Plasmodium falciparum malaria and invasive bacterial co-infection in young African children: The dysfunctional spleen hypothesis

Malaria Journal

Volumn 13, Issue 1, 2014, Pages

  Gómez Pérez, Gloria P ^a,b   Van Bruggen, Robin ^b   Grobusch, Martin P ^b   Dobaño, Carlota ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Children; Hyposplenism; Invasive bacterial infection; Malaria; Marginal zone B cells; Plasmodium; Spleen

Indexed keywords

ANTIBODY; COMPLEMENT;

AFRICAN; ANTIBODY RESPONSE; B LYMPHOCYTE; BACTERIAL INFECTION; BRAIN MALARIA; CHILDHOOD DISEASE; COMPLEMENT ALTERNATIVE PATHWAY; DISEASE ASSOCIATION; HUMAN; IMMATURITY; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOCOMPROMISED PATIENT; INFECTION RISK; INFLAMMATION; INVASIVE BACTERIAL INFECTION; MALARIA; MALARIA FALCIPARUM; MIXED INFECTION; MONOCYTE; NEUTROPHIL; NONHUMAN; OPSONIZATION; PREVALENCE; RETINOL DEFICIENCY; REVIEW; RISK ASSESSMENT; RISK FACTOR; SPLEEN DEFECT; SPLEEN FUNCTION; SPLENECTOMY; SPLENOMEGALY; BACTERIAL INFECTIONS; CHILD; COINFECTION; COMPLICATION; DISEASE PREDISPOSITION; IMMUNOLOGY; SPLEEN;

BACTERIAL INFECTIONS; CHILD; COINFECTION; DISEASE SUSCEPTIBILITY; HUMANS; MALARIA, FALCIPARUM; SPLEEN;

EID: 84907982676     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/1475-2875-13-335     Document Type: Review

References (141)

1. Ogilvie C, Evans C: Splenomegaly. In Chamberlaine's Symptoms and Signs in Clinical Medicine. 11th edition. Edited by Ogilvie C, Evans C. Brucks, Butterworth: EBLS; 1987.
2. Doolan DL: Malaria Methods and Protocols. Totowa, New Yersey: Humana Press Inc; 2002.
3. Weill JC, Weller S, Reynaud CA: Human marginal zone B cells. Annu Rev Immunol 2009, 27:267-285.
4. Weller S, Mamani-Matsuda M, Picard C, Cordier C, Lecoeuche D, Gauthier F, Weill JC, Reynaud CA: Somatic diversification in the absence of antigen-driven responses is the hallmark of the IgM + IgD + CD27+ B cell repertoire in infants. J Exp Med 2008, 205:1331-1342.
5. Timens W, Boes A, Rozeboom-Uiterwijk T, Poppema S: Immaturity of the human splenic marginal zone in infancy. Possible contribution to the deficient infant immune response. J Immunol 1989, 143:3200-3206.
6. Bowdler A: The Complete Spleen: Structure, Function and Clinical Disorders. 2nd edition. New Yersey: Humana Press; 2002.
7. Zandvoort A, Timens W: The dual function of the splenic marginal zone: essential for initiation of anti-TI-2 responses but also vital in the general first-line defense against blood-borne antigens. Clin Exp Immunol 2002, 130:4-11.
8. Martin F, Oliver AM, Kearney JF: Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens. Immunity 2001, 14:617-629.
9. Magri G, Miyajima M, Bascones S, Mortha A, Puga I, Cassis L, Barra CM, Comerma L, Chudnovskiy A, Gentile M, Llige D, Cols M, Serrano S, Arostegui JI, Juan M, Yague J, Merad M, Fagarasan S, Cerutti A: Innate lymphoid cells integrate stromal and immunological signals to enhance antibody production by splenic marginal zone B cells. Nat Immunol 2014, 15:354-364.
10. Mebius RE, Kraal G: Structure and function of the spleen. Nat Rev Immunol 2005, 5:606-616.
11. Lammers AJ, de Porto AP, Bennink RJ, van Leeuwen EM, Biemond BJ, Goslings JC, van Marle J, ten Berge IJ, Speelman P, Hoekstra JB: Hyposplenism: comparison of different methods for determining splenic function. Am J Hematol 2012, 87:484-489.
12. Krucken J, Mehnert LI, Dkhil MA, El-Khadragy M, Benten WP, Mossmann H, Wunderlich F: Massive destruction of malaria-parasitized red blood cells despite spleen closure. Infect Immun 2005, 73:6390-6398.
