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OBJECTIVES

Describe characteristics of gastroenteritis, bacteremia, and meningitis caused by nontyphoidal Salmonella among US infants.

METHODS

We analyze national surveillance data during 1968–2015 and active, sentinel surveillance data during 1996–2015 for culture-confirmed Salmonella infections by syndrome, year, serotype, age, and race.

RESULTS

During 1968–2015, 190 627 culture-confirmed Salmonella infections among infants were reported, including 165 236 (86.7%) cases of gastroenteritis, 6767 (3.5%) bacteremia, 371 (0.2%) meningitis, and 18 253 (9.7%) with other or unknown specimen sources. Incidence increased during the late 1970s–1980s, declined during the 1990s–early 2000s, and has gradually increased since the mid-2000s. Infants’ median age was 4 months for gastroenteritis and bacteremia and 2 months for meningitis. The most frequently reported serotypes were Typhimurium (35 468; 22%) for gastroenteritis and Heidelberg for bacteremia (1954; 29%) and meningitis (65; 18%). During 1996–2015 in sentinel site surveillance, median annual incidence of gastroenteritis was 120, bacteremia 6.2, and meningitis 0.25 per 100 000 infants. Boys had a higher incidence of each syndrome than girls in both surveillance systems, but most differences were not statistically significant. Overall, hospitalization and fatality rates were 26% and 0.1% for gastroenteritis, 70% and 1.6% for bacteremia, and 96% and 4% for meningitis. During 2004–2015, invasive salmonellosis incidence was higher for Black (incident rate ratio, 2.7; 95% confidence interval, 2.6–2.8) and Asian (incident rate ratio, 1.8; 95% confidence interval, 1.7–1.8) than white infants.

CONCLUSIONS

Salmonellosis causes substantial infant morbidity and mortality; serotype heidelberg caused the most invasive infections. Infants with meningitis were younger than those with bacteremia or gastroenteritis. Research into risk factors for infection and invasive illness could inform prevention efforts.

What’s Known on This Subject:

Infants experience a disproportionate share of reported Salmonella infections, but little is known about the relative importance of various sources of Salmonella for infants or factors that contribute to invasive infections.

What This Study Adds:

Salmonella among infants continues to be associated with substantial morbidity and mortality. Infants with meningitis are younger than infants with gastroenteritis and bacteremia. Infants identified as Black and Asian have higher rates of invasive illness than infants identified as white. Information about illnesses may lead to hypotheses about routes of exposure.

Salmonella enterica is estimated to cause 1.35 million illnesses, 26 000 hospitalizations, and 420 deaths annually in the United States.1  United States cases of typhoid and paratyphoid fever, which cause severe, invasive infections, are rare and usually follow international travel.2,3  Nontyphoidal Salmonella infection, called salmonellosis, is primarily acquired through consumption of contaminated food and through consumption of contaminated water or contact with an animal, person, or the environment.2,4,5  Salmonellosis is associated with a variety of manifestations; the most common is gastroenteritis. Bacteremia and meningitis can be life-threatening.6,7 

Infants experience more reported salmonellosis than other age groups8 ; 9% to 10% of culture-confirmed cases reported during 2013–2015 occurred in infants.911  Little is known about the relative importance of sources or factors that contribute to invasive Salmonella infections for infants. We describe characteristics of gastroenteritis, bacteremia, and meningitis caused by nontyphoidal Salmonella among United States infants to inform prevention strategies. We hypothesize that all infants are at risk for severe salmonellosis, but risk differs by exposures and host factors.

The Centers for Disease Control and Prevention (CDC) conducts United States surveillance for culture-confirmed salmonellosis. Clinical diagnostic laboratories submit isolates from ill persons to public health laboratories, where, during the study period, they were confirmed and serotyped by the Kauffmann-White Scheme.12  The CDC Laboratory-based Enteric Disease Surveillance (LEDS) system conducts passive, national laboratory surveillance of salmonellosis in all states and the District of Columbia. Data include self-reported demographics, serotype, and specimen source. Since 1996, the Foodborne Diseases Active Surveillance Network (FoodNet) has conducted population-based salmonellosis surveillance; since 2004, the catchment area has been stable and included Connecticut, Georgia, Maryland, Minnesota, New Mexico, Oregon, Tennessee, and selected counties in California, Colorado, and New York (approximately 15% of the United States population). Investigators attempt to collect demographic, hospitalization, and outcome data on every salmonellosis case via patient/parent interviews, electronic laboratory reports, and other health records; methods of collecting data have not changed over this period. Each surveillance system was analyzed separately; both systems count only 1 case when specimens collected ≤30 days apart yielded the same pathogen. When isolates from multiple specimen sources are available for the same case, data from the source indicating the most invasive infection (cerebrospinal fluid > blood > stool) are analyzed. We excluded cases after 2015 because the increasing use of culture-independent diagnostic tests for Salmonella increases pathogen detection but decreases availability of isolates for serotyping.13,14 

