Immune responses to cholera in children

Expert Review of Anti-Infective Therapy

Volumn 10, Issue 4, 2012, Pages 435-444

  Leung, Daniel T ^a,b,c   Chowdhury, Fahima ^a   Calderwood, Stephen B ^b,c   Qadri, Firdausi ^a   Ryan, Edward T ^b,c,d  

^a INTERNATIONAL CENTRE FOR DIARRHOEAL DISEASE RESEARCH   (Bangladesh)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

children; cholera; memory B cells; mucosal immunity; oral cholera vaccines

Indexed keywords

CHOLERA HOLOTOXIN; CHOLERA TOXIN; CHOLERA VACCINE; DEFENSIN; GAMMA INTERFERON; IMMUNOGLOBULIN A; IMMUNOGLOBULIN M; INTERLEUKIN 17; INTERLEUKIN 1BETA; LEUKOTRIENE B4; LIPOPOLYSACCHARIDE; MYELOPEROXIDASE; NITRIC OXIDE; PLACEBO; RETINOIC ACID; RETINOL; SECRETORY IMMUNOGLOBULIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; ZINC;

ADAPTIVE IMMUNITY; ANTIBODY AFFINITY; ANTIBODY RESPONSE; ANTIBODY TITER; ANTIGEN DETECTION; ANTIGEN SPECIFICITY; B LYMPHOCYTE; CELLULAR IMMUNITY; CHOLERA; DRUG EFFICACY; DUODENUM BIOPSY; GASTROINTESTINAL MUCOSA; HEREDITY; HUMAN; HUMORAL IMMUNITY; IMMUNOGENICITY; IMMUNOHISTOCHEMISTRY; INFECTION CONTROL; INFECTION PREVENTION; INNATE IMMUNITY; LYMPHOCYTE HOMING; MALNUTRITION; MASS IMMUNIZATION; MEMORY CELL; MIXED INFECTION; NUTRITIONAL DEFICIENCY; PATHOGENESIS; REVIEW; T LYMPHOCYTE; TH1 CELL; TH17 CELL; VIBRIO CHOLERAE; VITAMIN SUPPLEMENTATION; ZINC DEFICIENCY;

B-LYMPHOCYTES; CHILD; CHILD, PRESCHOOL; CHOLERA; CHOLERA VACCINES; HUMANS; IMMUNITY, MUCOSAL; IMMUNOLOGIC MEMORY; INFANT; VIBRIO CHOLERAE O1; VIBRIO CHOLERAE O139;

EID: 84860208692     PISSN: 14787210     EISSN: 17448336     Source Type: Journal    
DOI: 10.1586/eri.12.23     Document Type: Review

References (105)

1. Zuckerman JN, Rombo L, Fisch A. The true burden and risk of cholera: implications for prevention and control. Lancet Infect. Dis. 7(8), 521-530 (2007) (Pubitemid 47079151)
2. Cholera: global surveillance summary, 2008. Wkly Epidemiol. Rec. 84(31), 309-324 (2009).
3. Penrose K, de Castro MC, Werema J, Ryan ET. Informal urban settlements and cholera risk in Dar es Salaam, Tanzania. PLoS Negl. Trop. Dis. 4(3), e631 (2010)
4. Cholera, 2010. Wkly. Epidemiol. Rec. 86(31), 325-339 (2011).
5. Deen JL, von Seidlein L, Sur D et al. The high burden of cholera in children: comparison of incidence from endemic areas in Asia and Africa. PLoS Negl. Trop. Dis. 2(2), e173 (2008).
6. Agtini MD, Soeharno R, Lesmana M et al. The burden of diarrhoea, shigellosis, and cholera in North Jakarta, Indonesia: fndings from 24 months surveillance. BMC Infect. Dis. 5, 89 (2005).