13. Cerutti A, Cols M, Puga I: Marginal zone B cells: virtues of innate-like antibody-producing lymphocytes. Nat Rev Immunol 2013, 13:118-132.
14. Barral P, Sanchez-Nino MD, van Rooijen N, Cerundolo V, Batista FD: The location of splenic NKT cells favours their rapid activation by blood-borne antigen. EMBO J 2012, 31:2378-2390.
15. Steiniger B, Barth P, Hellinger A: The perifollicular and marginal zones of the human splenic white pulp : do fibroblasts guide lymphocyte immigration? Am J Pathol 2001, 159:501-512.
16. Puga I, Cols M, Barra CM, He B, Cassis L, Gentile M, Comerma L, Chorny A, Shan M, Xu W, Magri G, Knowles DM, Tam W, Chiu A, Bussel JB, Serrano S, Lorente JA, Bellosillo B, Lloreta J, Juanpere N, Alameda F, Baro T, de Heredia CD, Toran N, Catala A, Torrebadell M, Fortuny C, Cusi V, Carreras C, Diaz GA: B cell-helper neutrophils stimulate the diversification and production of immunoglobulin in the marginal zone of the spleen. Nat Immunol 2012, 13:170-180.
17. Henry K, Symmers WSC: Thymus, Lymph Nodes, Spleen and Lymphatics. In Sytemic Pathology. 3rd edition. New York: Churchill Livingstone; 1992.
18. Buffet PA, Safeukui I, Deplaine G, Brousse V, Prendki V, Thellier M, Turner GD, Mercereau-Puijalon O: The pathogenesis of Plasmodium falciparum malaria in humans: insights from splenic physiology. Blood 2011, 117:381-392.
19. Kraal G, Mebius R: New insights into the cell biology of the marginal zone of the spleen. Int Rev Cytol 2006, 250:175-215.
20. Weiss L: The spleen in malaria: the role of barrier cells. Immunol Lett 1990, 25:165-172.
21. Schwarzer E, Turrini F, Ulliers D, Giribaldi G, Ginsburg H, Arese P: Impairment of macrophage functions after ingestion of Plasmodium falciparum-infected erythrocytes or isolated malarial pigment. J Exp Med 1992, 176:1033-1041.
22. Cunnington AJ, de Souza JB, Walther M, Riley EM: Malaria impairs resistance to Salmonella through heme-and heme oxygenase-dependent dysfunctional granulocyte mobilization. Nat Med 2012, 18:120-127.
23. Urban BC, Roberts DJ: Malaria, monocytes, macrophages and myeloid dendritic cells: sticking of infected erythrocytes switches off host cells. Curr Opin Immunol 2002, 14:458-465.
24. Weiss GE, Crompton PD, Li S, Walsh LA, Moir S, Traore B, Kayentao K, Ongoiba A, Doumbo OK, Pierce SK: Atypical memory B cells are greatly expanded in individuals living in a malaria-endemic area. J Immunol 2009, 183:2176-2182.
25. Weiss GE, Clark EH, Li S, Traore B, Kayentao K, Ongoiba A, Hernandez JN, Doumbo OK, Pierce SK, Branch OH, Crompton PD: A positive correlation between atypical memory B cells and Plasmodium falciparum transmission intensity in cross-sectional studies in Peru and Mali. PLoS One 2011, 6:e15983.
26. Illingworth J, Butler NS, Roetynck S, Mwacharo J, Pierce SK, Bejon P, Crompton PD, Marsh K, Ndungu FM: Chronic exposure to Plasmodium falciparum is associated with phenotypic evidence of B and T cell exhaustion. J Immunol 2013, 190:1038-1047.
27. Greenwood BM, Bradley AK, Blakebrough IS, Whittle HC, Marshall TF, Gilles HM: The immune response to a meningococcal polysaccharide vaccine in an African village. Trans R Soc Trop Med Hyg 1980, 74:340-346.
28. Portugal S, Moebius J, Skinner J, Doumbo S, Doumtabe D, Kone Y, Dia S, Kanakabandi K, Sturdevant DE, Virtaneva K, Porcella SF, Li S, Doumbo OK, Kayentao K, Ongoiba A, Traore B, Crompton PD: Exposure-dependent control of malaria-induced inflammation in children. PLoS Pathog 2014, 10:e1004079.
29. Mooney JP, Butler BP, Lokken KL, Xavier MN, Chau JY, Schaltenberg N, Dandekar S, George MD, Santos RL, Luckhart S, Tsolis RM: The mucosal inflammatory response to non-typhoidal Salmonella in the intestine is blunted by IL-10 during concurrent malaria parasite infection. Mucosal Immunol 2014. Advance online publication, 26 March 2014.