We defined infants as persons aged <1 year. We defined syndromes based on specimen source: gastroenteritis from stool, bacteremia from blood, and meningitis from cerebrospinal fluid. We excluded cases with isolates from other sources. We combined meningitis and bacteremia as invasive infections in some analyses because of sparse data.

We identified cases of Salmonella gastroenteritis, bacteremia, and meningitis reported to national surveillance (LEDS) during 1968–2015 and compared syndromes by incidence, age, sex, month of specimen collection, and serotype. Race was available for only 11% and ethnicity for 6% in LEDS, and they were not assessed. We report incidence trends using 4-year age intervals; we used 12-year intervals for serotypes because of greater year-to-year variability. Because LEDS did not collect birth data until 1995 and reporters might have rounded age to months (eg, 4 months and 20 days to 5 months), we minimized any resulting bias by reporting median age with first and third quartiles per time interval or used categories (<1–2, 3–5, 6–8, and 9–11 months). We assessed seasonality by comparing the percentage of cases in each month with the expected percentage (8.3%) if cases were evenly distributed.

We assessed incidence, age, sex, and patient outcomes, including hospitalization, length of hospitalization, and death, using FoodNet data reported during 1996–2015. Comparisons by race were limited to 2004–2015 because data were missing for >20% of cases for most earlier years; ethnicity was not assessed because data were missing for >20% of cases for most years. Hospitalization was defined as admission occurring within seven days of specimen collection. Patient outcome (alive, dead, or unknown) was determined by interview or medical chart review and recorded 7 days after specimen collection or at hospital discharge, whichever was later.

We used census population estimates for infants during 1990–2015 to estimate annual incidence by syndrome for national surveillance. During 1970–1989, census estimates of infants were unavailable. We estimated infant population size during 1970–1989 by applying the mean proportion of children aged 0–4 years who were infants during 1990–2015 to census estimates for children aged 0–4 years during 1970–1989. We estimated annual incidence by syndrome for FoodNet using census population estimates for FoodNet surveillance sites. We report incidence trends by race using four-year intervals; incidence estimates were limited to groups with ≥10 cases of invasive salmonellosis. We express all incidence estimates per 100 000 infants. We compared incidence rate ratios (IRRs) and 95% confidence intervals (95% CI) for boys and girls in national surveillance (1990–2015) and FoodNet (1996–2015). We compared IRRs for Black and Asian infants with white infants in FoodNet (2004–2015). We selected the referent group based on largest infant population size and lowest incidence rate for invasive salmonellosis. We compared continuous variables using 95% CIs and proportions using a 1-sample test for binomial proportion and Fisher exact test with the mid-P method. Analyses were conducted using SAS version 9.4 (SAS Institute, Inc., Cary, North Carolina), OpenEpi version 3.01 (Dean et al., Emory University, Atlanta, Georgia), and Microsoft Excel 2013.

We identified 190 627 culture-confirmed Salmonella infections among infants reported to national surveillance during 1968–2015, which composed 165 236 (86.7%) cases of gastroenteritis, 6767 (3.5%) bacteremia, 371 (0.2%) meningitis (Table 1), and 18 253 (9.7%) with other or unknown specimen sources. The median annual incidence (range) during 1970–2015 was 93 (27–162) gastroenteritis cases, 3.9 (1.4–6.7) bacteremia cases, and 0.21 (0.07–0.49) meningitis cases (Table 1). Incidence of each syndrome increased during the late 1970s or the 1980s, declined during the 1990s–early 2000s, and gradually has increased since the mid-2000s (Fig 1).

Cases were highest during August–October for gastroenteritis (10.9% to 11.4%) and bacteremia (10.1% to 10.8%). The number of meningitis cases was much higher than expected (if evenly distributed by month) in October (17.8% vs 8.3%; 95% CI, 14.0–22.1). (Fig 2). This increase was not associated with a specific serotype, period, or age (data not shown).

