A 1998 investigation of an outbreak of Salmonella serotype Typhimurium infections among children tasting unpasteurized milk during tours of a dairy farm demonstrated a distribution of unusually long incubation periods (median, 8 days; interquartile range [IQR], 6–14 days). Bacterial isolates were highly acid tolerant and contained genes associated with protection against destructive phagocytic reactive oxygen intermediates. We hypothesize that exposure to low-dose oral inoculum of a pathogen with these properties could have contributed to cases of non-typhoidal salmonellosis with the longest incubation period reported to the Centers for Disease Control and Prevention (CDC).
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References
1.
AbeKK, SaitoNN, KasugaFFet al.Prolonged incubation period of salmonellosis associated with low bacterial doses. J Food Prot, 2004; 67:2735–2740.
2.
AmmendolaS, AjelloM, PasqualiPet al.Differential contribution of sodC1 and sodC2 to intracellular survival and pathogenicity of Salmonella enterica serovar Choleraesuis. Microbes Infect, 2005; 7:698–707.
3.
BlaserMJ, NewmanLS. A review of human salmonellosis. I. Infective dose. Rev Infect Dis, 1982; 4:1096–1106.
4.
[CDC] Centers for Disease Control and Prevention. Human tuberculosis caused by Mycobacterium bovis—New York City, 2001–2004. MMWR Morb Mortal Wkly Rep, 2005; 54:605–608.
5.
[CDC] Centers for Disease Control and Prevention. Salmonella Typhimurium infection associated with raw milk and cheese consumption—Pennsylvania, 2007. MMWR Morb Mortal Wkly Rep, 2007a. 56:1161–1164.
6.
[CDC] Centers for Disease Control and Prevention. Escherichia coli O157:H7 infection associated with drinking raw milk—Washington and Oregon, November–December 2005. MMWR Morb Mortal Wkly Rep, 2007b. 56:165–167.
7.
[CDC] Centers for Disease Control and Prevention. Escherichia coli 0157:H7 infections in children associated with raw milk and raw colostrum from cows—California, 2006. MMWR Morb Mortal Wkly Rep, 2008; 57:625–628.
8.
CurrierRW. Raw milk and human gastrointestinal disease: Problems resulting from legalized sale of “certified raw milk.”J Public Health Policy, 1981; 2:226–234.
9.
DeGrooteMA, OchsnerUA, ShilohMUet al.Periplasmic superoxide dismutase protects Salmonella from products of phagocyte NADPH-oxidase and nitric oxide synthase. Proc Natl Acad Sci USA, 1997; 94:13997–4001.
10.
EthelbergS, LisbyM, TorpdahlMet al.Prolonged restaurant-associated outbreak of multidrug-resistant Salmonella Typhimurium among patients from several European countries. Clin Microbiol Infect, 2004; 10:904–910.
11.
FangFC, DeGrooteMA, FosterJWet al.Virulent Salmonella Typhimurium has two periplasmic Cu,Zn-superoxide dismutases. Proc Natl Acad Sci USA, 1999; 96:7502–7507.
12.
FiererJ. Invasive Salmonella dublin infections associated with drinking raw milk. West J Med, 1983; 138:665–669.
13.
FiererJ, KrauseM, TauxeRVet al.Salmonella Typhimurium bacteremia: Association with the virulence plasmid. J Infect Dis, 1992; 166:639–642.
14.
GillespieIA, AdakGK, O'BrienSJet al.Milkborne general outbreaks of infectious intestinal disease, England and Wales, 1992–2000. Epidemiol Infect, 2003; 130:461–468.
15.
GlynnJJR, PalmerSSR. Incubation period, severity of disease, and infecting dose: Evidence from a Salmonella outbreak. Am J Epidemiol, 1992; 136:1369–1377.
16.
GuineyDG, FangFC, KrauseMet al.Plasmid-mediated virulence genes in non-typhoid Salmonella serovars. FEMS Microbiol Lett, 1994; 124:1–9.
17.
GuligPA, DanbaraH, GuineyDGet al.Molecular analysis of spv virulence genes of the Salmonella virulence plasmids. Mol Microbiol, 1993; 7:825–830.
18.
GuptaA, FontanaJ, CroweCet al.Emergence of multidrug-resistant Salmonella enterica serotype Newport infections resistant to expanded-spectrum cephalosporins in the United States. J Infect Dis, 2003; 188:1707–1716.
19.
HardtWD, UrlaubH, GalanJE. A substrate of the centisome 63 type III protein secretion system of Salmonella Typhimurium is encoded by a cryptic bacteriophage. Proc Natl Acad Sci USA, 1998; 95:2574–2579.
20.
HeadrickML, KorangyS, BeanNHet al.The epidemiology of raw milk–associated foodborne disease outbreaks reported in the United States, 1973 through 1992. Am J Public Health, 1998; 88:1219–1221.
21.
HeffernanEJ, FiererJ, ChikamiGet al.Natural history of oral Salmonella dublin infection in BALB/c mice: Effect of an 80-kilobase-pair plasmid on virulence. J Infect Dis, 1987; 155:1254–1259.
22.
KeeneWE, HedbergK, HerriottDEet al.A prolonged outbreak of Escherichia coli O157:H7 infections caused by commercially distributed raw milk. J Infect Dis, 1997; 176:815–818.
23.
KleinBS, VergerontJM, BlaserMJet al.Campylobacter infection associated with raw milk. An outbreak of gastroenteritis due to Campylobacter jejuni and thermotolerant Campylobacter fetus subsp fetus. JAMA, 1986; 255:361–364.
24.
LeedomJM. Milk of nonhuman origin and infectious diseases in humans. Clin Infect Dis, 2006; 43:610–615.
25.
MatsuiT, SuzukiS, TakahashiHet al.Salmonella Enteritidis outbreak associated with a school-lunch dessert: Cross-contamination and a long incubation period, Japan, 2001. Epidemiol Infect, 2004; 132:873–879.
26.
MazurekJ, SalehiE, PropesDet al.A multistate outbreak of Salmonella enterica serotype Typhimurium infection linked to raw milk consumption—Ohio, 2003. J Food Prot, 2004; 67:2165–2170.
27.
MintzED, CartterML, HadlerJLet al.Dose-response effects in an outbreak of Salmonella Enteritidis. Epidemiol Infect, 1994; 112:13–23.
28.
NagaiKK, MoriTT, TsudaSSet al.Prolonged incubation period of salmonellosis in an outbreak of Salmonella Enteritidis infection. Microbiol Immunol, 1999; 43:69–71.
29.
O'MahonyMM, BarnesHH, Stanwell-SmithRRet al.An outbreak of Salmonella heidelberg infection associated with a long incubation period. J Public Health Med, 1990; 12:19–21.
30.
PotterME, BlaserMJ, SikesRKet al.Human Campylobacter infection associated with certified raw milk. Am J Epidemiol, 1983; 117:475–483.
31.
SealsJE, ParrottPL, McGowanJEJret al.Nursery salmonellosis: Delayed recognition due to unusually long incubation period. Infect Control, 1983; 4:205–208.
32.
TaylorPR, WeinsteinWM, BrynerJH. Campylobacter fetus infection in human subjects: Association with raw milk. Am J Med, 1979; 66:779–783.
33.
TeshVL, SamuelJE, PereraLPet al.Evaluation of the role of Shiga and Shiga-like toxins in mediating direct damage to human vascular endothelial cells. J Infect Dis, 1991; 164:344–352.