7. Glass RI, Becker S, Huq MI et al. Endemic cholera in rural Bangladesh, 1966-1980. Am. J. Epidemiol. 116(6), 959-970 (1982). (Pubitemid 13209569)
8. Taylor RK, Miller VL, Furlong DB, Mekalanos JJ. Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. Proc. Natl Acad. Sci. USA 84(9), 2833-2837 (1987). (Pubitemid 17064736)
9. Sharp GW, Hynie S. Stimulation of intestinal adenyl cyclase by cholera toxin. Nature 229(5282), 266-269 (1971).
10. Sack DA, Sack RB, Nair GB, Siddique AK. Cholera. Lancet 363(9404), 223-233 (2004). (Pubitemid 38114723)
11. Lindenbaum J, Akbar R, Gordon RS Jr, Greenough WB 3rd, Hirschorn N, Islam MR. Cholera in children. Lancet 1(7446), 1066-1068 (1966).
12. Ryan ET, Dhar U, Khan WA et al. Mortality, morbidity, and microbiology of endemic cholera among hospitalized patients in Dhaka, Bangladesh. Am. J. Trop. Med. Hyg. 63(1-2), 12-20 (2000). (Pubitemid 32423089)
13. Molla AM, Ahmed SM, Greenough WB 3rd. Rice-based oral rehydration solution decreases the stool volume in acute diarrhea. Bull. World Health Organ. 63(4), 751-756 (1985). (Pubitemid 16214160)
14. Lindenbaum J, Greenough WB, Islam MR. Antibiotic therapy of cholera in children. Bull. World Health Organ. 37(4), 529-538 (1967).
15. Lindenbaum J, Greenough WB, Islam MR. Antibiotic therapy of cholera. Bull. World Health Organ. 36(6), 871-883 (1967).
16. Saha D, Karim MM, Khan WA, Ahmed S, Salam MA, Bennish ML. Single-dose azithromycin for the treatment of cholera in adults. N Engl. J. Med. 354(23), 2452-2462 (2006). (Pubitemid 43855048)
17. Harris JB, Larocque RC, Charles RC, Mazumder RN, Khan AI, Bardhan PK. Cholera's western front. Lancet 376 (9757), 1961-1965 (2010).
18. Harris JB, LaRocque RC, Chowdhury F et al. Susceptibility to Vibrio cholerae infection in a cohort of household contacts of patients with cholera in Bangladesh. PLoS Negl. Trop. Dis. 2(4), e221 (2008)
19. Cholera vaccines: WHO position paper. Wkly Epidemiol. Rec. 85(13), 117-128 (2010).
20. Sinclair D, Abba K, Zaman K, Qadri F, Graves PM. Oral vaccines for preventing cholera. Cochrane Database Syst. Rev. 3, CD008603 (2011).
21. Sur D, Kanungo S, Sah B et al. Effcacy of a low-cost, inactivated whole-cell oral cholera vaccine: results from 3 years of follow-up of a randomized, controlled trial. PLoS Negl. Trop. Dis. 5(10), e1289 (2011).
22. Ali M, Emch M, Park JK, Yunus M, Clemens J. Natural cholera infection-derived immunity in an endemic setting. J. Infect. Dis. 204(6), 912-918 (2011).
23. Levine MM, Black RE, Clements ML, Cisneros L, Nalin DR, Young CR. Duration of infection-derived immunity to cholera. J. Infect. Dis. 143(6), 818-820 (1981). (Pubitemid 11062231)
24. Koelle K, Rodo X, Pascual M, Yunus M, Mostafa G. Refractory periods and climate forcing in cholera dynamics. Nature 436(7051), 696-700 (2005). (Pubitemid 41117271)
25. Qadri F, Raqib R, Ahmed F et al. Increased levels of infammatory mediators in children and adults infected with Vibrio cholerae O1 and O139. Clin. Diagn. Lab. Immunol. 9(2), 221-229 (2002). (Pubitemid 34226010)
26. Qadri F, Bhuiyan TR, Dutta KK et al. Acute dehydrating disease caused by Vibrio cholerae serogroups O1 and O139 induce increases in innate cells and infammatory mediators at the mucosal surface of the gut. Gut 53(1), 62-69 (2004). (Pubitemid 38083012)
27. Flach CF, Qadri F, Bhuiyan TR et al Broad up-regulation of innate defense factors during acute cholera. Infect. Immun. 75(5), 2343-2350 (2007). (Pubitemid 46744323)
28. Rabbani GH, Islam S, Chowdhury AK, Mitra AK, Miller MJ, Fuchs G. Increased nitrite and nitrate concentrations in sera and urine of patients with cholera or shigellosis. Am. J. Gastroenterol. 96(2), 467-472 (2001).
