Impaired Haemophilus influenzae type b transplacental antibody transmission and declining antibody avidity through the first year of life represent potential vulnerabilities for HIV-exposed but-uninfected infants

Clinical and Vaccine Immunology

Volumn 21, Issue 12, 2014, Pages 1661-1667

  Gaensbauer, James T ^a,d   Rakhola, Jeremy T ^b,e,f   Onyango Makumbi, Carolyne ^c   Mubiru, Michael ^c   Westcott, Jamie E ^a   Krebs, Nancy F ^a   Asturias, Edwin J ^a,d   Fowler, Mary Glenn ^c   McFarland, Elizabeth ^a,e   Janoff, Edward N ^b,e,f  

^a Children's Hospital Colorado   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

^d Global Health and Health Disparities   (United States)

^e Mucosal and Vaccine Research Program Colorado   (United States)

^f VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM ANTIBODY; HAEMOPHILUS INFLUENZAE TYPE B POLYSACCHARIDE VACCINE; HAEMOPHILUS VACCINE; VACCINE;

ADULT; ANTIBODY AFFINITY; BACTERIAL CAPSULE; BLOOD; FEMALE; FETOMATERNAL TRANSFUSION; HAEMOPHILUS INFLUENZAE TYPE B; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; INFANT; MALE; NEWBORN; PREGNANCY; PREGNANCY COMPLICATION; VACCINATION;

ADULT; ANTIBODIES, BACTERIAL; ANTIBODY AFFINITY; BACTERIAL CAPSULES; FEMALE; HAEMOPHILUS INFLUENZAE TYPE B; HAEMOPHILUS VACCINES; HIV INFECTIONS; HUMANS; INFANT; INFANT, NEWBORN; MALE; MATERNAL-FETAL EXCHANGE; PREGNANCY; PREGNANCY COMPLICATIONS, INFECTIOUS; VACCINATION; VACCINES, CONJUGATE;

EID: 84914145028     PISSN: 15566811     EISSN: 1556679X     Source Type: Journal    
DOI: 10.1128/CVI.00356-14     Document Type: Article

References (49)

