Vaccines for viral and bacterial pathogens causing acute gastroenteritis: Part II: Vaccines for Shigella, Salmonella, enterotoxigenic E. coli (ETEC) enterohemorragic E. coli (EHEC) and Campylobacter jejuni

Figures & data

Table 1. Human vaccines for individual enteric pathogens including status of development, main feature(s) and selected references

Pathogen	Vaccine (s)	Status*	Comment	Selected references
Shigella	Intramuscularly administrated, conjugates from LPS with protein carriers such as rEPA	Advanced clinical development	Phase III was well tolerated by children under 4 years of age. Coupling different LPS from the species allows for the development of multivalent vaccines.	Passwell et al. 2001^20; 2003^19, 2010^22
	Orally administrated Shigella flexneri 2a SC602	Early clinical development	Phase I and phase II in volunteers. However, this candidate does not show cross-reaction against other species of Shigella.	Rahman et al., 2011^26
	Orally administrated Shigella dysenteriae 1 SC599	Early clinical development	Phase I, was immunogenic and well tolerated by volunteers.	Sadorge et al., 2008^28; Launay et al., 2009^27,28
	Killed whole-cell vaccine, intranasally administered	Early clinical development	An increased level of antibodies against LPS from the species used were present in animal experiments.	Barman et al., 2011^13
	Orally administered Shigella sonnei WRSS1	Early clinical development	Phase I, developed antibodies against S. sonnei LPS, but reactogenic when high doses are used.	Kotloff et al., 2002^30; Orr et al., 2005^31
	Orally administered Shigella dysenteriae 1 WRSd1	Early clinical development	Phase I, vaccinated volunteers do not developed Shigellosis symptoms.	McKenzie et al., 2008^33
	Intranasally administered INVAPLEX®	Early clinical development	Phase I, this candidate contains the Ipa proteins plus LPS and has been shown to develop a good intestinal immune response.	Tribble et al., 2010^43; Riddle et al., 2011^42
	Intranasally or ocularly administered Shigella flexneri 2a WRSf2G11, WRSf2G12 and WRSf2G15	Preclinical development	Second generation of vaccines, shown in animal model to protect against S. flexneri and to induce an immune response.	Ranallo et al., 2012^51; 2014^52
	Nasogastrically administered Shigella sonnei WRSs2 and WRSs3	Preclinical development	Second generation of vaccines from WRSS1. Shown by animals models to be safety and immunogenic.	Barnoy et al., 2010^53; 2011^54
	Proteins and conjugates vaccines (subcutaneous, intraperitoneal and intramuscular injections)	Preclinical development	Using synthetic carbohydrates derived from the LPS, it is possible to generate a multivalent vaccine diminishing the reactogenicity of LPS.	Pozsgay et al., 1999^38; Phalipon et al., 2006^36; 2009^37; Robbins et al., 2009^39
Nontyphoidal Salmonella	Orally administered live attenuated S. Typhimurium WT05	Early clinical development	Phase I, immune response observed in volunteers receiving a high dose (10^9 CFU).	Hindle et at, 2002^63
	O antigen conjugated to tetanus toxoid, administered by subcutaneous injection	Preclinical development	This vaccine candidate showed protection in animal models by challenged an passive immunization	Watson et al 1992^65
	O antigen conjugated with porins or BSA, antibodies injected intravenously	Preclinical development	This candidate confer protection thought passive immunization	Svenson et al 1979^66, 1981^67
	O antigen conjugated with CRM197, administered by subcutaneous injection	Preclinical development	This vaccine candidate produce antibodies against LPS	Stefanetti et al 2014^68
	Core O LPS conjugated to H antigen, administered by intramuscular injection.	Preclinical development	This vaccine candidate showed protection in animal models.	Simon et al., 2011^69; 2013^70
	Orally administered S. Enteritidis: CVD1941 and CVD1943	Preclinical development	These live attenuated strains induce antibodies against LPS and flagellin in mice.	Tennant et al., 2011^75
ETEC	Dukoral® (Oral administration)	Worldwide License	Licensed to prevent cholera. Cross protection by similitude between CT and LT. Recommended for travelers to endemic regions.	Clemens et al., 1988^84
	LT patch	Advanced clinical development	Limited protection evidenced after phase III trial.	Behrens et al., 2014^89
	Orally administered live attenuated ETEC expressing CFA/I, CS1, CS2, CS3, CS5 and CS6 (ACE257)	Advanced clinical development	No protection evidenced after phase IIb trial.	Darsley et al., 2012^90
	Orally administered killed whole cells + CTB	Advanced clinical development	Limited protection evidenced after phase III trial. Reduction in the number of severe diarrhea cases noted.	Wiedermann et al., 2000^95
	Orally administered double mutant LT (dmLT)	Early clinical development	Safe and immunogenic after phase I trial. Currently used as an adjuvant in newer formulations.	El-Kamary et al., 2013^102
	Orally administrated live attenuated ETEC expressing CS1 and CS3 (PTL-003)	Early clinical development	Safe and immunogenic after phase I trial. No significant protection in phase II trial.	McKenzie et al., 2008^99
	Orally administered CS6 coated microspheres	Early clinical development	Limited immunogenicity after phase I trial.	Lapa et al., 2008^100
	CS6 patch	Early clinical development	Limited immunogenicity after phase I trial.	Güereña-Buegueño et al., 2002^101
	Intragastrically administered killed whole cells + CTB/LTB + dmLT	Preclinical development	Safe and immunogenic in mice.	Holmgren et al., 2013^103
	Intranasally administered Shigella carrying ETEC CFs	Preclinical development	Safe and immunogenic in guinea pigs.	Barry et al., 2006^104
	Intranasally administered Vibrio cholerae Peru-15-pCTB	Preclinical development	Stimulates production of anti-LT antibodies in mice.	Roland et al., 2007^105
	STh/dmLT administered by intraperitoneal injection	Preclinical development	Safe and immunogenic. Stimulates production of anti-LT and anti-STh antibodies.	Ruan et al., 2014^106
	Intranasally administered type V-secreted proteins (EtpA, Ag43, pAT)	Preclinical development	Reduce intestinal colonization in mice.	Harris et al., 2011^110; Roy et al., 2008^111
Shiga-toxin producing Escherichia coli	O157-rEPA Vaccine based on E. coli O157:H7 O-specific polysaccharide conjugated to recombinant exotoxin A of Pseudomonas aeruginosa . Intramuscular injection (administered into the deltoid muscle)	Early clinical development	Phase I trial in adults, vaccine was safe and immunogenic; phase II trial in children, no significant adverse reactions were observed, concluding that the vaccine was safe and immunogenic.	Konadu et al., 1998^176; Ahmed et al., 2006^176,177
Campylobacter jejuni	Capsular polysaccharide conjugates administered by subcutaneous injection.	Preclinical development	Conferred significant protection to an oral challenge in monkeys (Aotus nancymaae).	Monteiro et al., 2009^190

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