29. Mathan MM, Chandy G, Mathan VI. Ultrastructural changes in the upper small intestinal mucosa in patients with cholera. Gastroenterology 109(2), 422-430 (1995).
30. Shirin T, Rahman A, Danielsson A et al. Antimicrobial peptides in the duodenum at the acute and convalescent stages in patients with diarrhea due to Vibrio cholerae O1 or enterotoxigenic Escherichia coli infection. Microbes Infect. 13(12-13), 1111-1120 (2011).
31. Shin OS, Uddin T, Citorik R et al. LPLUNC1 modulates innate immune responses to Vibrio cholerae. J. Infect. Dis. 204(9), 1349-1357 (2011).
32. PrabhuDas M, Adkins B, Gans H et al. Challenges in infant immunity: implications for responses to infection and vaccines. Nat. Immunol. 12(3), 189-194 (2011).
33. Corbett NP, Blimkie D, Ho KC et al. Ontogeny of Toll-like receptor mediated cytokine responses of human blood mononuclear cells. PLoS One 5(11), e15041 (2010).
34. Sheikh A, Shamsuzzaman S, Ahmad SM et al. Zinc infuences innate immune responses in children with enterotoxigenic Escherichia coli-induced diarrhea. J. Nutr. 140 (5), 1049-1056 (2010).
35. Neoh SH, Rowley D. The antigens of Vibrio cholerae involved in the vibriocidal action of antibody and complement. J. Infect. Dis. 121(5), 505-513 (1970).
36. Losonsky GA, Yunyongying J, Lim V et al. Factors infuencing secondary vibriocidal immune responses: relevance for understanding immunity to cholera. Infect. Immun. 64(1), 10-15 (1996). (Pubitemid 26009334)
37. Majumdar AS, Ghose AC. Evaluation of the biological properties of different classes of human antibodies in relation to cholera. Infect. Immun. 32(1), 9-14 (1981). (Pubitemid 11156894)
38. Mosley WH, Ahmad S, Benenson AS, Ahmed A. The relationship of vibriocidal antibody titre to susceptibility to cholera in family contacts of cholera patients. Bull. World Health Organ. 38(5), 777-785 (1968).
39. Harris AM, Bhuiyan MS, Chowdhury F et al. Antigen-specific memory B-cell responses to Vibrio cholerae O1 infection in Bangladesh. Infect. Immun. 77(9), 3850-3856 (2009).
40. Clements ML, Levine MM, Young CR et al. Magnitude, kinetics, and duration of vibriocidal antibody responses in North Americans after ingestion of Vibrio cholerae. J. Infect. Dis. 145(4), 465-473 (1982). (Pubitemid 12158331)
41. Mosley WH, Benenson AS, Barui R. A serological survey for cholear antibodies in rural east Pakistan. 1. The distribution of antibody in the control population of a cholera-vaccine feld-trial area and the relation of antibody titre to the pattern of endemic cholera. Bull. World Health Organ. 38(3), 327-334 (1968).
