Salmonella Poisoning

Hello. I just recently got over a case of somewhat bad salmonella. We believe it came from a new crested gecko I received, because about a week to two weeks after I got him, I got what I thought was a severe stomache bug. Test results came back, and it's salmonella. I have a few questions; Do I need to do anything to the crested gecko? Could it transfer to my other snakes? Has anyone ever got this before?

We aren't positive it came from him, but I don't eat eggs, and meat rarely, and the doctor said a new reptile probably caused it. So thanks.

Well, it's probably much more likely you got it from food. I believe they can ID the salmonella to know for sure. It's found on fruits, veggies and lettuce, things like that, too.

You could have the gecko checked- but it's quite likely he _will_ have it. So the question is, and I don't know the answer, is it effectively treatable? I'll check in my parasite book...

No info there. I know I read a really good article last year when I was helping someone research test results. I think I need to be on a computer with access to academic articles, though. I'll look tomorrow.

Nanci said:

No info there. I know I read a really good article last year when I was helping someone research test results. I think I need to be on a computer with access to academic articles, though. I'll look tomorrow.

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Alright! Thanks a bunch! Personally, I don't think it came from him, I think it was on something I ate. The doctors said they thought it was from mayo, eggs, or a reptile, so they don't know for sure. Thank you though, I appreciate it!

Well, you have to assume any reptile has it, and take appropriate protective measures, for yourself. Wash your hands after handling reptiles. Don't put them in your mouth. That being said, I kiss on my snakes and lizards all the time, and I've never gotten salmonella.

Nanci said:

Well, you have to assume any reptile has it, and take appropriate protective measures, for yourself. Wash your hands after handling reptiles. Don't put them in your mouth. That being said, I kiss on my snakes and lizards all the time, and I've never gotten salmonella.

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Oh, I know. And I do assume that with all my reptiles, that they possibly have it. I use hand sanitizer before and then after handling I wash my hands EVERY time. I think everybody has kissed their reptiles at least once, but now I am going to be more careful.

I still think it's way, way more likely that you got it from food.

Nanci said:

I still think it's way, way more likely that you got it from food.

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I 100% agree with you. By the way, thank you for answering my questions. But also ; Does it harm the reptile? Will it get transferred to my snakes? Should I worry?

I just mean if he does have it.

I have also read that tests can be performed to determine whether you and the reptile have the same strain or not. But they may be expensive - I don't know. It would be nice to know for sure, if it is affordable to find out.

Most reptiles are pretty resistant to showing symptoms - they seem to live with it pretty well, unless their immune system is compromised. Actually, healthy people seem to shrug it off most of the time, too, unless they either ingest A LOT at one time and become overwhelmed, or unless their immune system is compromised. But I understand that some strains are more virulent than others. If you are susceptible to infections for one reason or another, you may have to take more care than most. You might want to consider building up your immune system through diet and supplements, if it is low. Your doctor should be able to give you more info, although a holistic type doctor is more likely to be helpful than the usual docs.

Salmonella is actually present in all reptiles- they are immune to it and it may even serve some purpose in their digestive systems... the truth is that we just don't know what's its' function save for the fact that it is present in ALL reptiles.

If you practice minimal hygiene, there's simply no reason for you to contract Salmonella... since it passes orally and the only points of contraction are either poo or cloaca... and those need to come in contact with your mouth...

Disturbing mental images asidelaugh, the point was that it is quite unlikely.

I have also read that tests can be performed to determine whether you and the reptile have the same strain or not.

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Yep, this is the case. The reptile-specific strain can be distinguished from others.

However, testing is expensive and if found not to be reptile-based, can cause public health scares. For this reason, the medical community tends to seize on the reptile aspect without the appropriate testing to prove or disprove it.

Intensively produced eggs and poultry are a more likely source here in the UK, so I'd be more inclined towards those as the cause.

Basic hand washing after handling will ensure that no harm comes from your reptile.

Reptiles, Amphibians, and Human Salmonella Infection: A Population-Based, Case-Control Study

Jonathan Mermin1,
Lori Hutwagner1,
Duc Vugia3,
Sue Shallow4,
Pamela Daily4,
Jeffrey Bender5,
Jane Koehler2,
Ruthanne Marcus6,
Frederick J. Angulo1, and
for the Emerging Infections Program FoodNet Working Groupa

+ Author Affiliations

1Centers for Disease Control and Prevention, Atlanta
2Georgia Department of Human Resources, Atlanta
3California Department of Health Services, Berkeley
4California Emerging Infections Program, San Francisco and Oakland
5Minnesota Department of Health, Minneapolis
6Connecticut Emerging Infections Program, New Haven

+ Author Notes

↵Working group members are listed at the end of the text.

