Neutropenia as an adverse event following vaccination: Results from randomized clinical trials in healthy adults and systematic review

PLoS ONE

Volumn 11, Issue 8, 2016, Pages

  Muturi Kioi, Vincent ^a,e   Lewis, David ^b,f   Launay, Odile ^c   Leroux Roels, Geert ^d   Anemona, Alessandra ^a,g   Loulergue, Pierre ^c   Bodinham, Caroline L ^b   Aerssens, Annelies ^d   Groth, Nicola ^a,g   Saul, Allan ^a,g   Podda, Audino ^a,g  

^a NOVARTIS VACCINES AND DIAGNOSTICS   (Italy)

^b UNIVERSITY OF SURREY   (United Kingdom)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d GHENT UNIVERSITY HOSPITAL   (Belgium)

^e GLAXOSMITHKLINE   (United Kingdom)

^f IMPERIAL COLLEGE LONDON   (United Kingdom)

^g GSK   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

PLACEBO; SHIGELLA VACCINE; VACCINE;

ADULT; DRUG DOSE ESCALATION; DRUG SAFETY; FEMALE; HUMAN; HUMAN EXPERIMENT; IMMUNOGENICITY; LICENCE; MALE; NEUTROPENIA; NEUTROPHIL COUNT; NORMAL HUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SHIGELLA SONNEI; SHIGELLOSIS; SYSTEMATIC REVIEW; VACCINATION; BLOOD EXAMINATION; DYSENTERY, BACILLARY; FACTUAL DATABASE; IMMUNOLOGY; PATHOLOGY; SEVERITY OF ILLNESS INDEX;

DATABASES, FACTUAL; DYSENTERY, BACILLARY; HEMATOLOGIC TESTS; HUMANS; NEUTROPENIA; RANDOMIZED CONTROLLED TRIALS AS TOPIC; SEVERITY OF ILLNESS INDEX; SHIGELLA SONNEI; SHIGELLA VACCINES; VACCINES;

EID: 84983271847     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0157385     Document Type: Review

References (46)