30. Scott JA, Berkley JA, Mwangi I, Ochola L, Uyoga S, Macharia A, Ndila C, Lowe BS, Mwarumba S, Bauni E, Marsh K, Williams TN: Relation between falciparum malaria and bacteraemia in Kenyan children: a populationbased, case-control study and a longitudinal study. Lancet 2011, 378:1316-1323.
31. Bassat Q, Guinovart C, Sigauque B, Mandomando I, Aide P, Sacarlal J, Nhampossa T, Bardaji A, Morais L, Machevo S, Letang E, Macete E, Aponte JJ, Roca A, Menendez C, Alonso PL: Severe malaria and concomitant bacteraemia in children admitted to a rural Mozambican hospital. Trop Med Int Health 2009, 14:1011-1019.
32. Bronzan RN, Taylor TE, Mwenechanya J, Tembo M, Kayira K, Bwanaisa L, Njobvu A, Kondowe W, Chalira C, Walsh AL, Phiri A, Wilson LK, Molyneux ME, Graham SM: Bacteremia in Malawian children with severe malaria: prevalence, etiology, HIV coinfection, and outcome. J Infect Dis 2007, 195:895-904.
33. Church J, Maitland K: Invasive bacterial co-infection in African children with Plasmodium falciparum malaria: a systematic review. BMC Med 2014, 12:31.
34. Nadjm B, Mtove G, Amos B, Walker NF, Diefendal H, Reyburn H, Whitty CJ: Severe febrile illness in adult hospital admissions in Tanzania: a prospective study in an area of high malaria transmission. Trans R Soc Trop Med Hyg 2012, 106:688-695.
35. Berkley JA, Lowe BS, Mwangi I, Williams T, Bauni E, Mwarumba S, Ngetsa C, Slack MP, Njenga S, Hart CA, Maitland K, English M, Marsh K, Scott JA: Bacteremia among children admitted to a rural hospital in Kenya. N Engl J Med 2005, 352:39-47.
36. Mtove G, Amos B, von Seidlein L, Hendriksen I, Mwambuli A, Kimera J, Mallahiyo R, Kim DR, Ochiai RL, Clemens JD, Reyburn H, Magesa S, Deen JL: Invasive salmonellosis among children admitted to a rural Tanzanian hospital and a comparison with previous studies. PLoS One 2010, 5:e9244.
37. Oundo JO, Muli F, Kariuki S, Waiyaki PG, Iijima Y, Berkley J, Kokwaro GO, Ngetsa CJ, Mwarumba S, Torto R, Lowe B: Non-typhi salmonella in children with severe malaria. East Afr Med J 2002, 79:633-639.
38. Brent AJ, Oundo JO, Mwangi I, Ochola L, Lowe B, Berkley JA: Salmonella bacteremia in Kenyan children. Pediatr Infect Dis J 2006, 25:230-236.
39. Feasey NA, Dougan G, Kingsley RA, Heyderman RS, Gordon MA: Invasive non-typhoidal salmonella disease: an emerging and neglected tropical disease in Africa. Lancet 2012, 379:2489-2499.
40. Graham SM, Walsh AL, Molyneux EM, Phiri AJ, Molyneux ME: Clinical presentation of non-typhoidal Salmonella bacteraemia in Malawian children. Trans R Soc Trop Med Hyg 2000, 94:310-314.
41. Feasey NA, Archer BN, Heyderman RS, Sooka A, Dennis B, Gordon MA, Keddy KH: Typhoid fever and invasive nontyphoid salmonellosis, Malawi and South Africa. Emerg Infect Dis 2010, 16:1448-1451.
42. Mandomando I, Macete E, Sigauque B, Morais L, Quinto L, Sacarlal J, Espasa M, Valles X, Bassat Q, Aide P, Nhampossa T, Machevo S, Ruiz J, Nhacolo A, Menendez C, Kotloff KL, Roca A, Levine MM, Alonso PL: Invasive non-typhoidal Salmonella in Mozambican children. Trop Med Int Health 2009, 14:1467-1474.
43. Maclennan CA: Out of Africa: links between invasive nontyphoidal salmonella disease, typhoid Fever, and malaria. Clin Infect Dis 2014, 58:648-650.
44. Morpeth SC, Ramadhani HO, Crump JA: Invasive non-Typhi Salmonella disease in Africa. Clin Infect Dis 2009, 49:606-611.