1. St. Geme J. 2008. Haemophilus influenzae, p 892-897. In Long S, Pickering L, Prober C (ed), Principles and practice of pediatric infectious diseases, 3rd ed. Elsevier, Inc., Philadelphia, PA.
2. Peltola H. 2000. Worldwide Haemophilus influenzae type b disease at the beginning of the 21st century: global analysis of the disease burden 25 years after the use of the polysaccharide vaccine and a decade after the advent of conjugates. Clin. Microbiol. Rev. 13:302-317. http://dx.doi.org/10.1128/CMR.13.2.302-317.2000.
3. Watt JP, Wolfson LJ, O'Brien KL, Henkle E, Deloria-Knoll M, McCall N, Lee E, Levine OS, Hajjeh R, Mulholland K, Cherian T. 2009. Burden of disease caused by Haemophilus influenzae type b in children younger than 5 years: global estimates. Lancet 374:903-911. http://dx.doi.org/10.1016/S0140-6736(09)61203-4.
4. von Gottberg A, Cohen C, Whitelaw A, Chhagan M, Flannery B, Cohen AL, de Gouveia L, Plessis MD, Madhi SA, Klugman KP, Group for Enteric, Respiratory, Meningeal Disease Surveillance in South Africa (GERMS-SA). 2012. Invasive disease due to Haemophilus influenzae serotype b ten years after routine vaccination, South Africa, 2003-2009. Vaccine 30:565-571. http://dx.doi.org/10.1016/j.vaccine.2011.11.066.
5. Lee EH, Lewis RF, Makumbi I, Kekitiinwa A, Ediamu TD, Bazibu M, Braka F, Flannery B, Zuber PL, Feikin DR. 2008. Haemophilus influenzae type b conjugate vaccine is highly effective in the Ugandan routine immunization program: a case-control study. Trop. Med. Int. Health 13:495-502. http://dx.doi.org/10.1111/j.1365-3156.2008.02027.x.
6. World Health Organization. 2013. Mother-to-child transmission of HIV: data and statistics. World Health Organization, Geneva, Switzerland. http://www.who.int/hiv/topics/mtct/data/en/index1.html. Accessed 18 June 2013.
7. Brahmbhatt H, Kigozi G, Wabwire-Mangen F, Serwadda D, Lutalo T, Nalugoda F, Sewankambo N, Kiduggavu M, Wawer M, Gray R. 2006. Mortality in HIV-infected and uninfected children of HIV-infected and uninfected mothers in rural Uganda. J. Acquir. Immune Defic. Syndr. 41:504-508. http://dx.doi.org/10.1097/01.qai.0000188122.15493.0a.
8. Shapiro RL, Lockman S, Kim S, Smeaton L, Rahkola JT, Thior I, Wester C, Moffat C, Arimi P, Ndase P, Asmelash A, Stevens L, Montano M, Makhema J, Essex M, Janoff EN. 2007. Infant morbidity, mortality, and breast milk immunologic profiles among breast-feeding HIV-infected and HIV-uninfected women in Botswana. J. Infect. Dis. 196:562-569. http: //dx.doi.org/10.1086/519847.
9. Miyamoto M, Pessoa SD, Ono E, Machado DM, Salomao R, Succi RC, Pahwa S, de Moraes-Pinto MI. 2010. Low CD4 T-cell levels and B-cell apoptosis in vertically HIV-exposed noninfected children and adolescents. J. Trop. Pediatr. 56:427-432. http://dx.doi.org/10.1093/tropej/fmq024.
10. Bunders M, Pembrey L, Kuijpers T, Newell ML. 2010. Evidence of impact of maternal HIV infection on immunoglobulin levels in HIVexposed uninfected children. AIDS Res. Hum. Retroviruses 26:967-975. http://dx.doi.org/10.1089/aid.2009.0241.
11. Borges-Almeida E, Milanez HM, Vilela MM, Cunha F, Abramczuk BM, Reis-Alves SC, Metze K, Lorand-Metze I. 2011. The impact of maternal HIV infection on cord blood lymphocyte subsets and cytokine profile in exposed non-infected newborns.BMCInfect. Dis. 11:38. http://dx.doi.org/10.1186/1471-2334-11-38.
12. Jones C, Pollock L, Barnett SM, Battersby A, Kampmann B. 2013. Specific antibodies against vaccine-preventable infections: a motherinfant cohort study. BMJ Open 3(4):e002473. http://dx.doi.org/10.1136/bmjopen-2012-002473.
13. Palmeira P, Quinello C, Silveira-Lessa AL, Zago CA, Carneiro-Sampaio M. 2012. IgG placental transfer in healthy and pathological pregnancies. Clin. Dev. Immunol. 2012:985646. http://dx.doi.org/10.1155/2012/985646.
14. Agbarakwe AE, Griffiths H, Begg N, Chapel HM. 1995. Avidity of specific IgG antibodies elicited by immunisation against Haemophilus influenzae type b. J. Clin. Pathol. 48:206-209. http://dx.doi.org/10.1136/jcp.48.3.206.
15. Hetherington SV, Lepow ML. 1992. Correlation between antibody affinity and serum bactericidal activity in infants. J. Infect. Dis. 165:753-756. http://dx.doi.org/10.1093/infdis/165.4.753.
16. Weiss PJ, Wallace MR, Oldfield EC, III, O'Brien J, Janoff EN. 1995. Response of recent human immunodeficiency virus seroconverters to the pneumococcal polysaccharide vaccine and Haemophilus influenzae type b conjugate vaccine. J. Infect. Dis. 171:1217-1222. http://dx.doi.org/10.1093/infdis/171.5.1217.