1. Reading R. Risk of immune thrombocytopenic purpura after measles-mumps-rubella immunization in children. Child: Care, Health and Development. 2008; 34(4):548-. doi: 10.1111/j.1365-2214.2008. 00864-6.x
2. O'Leary ST, Glanz JM, McClure DL, Akhtar A, Daley MF, Nakasato C, et al. The risk of immune thrombocytopenic purpura after vaccination in children and adolescents. Pediatrics. 2012; 129(2):248-55. Epub 2012/01/11. doi: 10.1542/peds.2011-1111 PMID: 22232308.
3. Haddy TB, Rana SR, Castro O. Benign ethnic neutropenia: what is a normal absolute neutrophil count? The Journal of laboratory and clinical medicine. 1999; 133(1):15-22. Epub 1999/06/29. doi: 10.1053/lc. 1999.v133.a94931 PMID: 10385477.
4. Reed WW, Diehl LF. Leukopenia, neutropenia, and reduced hemoglobin levels in healthy American blacks. Archives of internal medicine. 1991; 151(3):501-5. Epub 1991/03/01. PMID: 2001132.
5. Bain BJ. Ethnic and sex differences in the total and differential white cell count and platelet count. Journal of clinical pathology. 1996; 49(8):664-6. Epub 1996/08/01. PMID: 8881919; PubMed Central PMCID: PMCPmc500612.
6. von Vietinghoff S, Ley K. Homeostatic regulation of blood neutrophil counts. Journal of immunology (Baltimore, Md: 1950). 2008; 181(8):5183-8. Epub 2008/10/04. PMID: 18832668; PubMed Central PMCID: PMCPmc2745132.
7. Reich D, Nalls MA, Kao WH, Akylbekova EL, Tandon A, Patterson N, et al. Reduced neutrophil count in people of African descent is due to a regulatory variant in the Duffy antigen receptor for chemokines gene. PLoS Genet. 2009; 5(1):e1000360. Epub 2009/01/31. doi: 10.1371/journal.pgen.1000360 PMID: 19180233; PubMed Central PMCID: PMCPMC2628742.
8. Shoenfeld Y, Ben-Tal O, Berliner S, Pinkhas J. The outcome of bacterial infection in subjects with benign familial leukopenia (BFL). Biomed Pharmacother. 1985; 39(1):23-6. Epub 1985/01/01. PMID: 4027348.
9. Gerke C, Colucci AM, Giannelli C, Sanzone S, Vitali CG, Sollai L, et al. Production of a Shigella sonnei Vaccine Based on Generalized Modules for Membrane Antigens (GMMA), 1790GAHB. PloS one. 2015; 10(8):e0134478. Epub 2015/08/08. doi: 10.1371/journal.pone.0134478 PMID: 26248044; PubMed Central PMCID: PMCPmc4527750.
10. Administration FUSFaD. Toxicity Grading Scale for Healthy Adult and Adolescent Volunteers Enrolled in Preventive Vaccine Clinical Trials.
11. Durbin AP, Whitehead SS, Shaffer D, Elwood D, Wanionek K, Thumar B, et al. A single dose of the DENV-1 candidate vaccine rDEN1Delta30 is strongly immunogenic and induces resistance to a second dose in a randomized trial. PLoS neglected tropical diseases. 2011; 5(8):e1267. Epub 2011/08/11. doi: 10.1371/journal.pntd.0001267 PMID: 21829748; PubMed Central PMCID: PMCPmc3149013.
12. Morrison D, Legg TJ, Billings CW, Forrat R, Yoksan S, Lang J. A novel tetravalent dengue vaccine is well tolerated and immunogenic against all 4 serotypes in flavivirus-naive adults. The Journal of infectious diseases. 2010; 201(3):370-7. Epub 2010/01/12. doi: 10.1086/649916 PMID: 20059357.
13. Cunningham CK, Wara DW, Kang M, Fenton T, Hawkins E, McNamara J, et al. Safety of 2 recombinant human immunodeficiency virus type 1 (HIV-1) envelope vaccines in neonates born to HIV-1-infected women. Clinical infectious diseases: an official publication of the Infectious Diseases Society of America. 2001; 32(5):801-7. Epub 2001/03/07. doi: 10.1086/319215 PMID: 11229849.
14. Kotloff KL, Corretti M, Palmer K, Campbell JD, Reddish MA, Hu MC, et al. Safety and immunogenicity of a recombinant multivalent group a streptococcal vaccine in healthy adults: phase 1 trial. Jama. 2004; 292(6):709-15. Epub 2004/08/12. doi: 10.1001/jama.292.6.709 PMID: 15304468.