Median (first–third quartile) ages were 4 (3–7) months for gastroenteritis, 4 (2–7) months for bacteremia, and 2 months (1–3) for meningitis (Table 1). Comparing national surveillance data for 1968–1971 with 2012–2015, median age increased from 4 (1–7) to 5 (3–8) months for gastroenteritis and from 3 (1–4) to 4 (<1–8) months for bacteremia but decreased from 1 (1–4) to <1 (<1–2) month for meningitis. The decrease in age with meningitis occurred primarily because of an increase in cases among infants aged <3 months during 2004–2015 (Fig 1). Incidence of gastroenteritis was slightly higher for boys (73) than girls (67) (IRR, 1.1; 95% CI, 1.1–1.1), as was incidence of bacteremia (4.0 vs 3.6; IRR, 1.1; 95% CI, 1.0–1.2) and meningitis (0.20 vs 0.16; IRR, 1.2; 95% CI, 0.9–1.6) (Table 1).

During 1968–2015, the most frequently reported serotypes for gastroenteritis were Typhimurium (21.5%), Newport (8.7%), and Heidelberg (7.4%). The most frequently reported serotypes for invasive salmonellosis were Heidelberg (28.3%), Typhimurium (12.6%), and Enteritidis (10.2%) (Table 2). Comparing serotypes during 1968–79 with 2004–2015, the percentage of infections decreased from 23.2% to 12.3% for Typhimurium, 8.8% to 2.8% for Heidelberg, and 6.0% to 2.1% for infantis. The percentage of infections increased from 7.3% to 12.8% for Newport and 2.2% to 6.8% for Javiana. However, the percentage of unknown serotype or partially serotyped isolates increased, from 1.0% to 10.7%. The percentage that was Enteritidis was stable at 5.4%. Serotype 4,[5],12:i:- emerged after the 1990s, accounting for 2.5% of cases during 2004–2015. During 2012–2015, Newport (13.9%), Typhimurium (9.9%), and Javiana (7.9%) were the most frequently identified serotypes, but Heidelberg (14.2%) and Enteritidis (8.8%) caused the most invasive infections.

During 1996–2015, FoodNet sites reported 13 151 cases of infant salmonellosis, including 12 241 (93%) cases of gastroenteritis, 624 (4.7%) bacteremia, 25 (0.2%) meningitis (Table 1), and 261 (2%) with other or unknown specimen sources. Median annual incidence (range) for gastroenteritis was 120 (101–149), bacteremia 6.2 (3.6–9.8), and meningitis 0.25 (0.00–0.84) (Table 1). Incidence of bacteremia decreased from 7.6 (95% CI, 6.2–9.1) during 1996–1999 to 5.1 (95% CI, 4.0–6.1) during 2012–2015; incidence of overall salmonellosis, gastroenteritis, and meningitis did not change significantly over time. Incidence of meningitis was 1.4 times higher for boys than girls (0.29 vs 0.20; 95% CI, 1.1–1.9), incidence of gastroenteritis was 1.1 times higher (126 vs 113; 95% CI, 1.1–1.1), and incidence of bacteremia was 1.1 times higher (6.2 vs 5.9; IRR, 1.1; 95% CI, 1.0–1.1).

During 2004–2015, race data were available for 413 (90%) infants with invasive salmonellosis and 8018 (88%) of infants with gastroenteritis. Compared with white infants, incidence of invasive salmonellosis was 2.7 times higher for Black infants (10.4 vs 3.9; 95% CI, 2.6– 2.8) and 1.8 times higher for Asian infants (6.8 vs 3.9; 95% CI, 1.7–1.8). Compared with white infants, the incidence of gastroenteritis was 1.2 times higher for Black infants (119 vs 99; 95% CI, 1.19–1.21) and 0.89 times lower for Asian infants (88 vs 99; IRR, 0.89; 95% CI, 0.88–0.90).

Comparing 2004–2007 with 2012–2015, incidence (95% CI) of gastroenteritis increased from 87 (83–92) to 102 (97–107) for white infants, decreased from 127 (117–138) to 105 (96–115) for Black infants, and increased from 68 (54–84) to 107 (90–126) for Asian infants. During that time, incidence of invasive salmonellosis increased from 2.8 (2.1–3.6) to 4.3 (3.4–5.4) for white infants, decreased from 15.8 (12.4–19.9) to 6.7 (4.6–9.5) for Black infants, and increased from 4.3 (1.6–9.5) to 7.7 (3.9–13.8) for Asian infants (Fig 3).