42. Glass RI, Svennerholm AM, Khan MR, Huda S, Huq MI, Holmgren J. Seroepidemiological studies of El Tor cholera in Bangladesh: association of serum antibody levels with protection. J. Infect. Dis. 151(2), 236-242 (1985). (Pubitemid 15162711)
43. Mosley WH, McCormack WM, Ahmed A, Chowdhury AK, Barui RK. Report of the 1966-67 cholera vaccine feld trial in rural East Pakistan. 2. Results of the serological surveys in the study population-the relationship of case rate to antibody titre and an estimate of the inapparent infection rate with Vibrio cholerae. Bull. World Health Organ. 40(2), 187-197 (1969).
44. Saha D, LaRocque RC, Khan AI et al Incomplete correlation of serum vibriocidal antibody titer with protection from Vibrio cholerae infection in urban Bangladesh. J. Infect. Dis. 189(12), 2318-2322 (2004). (Pubitemid 38757206)
45. Chowdhury F, Khan AI, Harris JB et al A comparison of clinical and immunologic features in children and older patients hospitalized with severe cholera in Bangladesh. Pediatr. Infect. Dis. J. 27(11), 986-992 (2008).
46. Leung DT, Rahman MA, Mohasin M et al A comparison of memory B cell, antibody secreting cell, and plasma antibody responses in young children, older children, and adults with infection caused by Vibrio cholerae O1 El Tor Ogawa in Bangladesh. Clin. Vaccine Immunol. 18(8), 1317-1325 (2011).
47. Clemens JD, Stanton BF, Chakraborty J et al. B subunit-whole cell and whole cell-only oral vaccines against cholera: studies on reactogenicity and immunogenicity. J. Infect. Dis. 155(1), 79-85 (1987). (Pubitemid 17225086)
48. Sack DA, Clemens JD, Huda S et al Antibody responses after immunization with killed oral cholera vaccines during the 1985 vaccine feld trial in Bangladesh. J. Infect. Dis. 164(2), 407-411 (1991).
49. Saha A, Chowdhury MI, Khanam F et al. Safety and immunogenicity study of a killed bivalent (O1 and O139) whole-cell oral cholera vaccine Shanchol, in Bangladeshi adults and children as young as 1 year of age. Vaccine 29(46), 8285-8292 (2011).
50. Qadri F, Chowdhury MI, Faruque SM et al. Peru-15, a live attenuated oral cholera vaccine, is safe and immunogenic in Bangladeshi toddlers and infants. Vaccine 25(2), 231-238 (2007). (Pubitemid 44856084)
51. Taylor DN, Cardenas V, Perez J, Puga R, Svennerholm AM. Safety, immunogenicity, and lot stability of the whole cell/recombinant B subunit (WC/rCTB) cholera vaccine in Peruvian adults and children. Am. J. Trop. Med. Hyg. 61(6), 869-873 (1999). (Pubitemid 30084104)
52. Su-Arehawaratana P, Singharaj P, Taylor DN et al. Safety and immunogenicity of different immunization regimens of CVD 103-HgR live oral cholera vaccine in soldiers and civilians in Thailand. J. Infect. Dis. 165(6), 1042-1048 (1992).
53. Kanungo S, Paisley A, Lopez AL et al Immune responses following one and two doses of the reformulated, bivalent, killed, whole-cell, oral cholera vaccine among adults and children in Kolkata, India: a randomized, placebo-controlled trial. Vaccine 27(49), 6887-6893 (2009).
54. Mahalanabis D, Lopez AL, Sur D et al A randomized, placebo-controlled trial of the bivalent killed, whole-cell, oral cholera vaccine in adults and children in a cholera endemic area in Kolkata, India. PLoS One 3(6), e2323 (2008).
55. Mantis NJ, Rol N, Corthesy B. Secretory IgA's complex roles in immunity and mucosal homeostasis in the gut. Mucosal Immunol. 4(6), 603-611 (2011).
56. Stiehm ER, Fudenberg HH. Serum levels of immune globulins in health and disease: a survey. Pediatrics 37(5), 715-727 (1966).