17. Janoff EN, Hardy WD, Smith PD, Wahl SM. 1991. Humoral recall responses in HIV infection. Levels, specificity, and affinity of antigenspecific IgG. J. Immunol. 147:2130-2135.
18. Goldblatt D, Vaz AR, Miller E. 1998. Antibody avidity as a surrogate marker of successful priming by Haemophilus influenzae type b conjugate vaccines following infant immunization. J. Infect. Dis. 177:1112-1115. http://dx.doi.org/10.1086/517407.
19. Englund JA, Glezen WP. 2003. Maternal immunization with Haemophilus influenzae type b vaccines in different populations. Vaccine 21:3455-3459. http://dx.doi.org/10.1016/S0264-410X(03)00350-5.
20. Jones CE, Naidoo S, De Beer C, Esser M, Kampmann B, Hesseling AC. 2011. Maternal HIV infection and antibody responses against vaccinepreventable diseases in uninfected infants. JAMA 305:576-584. http://dx.doi.org/10.1001/jama.2011.100.
21. Englund JA, Glezen WP, Turner C, Harvey J, Thompson C, Siber GR. 1995. Transplacental antibody transfer following maternal immunization with polysaccharide and conjugate Haemophilus influenzae type b vaccines. J. Infect. Dis. 171:99-105. http://dx.doi.org/10.1093/infdis/171.1.99.
22. Mulholland K, Suara RO, Siber G, Roberton D, Jaffar S, N=Jie J, Baden L, Thompson C, Anwaruddin R, Dinan L, Glezen WP, Francis N, Fritzell B, Greenwood BM. 1996. Maternal immunization with Haemophilus influenzae type b polysaccharide-tetanus protein conjugate vaccine in The Gambia. JAMA 275:1182-1188. http://dx.doi.org/10.1001/jama.275.15.1182.
23. Wesumperuma HL, Perera AJ, Pharoah PO, Hart CA. 1999. The influence of prematurity and low birthweight on transplacental antibody transfer in Sri Lanka. Ann. Trop. Med. Parasitol. 93:169-177. http://dx.doi.org/10.1080/00034989958654.
24. de Moraes-Pinto MI, Farhat CK, Carbonare SB, Curti SP, Otsubo ME, Lazarotti DS, Campagnoli RC, Carneiro-Sampaio MM. 1993. Maternally acquired immunity in newborns from women infected by the human immunodeficiency virus. Acta Paediatr. 82:1034-1038. http://dx.doi.org/10.1111/j.1651-2227.1993.tb12805.x.
25. Cumberland P, Shulman CE, Maple PA, Bulmer JN, Dorman EK, Kawuondo K, Marsh K, Cutts FT. 2007. Maternal HIV infection and placental malaria reduce transplacental antibody transfer and tetanus antibody levels in newborns in Kenya. J. Infect. Dis. 196:550-557. http://dx.doi.org/10.1086/519845.
26. Scott S, Cumberland P, Shulman CE, Cousens S, Cohen BJ, Brown DW, Bulmer JN, Dorman EK, Kawuondo K, Marsh K, Cutts F. 2005. Neonatal measles immunity in rural Kenya: the influence of HIV and placental malaria infections on placental transfer of antibodies and levels of antibody in maternal and cord serum samples. J. Infect. Dis. 191:1854-1860. http://dx.doi.org/10.1086/429963.
27. de Moraes-Pinto MI, Almeida AC, Kenj G, Filgueiras TE, Tobias W, Santos AM, Carneiro-Sampaio MM, Farhat CK, Milligan PJ, Johnson PM, Hart CA. 1996. Placental transfer and maternally acquired neonatal IgG immunity in human immunodeficiency virus infection. J. Infect. Dis. 173:1077-1084. http://dx.doi.org/10.1093/infdis/173.5.1077.
28. Gupta A, Mathad JS, Yang WT, Singh HK, Gupte N, Mave V, Bharadwaj R, Zaman K, Roy E, Bollinger RC, Bhosale R, Steinhoff MC. 2014. Maternal pneumococcal capsular IgG antibodies and transplacental transfer are low in South Asian HIV-infected mother-infant pairs. Vaccine 32:1466-1472. http://dx.doi.org/10.1016/j.vaccine.2014.01.033.
29. van den Berg JP, Westerbeek EA, van der Klis FR, Berbers GA, van Elburg RM. 2011. Transplacental transport of IgG antibodies to preterm infants: a review of the literature. Early Hum. Dev. 87:67-72. http://dx.doi.org/10.1016/j.earlhumdev.2010.11.003.
30. Simister NE. 2003. Placental transport of immunoglobulin G. Vaccine 21:3365-3369. http://dx.doi.org/10.1016/S0264-410X(03)00334-7.
31. Nahm MH, Glezen P, Englund J. 2003. The influence of maternal immunization on light chain response to Haemophilus influenzae type b vaccine. Vaccine 21:3393-3397. http://dx.doi.org/10.1016/S0264-410X(03)00340-2.
32. Carson PJ, Schut RL, Simpson ML, O'Brien J, Janoff EN. 1995. Antibody class and subclass responses to pneumococcal polysaccharides following immunization of human immunodeficiency virus-infected patients. J. Infect. Dis. 172:340-345. http://dx.doi.org/10.1093/infdis/172.2.340.
33. Soininen A, Seppala I, Nieminen T, Eskola J, Kayhty H. 1999. IgG subclass distribution of antibodies after vaccination of adults with pneumococcal conjugate vaccines. Vaccine 17:1889-1897. http://dx.doi.org/10.1016/S0264-410X(98)00475-7.