Among infants with gastroenteritis with information on hospitalization and death, 2790 (26%) were hospitalized and 7 (0.1%) died. Among infants with bacteremia, 407 (70%) were hospitalized and 9 (1.6%) died. Among infants with meningitis, 22 (96%) were hospitalized and 1 died. Among infants who were hospitalized, the median (interquartile range) length of hospital stay was 2 (2–3) days for gastroenteritis, 4 (3–7) days for bacteremia, and 20 (10–33) days for meningitis (Table 1).

These analyses characterize the epidemiology of infant salmonellosis by syndrome using 48 years of passive national surveillance data and 20 years of active sentinel surveillance data. Both systems show that infants continue to experience substantial morbidity from salmonellosis, including gastrointestinal and invasive illness. However, the incidence of bacteremia has decreased since the 1990s. Infants with meningitis were younger than those with bacteremia or gastroenteritis, and serotype Heidelberg caused the highest percentage of invasive infections, even in the most recent 4 years when the overall incidence of Heidelberg infections markedly decreased.11 

The annual incidence varied over time for all syndromes. Incidence estimates based on primarily passive (national) surveillance suggest moderate increases for each syndrome during the past 20 years. Incidence estimates based on active (FoodNet) sentinel site surveillance are 25% to 50% higher than estimates from passive surveillance and suggest steady rates for meningitis and gastroenteritis and a decreasing rate for bacteremia. Different patterns over time might be due to better reporting from FoodNet active surveillance sites or to different population structure, patterns of diagnosis, or reporting compared with the entire country.

These data do not provide information to assess sources of Salmonella or risk factors for invasive disease; demographic characteristics are described as risk indicators. Reported risk factors for infant salmonellosis include exposure to animals, exposure to a household member or attending day care with a child with recent diarrhea, international travel, riding in a shopping cart with raw meat or poultry, and other indoor and outdoor environmental exposures.1518  Use of infant formula and lack of breastfeeding are correlated risk markers.15,19 Salmonella has only rarely been identified in commercial formula.20,21  Breastfeeding might be protective because of immunity (eg, maternal antibodies from breastmilk) or to lack of exposure to bottles contaminated by household members.

Infants are at increased risk of invasive infection.22,23  Reported risk factors for extraintestinal salmonellosis include age, serotype, other infections such as HIV and rotavirus, and underlying health conditions such as sickle cell anemia and gastrointestinal conditions.2225  In children, invasive infections are often secondary to gastroenteritis; decreased gastric acidity or gut immaturity may increase vulnerability to invasive infections.2528 

The median age of infants differed by syndrome and over time; infants with meningitis are younger than infants with gastroenteritis and bacteremia, and the average age for meningitis decreased over time, primarily from an increase in meningitis among infants <3 months of age over the past 2 decades. A similar increase in bacterial meningitis from all causes was reported for infants <2 months old from 1998–1999 to 2006–2007, whereas incidence of bacterial meningitis decreased over the same period for all other age groups.29  Increased survival of premature infants,30  changes in exposure patterns, or changes in testing or care-seeking practices might contribute to the increase in meningitis cases among the youngest infants.

Serotypes Heidelberg and Enteritidis accounted for a larger proportion of invasive salmonellosis than of gastroenteritis, and Typhimurium accounted for a smaller proportion. However, Typhimurium still accounts for a substantial burden of infant invasive infections. Our findings are consistent with other reports that Heidelberg and Enteritidis are more likely to cause invasive infections than Typhimurium and Newport.31,32  Among all persons, both Heidelberg and Typhimurium incidence have decreased dramatically in the past 20 years, most likely because of vaccination of poultry.14,33,34 

During 2012–2015, Typhimurium and Newport were the most common serotypes causing infant salmonellosis. The number and percentage of cases caused by Heidelberg decreased since the 1980s for gastroenteritis, but Heidelberg and Enteritidis still cause 23% of invasive infections in infants. Heidelberg, Typhimurium, and Enteritidis infections among adults are often associated with egg and poultry products, and Newport infections are often associated with meat products. The extent to which these sources contribute to infant salmonellosis is unknown. However, declines in serotypes causing infant salmonellosis paralleling declines in overall salmonellosis suggest that food is the ultimate source. It seems likely that infants are exposed from contamination of their food or environment directly from food (eg, poultry, meat, eggs), or from the fecal matter of infected caretakers. Avenues for further exploration include whether infant formula could be a more common source than is recognized and whether the presence of certain food products in the home or the food consumption habits of caretakers are risk factors for infant salmonellosis.