57. Chowdhury F, Rahman MA, Begum YA et al. Impact of rapid urbanization on the rates of infection by Vibrio cholerae O1 and enterotoxigenic Escherichia coli in Dhaka, Bangladesh. PLoS Negl. Trop. Dis. 5(4), e999 (2011).
58. Smith NW, Sack RB. Immunologic cross-reactions of enterotoxins from Escherichia coli and Vibrio cholerae. J. Infect. Dis. 127(2), 164-170 (1973).
59. Qadri F, Ahmed T, Wahed MA et al. Suppressive effect of zinc on antibody response to cholera toxin in children given the killed, B subunit-whole cell, oral cholera vaccine. Vaccine 22(3-4), 416-421 (2004). (Pubitemid 37510272)
60. Ahmed T, Svennerholm AM, Al Tarique A, Sultana GN, Qadri F. Enhanced immunogenicity of an oral inactivated cholera vaccine in infants in Bangladesh obtained by zinc supplementation and by temporary withholding breast-feeding. Vaccine 27(9), 1433-1439 (2009).
61. Nandy RK, Albert MJ, Ghose AC. Serum antibacterial and antitoxin responses in clinical cholera caused by Vibrio cholerae O139 Bengal and evaluation of their importance in protection. Vaccine 14 (12), 1137-1142 (1996). (Pubitemid 26348832)
62. Qadri F, Mohi G, Hossain J et al. Comparison of the vibriocidal antibody response in cholera due to Vibrio cholerae O139 Bengal with the response in cholera due to Vibrio cholerae O1. Clin. Diagn. Lab. Immunol. 2(6), 685-688 (1995).
63. Qadri F, Chowdhury MI, Faruque SM et al. Randomized, controlled study of the safety and immunogenicity of Peru-15, a live attenuated oral vaccine candidate for cholera, in adult volunteers in Bangladesh. J. Infect. Dis. 192(4), 573-579 (2005). (Pubitemid 41099305)
64. Clutterbuck EA, Oh S, Hamaluba M, Westcar S, Beverley PC, Pollard AJ. Serotype-specific and age-dependent generation of pneumococcal polysaccharide-specific memory B-cell and antibody responses to immunization with a pneumococcal conjugate vaccine. Clin. Vaccine Immunol. 15(2), 182-193 (2008). (Pubitemid 352025528)
65. Alam MM, Riyadh MA, Fatema K et al. Antigen-specific memory B-cell responses in Bangladeshi adults after one-or two-dose oral killed cholera vaccination and comparison with responses in patients with naturally acquired cholera. Clin. Vaccine Immunol. 18(5), 844-850 (2011).
66. Qadri F, Ahmed F, Karim MM et al. Lipopolysaccharide-and cholera toxinspecific subclass distribution of B-cell responses in cholera. Clin. Diagn. Lab. Immunol. 6(6), 812-818 (1999). (Pubitemid 29529971)
67. Boes M. Role of natural and immune IgM antibodies in immune responses. Mol. Immunol. 37(18), 1141-1149 (2000).
68. Brandtzaeg P. The mucosal immune system and its integration with the mammary glands. J. Pediatr. 156(2 Suppl.), S8-S15 (2010).
69. Belgemen T, Suskan E, Dogu F, Ikinciogullari A. Selective immunoglobulin M defciency presenting with recurrent impetigo: a case report and review of the literature. Int. Arch. Allergy Immunol. 149(3), 283-288 (2009).
70. Croft NM, Hodges M. IgM: mucosal response in acute diarrhoeal disease of infants. Scand. J. Gastroenterol. 40(8), 965-971 (2005). (Pubitemid 41117022)
71. Kendall EA, Tarique AA, Hossain A et al. Development of immunoglobulin M memory to both a T-cell-independent and a T-cell-dependent antigen following infection with Vibrio cholerae O1 in Bangladesh. Infect. Immun. 78 (1), 253-259 (2010).
