Postnatal Cytomegalovirus Infection Through Human Milk in Preterm Infants: Transmission, Clinical Presentation, and Prevention

Clinics in Perinatology

Volumn 44, Issue 1, 2017, Pages 121-130

  Hamprecht, Klaus ^a   Goelz, Rangmar ^a  

^a UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

Author keywords

Cytomegalovirus; Ganciclovir; Lactation; Native breast milk; Short and long term outcome; Very low birth weight infants (VLBW); Virus inactivation; Virus reactivation

Indexed keywords

ANTIVIRAL THERAPY; BREAST FEEDING; BREAST MILK; CELLS; COGNITION; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; FREEZE THAWING; HEAT TREATMENT; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INFANT; LACTATION; MILK CELL; MIXED INFECTION; NONHUMAN; PASTEURIZATION; PERINATAL PERIOD; PREMATURITY; PROPHYLAXIS; REVIEW; RISK; SYMPTOMATOLOGY; VIRUS DETECTION; VIRUS LOAD; VIRUS REACTIVATION; VIRUS SHEDDING; VIRUS TRANSMISSION; VIRUS TRANSMISSION PREVENTION; HEAT; NEWBORN; PREVENTION AND CONTROL; TRANSMISSION; VERTICAL TRANSMISSION; VERY LOW BIRTH WEIGHT; VIROLOGY; VIRUS INACTIVATION;

BREAST FEEDING; CYTOMEGALOVIRUS INFECTIONS; HOT TEMPERATURE; HUMANS; INFANT, NEWBORN; INFANT, PREMATURE; INFANT, VERY LOW BIRTH WEIGHT; INFECTIOUS DISEASE TRANSMISSION, VERTICAL; MILK, HUMAN; VIRUS INACTIVATION;

EID: 85009178440     PISSN: 00955108     EISSN: 15579840     Source Type: Journal    
DOI: 10.1016/j.clp.2016.11.012     Document Type: Review

References (58)

