PEDIATRICS Vol. 118 No. 6 December 2006, pp. 2380-2387 (doi:10.1542/peds.2006-1218)
ARTICLE |
A Case-Control Study of the Epidemiology of Sporadic Salmonella Infection in Infants
a Tennessee Department of Health, Nashville, Tennessee
b Centers for Disease Control and Prevention, Atlanta, Georgia
c Connecticut Emerging Infections Program, New Haven, Connecticut
d New York State Department of Health, Albany, New York
e Center for Food Safety and Applied Nutrition, Food and Drug Administration, Washington, DC
f California Department of Health Services, Berkeley, California
g Oregon Department of Human Services, Portland, Oregon
h Colorado Department of Public Health and Environment, Denver, Colorado
i Minnesota Department of Health, Minneapolis, Minnesota
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ABSTRACT |
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 TOP ABSTRACT METHODSRESULTSDISCUSSIONREFERENCES |
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OBJECTIVE. Rates of Salmonella infection are highest in infants, but little is known about potential sources of infection in this high-risk population. We performed a case-control study to identify dietary and environmental risk factors for sporadic salmonellosis among infants.
PATIENTS AND METHODS. In 2002–2004, the Foodborne Diseases Active Surveillance Network conducted a population-based, case-control study of sporadic salmonellosis among infants <1 year of age in 8 states. Cases were identified via active laboratory-based surveillance. Healthy controls were frequency matched by age and identified through birth registries or published birth announcements. We assessed diet and environmental exposures in the 5 days before illness onset or interview. Data were analyzed by using logistic regression adjusting for age.
RESULTS. The study enrolled 442 subjects and 928 controls. Compared with healthy controls, infants with Salmonella infection were less likely to have been breastfed and more likely to have had exposure to reptiles, to have ridden in a shopping cart next to meat or poultry, or to have consumed concentrated liquid infant formula during the 5-day exposure period. Travel outside the United States was associated with illness in infants 3 to 6 and >6 months of age. Attending day care with a child with diarrhea was associated with salmonellosis in infants >6 months of age.
CONCLUSIONS. We identified a number of modifiable protective and risk factors for salmonellosis in infants. Attention should be directed at developing effective preventive measures for this high-risk population.
Key Words: Salmonella • infant • epidemiology
Abbreviations: FoodNet—Foodborne Diseases Active Surveillance Network • OR—odds ratio • CI—confidence interval
Salmonella is estimated to cause 1.4 million illnesses and 400 deaths each year in the United States.1 The incidence of laboratory-confirmed nontyphoidal Salmonella infection is much greater in infants (children <1 year of age) than it is among other age groups (Fig 1). 2 Furthermore, infants can suffer substantial morbidity from invasive Salmonella,3 and infants are at higher risk of complications from diarrheal disease.4 Much of what is understood about the epidemiology of this pathogen is derived from investigation of foodborne outbreaks, which typically have included few infants. Although there have been dramatic point-source outbreaks of salmonellosis in infants because of foods, fomites, and nursery exposures,3,5–8 the large majority of reported cases are not associated with recognized clusters.
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Sources of Salmonella in infants may be substantially different from those in older populations because of markedly different behaviors and more limited dietary and environmental exposures. However, aside from occasional case reports,9–13 few epidemiologic studies have examined potential sources of sporadic Salmonella infection in infants. Of the limited studies that were reported, many were performed in Guam, which has had a protracted epidemic of infant salmonellosis.14–17 Some studies have demonstrated that infants infected with Salmonella are less likely to be breastfed,16,18 more likely to be fed high-iron formula,16 and more likely to have a household member with diarrhea19 than healthy infants. We performed a large case-control study of sporadic infant salmonellosis to more completely examine factors associated with illness in this high-risk population.
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METHODS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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A case-control study was performed in the Foodborne Diseases Active Surveillance Network (FoodNet) surveillance area during a 24-month period in 2002–2004, with variable start dates among sites. FoodNet is a collaborative project involving the Centers for Disease Control and Prevention's Emerging Infections Program, the US Food and Drug Administration, the US Department of Agriculture Food Safety Inspection Service, and selected state health departments. During the study period, population-based active surveillance at all clinical laboratories for laboratory-confirmed Salmonella infections was performed in 8 sites (Connecticut, Minnesota, Oregon, and selected counties in California, Colorado, Georgia, New York, and Tennessee) covering a population of
35.2 million persons (12.1% of the US population), including 450 000 infants.20 This study was approved by the institutional review boards of the Centers for Disease Control and Prevention and all participating sites. All infants (children <1 year of age) residing within the catchment area during the study period were eligible for the study. A case was defined as a Salmonella infection in an infant from whom any serotype of Salmonella other than Typhi was isolated from a clinical specimen, with onset of disease or collection of the positive specimen occurring before their first birthday. Subjects were excluded if the family could not be contacted after at least 15 attempts (including evenings and weekends) or within 45 days of the specimen collection date, if the caretaker refused or did not speak English or Spanish (or Mandarin or Cantonese in California), or if the infant was asymptomatic or a chronic carrier (defined as persistent positive stool cultures >30 days after an acute illness). Subjects were not eligible if the illness was part of an outbreak investigated by public health officials and in which the vehicle of transmission was identified.