45. Di Sabatino A, Carsetti R, Corazza GR: Post-splenectomy and hyposplenic states. Lancet 2011, 378:86-97.
46. Gordon MA: Salmonella infections in immunocompromised adults. J Infect 2008, 56:413-422.
47. Noriega LM, Van der Auwera P, Daneau D, Meunier F, Aoun M: Salmonella infections in a cancer center. Support Care Cancer 1994, 2:116-122.
48. Ram S, Lewis LA, Rice PA: Infections of people with complement deficiencies and patients who have undergone splenectomy. Clin Microbiol Rev 2010, 23:740-780.
49. Roberts AR, Hilburg LE: Sickle cell disease with Salmonella osteomyelitis. J Pediatr 1958, 52:170-175.
50. Zumla A, Lewis D, Brown J: Ciprofloxacin treatment of recurrent Salmonella typhimurium septicaemia in a splenectomized and immunosuppressed patient. J Antimicrob Chemother 1988, 21:809-810.
51. Angelski CL, McKay E, Blackie B: A case of functional asplenia and pneumococcal sepsis. Pediatr Emerg Care 2011, 27:639-641.
52. Foschi FG, Trevisani F, Loggi E, Parazza M, Melotti C, Bedeschi E, Mingazzini L, Cappa FM, Cescon M, Andreone P, Grazi G, Stefanini GF, Bernardi M: Effect of liver transplantation on tuftsin activity and phagocytic activity of neutrophil granulocytes in patients with liver cirrhosis. Int Arch Allergy Immunol 2005, 137:258-262.
53. Hsu RB, Chen RJ, Chu SH: Nontyphoid Salmonella bacteremia in patients with liver cirrhosis. Am J Med Sci 2005, 329:234-237.
54. Eraklis AJ, Filler RM: Splenectomy in childhood: a review of 1413 cases. J Pediatr Surg 1972, 7:382-388.
55. Lammers AJ: Living without a spleen. Ned Tijdschr Tandheelkd 2010, 117:611-614.
56. van Egmond M, van Garderen E, van Spriel AB, Damen CA, van Amersfoort ES, van Zandbergen G, van Hattum J, Kuiper J, van de Winkel JG: FcalphaRI-positive liver Kupffer cells: reappraisal of the function of immunoglobulin A in immunity. Nat Med 2000, 6:680-685.
57. Overturf G, Powars D: Infections in sickle cell anemia: pathogenesis and control. Tex Rep Biol Med 1980, 40:283-292.
58. Wong WY, Overturf GD, Powars DR: Infection caused by Streptococcus pneumoniae in children with sickle cell disease: epidemiology, immunologic mechanisms, prophylaxis, and vaccination. Clin Infect Dis 1992, 14:1124-1136.
59. Luzzatto L: Sickle cell anaemia and malaria. Mediterr J Hematol Infect Dis 2012, 4:e2012065.
60. Kruetzmann S, Rosado MM, Weber H, Germing U, Tournilhac O, Peter HH, Berner R, Peters A, Boehm T, Plebani A, Quinti I, Carsetti R: Human immunoglobulin M memory B cells controlling Streptococcus pneumoniae infections are generated in the spleen. J Exp Med 2003, 197:939-945.
61. Wong WY: Prevention and management of infection in children with sickle cell anaemia. Paediatr Drugs 2001, 3:793-801.
62. El-Hazmi MA: Infections in sickle cell disease. Ann Saudi Med 1986, 6:33-41.
63. Romero-Legro I, Kadaria D, Murillo LC, Freire AX: Intravenous gammaglobulin as rescue therapy in a patient with sickle cell and septic shock. Tenn Med 2013, 106:29-31.
64. Navolotskaya EV: The second life of antibodies. Biochemistry (Mosc) 2014, 79:1-7.
65. Spirer Z, Weisman Y, Zakuth V, Fridkin M, Bogair N: Decreased serum tuftsin concentrations in sickle cell disease. Arch Dis Child 1980, 55:566-567.
66. Humbert JR, Winsor EL, Githens JM, Schmitz JB: Neutrophil dysfunctions in sickle cell disease. Biomed Pharmacother 1990, 44:153-158.
67. Agrawal AK, Gupta CM: Tuftsin-bearing liposomes in treatment of macrophage-based infections. Adv Drug Deliv Rev 2000, 41:135-146.
68. Horvati K, Bacsa B, Szabo N, David S, Mezo G, Grolmusz V, Vertessy B, Hudecz F, Bosze S: Enhanced cellular uptake of a new, in silico identified antitubercular candidate by peptide conjugation. Bioconjug Chem 2012, 23:900-907.