15. Ellis RD, Mullen GE, Pierce M, Martin LB, Miura K, Fay MP, et al. A Phase 1 study of the blood-stage malaria vaccine candidate AMA1-C1/Alhydrogel with CPG 7909, using two different formulations and dosing intervals. Vaccine. 2009; 27(31):4104-9. Epub 2009/05/05. doi: 10.1016/j.vaccine.2009.04.077 PMID: 19410624; PubMed Central PMCID: PMCPmc2722923.
16. Duncan CJ, Sheehy SH, Ewer KJ, Douglas AD, Collins KA, Halstead FD, et al. Impact on malaria parasite multiplication rates in infected volunteers of the protein-in-adjuvant vaccine AMA1-C1/Alhydrogel +CPG 7909. PloS one. 2011; 6(7):e22271. Epub 2011/07/30. doi: 10.1371/journal.pone.0022271 PMID: 21799809; PubMed Central PMCID: PMCPmc3142129.
17. Sheldon EA, Schwartz H, Jiang Q, Giardina PC, Perez JL. A phase 1, randomized, open-label, activecontrolled trial to assess the safety of a meningococcal serogroup B bivalent rLP2086 vaccine in healthy adults. Human vaccines & immunotherapeutics. 2012; 8(7):888-95. Epub 2012/07/27. doi: 10. 4161/hv.19983 PMID: 22832260.
18. McFarland EJ, Johnson DC, Muresan P, Fenton T, Tomaras GD, McNamara J, et al. HIV-1 vaccine induced immune responses in newborns of HIV-1 infected mothers. AIDS (London, England). 2006; 20 (11):1481-9. Epub 2006/07/19. doi: 10.1097/01.aids.0000237363.33994.45 PMID: 16847402.
19. Dieye TN, Ndiaye BP, Dieng AB, Fall M, Brittain N, Vermaak S, et al. Two doses of candidate TB vaccine MVA85A in antiretroviral therapy (ART) naive subjects gives comparable immunogenicity to one dose in ART+ subjects. PloS one. 2013; 8(6):e67177. Epub 2013/07/11. doi: 10.1371/journal.pone. 0067177 PMID: 23840618; PubMed Central PMCID: PMCPmc3696007.
20. Durbin AP, McArthur J, Marron JA, Blaney JE Jr., Thumar B, Wanionek K, et al. The live attenuated dengue serotype 1 vaccine rDEN1Delta30 is safe and highly immunogenic in healthy adult volunteers. Human vaccines. 2006; 2(4):167-73. Epub 2006/10/03. PMID: 17012875.
21. Edelman R, Wasserman SS, Bodison SA, Putnak RJ, Eckels KH, Tang D, et al. Phase I trial of 16 formulations of a tetravalent live-attenuated dengue vaccine. The American journal of tropical medicine and hygiene. 2003; 69(6 Suppl):48-60. Epub 2004/01/27. PMID: 14740955.
22. Jaoko W, Nakwagala FN, Anzala O, Manyonyi GO, Birungi J, Nanvubya A, et al. Safety and immunogenicity of recombinant low-dosage HIV-1 A vaccine candidates vectored by plasmid pTHr DNA or modified vaccinia virus Ankara (MVA) in humans in East Africa. Vaccine. 2008; 26(22):2788-95. Epub 2008/04/29. doi: 10.1016/j.vaccine.2008.02.071 PMID: 18440674.
23. Karron RA, Talaat K, Luke C, Callahan K, Thumar B, Dilorenzo S, et al. Evaluation of two live attenuated cold-adapted H5N1 influenza virus vaccines in healthy adults. Vaccine. 2009; 27(36):4953-60. Epub 2009/06/23. doi: 10.1016/j.vaccine.2009.05.099 PMID: 19540952.
24. Kitchener S, Nissen M, Nasveld P, Forrat R, Yoksan S, Lang J, et al. Immunogenicity and safety of two live-attenuated tetravalent dengue vaccine formulations in healthy Australian adults. Vaccine. 2006; 24 (9):1238-41. Epub 2005/10/11. doi: 10.1016/j.vaccine.2005.09.029 PMID: 16213632.
25. McArthur JH, Durbin AP, Marron JA, Wanionek KA, Thumar B, Pierro DJ, et al. Phase I clinical evaluation of rDEN4Delta30-200,201: a live attenuated dengue 4 vaccine candidate designed for decreased hepatotoxicity. The American journal of tropical medicine and hygiene. 2008; 79(5):678-84. Epub 2008/11/05. PMID: 18981503; PubMed Central PMCID: PMCPmc2590927.