Controls were frequency matched by 1-month age categories on the basis of the incidence of laboratory-confirmed infant Salmonella and Campylobacter infection in each site in the preceding 3 years. Controls were selected randomly from all births in the catchment area reported in state birth registries. For part of the study period, the New York site used published birth announcements to identify controls. Controls were excluded if they could not be contacted after at least 15 attempts (including evenings and weekends), if their caretaker did not speak a language included in the study, or if they reported culture-confirmed Salmonella infection within the previous 30 days. A study of infant Campylobacter infection was performed concurrently in participating sites with identical questionnaires, and the same controls were used for both studies.21 Some sites offered $10 retail store gift certificates or checks to subjects and controls after completing the survey.
After obtaining informed consent, an extensive questionnaire was administered by telephone to the parents or guardians of the subjects and controls. Questionnaires were administered in English, Spanish, Mandarin, or Cantonese (the latter 2 in California only) to collect information on demographic characteristics, general health status and medications, symptoms of illness, food exposures, and potential social and environmental risk factors. Extensive information was collected on exposures including water source, formula types, various foods and manner of preparation, previous antibiotic use, and animal exposures. Subject caregivers were interviewed regarding exposures in the 5 days preceding onset of illness. Control caregivers were interviewed regarding the 5 days before interview. Because of the time lag in the availability of birth registries, information for controls with a target age of 0 to 2 months was gathered for a 5-day period preceding a specified date within the first 2 months of age.
Data were entered into an electronic database at each participating site. Analyses were performed by using Epi Info 3.3.2 (Centers for Disease Control and Prevention, Atlanta, GA) and SAS 9.1 (SAS Institute, Inc, Cary, NC). Unconditional logistic regression models were adjusted for age of the case patient and education of the caregiver. Variables included in the model were those hypothesized a priori as potential risk factors and those that were significant on univariate analysis.
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RESULTS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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During the study period, 7194 cases of non-Typhi Salmonella infection were ascertained in the surveillance population, of which 677 (9.4%) occurred in infants. Of the infant cases, 15 (2.2%) were not eligible for inclusion because they were associated with recognized outbreaks or were identified in chronic carriers (Fig 2). Of the 10 outbreak cases, 5 were associated with infant chick exposure, 1 with reptiles, 1 with honeydew melons, and 3 with day care centers. No subjects were excluded because of being asymptomatic. Of the eligible subjects, 442 (67%) were enrolled. Among the 217 nonenrolled subjects, the most common reasons included being unable to contact the family (61%), refusal (19%), and not speaking a study language (10%). Nonenrolled subjects did not differ significantly from enrolled subjects with respect to age, gender, month of illness, type of specimen from which Salmonella was isolated, or outcome (data not shown). A total of 928 controls were enrolled in the study (Table 1). Of those enrolled, 28 (6%) subject and 14 (2%) control interviews were performed in Spanish, with 6 (1%) subject and 2 (0.2%) control interviews completed in Cantonese.
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Diarrhea and fever were commonly identified symptoms among infants with salmonellosis (Table 2). The median duration of diarrhea was 7 days (range: 1–31 days). Half of the case patients were treated with antibiotics, 30% received intravenous hydration, and one quarter were hospitalized for a median of 3 days (range: 1–38 days). Fatal infections were reported in 2 (0.5%) case patients. Among case patients, 405 (92%) had Salmonella isolated from stool specimens, 32 (7%) from blood, 1 (0.2%) from urine, 1 (0.2%) from cerebrospinal fluid, and 3 from an unknown site. Infant illness was associated with a substantial burden on families, resulting in a median of 3 days (range: 0–21 days) of parental or guardian work absence; 21% of households reported another person with diarrhea within 10 days after the infants' illness.
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In multivariable regression analysis, case infants were significantly more likely than controls to have traveled outside the United States (odds ratio [OR]: 8.9; 95% confidence interval [CI]: 2.6–31.0), to have attended day care with a child with diarrhea (OR: 4.4; 95% CI: 1.8–10.7), to have ridden in a shopping cart next to meat or poultry (OR: 3.2; 95% CI: 2.1–5.1), or to have had exposure to reptiles (OR: 5.2; 95% CI: 3.4–7.9). The reptiles to which case infants were most commonly exposed included iguanas (25), lizards (25), snakes (20), and turtles or tortoises (14). Infection was also associated with consumption of meat and concentrated liquid infant formula during the 5-day exposure period (Table 3). Salmonellosis was not associated with consumption of ready-to-drink liquid formula or powdered infant formula (data not shown). Breastfeeding was protective; case patients were less likely to have been breastfed during the 5-day exposure period than controls (OR: 0.5; 95% CI: 0.3–0.6). Infant mobility (crawling or walking) and preparation of raw meats within the home in the previous 5 days were also associated with a lower risk of illness.