Although infant ages differed, serotype distributions for meningitis and bacteremia were similar, suggesting that infants who develop meningitis and bacteremia are exposed to a similar distribution of sources, and that age-related factors influence clinical presentation. In contrast, infants with bacteremia have a similar age distribution but a different serotype distribution from infants with gastroenteritis, suggesting that differences in factors not related to age (eg, exposure to particular sources, susceptibility to particular serotypes) play a greater role in determining clinical presentation. Further study is needed to determine whether serotype differences by syndrome can be attributed to different exposure sources or routes, host factors, or invasiveness of serotypes.

Previous analyses using FoodNet data identified racial differences in incidence of Salmonella gastroenteritis and invasive salmonellosis among infants and showed that differences by race decreased between 1996 and 2008.22,23  Our findings indicate that differences by race continued to decrease after 2008. The rate of invasive salmonellosis declined among Black infants but increased among Asian infants. Social determinates of health, including income inequality, discrimination, and differences in health care access and use, are drivers of poor health and might contribute to differences by race.3538  More information about social determinants of health is needed to better understand the reasons for differences by race and improve prevention measures. Differences in exposures, including differences in breastfeeding initiation and duration, and underlying health conditions might also contribute to differences by race.23,25,39  Focusing on decreasing exposures that lead to illness and identifying subpopulations of infants with host factors that put them at increased risk for illness could help to decrease these illnesses. It is also possible that changes by race reflect changing access to and use of health care or diagnostic practices, rather than a true change in incidence. Salmonellosis incidence was slightly higher among boys than girls across syndromes and surveillance systems, consistent with previous reports.22,23 

Infant salmonellosis peaked in the summer and fall for each syndrome, but the pattern differed for meningitis compared with gastroenteritis and bacteremia. Previous reports have found that Salmonella gastroenteritis and bacteremia are seasonal, occurring more frequently during warm and rainy seasons, suggesting that environmental factors play a role.8,2628  However, the distinct spike in meningitis cases in October is a new finding, and its implications are unknown.

Limitations of these analyses include that salmonellosis is underdiagnosed and underreported2 ; the degree likely differs by syndrome because persons with more severe illness are more likely to receive medical care.2,40  For bacteremia and meningitis, underestimation may occur because of treatment with antibiotics occurring before collecting specimens. The data do not provide information about factors that may contribute to the observed differences by race. Changes over time could be partly because of unrecognized changes in diagnosis and reporting of illness and race. The completeness and representativeness of passive national surveillance data, including age, varies over time and by reporting site. Extrapolated infant population size for 1970–1989 might bias incidence estimates if variability in birth rates or child mortality changed pediatric population distribution over time; however, birth rates were relatively stable throughout most of the 1970s–1990s, and child mortality improved for all ages.41,42 

All syndromes of salmonellosis are associated with substantial morbidity and mortality among infants. We observed a higher rate of invasive illness among infants identified as Black and Asian than white. Although infants with meningitis had the highest case fatality and hospitalization rates, the largest mortality burden occurred among those with bacteremia, and the total number of hospitalization days was highest for infants with gastroenteritis. In addition to acute morbidity, risk of death, and stress to families, invasive salmonellosis among infants can be associated with moderate to severe sequelae, including fine motor, cognitive, behavioral, neuropsychologic, and auditory dysfunctions over a lifetime.4345 

To inform prevention efforts for infant salmonellosis, further research is needed into modifiable risk factors. Many infants are probably exposed to Salmonella in the home; they might become infected from the same exposures that could infect other family members, including consumption of foods and contact with contaminated surfaces, or they might acquire illness from family members.46  Food is the major source of salmonellosis for the general population, so the most effective control measure might be to decrease Salmonella contamination of food.14,47 

The authors thank Beau B. Bruce, Robert M. Hoekstra, and Robert V. Tauxe for providing useful feedback on the analysis plans or earlier drafts of this report. Many thanks to Yuri Springer for insightful feedback on analyses including race. The authors also thank the local, state, and federal public health professionals who made these analyses possible, as well as the Centers for Disease Control and Prevention’s Laboratory-based Enteric Disease Surveillance and Foodborne Diseases Active Surveillance Network teams that provided access to these data. The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention.