34. Santosham M, Englund JA, McInnes P, Croll J, Thompson CM, Croll L, Glezen PW, Siber GR. 2001. Safety and antibody persistence following Haemophilus influenzae type b conjugate or pneumococcal polysaccharide vaccines given before pregnancy in women of childbearing age and their infants. Pediatr. Infect. Dis. J. 20:931-940. http://dx.doi.org/10.1097/00006454-200110000-00005.
35. Reikie BA, Naidoo S, Ruck CE, Slogrove AL, de Beer C, la Grange H, Adams RC, Ho K, Smolen K, Speert DP, Cotton MF, Preiser W, Esser M, Kollmann TR. 2013. Antibody responses to vaccination among South African HIV-exposed and unexposed uninfected infants during the first 2 years of life. Clin. Vaccine Immunol. 20:33-38. http://dx.doi.org/10.1128/CVI.00557-12.
36. Rutstein RM, Rudy BJ, Cnaan A. 1996. Response of human immunodeficiency virus-exposed and-infected infants to Haemophilus influenzae type b conjugate vaccine. Arch. Pediatr. Adolesc. Med. 150:838-841. http://dx.doi.org/10.1001/archpedi.1996.02170330064011.
37. Asturias EJ, Mayorga C, Caffaro C, Ramirez P, Ram M, Verstraeten T, Clemens R, Halsey NA. 2009. Differences in the immune response to hepatitis B and Haemophilus influenzae type b vaccines in Guatemalan infants by ethnic group and nutritional status. Vaccine 27:3650-3654. http://dx.doi.org/10.1016/j.vaccine.2009.03.035.
38. Metz JA, Hanieh S, Pradhan R, Joshi A, Shakya D, Shrestha L, Shrestha A, Upadhyay B, Kelly SC, John TM, Maharjan BD, Yu LM, Omar O, Borrow R, Findlow J, Kelly DF, Thorson SM, Adhikari N, Murdoch DR, Pollard AJ. 2012. Evaluation of Haemophilus influenzae type b vaccine for routine immunization in Nepali infants. Pediatr. Infect. Dis. J. 31:e66-72. http://dx.doi.org/10.1097/INF.0b013e31824a9c37.
39. Madhi SA, Kuwanda L, Saarinen L, Cutland C, Mothupi R, Kayhty H, Klugman KP. 2005. Immunogenicity and effectiveness of Haemophilus influenzae type b conjugate vaccine in HIV infected and uninfected African children. Vaccine 23:5517-5525. http://dx.doi.org/10.1016/j.vaccine.2005.07.038.
40. Tregnaghi M, Lopez P, Rocha C, Rivera L, David M, Ruttimann PR, Schuerman L. 2006. A new DTPw-HB/Hib combination vaccine for primary and booster vaccination of infants in Latin America. Rev. Panam. Salud Publica 19:179-188.
41. Lagos R, Valenzuela MT, Levine OS, Losonsky GA, Erazo A, Wasserman SS, Levine MM. 1998. Economisation of vaccination against Haemophilus influenzae type b: a randomised trial of immunogenicity of fractional-dose and two-dose regimens. Lancet 351:1472-1476. http://dx.doi.org/10.1016/S0140-6736(97)07456-4.
42. Eskola J, Ward J, Dagan R, Goldblatt D, Zepp F, Siegrist CA. 1999. Combined vaccination of Haemophilus influenzae type b conjugate and diphtheria-tetanus-pertussis containing acellular pertussis. Lancet 354: 2063-2068. http://dx.doi.org/10.1016/S0140-6736(99)04377-9.
43. Heath PT, Booy R, Azzopardi HJ, Slack MP, Bowen-Morris J, Griffiths H, Ramsay ME, Deeks JJ, Moxon ER. 2000. Antibody concentration and clinical protection after Hib conjugate vaccination in the United Kingdom. JAMA 284:2334-2340. http://dx.doi.org/10.1001/jama.284.18.2334.
44. Kayhty H, Peltola H, Karanko V, Makela PH. 1983. The protective level of serum antibodies to the capsular polysaccharide of Haemophilus influenzae type b. J. Infect. Dis. 147:1100. http://dx.doi.org/10.1093/infdis/147.6.1100.
45. World Health Organization. 2013.WHOposition paper on Haemophilus influenzae type b conjugate vaccines. World Health Organization, Geneva, Switzerland. http://www.who.int/immunization/REH-47-8-pages.pdf. Accessed 30 September 2013.
46. Gessner BD. 2009. Haemophilus influenzae type b vaccine impact in resource-poor settings in Asia and Africa. Expert Rev. Vaccines 8:91-102. http://dx.doi.org/10.1586/14760584.8.1.91.
47. Murphy TV, Pastor P, Medley F, Osterholm MT, Granoff DM. 1983. Decreased Haemophilus colonization in children vaccinated with Haemophilus influenzae type b conjugate vaccine. J. Pediatr. 122:517-523.
48. Fitzwater SP, Watt JP, Levine OS, Santosham M. 2010. Haemophilus influenzae type b conjugate vaccines: considerations for vaccination schedules and implications for developing countries. Hum. Vaccin. 6:810-818. http://dx.doi.org/10.4161/hv.6.10.13017.
49. Trotter CL, McVernon J, Ramsay ME, Whitney CG, Mulholland EK, Goldblatt D, Hombach J, Kieny MP, SAGE subgroup. 2008. Optimising the use of conjugate vaccines to prevent disease caused by Haemophilus influenzae type b, Neisseria meningitidis and Streptococcus pneumoniae. Vaccine 26:4434-4445. http://dx.doi.org/10.1016/j.vaccine.2008.05.073.