69. Liu X, Guo J, Han S, Yao L, Chen A, Yang Q, Bo H, Xu P, Yin J, Zhang Z: Enhanced immune response induced by a potential influenza A vaccine based on branched M2e polypeptides linked to tuftsin. Vaccine 2012, 30:6527-6533.
70. Kumar P, Biswas S, Rao DN: Potentiation of immune response against the RESA peptides of Plasmodium falciparum by incorporating a universal T-cell epitope (CS.T3) and an immunomodulator (polytuftsin), and delivery through liposomes. Microbiol Immunol 1999, 43:567-576.
71. Pawan K, Ivanov BB, Kabilan L, Rao DN: Construction of a synthetic immunogen: use of the natural immunomodulator polytuftsin in malaria vaccines against RESA antigen of Plasmodium falciparum. Vaccine 1994, 12:819-824.
72. Dutta RC, Puri A, Anand N: Immunomodulatory potential of hydrophobic analogs of Rigin and their role in providing protection against Plasmodium berghei infection in mice. Int Immunopharmacol 2001, 1:843-855.
73. Khan MA, Aljarbou A, Khan A, Owais M: Immune stimulating and therapeutic potential of tuftsin-incorporated nystatin liposomes against Cryptococcus neoformans in leukopenic BALB/C mice. FEMS Immunol Med Microbiol 2012, 66:88-97.
74. Shakya N, Sane SA, Haq W, Gupta S: Augmentation of antileishmanial efficacy of miltefosine in combination with tuftsin against experimental visceral leishmaniasis. Parasitol Res 2012, 111:563-570.
75. Wardowska A, Dzierzbicka K, Szarynska M, Dabrowska-Szponar M, Wisniewska K, Mysliwski A, Trzonkowski P: Analogues of muramyl dipeptide (MDP) and tuftsin limit infection and inflammation in murine model of sepsis. Vaccine 2009, 27:369-374.
76. Qari MH, Zaki WA: Flow cytometric assessment of leukocyte function in sickle cell anemia. Hemoglobin 2011, 35:367-381.
77. Hanscheid T, Egan TJ, Grobusch MP: Haemozoin: from melatonin pigment to drug target, diagnostic tool, and immune modulator. Lancet Infect Dis 2007, 7:675-685.
78. Kaye D, Gill FA, Hook EW: Factors influencing host resistance to Salmonella infections: the effects of hemolysis and erythrophagocytosis. Am J Med Sci 1967, 254:205-215.
79. Kraal G: Antigens take the shuttle. Nat Immunol 2008, 9:11-12.
80. Morente M, Piris MA, Orradre JL, Rivas C, Villuendas R: Human tonsil intraepithelial B cells: a marginal zone-related subpopulation. J Clin Pathol 1992, 45:668-672.
81. Cinamon G, Zachariah MA, Lam OM, Foss FW Jr, Cyster JG: Follicular shuttling of marginal zone B cells facilitates antigen transport. Nat Immunol 2008, 9:54-62.
82. Chan AC, Leeansyah E, Cochrane A, d'Udekem d'Acoz Y, Mittag D, Harrison LC, Godfrey DI, Berzins SP: Ex-vivo analysis of human natural killer T cells demonstrates heterogeneity between tissues and within established CD4(+) and CD4(-) subsets. Clin Exp Immunol 2013, 172:129-137.
83. Stevenson MM, Kraal G: Histological changes in the spleen and liver of C57BL/6 and A/J mice during Plasmodium chabaudi AS infection. Exp Mol Pathol 1989, 51:80-95.
84. Urban BC, Hien TT, Day NP, Phu NH, Roberts R, Pongponratn E, Jones M, Mai NT, Bethell D, Turner GD, Ferguson D, White NJ, Roberts DJ: Fatal Plasmodium falciparum malaria causes specific patterns of splenic architectural disorganization. Infect Immun 2005, 73:1986-1994.
85. Bockstal V, Geurts N, Magez S: Acute disruption of bone marrow b lymphopoiesis and apoptosis of transitional and marginal zone b cells in the spleen following a blood-stage Plasmodium chabaudi infection in mice. J Parasitol Res 2011, 2011:534697.
86. Sanchez-Torres L, Rodriguez-Ropon A, Aguilar-Medina M, Favila-Castillo L: Mouse splenic CD4+ and CD8+ T cells undergo extensive apoptosis during a Plasmodium chabaudi chabaudi AS infection. Parasite Immunol 2001, 23:617-626.
87. Kapoor G, Bagai U, Banyal HS: Plasmodium berghei induces apoptotic changes in splenic and peripheral blood cells. Trop Biomed 2011, 28:119-124.