1. 1 American Academy of Pediatrics, Breast feeding and the use of human milk. Pediatrics 129 (2012), e827–e841.
2. 2 Victora, C.G., Horta, B.L., Loret de Mola, C., et al. Association between breastfeeding and intelligence, educational attainment, and income at 30 years of age: a prospective cohort study from Brazil. Lancet Glob Health 3 (2015), e199–e205.
3. 3 Diosi, P., Babusceac, L., Nevinglovschi, O., et al. Cytomegalovirus infection associated with pregnancy. Lancet 2:7525 (1967), 1063–1066.
4. 4 Reynolds, D.W., Stagno, S., Hosty, T.S., et al. Maternal cytomegalovirus excretion and perinatal infection. N Engl J Med 289 (1973), 1–5.
5. 5 Stagno, S., Reynolds, D.W., Pass, R.F., et al. Breast milk and the risk of cytomegalovirus infection. N Engl J Med 302 (1980), 1073–1076.
6. 6 Benson, J.W., Bodden, S.J., Tobin, J.O., Cytomegalovirus and blood transfusion in neonates. Arch Dis Child 54:7 (1979), 538–541.
7. 7 Yeager, A.S., Grumet, F.C., Hafleigh, E.B., et al. Prevention of transfusion acquired cytomegalovirus infections in newborn infants. J Pediatr 98 (1981), 281–287.
8. 8 Goodrum, F., Caviness, K., Zagallo, P., Human cytomegalovirus persistence. Cell Microbiol 14 (2012), 644–655.
9. 9 Hamprecht, K., Maschmann, J., Vochem, M., et al. Epidemiology of transmission of cytomegalovirus from mother to preterm infant by breastfeeding. Lancet 357 (2001), 513–518.
10. 10 Meier, J., Lienicke, U., Tschirch, E., et al. Human cytomegalovirus reactivation during lactation and mother-to-child transmission in preterm infants. J Clin Microbiol 43 (2005), 1318–1324.
11. 11 Manicklal, S., Emery, V.C., Lazzarotto, T., et al. The ‘Silent’ Global burden of congenital cytomegalovirus. Clin Microbiol Rev, 26, 2013, 86.
12. 12 Hamprecht, K., Witzel, S., Maschmann, J., et al. Rapid detection and quantification of cell free cytomegalovirus by a high-speed centrifugation-based microculture assay: comparison to longitudinally analyzed viral DNA load and pp67 late transcript during lactation. J Clin Virol 28 (2003), 303–316.
13. 13 Maschmann, J., Goelz, R., Witzel, S., et al. Characterization of human breast milk leukocytes and their potential role in cytomegalovirus transmission to newborns. Neonatology 107 (2015), 213–219.
14. 14 Kaye, S., Miles, D., Antoine, P., et al. Virological and immunological correlates of mother-to-child transmission of cytomegalovirus in the Gambia. J Infect Dis 197 (2008), 1307–1314.
15. 15 Wakabayashi, H., Mizuno, K., Kohda, C., et al. Low HCMV DNA copies can establish infection and result in significant symptoms in extremely preterm infants: a prospective study. Am J Perinatol 29 (2012), 377–382.
16. 16 Chiavarini, M., Bragetti, P., Sensini, A., et al. Breastfeeding and transmission of cytomegalovirus to preterm infants. Case report and kinetic of CMV-DNA in breast milk. Ital J Pediatr, 37, 2011, 6.
17. 17 Mosca, F., Pugni, L., Barbi, M., et al. Transmission of cytomegalovirus. Lancet, 357(9270), 2001, 1800.
18. 18 Numazaki, K., Chiba, S., Asanuma, H., Transmission of cytomegalovirus. Lancet, 357(9270), 2001, 1799.
19. 19 Hamprecht, K., Maschmann, J., Vochem, M., et al. Transmission of cytomegalovirus to preterm infants by breastfeeding. Prösch, S., Cinatl, J., Scholz, M., (eds.) New aspects of CMV-related immunopathology, vol. 24, 2003, Karger, Basel (Switzerland), 43–52.
20. 20 Hamprecht, K., Vochem, M., Baumeister, A., et al. Detection of cytomegaloviral DNA in human milk cells and cell free milk whey by nested PCR. J Virol Methods 70 (1998), 167–176.
21. 21 Hamprecht, K., Witzel, S., Maschmann, J., et al. Transmission of cytomegalovirus infection through breast milk in term and preterm infants. The role of cell free milk whey and milk cells. Adv Exp Med Biol 478 (2000), 231–239.
22. 22 Hassiotou, F., Hartmann, P., At the dawn of a new discovery: the potential of breast milk stem cells. Adv Nutr 5 (2014), 770–778.
23. 23 van der Strate, B.W., Harmsen, M.C., Schäfer, P., et al. Viral load in breast milk correlates with transmission of human cytomegalovirus to preterm neonates, but lactoferrin concentrations do not. Clin Diagn Lab Immunol 8 (2001), 818–821.
24. 24 Jim, W.T., Shu, C.H., Chiu, N.C., et al. High cytomegalovirus load and prolonged virus excretion in breast milk increase risk for viral acquisition by very low birth weight infants. Pediatr Infect Dis J 28 (2009), 891–894.
25. 25 Ehlinger, E.P., Webster, E.M., Kang, H.H., et al. Maternal cytomegalovirus-specific immune responses and symptomatic postnatal cytomegalovirus transmission in very low-birth-weight preterm infants. J Infect Dis 204 (2011), 1672–1682.
26. 26 Viljoen, J., Tuaillon, E., Nagot, N., et al. Cytomegalovirus, and possibly Epstein–Barr virus, shedding in breast milk is associated with HIV-1 transmission by breastfeeding. AIDS 29 (2015), 145–153.
27. 27 Slyker, J., Farquhar, C., Atkinson, C., et al. Compartmentalized cytomegalovirus replication and transmission in the setting of maternal HIV-1 infection. Clin Infect Dis 58 (2014), 564–572.
28. 28 Sagar, M., Origin of the transmitted virus in HIV infection: infected cells versus cell-free virus. J Infect Dis 210:Suppl 3 (2014), S667–S673.
29. 29 Doctor, S., Friedman, S., Dunn, M.S., et al. Cytomegalovirus transmission to extremely low-birthweight infants through breast milk. Acta Paediatr 94 (2005), 53–58.
30. 30 Hamprecht, K., Maschmann, J., Jahn, G., et al. Cytomegalovirus transmission to preterm infants during lactation. J Clin Virol 41:3 (2008), 198–205.