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Logistic regression models controlled for infant age by month and parental education status. Additional analyses controlling for insurance status and family income did not significantly change the results. Exclusion of data from the New York site (the only site which temporarily used birth announcements to identify controls) did not affect any results significantly.
To better understand potential risk factors and their associated population-attributable fraction, the multivariable regression analysis was repeated with cases and controls categorized by age into 3 groups: <3, 3 to 6, and >6 months of age (Table 3). Previous antacid and antibiotic use were included in the age-specific models but not in the overall model because of complex interactions of this variable with age. Illness was associated with reptile exposure and riding in a shopping cart next to meat or poultry in all age groups. Recent antacid use was a significant risk factor in infants <3 months of age. Illness was associated with travel outside the United States in infants 
3 months of age. Attending day care with a child with diarrhea was associated with illness among infants >6 months of age, and recent antibiotic use was associated with decreased risk in infants in this group. Illness was associated with consumption of concentrated infant formula in infants 3 to 6 months of age and was inversely associated with breastfeeding among those 
6 months of age. No additional risk factors were identified among the subsets of enrollees speaking Spanish, Mandarin, or Cantonese when analyzed separately.
Among case patients, the most common Salmonella serotypes included Salmonella typhimurium (20%), Salmonella newport (9%), Salmonella heidelberg (6%), Salmonella enteritidis (5%), and Salmonella montevideo (3%). These proportions are similar to the distribution of serotypes within FoodNet among case patients 1 year of age during the same period, except that in the older population, S enteritidis accounts for 15% of cases. The results of multivariable regression analyses restricted to cases with the most common specific serotypes are shown in Table 4. Analyses of less common serotypes could not be performed because of low numbers.
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DISCUSSION |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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Laboratory-confirmed salmonellosis in infants is associated with a number of potentially modifiable risk factors. Not unexpectedly, potential sources in this population are remarkably different from those identified among older persons, primarily because of their substantially different dietary and environmental exposures. Consistent with other studies of Salmonella and many other enteric pathogens in the general population, illness among infants was significantly associated with international travel, but this exposure accounts for only a small proportion (3%) of cases in this population.
Breastfeeding was protective against salmonellosis among infants, particularly infants who were 6 months of age and younger, in whom other dietary exposures are limited and breastfeeding is more common. Other studies have also demonstrated this protective effect,16,18,22 and this finding is consistent with the large body of data suggesting that breastfeeding decreases the risk of a large array of diseases in infants.21,23 In our study, salmonellosis was associated with consumption of concentrated liquid infant formula in the 5-day exposure period, even when controlling for breastfeeding. Among infants <3 months of age, this was the second most important risk factor for disease (population attributable fraction: 15.1). In contrast, salmonellosis was not associated with consumption of ready-to-drink liquid infant formula or powdered infant formula. Powdered infant formula is not a sterile product and has been associated with outbreaks of Salmonella and other pathogens.7,24,25 Concentrated liquid formula is sterile, but added water and manipulation of the food during preparation are potential sources of contamination. However, illness was not associated independently with consumption of water from various sources or with powdered formula, to which water is also added. Details of formula preparation were not examined in this study, although it is possible that differences in storage and handling of opened cans of concentrated formula may be associated with illness. Additional studies may further elucidate the specific risks associated with concentrated formula. Of note, salmonellosis was not associated with consumption of iron-containing infant formula, in contrast to the results of a previous study.16
Illness in all infant age groups was associated with infants riding in a shopping cart with meat or poultry placed next to them, with a population-attributable fraction of 11%. To our knowledge, no previous studies have examined this risk factor specifically. A recent study from the United Kingdom demonstrated substantial levels of contamination with pathogens on the outside of packaged meats and poultry.26 Our findings suggest that attention should be directed at better understanding and preventing this potential route of infection. This commonly reported exposure might be addressed with nonleaking packaging and separation of infants from high-risk foods in the shopping cart. Mobility might also be expected to lead to the potential for more exposure to environmental contamination. Although we found that illness among 3 to 6 month olds was inversely associated with increased mobility of the infant (crawling or walking), few patients in this age group are mobile. Illness was associated with environmental exposure in studies in Guam, where Salmonella contamination in the environment may be more common.17 Environmental contamination may be less likely in the United States in the absence of exposures to reptiles, farm animals, or other identifiable animal sources. Although previous studies of infant salmonellosis have included culturing of specimens from the household environment,27 which can provide additional information about potential mechanisms of transmission, this was not performed in this study.