Dr Self conceptualized and designed the study, conducted analyses, drafted the initial manuscript, and reviewed and revised the manuscript; Mr Judd and Ms Huang contributed to conceptualization and design, data curation, analysis, and drafting and revising the manuscript; Dr Fields provided supervision and reviewed and revised the manuscript; Dr Griffin contributed to conceptualization, provided oversight and supervision, and reviewed and revised the manuscript; Dr Wong conceptualized and designed the study, contributed to analyses, provided supervision and oversight, and reviewed and revised the manuscript; and all authors approved the final manuscript as submitted and agree to be accountable for all aspects of the work.

The data are available by making a request to the corresponding author or to the Enteric Diseases Epidemiology Branch (edebadminsupport@cdc.gov). Because of personally identifiable information, not all data are publicly available.

FUNDING: No external funding.

CONFLICT OF INTEREST DISCLOSURES: The authors have indicated they have no potential conflicts of interest to disclose.

95% CI

95% confidence interval

CDC

Centers for Disease Control and Prevention

FoodNet

Foodborne Diseases Active Surveillance Network

IRR

incidence rate ratio

LEDS

Laboratory-based Enteric Disease Surveillance

1
Collier
SA
,
Deng
L
,
Adam
EA
, et al
.
Estimate of burden and direct healthcare cost of infectious waterborne disease in the United States
.
Emerg Infect Dis
.
2021
;
27
(
1
):
140
149
2
Scallan
E
,
Hoekstra
RM
,
Angulo
FJ
, et al
.
Foodborne illness acquired in the United States--major pathogens
.
Emerg Infect Dis
.
2011
;
17
(
1
):
7
15
3
Lynch
MF
,
Blanton
EM
,
Bulens
S
, et al
.
Typhoid fever in the United States, 1999-2006
.
JAMA
.
2009
;
302
(
8
):
859
865
4
Pires
SM
,
Vieira
AR
,
Hald
T
,
Cole
D
.
Source attribution of human salmonellosis: an overview of methods and estimates
.
Foodborne Pathog Dis
.
2014
;
11
(
9
):
667
676
5
Hale
CR
,
Scallan
E
,
Cronquist
AB
, et al
.
Estimates of enteric illness attributable to contact with animals and their environments in the United States
.
Clin Infect Dis
.
2012
;
54
(
Suppl 5
):
S472
S479
6
Hohmann
EL
.
Nontyphoidal salmonellosis
.
Clin Infect Dis
.
2001
;
32
(
2
):
263
269
7
Centers for Disease Control and Prevention (CDC)
.
National Salmonella Surveillance Annual Report, 2012
.
Atlanta, Georgia
:
US Department of Health and Human Services, CDC
;
2014
8
Olsen
SJ
,
Bishop
R
,
Brenner
FW
, et al
.
The changing epidemiology of salmonella: trends in serotypes isolated from humans in the United States, 1987-1997
.
J Infect Dis
.
2001
;
183
(
5
):
753
761
9
Centers for Disease Control and Prevention (CDC)
.
National Enteric Disease Surveillance: Salmonella Annual Report, 2013
.
10
Centers for Disease Control and Prevention (CDC)
.
National Enteric Disease Surveillance: Salmonella Annual Report, 2014
.
11
Centers for Disease Control and Prevention (CDC)
.
National Enteric Disease Surveillance: Salmonella Annual Report, 2015
.
12
Grimont
PAD
,
Weill
FX
.
Antigenic formulae of the Salmonella serovars
, 9th ed.
13
Marder
EP
,
Cieslak
PR
,
Cronquist
AB
, et al
.
Incidence and trends of infections with pathogens transmitted commonly through food and the effect of increasing use of culture-independent diagnostic tests on surveillance - Foodborne Diseases Active Surveillance Network, 10 U.S. Sites, 2013-2016
