal growth factor, lactoferrin, cortisol, and hormones. Later in postnatal development, IgA-producing plasma cells appear in the infant's intestinal tract.24 An infant's systemic immune response is also age dependent, with serum concentrations of IgM rising gradually after 6 days of age, and maternally acquired IgG declining gradually during the first 6 to 8 months of life.24,25
Although no human colostrum and mature human milk samples tested in this study at a 1:400 dilution were positive by the ELISA test for WNV-specific IgG, 76% of all of the milk samples tested neutralized WNV in the plaque-reduction neutralization test assay, reflecting relatively low ELISA test sensitivity with breast milk specimens, the presence of non-IgG virus-neutralizing antibody, and/or the presence of other nonimmunoglobulin virus-neutralizing components in the milk. Proportionally more colostrum samples than mature human milk samples contained WNV-specific IgM and IgA antibodies, which may reflect the shorter time from onset of illness to sample collection for these first postpartum milk samples and is consistent with expected immunoglobulin content in human milk in the first days postpartum.24 According to our data, WNV-specific IgM antibodies were detected more frequently in human milk after WNV infections than IgA antibodies. This may be because of the absence or transient nature of an IgA immune response to WNV infection or limitations in the assay's ability to detect WNV-specific IgA.
Because flaviviral RNA would be expected to decrease in tissues with increasing time after illness, WNV RNA may be more likely found in colostrum than breast milk from a woman who was infected with WNV during pregnancy. Furthermore, there are higher concentrations of macrophages in colostrum as compared with mature human milk,24 and WNV is thought to target monocytes and macrophages for the replication and spread of infection throughout tissues.27 Our data suggest that the presence of WNV RNA in milk seems to be rare after maternal WNV infection during pregnancy (only 2 colostrum samples were positive of 45 total milk samples). For both cases where colostrum was positive, WNV RNA was not detected in serum at 2 months after the onset of illness. Although no information has been published regarding the persistence of flavivirus nucleic acid in human breast tissues, tick-borne encephalitis virus has been isolated from brain tissues of animals and humans at >7 months after infection, and Powassan virus has been isolated from the brain of a fatal human case at 42 days after the onset of illness,28 indicating that arthropod-borne flaviviruses may sometimes persist in human tissues.
In this investigation, only 6 women and 4 infants who were breastfeeding at the time of their WNV infection were reported to the CDC. It is likely that these numbers are far below the actual number of breastfeeding women and infants who were infected with WNV since the 2002 transmission season. Thus, the information obtained from this sample of cases may not be representative of the entire pool of breastfeeding women or infants infected with WNV. Another limitation is the lack of knowledge regarding the validity of laboratory serology techniques used to detect WNV-specific antibodies in human milk, because these tests have not been standardized for milk samples. Variability in collection, shipment, and storage of these human milk specimens may have also compromised the ability to accurately measure immunoglobulins and RNA using standard testing techniques.
This article reports results for those few women or infants having clinical WNV illness who were reported to a national surveillance system by health care providers and health departments. The results do not support any change in infant feeding practices after infection with WNV. Additional information is needed to understand the potential for WNV transmission through breast milk. For areas where WNV is endemic, clinicians and public health authorities should include WNV in the differential diagnosis of illness among breastfeeding children and nursing mothers. The CDC continues to seek information and offer testing of specimens, including milk and blood samples, from women diagnosed with WNV while nursing.
|
ACKNOWLEDGMENTS |
|---|
We give special thanks to Stephanie Kuhn for assistance with case identification and specimen procurement. We also thank the state WNV surveillance coordinators and the following CDC staff: Theresa Smith and Roy Campbell for general advice; Robert Lanciotti, Roselyn Hochbein, Amanda Noga, Amy Lambert, Olga Kosoy, Janeen Laven, and Brandy Russell for laboratory analysis of specimens; and Peggy Collins for database development/management.
|
FOOTNOTES |
|---|
Accepted Oct 3, 2006.
Address correspondence to Alison F. Hinckley, PhD, Centers for Disease Control and Prevention, PO Box 2087, Fort Collins, CO 80522. E-mail: ahinckley{at}cdc.gov
The authors have indicated they have no financial relationships relevant to this article to disclose.
|
REFERENCES |
|---|
|
TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
- Hayes EB, O'Leary DR. West Nile virus infection: a pediatric perspective.
Pediatrics. 2004;113
:1375
–1381
[Abstract/Free Full Text] - Centers for Disease Control and Prevention. Possible West Nile virus transmission to an infant through breast-feeding: Michigan, 2002. MMWR Morb Mortal Wkly Rep. 2002;51 :877 –878[Medline]
- Mostashari F, Bunning ML, Kitsutani PT, et al. Epidemic West Nile encephalitis, New York, 1999: results of a household-based seroepidemiological survey. Lancet. 2001;358 :261 –264[CrossRef][Web of Science][Medline]
- Gresikova M, Sekeyova M, Stupalova S, Necas S. Sheep milk-borne epidemic of tick-borne encephalitis in Slovakia. Intervirology. 1975;5 :57 –61[Web of Science][Medline]
- Sixl W, Stunzner D, Withalm H, Kock M. Rare transmission mode of FSME (tick-borne encephalitis) by goat's milk. Geogr Med Suppl. 1989;2 :11 –14[Medline]
- Vereta LA, Skorobrekha VZ, Nikolaeva SP, et al. The transmission of the tick-borne encephalitis virus via cow's milk [in Russian]. Med Parazitol (Mosk). 1991;3 :54 –56[Medline]
- Reid HW, Buxton D, Pow I, Finlayson J. Transmission of louping-ill virus in goat milk. Vet Rec. 1984;114 :163 –165[Abstract]
- Woodall JP, Roz A. Experimental milk-borne transmission of Powassan virus in the goat.