88. Dkhil MA: Apoptotic changes induced in mice splenic tissue due to malaria infection. J Microbiol Immunol Infect 2009, 42:13-18.
89. Sponaas AM, Cadman ET, Voisine C, Harrison V, Boonstra A, O'Garra A, Langhorne J: Malaria infection changes the ability of splenic dendritic cell populations to stimulate antigen-specific T cells. J Exp Med 2006, 203:1427-1433.
90. Gozzelino R, Soares MP: Heme sensitization to TNF-mediated programmed cell death. Adv Exp Med Biol 2011, 691:211-219.
91. Asito AS, Piriou E, Jura WG, Ouma C, Odada PS, Ogola S, Fiore N, Rochford R: Suppression of circulating IgD + CD27+ memory B cells in infants living in a malaria-endemic region of Kenya. Malar J 2011, 10:362.
92. Sullivan RT, Ssewanyana Ssewanyana I, Wamala Wamala S, Ebusu C, Nankya F, Riley EM, Mayanja H, Drakeley C, Kakuru Muhindo M, Arinaitwe E, Tappero J, Kaharuza F, Dorsey G, Greenhouse B: Detailed Kinetics of B Cell Subsets Following Symptomatic Malaria in Children in Tororo, Uganda. In American Society of Tropical Medicine and Hygiene, 62nd Annual Meeting. Abstract: 1121. Washington, DC, USA: 2013.
93. Wykes MN, Zhou YH, Liu XQ, Good MF: Plasmodium yoelii can ablate vaccine-induced long-term protection in mice. J Immunol 2005, 175:2510-2516.
94. Reynaud CA, Descatoire M, Dogan I, Huetz F, Weller S, Weill JC: IgM memory B cells: a mouse/human paradox. Cell Mol Life Sci 2012, 69:1625-1634.
95. Gondwe EN, Molyneux ME, Goodall M, Graham SM, Mastroeni P, Drayson MT, MacLennan CA: Importance of antibody and complement for oxidative burst and killing of invasive nontyphoidal Salmonella by blood cells in Africans. Proc Natl Acad Sci U S A 2010, 107:3070-3075.
96. MacLennan CA, Gondwe EN, Msefula CL, Kingsley RA, Thomson NR, White SA, Goodall M, Pickard DJ, Graham SM, Dougan G, Hart CA, Molyneux ME, Drayson MT: The neglected role of antibody in protection against bacteremia caused by nontyphoidal strains of Salmonella in African children. J Clin Invest 2008, 118:1553-1562.
97. Eguchi M, Kikuchi Y: Binding of Salmonella-specific antibody facilitates specific T cell responses via augmentation of bacterial uptake and induction of apoptosis in macrophages. J Infect Dis 2010, 201:62-70.
98. Cunningham AF, Gaspal F, Serre K, Mohr E, Henderson IR, Scott-Tucker A, Kenny SM, Khan M, Toellner KM, Lane PJ, MacLennan IC: Salmonella induces a switched antibody response without germinal centers that impedes the extracellular spread of infection. J Immunol 2007, 178:6200-6207.
99. Buffet PA, Safeukui I, Milon G, Mercereau-Puijalon O, David PH: Retention of erythrocytes in the spleen: a double-edged process in human malaria. Curr Opin Hematol 2009, 16:157-164.
100. Kotlyar S, Nteziyaremye J, Olupot-Olupot P, Akech SO, Moore CL, Maitland K: Spleen volume and clinical disease manifestations of severe Plasmodium falciparum malaria in African children. Trans R Soc Trop Med Hyg 2014, 108:283-289.
101. Waitumbi JN, Donvito B, Kisserli A, Cohen JH, Stoute JA: Age-related changes in red blood cell complement regulatory proteins and susceptibility to severe malaria. J Infect Dis 2004, 190:1183-1191.
102. Looareesuwan S, Ho M, Wattanagoon Y, White NJ, Warrell DA, Bunnag D, Harinasuta T, Wyler DJ: Dynamic alteration in splenic function during acute falciparum malaria. N Engl J Med 1987, 317:675-679.
103. Were T, Davenport GC, Hittner JB, Ouma C, Vulule JM, Ong'echa JM, Perkins DJ: Bacteremia in Kenyan children presenting with malaria. J Clin Microbiol 2011, 49:671-676.
104. Biggs HM, Lester R, Nadjm B, Mtove G, Todd JE, Kinabo GD, Philemon R, Amos B, Morrissey AB, Reyburn H, Crump JA: Invasive Salmonella infections in areas of high and low malaria transmission intensity in Tanzania. Clin Infect Dis 2014, 58:638-647.