.
MMWR Morb Mortal Wkly Rep
.
2017
;
66
(
15
):
397
403
14
Tack
DM
,
Marder
EP
,
Griffin
PM
, et al
.
Preliminary incidence and trends of infections with pathogens transmitted commonly through food - Foodborne Diseases Active Surveillance Network, 10 U.S. Sites, 2015-2018
.
MMWR Morb Mortal Wkly Rep
.
2019
;
68
(
16
):
369
373
15
Jones
TF
,
Ingram
LA
,
Fullerton
KE
, et al
.
A case-control study of the epidemiology of sporadic Salmonella infection in infants
.
Pediatrics
.
2006
;
118
(
6
):
2380
2387
16
Meyer Sauteur
PM
,
Relly
C
,
Hug
M
, %
Wittenbrink
MM
,
Berger
C
.
Risk factors for invasive reptile-associated salmonellosis in children
.
Vector Borne Zoonotic Dis
.
2013
;
13
(
6
):
419
421
.
17
Sockett
PN
,
Rodgers
FG
.
Enteric and foodborne disease in children: a review of the influence of food- and environment- related risk factors
.
Paediatr Child Health
.
2001
;
6
(
4
):
203
209
18
Schutze
GE
,
Sikes
JD
,
Stefanova
R
,
Cave
MD
.
The home environment and salmonellosis in children
.
Pediatrics
.
1999
;
103
(
1
):
E1
19
Haddock
RL
,
Cousens
SN
,
Guzman
CC
.
Infant diet and salmonellosis
.
Am J Public Health
.
1991
;
81
(
8
):
997
1000
20
Centers for Disease Control and Prevention (CDC)
.
Salmonella serotype Tennessee in powdered milk products and infant formula--Canada and United States, 1993
.
MMWR Morb Mortal Wkly Rep
.
1993
;
42
(
26
):
516
517
21
Bornemann
R
,
Zerr
DM
,
Heath
J
, et al
.
An outbreak of Salmonella serotype Saintpaul in a children’s hospital
.
Infect Control Hosp Epidemiol
.
2002
;
23
(
11
):
671
676
22
Cheng
LH
,
Crim
SM
,
Cole
CR
,
Shane
AL
,
Henao
OL
,
Mahon
BE
.
Epidemiology of infant salmonellosis in the United States, 1996-2008: a Foodborne Diseases Active Surveillance Network Study
.
J Pediatric Infect Dis Soc
.
2013
;
2
(
3
):
232
239
23
Arshad
MM
,
Wilkins
MJ
,
Downes
FP
, et al
.
Epidemiologic attributes of invasive non-typhoidal Salmonella infections in Michigan, 1995--2001
.
Int J Infect Dis
.
2008
;
12
(
2
):
176
182
24
Varma
JK
,
Molbak
K
,
Barrett
TJ
, et al
.
Antimicrobial-resistant nontyphoidal Salmonella is associated with excess bloodstream infections and hospitalizations
.
J Infect Dis
.
2005
;
191
(
4
):
554
561
25
Wright
J
,
Thomas
P
,
Serjeant
GR
.
Septicemia caused by Salmonella infection: an overlooked complication of sickle cell disease
.
J Pediatr
.
1997
;
130
(
3
):
394
399
26
Shkalim
V
,
Amir
A
,
Samra
Z
,
Amir
J
.
Characteristics of non-typhi Salmonella gastroenteritis associated with bacteremia in infants and young children
.
Infection
.
2012
;
40
(
3
):
285
289
27
Finkelstein
Y
,
Moran
O
,
Avitzur
Y
, et al
.
Clinical dysentery in hospitalized children
.
Infection
.
2002
;
30
(
3
):
132
135
28
Henao
OL
,
Jones
TF
,
Vugia
DJ
,
Griffin
PM
;
Foodborne Diseases Active Surveillance Network (FoodNet) Workgroup
.
Foodborne Diseases Active Surveillance Network-2 decades of achievements, 1996-2015
.
Emerg Infect Dis
.
2015
;
21
(
9
):
1529
1536
29
Thigpen
MC
,
Whitney
CG
,
Messonnier
NE
, et al;
Emerging Infections Programs Network
.
Bacterial meningitis in the United States, 1998-2007
.
N Engl J Med
.
2011
;
364
(
21
):
2016
2025
30
Glass
HC
,
Costarino
AT
,
Stayer
SA
,
Brett
CM
,
Cladis
F
,
Davis
PJ
.
Outcomes for extremely premature infants
.