31. 31 Maschmann, J., Hamprecht, K., Dietz, K., et al. Cytomegalovirus infection of extremely low-birth weight infants via breast milk. Clin Infect Dis 33 (2001), 1998–2003.
32. 32 Mehler, K., Oberthuer, A., Lang-Roth, R., et al. High rate of symptomatic cytomegalovirus infection in extremely low gestational age preterm infants of 22-24 weeks’ gestation after transmission via breast milk. Neonatology 105:1 (2014), 27–32.
33. 33 Nijman, J., van Loon, A.M., Krediet, T.G., et al. Maternal and neonatal anti-cytomegalovirus IgG level and risk of postnatal cytomegalovirus transmission in preterm infants. J Med Virol 85 (2013), 689–695.
34. 34 Ballard, R.A., Drew, W.L., Hufnagle, K.G., et al. Acquired cytomegalovirus infection in preterm infants. Am J Dis Child 133 (1979), 482–485.
35. 35 Vochem, M., Hamprecht, K., Jahn, G., et al. Transmission of cytomegalovirus to preterm infants through breast milk. Pediatr Infect Dis J 17 (1998), 53–58.
36. 36 Kurath, S., Halwachs-Baumann, G., Müller, W., et al. Transmission of cytomegalovirus via breast milk to the prematurely born infant: a systematic review. Clin Microbiol Infect 16 (2010), 1172–1178.
37. 37 Neuberger, P., Hamprecht, K., Vochem, M., et al. Case-control study of symptoms and neonatal outcome of human milk-transmitted cytomegalovirus infection in premature infants. J Pediatr 148 (2006), 326–331.
38. 38 Hamele, M., Flanagan, R., Loomis, C.A., et al. Severe morbidity and mortality with breast milk associated cytomegalovirus infection. Pediatr Infect Dis J 29 (2010), 84–86.
39. 39 Lanzieri, T.M., Dollard, S.C., Josephson, C.D., et al. Breast milk-acquired cytomegalovirus infection and disease in VLBW and premature infants. Pediatrics 131 (2013), e1937–e1945.
40. 40 Goelz, R., Hamprecht, K., Klingel, K., et al. Intestinal manifestations of postnatal and congenital cytomegalovirus infection in term and preterm infants. J Clin Virol 83 (2016), 29–36.
41. 41 Sawyer, M.H., Edwards, D.K., Spector, S.A., Cytomegalovirus infection and bronchopulmonary dysplasia in premature infants. Am J Dis Child 141 (1987), 303–305.
42. 42 Kelly, M.S., Benjamin, D.K., Puopolo, K.M., et al. Postnatal cytomegalovirus infection and the risk for bronchopulmonary dysplasia. JAMA Pediatr, 169, 2015, e153785.
43. 43 Lopes, A.-A., Belhabri, S., Karaoui, L., Clinical findings and autopsy of a preterm infant with breast milk-acquired cytomegalovirus infection. AJP Rep 6 (2016), e198–e202.
44. 44 Kumar, M.L., Nankervis, G.A., Jacobs, I.B., et al. Congenital and postnatally acquired cytomegalovirus infections: long-term follow-up. J Pediatr 104 (1984), 674–679.
45. 45 Paryani, S.G., Yeager, A.S., Hosford-Dunn, H., et al. Sequelae of acquired cytomegalovirus infection in premature and sick term infants. J Pediatr 107 (1985), 451–456.
46. 46 Vollmer, B., Seibold-Weiger, K., Schmitz-Salue, C., et al. Postnatally acquired cytomegalovirus infection via breast milk: effects on hearing and development in preterm infants. Pediatr Infect Dis J 23 (2004), 322–327.
47. 47 Jim, W.T., Chiu, N.C., Ho, C.S., et al. Outcome of preterm infants with postnatal cytomegalovirus infection via breast milk: a two-year prospective follow-up study. Medicine (Baltimore), 94, 2015, e1835.
48. 48 Goelz, R., Meisner, C., Bevot, A., et al. Long-term cognitive and neurological outcome of preterm infants with postnatally acquired CMV infection through breast milk. Arch Dis Child Fetal Neonatal Ed 98 (2013), F430–F433.
49. 49 Bevot, A., Hamprecht, K., Krägeloh-Mann, I., et al. Long-term outcome in preterm children with human cytomegalovirus infection transmitted via breast milk. Acta Paediatr 101 (2012), e167–e172.
50. 50 Brecht, K.F., Goelz, R., Bevot, A., et al. Postnatal human cytomegalovirus infection in preterm infants has long-term neuropsychological sequelae. J Pediatr 166 (2015), 834–839.
51. 51 Nijman, J., Gunkel, J., de Vries, L.S., et al. Reduced occipital fractional anisotropy on cerebral diffusion tensor imaging in preterm infants with postnatally acquired cytomegalovirus infection. Neonatology 104 (2013), 143–150.
52. 52 Dorn, M., Lidzba, K., Bevot, A., et al. Long-term neurobiological consequences of early postnatal hCMV-infection in former preterms: a functional MRI study. Hum Brain Mapp 35 (2014), 2594–2606.
53. 53 Hamprecht, K., Maschmann, J., Müller, D., et al. Cytomegalovirus (CMV) inactivation in breast milk: reassessment of pasteurization and freeze-thawing. Pediatr Res 56 (2004), 529–535.
54. 54 Goelz, R., Hihn, E., Hamprecht, K., et al. Effects of different CMV-heat-inactivation-methods on growth factors in human breast milk. Pediatr Res 65 (2009), 458–461.
55. 55 Maschmann, J., Hamprecht, K., Weissbrich, B., et al. Freeze-thawing of breast milk does not prevent cytomegalovirus transmission to a preterm infant. Arch Dis Child Fetal Neonatal Ed 91 (2006), F288–F290.
56. 56 Curtis, N., Chau, L., Garland, S., et al. Cytomegalovirus remains viable in naturally infected breast milk despite being frozen for 10 days. Arch Dis Child Fetal Neonatal Ed 90 (2005), F529–F530.
57. 57 Ben-Shoshan, M., Mandel, D., Lubetzky, R., et al. Eradication of cytomegalovirus from human milk by microwave irradiation: a pilot study. Breastfeed Med 11 (2016), 186–187.
58. 58 Lloyd, M.L., Hod, N., Jayaraman, J., et al. Inactivation of cytomegalovirus in breast milk using ultraviolet-C irradiation: opportunities for a new treatment option in breast milk banking. PLoS One, 11(8), 2016, e0161116.