105. Stoute JA: Complement receptor 1 and malaria. Cell Microbiol 2011, 13:1441-1450.
106. Thomas BN, Diallo DA, Noumsi GT, Moulds JM: Circulating immune complex levels are associated with disease severity and seasonality in children with malaria from Mali. Biomark Insights 2012, 7:81-86.
107. Odhiambo CO, Otieno W, Adhiambo C, Odera MM, Stoute JA: Increased deposition of C3b on red cells with low CR1 and CD55 in a malariaendemic region of western Kenya: implications for the development of severe anemia. BMC Med 2008, 6:23.
108. Kai OK, Roberts DJ: The pathophysiology of malarial anaemia: where have all the red cells gone? BMC Med 2008, 6:24.
109. Yadava A, Kumar S, Dvorak JA, Milon G, Miller LH: Trafficking of Plasmodium chabaudi adami-infected erythrocytes within the mouse spleen. Proc Natl Acad Sci U S A 1996, 93:4595-4599.
110. Kirby AC, Beattie L, Maroof A, van Rooijen N, Kaye PM: SIGNR1-negative red pulp macrophages protect against acute streptococcal sepsis after Leishmania donovani-induced loss of marginal zone macrophages. Am J Pathol 2009, 175:1107-1115.
111. Mollison PL: The reticulo-endothelial system and red cell destruction. Proc R Soc Med 1962, 55:915-920.
112. Kariuki S, Revathi G, Kariuki N, Kiiru J, Mwituria J, Muyodi J, Githinji JW, Kagendo D, Munyalo A, Hart CA: Invasive multidrug-resistant nontyphoidal Salmonella infections in Africa: zoonotic or anthroponotic transmission? J Med Microbiol 2006, 55:585-591.
113. de Jong HK, Parry CM, van der Poll T, Wiersinga WJ: Host-pathogen interaction in invasive salmonellosis. PLoS Pathog 2012, 8:e1002933.
114. Roux CM, Butler BP, Chau JY, Paixao TA, Cheung KW, Santos RL, Luckhart S, Tsolis RM: Both hemolytic anemia and malaria parasite-specific factors increase susceptibility to nontyphoidal Salmonella enterica serovar typhimurium infection in mice. Infect Immun 2010, 78:1520-1527.
115. Mendes J, Goncalves M, Pita-Groz J, Leal MJ: Torsion of the spleen. Chir Pediatr 1988, 29:291-292.
116. Hart AL, Ng SC, Mann E, Al-Hassi HO, Bernardo D, Knight SC: Homing of immune cells: role in homeostasis and intestinal inflammation. Inflamm Bowel Dis 2010, 16:1969-1977.
117. Mora JR, von Andrian UH: Differentiation and homing of IgA-secreting cells. Mucosal Immunol 2008, 1:96-109.
118. Peterson LW, Artis D: Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat Rev Immunol 2014, 14:141-153.
119. Liu X, Li Y, Wang Y, Wang Q, Li X, Bi Y, Liu L, Wei X, Li T, Chen J: Gestational vitamin A deficiency reduces the intestinal immune response by decreasing the number of immune cells in rat offspring. Nutrition 2014, 30:350-357.
120. van de Pavert SA, Ferreira M, Domingues RG, Ribeiro H, Molenaar R, Moreira-Santos L, Almeida FF, Ibiza S, Barbosa I, Goverse G, Labao-Almeida C, Godinho-Silva C, Konijn T, Schooneman D, O'Toole T, Mizee MR, Habani Y, Haak E, Santori FR, Littman DR, Schulte-Merker S, Dzierzak E, Simas JP, Mebius RE, Veiga-Fernandes H: Maternal retinoids control type 3 innate lymphoid cells and set the offspring immunity. Nature 2014, 508:123-127.
121. Owusu-Agyei S, Newton S, Mahama E, Febir LG, Ali M, Adjei K, Tchum K, Alhassan L, Moleah T, Tanumihardjo SA: Impact of vitamin A with zinc supplementation on malaria morbidity in Ghana. Nutr J 2013, 12:131.
122. Semba RD: Vitamin A and immunity to viral, bacterial and protozoan infections. Proc Nutr Soc 1999, 58:719-727.
123. Mawson AR: The pathogenesis of malaria: a new perspective. Pathog Global Health 2013, 107:122-129.
124. Hussein MM, Mooij JM, Roujouleh HM, Hamour OA, Felemban H: Nontyphoid Salmonella septicemia and visceral leishmaniasis in a renal transplant patient. Transplantation 2001, 71:479-481.