Anesth Analg
.
2015
;
120
(
6
):
1337
1351
31
Angelo
KM
,
Reynolds
J
,
Karp
BE
,
Hoekstra
RM
,
Scheel
CM
,
Friedman
C
.
Antimicrobial resistance among nontyphoidal Salmonella isolated from blood in the United States, 2003-2013
.
J Infect Dis
.
2016
;
214
(
10
):
1565
1570
32
Jones
TF
,
Ingram
LA
,
Cieslak
PR
, et al
.
Salmonellosis outcomes differ substantially by serotype
.
J Infect Dis
.
2008
;
198
(
1
):
109
114
33
Marder Mph
EP
,
Griffin
PM
,
Cieslak
PR
, et al
.
Preliminary incidence and trends of infections with pathogens transmitted commonly through food - Foodborne Diseases Active Surveillance Network, 10 U.S. sites, 2006-2017
.
MMWR Morb Mortal Wkly Rep
.
2018
;
67
(
11
):
324
328
34
Dórea
FC
,
Cole
DJ
,
Hofacre
C
, et al
.
Effect of Salmonella vaccination of breeder chickens on contamination of broiler chicken carcasses in integrated poultry operations
.
Appl Environ Microbiol
.
2010
;
76
(
23
):
7820
7825
35
Kaplan
GA
,
Pamuk
ER
,
Lynch
JW
,
Cohen
RD
,
Balfour
JL
.
Inequality in income and mortality in the United States: analysis of mortality and potential pathways
.
BMJ
.
1996
;
312
(
7037
):
999
1003
36
Ronzio
CR
,
Pamuk
E
,
Squires
GD
.
The politics of preventable deaths: local spending, income inequality, and premature mortality in US cities
.
J Epidemiol Community Health
.
2004
;
58
(
3
):
175
179
37
U.S. Department of Health and Human Services
.
Healthy People 2030 Social Determinants of Health Literature Summaries: Discrimination
.
38
U.S. Department of Health & Human Services
.
Healthy People 2030 Social Determinants of Health Literature Summaries: Poverty
.
39
Beauregard
JL
,
Hamner
HC
,
Chen
J
,
Avila-Rodriguez
W
,
Elam-Evans
LD
,
Perrine
CG
.
Racial disparities in breastfeeding initiation and duration among U.S. infants born in 2015
.
MMWR Morb Mortal Wkly Rep
.
2019
;
68
(
34
):
745
748
40
Scallan
E
,
Jones
TF
,
Cronquist
A
, et al;
FoodNet Working Group
.
Factors associated with seeking medical care and submitting a stool sample in estimating the burden of foodborne illness
.
Foodborne Pathog Dis
.
2006
;
3
(
4
):
432
438
41
Guyer
B
,
Freedman
MA
,
Strobino
DM
,
Sondik
EJ
.
Annual summary of vital statistics: trends in the health of Americans during the 20th century
.
Pediatrics
.
2000
;
106
(
6
):
1307
1317
42
Hamilton
BE
,
Kirmeyer
SE
.
Trends and variations in reproduction and intrinsic rates: United States, 1990-2014
.
Natl Vital Stat Rep
.
2017
;
66
(
2
):
1
14
43
Wu
HM
,
Huang
WY
,
Lee
ML
,
Yang
AD
,
Chaou
KP
,
Hsieh
LY
.
Clinical features, acute complications, and outcome of Salmonella meningitis in children under one year of age in Taiwan
.
BMC Infect Dis
.
2011
;
11
:
30
44
Lee
WS
,
Puthucheary
SD
,
Omar
A
.
Salmonella meningitis and its complications in infants
.
J Paediatr Child Health
.
1999
;
35
(
4
):
379
382
45
Grimwood
K
,
Anderson
VA
,
Bond
L
, et al
.
Adverse outcomes of bacterial meningitis in school-age survivors
.
Pediatrics
.
1995
;
95
(
5
):
646
656
46
Wilson
R
,
Feldman
RA
,
Davis
J
,
LaVenture
M
.
Salmonellosis in infants: the importance of intrafamilial transmission
.
Pediatrics
.
1982
;
69
(
4
):
436
438
47
Beshearse
E
,
Bruce
BB
,
Nane
GF
, et al
.
Attribution of illnesses transmitted by food and water to comprehensive transmission pathways using structured expert judgment, United States
.
Emerg Infect Dis
.
2021
;
27
(
1
):
182
195