Am J Trop Med Hyg. 1977;26
:190
–192
[Abstract/Free Full Text] - Centers for Disease Control and Prevention. Update: investigations of West Nile virus infections in recipients of organ transplantation and blood transfusion: Michigan, 2002. MMWR Morb Mortal Wkly Rep. 2002;51 :879[Medline]
- O'Leary DR, Marfin AA, Montgomery SP, et al. The epidemic of West Nile virus in the United States, 2002. Vector Borne Zoonotic Dis. 2004;4 :61 –70[CrossRef][Web of Science][Medline]
- O'Leary DR, Kuhn S, Kniss KL, et al. Birth outcomes following West Nile virus infection of pregnant women, United States, 2003–2004. Pediatrics. 2006;117(3) . Available at: www.pediatrics.org/cgi/content/full/117/3/e537.
- Martin DA, Biggerstaff BJ, Allen BA, et al. Use of immunoglobulin M cross-reactions in differential diagnosis of human flaviviral encephalitis infections in the United States. Clin Diagn Lab Immunol. 2002;9 :544 –549[CrossRef][Medline]
- Beaty BJ, Calisher CH, Shope R. Arboviruses. In: Lennette EH, Lennette DA, Lennette ET, eds. Diagnostic Procedures for Viral, Rickettsial, and Chlamydial Infections. 7th ed. Washington, DC: American Public Health Association; 1995:189 –209
- Lanciotti RS, Kerst AJ, Nasci RS, et al. Rapid detection of West Nile virus from human clinical specimens, field-collected mosquitoes, and avian samples by a TaqMan reverse transcriptase-PCR assay.
J Clin Microbiol. 2000;38
:4066
–4071
[Abstract/Free Full Text] - Goldblum N, Sterk VV, Paderski B. West Nile fever; the clinical features of the disease and the isolation of West Nile virus from the blood of nine human cases. Am J Hyg. 1954;59 :89 –103[Web of Science][Medline]
- Iliff PJ, Piwoz EG, Tavengwa NV, et al. Early exclusive breastfeeding reduces the risk of postnatal HIV-1 transmission and increases HIV-free survival. AIDS. 2005;19 :699 –708[Web of Science][Medline]
- Campbell GL, Marfin AA, Lanciotti RS, Gubler DJ. West Nile virus. Lancet Infect Dis. 2002;2 :519 –529[CrossRef][Web of Science][Medline]
- Isaacs CE. Human milk inactivates pathogens individually, additively, and synergistically.
J Nutr. 2005;135
:1286
–1288
[Abstract/Free Full Text] - Goldman AS. Modulation of the gastrointestinal tract of infants by human milk. Interfaces and interactions. An evolutionary perspective. J Nutr. 2000;130(2S suppl) :426S –431S
- May JT. Antimicrobial properties and microbial contaminants of breast milk: an update. Aust Paediatr J. 1984;20 :265 –269[Web of Science][Medline]
- Falkler WA Jr, Diwan AR, Halstead SB. A lipid inhibitor of dengue virus in human colostrum and milk; with a note on the absence of anti-dengue secretory antibody. Arch Virol. 1975;47 :3 –10[CrossRef][Web of Science][Medline]
- Thormar H, Isaacs CE, Brown HR, et al. Inactivation of enveloped viruses and killing of cells by fatty acids and monoglycerides.
Antimicrob Agents Chemother. 1987;31
:27
–31
[Abstract/Free Full Text] - Jatsyk GV, Kuvaeva IB, Gribakin SG. Immunological protection of the neonatal gastrointestinal tract: the importance of breast feeding. Acta Paediatr Scand. 1985;74 :246 –249[Web of Science][Medline]
- Lawrence RM. Host-resistance factors and immunologic significance of human milk. In: Lawrence RA, Lawrence RM, eds. Breastfeeding: A Guide for the Medical Profession. 5th ed. St Louis, MO: Mosby; 1999:159 –195
- Goldman AS, Chheda S, Garofalo R. Evolution of immunologic functions of the mammary gland and the postnatal development of immunity. Pediatr Res. 1998;43 :155 –162[Web of Science][Medline]
- Naarding MA, Ludwig IS, Groot F, et al. Lewis X component in human milk binds DC-SIGN and inhibits HIV-1 transfer to CD4+ T lymphocytes. J Clin Invest. 2005;115 :3256 –3264[CrossRef][Web of Science][Medline]
- Weingartl HM, Neufeld JL, Copps J, Marszal P. Experimental West Nile virus infection in blue jays (Cyanocitta cristata) and crows (Corvus brachyrhynchos).
Vet Pathol. 2004;41
:362
–370
[Abstract/Free Full Text] - Kuno G. Persistence of arboviruses and antiviral antibodies in vertebrate hosts: its occurrence and impacts. Rev Med Virol. 2001;11 :165 –190[CrossRef][Web of Science][Medline]
PEDIATRICS (ISSN 1098-4275). ©2007 by the American Academy of Pediatrics
CiteULike 
Connotea 
Del.icio.us 
Digg 
Facebook 
Reddit 
Technorati 
Twitter What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