The inverse association of illness with recent preparation of meat or poultry in the home (independent of consumption of meat or poultry by the infant) was also unexpected. An inverse association between illness and diet diversity was noted in a study of sporadic S enteriditis disease in the general population,28 and it is possible that our finding is somehow correlated with dietary diversity in the family in a manner we could not identify further. Ongoing work in FoodNet is directed at better understanding the potential implications of dietary diversity on foodborne illness in all populations.29
Salmonella infection in infants is clearly a substantial burden to the patients and their affected families. Routine treatment of Salmonella infection with antimicrobial agents in low-risk populations is not recommended, although infants may be at increased risk for severe disease compared with older persons.3,4 It is interesting, therefore, that the proportion of infants in this study receiving antibiotics was less than the proportion of case patients 1 year of age who took antibiotics for S newport infections (67%) or S enteritidis infections (70%) in recent studies in FoodNet sites.30 Attention should be devoted to better understanding determinants of antimicrobial use and encouraging adherence to national guidelines for diagnosis and treatment of bacterial gastroenteritis.31 Subsequent diarrhea was reported in other household members in more than one fifth of our cases. Although these illnesses were not confirmed to be salmonellosis, this rate is substantially higher than the rate of diarrhea in the general population,32 suggesting that intrafamilial spread after infant illness may be common.33 Likewise, 13% of infant case patients with Salmonella had illness onset within 5 days after diarrhea in another household member, suggesting that person-to-person spread may be an important source of infant infection. Unfortunately, data on diarrhea in household members was not collected for controls, so we were unable to quantify the magnitude of this risk. Furthermore, household members with diarrhea before or after the infant case were not cultured as part of this study, thus limiting conclusions that can be made about household transmission. Likewise, we did not have culture confirmation of illness among other day care attendees to assess person-to-person transmission in that setting.
That Salmonella infection in children is associated with reptile exposure was well documented in several previous studies,34,35 although none have studied infants specifically. In this study, reptile exposure had the highest population-attributable fraction of any of the risk factors identified: 17% for all infants. Although it is possible that some older infants could have had direct contact with reptiles within their homes, it is more likely that most infants were infected indirectly either through contact with the reptile-contaminated environment or via contaminated hands of caretakers. The Centers for Disease Control and Prevention has recommended that households with children <5 years of age should not own reptiles.34
In the general population, a wide variety of potential sources of Salmonella infection have been identified, with substantial variation among serotypes. Most of these potential sources involve consumption of specific food items. Because we suspected that foodborne transmission is less commonly a factor in infants than it is in older populations, we analyzed data for all serotypes combined. As expected, the primary risk factors identified were associated with environmental exposures and not with specific food products. Analysis of potential sources associated with specific Salmonella serotypes was limited somewhat by low numbers of cases, particularly for less common serotypes. Because the serotype-specific analyses involved multiple comparisons without adjustment for multiple testing, the associated uncertainties may be underrepresented. Despite this, the findings are consistent with our initial assumptions. For example, Salmonella infection in infants was not associated with consumption of eggs and poultry, which are established sources of S enteriditis in older populations; however, S enteriditis infection in infants was associated with exposure to meat and poultry in shopping carts.
Subjects and controls differed with regard to race, caregiver educational status, medical insurance coverage, and household income, each of which may correlate with socioeconomic status. We included caregiver educational status in the final model as a proxy for socioeconomic status. Inclusion of additional factors such as income and insurance status led to loss of data (because of missing information) and did not change results significantly. Additional understanding of the risk factors associated with sociodemographic status will be an important part of further controlling this disease among infants.
To our knowledge, this is the largest reported population-based case-control study of infant salmonellosis. In contrast to older populations with diverse dietary exposures, potential sources among infants reflect their more limited diets and the relatively greater contribution of environmental exposures to disease transmission. Nevertheless, contamination of the environment can occur, in part, through sources of Salmonella (such as poultry and reptiles) that are common among older populations. Many of the risk factors identified in this study are potentially modifiable through targeted preventive education and behavioral change among the caretakers of infants. Attention should be directed at developing practical and effective measures to prevent Salmonella infection in this high-risk population.
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FOOTNOTES |
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Accepted Jun 8, 2006.
Address correspondence to Timothy F. Jones, MD, Communicable and Environmental Disease Services, Tennessee Department of Health, 4th Floor, Cordell Hull Building, 425 5th Ave N, Nashville, TN 37247. E-mail: tim.f.jones{at}state.tn.us
The authors have indicated they have no financial relationships relevant to this article to disclose.
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PEDIATRICS (ISSN 1098-4275). ©2006 by the American Academy of Pediatrics
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