26. Ouedraogo A, Tiono AB, Kargougou D, Yaro JB, Ouedraogo E, Kabore Y, et al. A phase 1b randomized, controlled, double-blinded dosage-escalation trial to evaluate the safety, reactogenicity and immunogenicity of an adenovirus type 35 based circumsporozoite malaria vaccine in Burkinabe healthy adults 18 to 45 years of age. PloS one. 2013; 8(11):e78679. Epub 2013/11/19. doi: 10.1371/journal. pone.0078679 PMID: 24244339; PubMed Central PMCID: PMCPmc3823848.
27. Sun W, Cunningham D, Wasserman SS, Perry J, Putnak JR, Eckels KH, et al. Phase 2 clinical trial of three formulations of tetravalent live-attenuated dengue vaccine in flavivirus-naive adults. Human vaccines. 2009; 5(1):33-40. Epub 2008/08/02. PMID: 18670195.
28. Talaat KR, Karron RA, Callahan KA, Luke CJ, DiLorenzo SC, Chen GL, et al. A live attenuated H7N3 influenza virus vaccine is well tolerated and immunogenic in a Phase I trial in healthy adults. Vaccine. 2009; 27(28):3744-53. Epub 2009/05/26. doi: 10.1016/j.vaccine.2009.03.082 PMID: 19464558; PubMed Central PMCID: PMCPmc2771405.
29. Chuang I, Sedegah M, Cicatelli S, Spring M, Polhemus M, Tamminga C, et al. DNA prime/Adenovirus boost malaria vaccine encoding P. falciparum CSP and AMA1 induces sterile protection associated with cell-mediated immunity. PloS one. 2013; 8(2):e55571. Epub 2013/03/05. doi: 10.1371/journal. pone.0055571 PMID: 23457473; PubMed Central PMCID: PMCPmc3573028.
30. Sedegah M, Tamminga C, McGrath S, House B, Ganeshan H, Lejano J, et al. Adenovirus 5-vectored P. falciparum vaccine expressing CSP and AMA1. Part A: safety and immunogenicity in seronegative adults. PloS one. 2011; 6(10):e24586. Epub 2011/10/18. doi: 10.1371/journal.pone.0024586 PMID: 22003383; PubMed Central PMCID: PMCPmc3189181.
31. Watanaveeradej V, Simasathien S, Nisalak A, Endy TP, Jarman RG, Innis BL, et al. Safety and immunogenicity of a tetravalent live-attenuated dengue vaccine in flavivirus-naive infants. The American journal of tropical medicine and hygiene. 2011; 85(2):341-51. Epub 2011/08/05. doi: 10.4269/ajtmh. 2011.10-0501 PMID: 21813857; PubMed Central PMCID: PMCPmc3144835.
32. Chang LJ, Dowd KA, Mendoza FH, Saunders JG, Sitar S, Plummer SH, et al. Safety and tolerability of chikungunya virus-like particle vaccine in healthy adults: a phase 1 dose-escalation trial. Lancet. 2014; 384(9959):2046-52. Epub 2014/08/19. doi: 10.1016/s0140-6736(14)61185-5 PMID: 25132507.
33. Njuguna IN, Ambler G, Reilly M, Ondondo B, Kanyugo M, Lohman-Payne B, et al. PedVacc 002: a phase I/II randomized clinical trial of MVA.HIVA vaccine administered to infants born to human immunodeficiency virus type 1-positive mothers in Nairobi. Vaccine. 2014; 32(44):5801-8. Epub 2014/09/01. doi: 10.1016/j.vaccine.2014.08.034 PMID: 25173484; PubMed Central PMCID: PMCPmc4414927.
34. Durbin AP, Wright PF, Cox A, Kagucia W, Elwood D, Henderson S, et al. The live attenuated chimeric vaccine rWN/DEN4Delta30 is well-tolerated and immunogenic in healthy flavivirus-naive adult volunteers. Vaccine. 2013; 31(48):5772-7. Epub 2013/08/24. doi: 10.1016/j.vaccine.2013.07.064 PMID: 23968769; PubMed Central PMCID: PMCPmc3833717.
35. Sun W, Edelman R, Kanesa-Thasan N, Eckels KH, Putnak JR, King AD, et al. Vaccination of human volunteers with monovalent and tetravalent live-attenuated dengue vaccine candidates. The American journal of tropical medicine and hygiene. 2003; 69(6 Suppl):24-31. Epub 2004/01/27. PMID: 14740952.
36. Capeding RZ, Luna IA, Bomasang E, Lupisan S, Lang J, Forrat R, et al. Live-attenuated, tetravalent dengue vaccine in children, adolescents and adults in a dengue endemic country: randomized controlled phase I trial in the Philippines. Vaccine. 2011; 29(22):3863-72. Epub 2011/04/12. doi: 10.1016/j. vaccine.2011.03.057 PMID: 21477675.