125. Kayserili E, Hizarcioglu M, Gulez P, Apa H, Keskin S: Co-existence of Kala-azar and salmonellosis in a 16 month-old baby? Or a false positive widal reaction in Kala-azar?(in Turkish). Turkiye Parazitol Derg 2005, 29:141-144.
126. Carvalho EM, Bacellar O, Barral A, Badaro R, Johnson WD Jr: Antigen-specific immunosuppression in visceral leishmaniasis is cell mediated. J Clin Invest 1989, 83:860-864.
127. Gendrel D, Kombila M, Beaudoin-Leblevec G, Richard-Lenoble D: Nontyphoidal salmonellal septicemia in Gabonese children infected with Schistosoma intercalatum. Clin Infect Dis 1994, 18:103-105.
128. Gordon MA, Zijlstra EE, Naus CW, Visser LG, Molyneux ME, van Lieshout L: Schistosomiasis does not contribute to death or recurrence of nontyphoid Salmonella bacteremia in human immunodeficiency virus-infected Malawian adults. Clin Infect Dis 2003, 37:e177-e179.
129. Piyaphanee W, Issarachaikul R, Soontarach P, Silachamroon U: Concurrent salmonella bacteremia in P. vivax infection-a report of 2 cases at the Hospital for Tropical Diseases, Thailand. Southeast Asian J Trop Med Public Health 2007, 38:616-618.
130. Sur D, von Seidlein L, Manna B, Dutta S, Deb AK, Sarkar BL, Kanungo S, Deen JL, Ali M, Kim DR, Gupta VK, Ochiai RL, Tsuzuki A, Acosta CJ, Clemens JD, Bhattacharya SK: The malaria and typhoid fever burden in the slums of Kolkata, India: data from a prospective community-based study. Trans R Soc Trop Med Hyg 2006, 100:725-733.
131. Keong BC, Sulaiman W: Typhoid and malaria co-infection-an interesting finding in the investigation of a tropical fever. Malays J Med Sci 2006, 13:74-75.
132. Kumar A, Katiyar GP: Mixed infection with Plasmodium-vivax and Salmonella typhi in an infant. Indian Pediatr 1995, 32:243-244.
133. Shanks GD, White NJ: The activation of vivax malaria hypnozoites by infectious diseases. Lancet Infect Dis 2013, 13:900-906.
134. Bynum B: Typhomalaria. Lancet 2002, 360:1339.
135. Bhattacharya SK, Sur D, Dutta S, Kanungo S, Ochiai RL, Kim DR, Anstey NM, von Seidlein L, Deen J: Vivax malaria and bacteraemia: a prospective study in Kolkata. India Malar J 2013, 12:176.
136. Burger P, Hilarius-Stokman P, de Korte D, van den Berg TK, van Bruggen R: CD47 functions as a molecular switch for erythrocyte phagocytosis. Blood 2012, 119:5512-5521.
137. Liu J, Guo X, Mohandas N, Chasis JA, An X: Membrane remodeling during reticulocyte maturation. Blood 2010, 115:2021-2027.
138. Liu J, Mohandas N, An X: Membrane assembly during erythropoiesis. Curr Opin Hematol 2011, 18:133-138.
139. Zhao XW, van Beek EM, Schornagel K, Van der Maaden H, Van Houdt M, Otten MA, Finetti P, Van Egmond M, Matozaki T, Kraal G, Birnbaum D, van Elsas A, Kuijpers TW, Bertucci F, van den Berg TK: CD47-signal regulatory protein-alpha (SIRPalpha) interactions form a barrier for antibody-mediated tumor cell destruction. Proc Natl Acad Sci U S A 2011, 108:18342-18347.
140. Pinaki Panigrahi SP, Lingaraj P, Nimai N, Radhanath Satpathy DC, Rama C, Pravas M, Hegang, Chen JAJ, Glenn Morris J Jr, Nigel P, Gewolb IH: Effectiveness of a Lactobacillus Plantarum Synbiotic Therapy for Preventing Late Onset Sepsis in Neonates. In 2013 Pediatric Academic Societies Annual Meeting. Abstract: 3618.2. Washington DC, USA: 2013.
141. Deshmukh HS, Liu Y, Menkiti OR, Mei J, Dai N, O'Leary CE, Oliver PM, Kolls JK, Weiser JN, Worthen GS: The microbiota regulates neutrophil homeostasis and host resistance to Escherichia coli K1 sepsis in neonatal mice. Nat Med 2014, 20:524-530.