72. Mond JJ, Vos Q, Lees A, Snapper CM. T cell independent antigens. Curr. Opin. Immunol. 7(3), 349-354 (1995).
73. Kelly DF, Pollard AJ, Moxon ER. Immunological memory: the role of B cells in long-term protection against invasive bacterial pathogens. JAMA 294(23), 3019-3023 (2005). (Pubitemid 41817664)
74. Jertborn M, Svennerholm AM, Holmgren J. Saliva, breast milk, and serum antibody responses as indirect measures of intestinal immunity after oral cholera vaccination or natural disease. J. Clin. Microbiol. 24(2), 203-209 (1986). (Pubitemid 16077190)
75. Svennerholm AM, Jertborn M, Gothefors L, Karim AM, Sack DA, Holmgren J. Mucosal antitoxic and antibacterial immunity after cholera disease and after immunization with a combined B subunit-whole cell vaccine. J. Infect. Dis. 149(6), 884-893 (1984). (Pubitemid 14082150)
76. Uddin T, Harris JB, Bhuiyan TR et al. Mucosal immunologic responses in cholera patients in Bangladesh. Clin. Vaccine Immunol. 18(3), 506-512 (2011).
77. Czerkinsky C, Prince SJ, Michalek SM et al. IgA antibody-producing cells in peripheral blood after antigen ingestion: evidence for a common mucosal immune system in humans. Proc. Natl Acad. Sci. USA 84(8), 2449-2453 (1987). (Pubitemid 17082366)
78. Qadri F, Wenneras C, Albert MJ et al. Comparison of immune responses in patients infected with Vibrio cholerae O139 and O1. Infect. Immun. 65(9), 3571-3576 (1997). (Pubitemid 27398109)
79. Datta SK, Sabet M, Nguyen KP et al. Mucosal adjuvant activity of cholera toxin requires Th17 cells and protects against inhalation anthrax. Proc. Natl Acad. Sci. USA 107(23), 10638-10643 (2010).
80. Velaga S, Herbrand H, Friedrichsen M et al. Chemokine receptor CXCR5 supports solitary intestinal lymphoid tissue formation, B cell homing, and induction of intestinal IgA responses. J. Immunol. 182(5), 2610-2619 (2009).
81. Bhuiyan TR, Lundin SB, Khan AI et al Cholera caused by Vibrio cholerae O1 induces T-cell responses in the circulation. Infect. Immun. 77(5), 1888-1893 (2009).
82. Weil AA, Arifuzzaman M, Bhuiyan TR et al. Memory T-cell responses to Vibrio cholerae O1 infection. Infect. Immun. 77(11), 5090-5096 (2009).
83. + T-cell responses in blood and intestinal mucosa of infected humans. Clin. Vaccine Immunol. 18(8), 1371-1377 (2011).
84. + T-cell responses to an oral inactivated cholera vaccine in young children in a cholera endemic country and the enhancing effect of zinc supplementation. Vaccine 28(2), 422-429 (2009).
85. Levine MM. Immunogenicity and effcacy of oral vaccines in developing countries: lessons from a live cholera vaccine. BMC Biol. 8, 129 (2010).
86. Saha DR, Rajendran K, Ramamurthy T, Nandy RK, Bhattacharya SK. Intestinal parasitism and Vibrio cholerae infection among diarrhoeal patients in Kolkata, India. Epidemiol. Infect. 136(5), 661-664 (2008). (Pubitemid 351472176)
87. Cooper PJ, Chico ME, Losonsky G et al Albendazole treatment of children with ascariasis enhances the vibriocidal antibody response to the live attenuated oral cholera vaccine CVD 103-HgR. J. Infect. Dis. 182(4), 1199-1206 (2000).
88. Harris JB, Podolsky MJ, Bhuiyan TR et al. Immunologic responses to Vibrio cholerae in patients co-infected with intestinal parasites in Bangladesh. PLoS Negl. Trop. Dis. 3(3), e403 (2009).