37. Durbin AP, McArthur JH, Marron JA, Blaney JE, Thumar B, Wanionek K, et al. rDEN2/4Delta30(ME), a live attenuated chimeric dengue serotype 2 vaccine is safe and highly immunogenic in healthy denguenaive adults. Human vaccines. 2006; 2(6):255-60. Epub 2006/11/16. PMID: 17106267.
38. Vardas E, Kaleebu P, Bekker LG, Hoosen A, Chomba E, Johnson PR, et al. A phase 2 study to evaluate the safety and immunogenicity of a recombinant HIV type 1 vaccine based on adeno-associated virus. AIDS research and human retroviruses. 2010; 26(8):933-42. Epub 2010/07/30. doi: 10.1089/aid. 2009.0242 PMID: 20666584.
39. Kanesa-thasan N, Smucny JJ, Hoke CH, Marks DH, Konishi E, Kurane I, et al. Safety and immunogenicity of NYVAC-JEV and ALVAC-JEV attenuated recombinant Japanese encephalitis virus-poxvirus vaccines in vaccinia-nonimmune and vaccinia-immune humans. Vaccine. 2000; 19(4-5):483-91. Epub 2000/10/12. PMID: 11027812.
40. Gershon AA, Levin MJ, Weinberg A, Song LY, LaRussa PS, Steinberg SP, et al. A phase I-II study of live attenuated varicella-zoster virus vaccine to boost immunity in human immunodeficiency virusinfected children with previous varicella. The Pediatric infectious disease journal. 2009; 28(7):653-5. Epub 2009/06/30. doi: 10.1097/INF.0b013e3181998f06 PMID: 19561431; PubMed Central PMCID: PMCPmc2868313.
41. Lindow JC, Durbin AP, Whitehead SS, Pierce KK, Carmolli MP, Kirkpatrick BD. Vaccination of volunteers with low-dose, live-attenuated, dengue viruses leads to serotype-specific immunologic and virologic profiles. Vaccine. 2013; 31(33):3347-52. Epub 2013/06/06. doi: 10.1016/j.vaccine.2013.05.075 PMID: 23735680; PubMed Central PMCID: PMCPmc3777849.
42. Siberry GK, Williams PL, Lujan-Zilbermann J, Warshaw MG, Spector SA, Decker MD, et al. Phase I/II, open-label trial of safety and immunogenicity of meningococcal (groups A, C, Y, and W-135) polysaccharide diphtheria toxoid conjugate vaccine in human immunodeficiency virus-infected adolescents. The Pediatric infectious disease journal. 2010; 29(5):391-6. Epub 2010/05/01. doi: 10.1097/INF. 0b013e3181c38f3b PMID: 20431379; PubMed Central PMCID: PMCPmc2868314.
43. Siberry GK, Warshaw MG, Williams PL, Spector SA, Decker MD, Jean-Philippe P, et al. Safety and immunogenicity of quadrivalent meningococcal conjugate vaccine in 2- to 10-year-old human immunodeficiency virus-infected children. The Pediatric infectious disease journal. 2012; 31(1):47-52. Epub 2011/10/12. doi: 10.1097/INF.0b013e318236c67b PMID: 21987006; PubMed Central PMCID: PMCPmc3252429.
44. Wright PF, Ankrah S, Henderson SE, Durbin AP, Speicher J, Whitehead SS, et al. Evaluation of the Langat/dengue 4 chimeric virus as a live attenuated tick-borne encephalitis vaccine for safety and immunogenicity in healthy adult volunteers. Vaccine. 2008; 26(7):882-90. Epub 2008/01/22. doi: 10. 1016/j.vaccine.2007.12.015 PMID: 18207289; PubMed Central PMCID: PMCPmc2254188.
45. Sanchez V, Gimenez S, Tomlinson B, Chan PK, Thomas GN, Forrat R, et al. Innate and adaptive cellular immunity in flavivirus-naive human recipients of a live-attenuated dengue serotype 3 vaccine produced in Vero cells (VDV3). Vaccine. 2006; 24(23):4914-26. Epub 2006/04/25. doi: 10.1016/j.vaccine. 2006.03.066 PMID: 16632108.
46. Karita E, Ketter N, Price MA, Kayitenkore K, Kaleebu P, Nanvubya A, et al. CLSI-derived hematology and biochemistry reference intervals for healthy adults in eastern and southern Africa. PloS one. 2009; 4(2):e4401. doi: 10.1371/journal.pone.0004401 PMID: 19197365; PubMed Central PMCID: PMC2632744.