89. Cooper PJ, Chico M, Sandoval C et al. Human infection with Ascaris lumbricoides is associated with suppression of the interleukin-2 response to recombinant cholera toxin B subunit following vaccination with the live oral cholera vaccine CVD 103-HgR. Infect. Immun. 69 (3), 1574-1580 (2001). (Pubitemid 32187611)
90. Chowdhury F, Begum YA, Alam MM et al. Concomitant enterotoxigenic Escherichia coli infection induces increased immune responses to Vibrio cholerae O1 antigens in patients with cholera in Bangladesh. Infect. Immun. 78(5), 2117-2124 (2010).
91. Glass RI, Holmgren J, Haley CE et al. Predisposition for cholera of individuals with O blood group. Possible evolutionary signifcance. Am. J. Epidemiol. 121(6), 791-796 (1985). (Pubitemid 15028255)
92. Harris JB, Khan AI, LaRocque RC et al. Blood group, immunity, and risk of infection with Vibrio cholerae in an area of endemicity. Infect. Immun. 73(11), 7422-7427 (2005). (Pubitemid 41587645)
93. LaRocque RC, Sabeti P, Duggal P et al. A variant in long palate, lung and nasal epithelium clone 1 is associated with cholera in a Bangladeshi population. Genes Immun. 10(3), 267-272 (2009).
94. Barry WS, Pierce NF. Protein deprivation causes reversible impariment of mucosal immune response to cholera toxoid/toxin in rat gut. Nature 281(5726), 64-65 (1979). (Pubitemid 9247991)
95. Flo J, Roux ME, Massouh E. Defcient induction of the immune response to oral immunization with cholera toxin in malnourished rats during suckling. Infect. Immun. 62(11), 4948-4954 (1994). (Pubitemid 24332800)
96. Guerrant RL, Oria RB, Moore SR, Oria MO, Lima AA. Malnutrition as an enteric infectious disease with long-term effects on child development. Nutr. Rev. 66(9), 487-505 (2008).
97. Baqui AH, Black RE, Arifeen SE, Hill K, Mitra SN, al Sabir A. Causes of childhood deaths in Bangladesh: results of a nationwide verbal autopsy study. Bull. World Health Organ. 76(2), 161-171 (1998). (Pubitemid 28305229)
98. Black RE, Allen LH, Bhutta ZA et al. Maternal and child undernutrition: global and regional exposures and health consequences. Lancet 371(9608), 243-260 (2008).
99. Palmer DL, Koster FT, Alam AK, Islam MR. Nutritional status: a determinant of severity of diarrhea in patients with cholera. J. Infect. Dis. 134(1), 8-14 (1976).
100. + T cell-mediated immunity. J. Exp. Med. 208(9), 1767-1775 (2011).
101. Mayo-Wilson E, Imdad A, Herzer K, Yakoob MY, Bhutta ZA. Vitamin A supplements for preventing mortality, illness, and blindness in children aged under 5: systematic review and meta analysis. BMJ 343, d5094 (2011).
102. Albert MJ, Qadri F, Wahed MA et al. Supplementation with zinc, but not vitamin A, improves seroconversion to vibriocidal antibody in children given an oral cholera vaccine. J. Infect. Dis. 187(6), 909-913 (2003). (Pubitemid 36337903)
103. Aggarwal R, Sentz J, Miller MA. Role of zinc administration in prevention of childhood diarrhea and respiratory illnesses: a meta-analysis. Pediatrics 119 (6), 1120-1130 (2007). (Pubitemid 46871267)
104. Roy SK, Hossain MJ, Khatun W et al. Zinc supplementation in children with cholera in Bangladesh: randomised controlled trial. BMJ 336(7638), 266-268 (2008). (Pubitemid 351251628)
105. Humphrey JH. Child undernutrition, tropical enteropathy, toilets, and handwashing. Lancet 374(9694), 1032-1035 (2009).