Reprints or correspondence: Dr. Frederick J. Angulo, Centers for Disease Control and Prevention, MS-D63, 1600 Clifton Rd., Atlanta, GA 30333 ([email protected]).


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Abstract

To estimate the burden of reptile- and amphibian-associated Salmonella infections, we conducted 2 case-control studies of human salmonellosis occurring during 1996–1997. The studies took place at 5 Foodborne Diseases Active Surveillance Network (FoodNet) surveillance areas: all of Minnesota and Oregon and selected counties in California, Connecticut, and Georgia. The first study included 463 patients with serogroup B or D Salmonella infection and 7618 population-based controls. The second study involved 38 patients with non-serogroup B or D Salmonella infection and 1429 controls from California only. Patients and controls were interviewed about contact with reptiles and amphibians. Reptile and amphibian contact was associated both with infection with serogroup B or D Salmonella (multivariable odds ratio [OR], 1.6; 95% confidence interval [CI], 1.1–2.2; P < .009) and with infection with non-serogroup B or D Salmonella (OR, 4.2; CI, 1.8–9.7; P < .001). The population attributable fraction for reptile or amphibian contact was 6% for all sporadic Salmonella infections and 11% among persons <21 years old. These data suggest that reptile and amphibian exposure is associated with ∼74,000 Salmonella infections annually in the United States.

Approximately 1.4 million human Salmonella infections and an estimated 600 associated deaths occur each year in the United States [1]. Although infection with nontyphoidal Salmonella usually causes self-limited diarrheal illness, serious sequelae, including meningitis, sepsis, and death may occur, especially among infants, elderly persons, and immunocompromised persons [2–5]. Most infections are caused by the consumption of contaminated meat, poultry, or eggs [6, 7]. However, investigations of outbreaks [8, 9] and sporadic infections [10–12] have revealed cases of salmonellosis that occurred after direct or indirect contact with reptiles. Reptile-associated Salmonella infections are more likely to be associated with invasive disease [13], more commonly lead to hospitalization [14], and more frequently involve infants [15] than do other Salmonella infections.

Salmonellae are divided into 60 serogroups and >2300 serotypes [16]. Except for characterizing clinical aspects of a few serotypes, such as Salmonella enterica serotype Typhi, serogrouping and serotyping are mainly used as public health tools to recognize outbreaks and identify and control sources of infection. Salmonellae from serogroups B and D account for approximately two-thirds of all reported Salmonella infections and include the 2 most common serotypes, S. enterica serotype Enteritidis and S. enterica serotype Typhimurium, which together cause approximately one-half of all human infections in the United States.

Salmonellae are naturally found in the gastrointestinal tract of reptiles (e.g., lizards, snakes, and turtles) and amphibians (e.g., frogs and newts) [17–27]. Of all Salmonella serotypes, 40% have been cultured predominantly from reptiles and are rarely found in other animals or humans. Human infections with these serotypes frequently indicate a reptile source [14]. However, <1% of human Salmonella infections are caused by these “reptile-associated” serotypes [13]. Neither the extent to which reptiles are also the source of human Salmonella infections by more common serotypes nor the possibility that amphibians as well as reptiles can cause human salmonellosis have been examined. We therefore conducted 2 population-based, case-control studies of nontyphoidal Salmonella infection in the United States to investigate whether reptiles and amphibians spread serotypes commonly found in human infections (serogroup B or D Salmonella) as well as less common serotypes (non-serogroup B or D Salmonella that include “reptile-associated” serotypes). We used data collected in these studies to estimate the burden of reptile- and amphibian-associated salmonellosis in the United States.
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Methods

The Foodborne Diseases Active Surveillance Network (FoodNet). FoodNet is a collaborative effort among the Centers for Disease Control and Prevention (CDC), selected state health departments, the US Department of Agriculture, and the US Food and Drug Administration [28]. FoodNet conducts active, population-based surveillance for laboratory-confirmed illnesses caused by infection with primarily foodborne pathogens. For that surveillance, public health officials regularly contact all microbiology laboratories that test stool samples in selected sites in the country. For this study, we reviewed data from laboratories throughout Minnesota and Oregon and in specific counties in California (San Francisco and Alameda), Connecticut (Hartford and New Haven), and Georgia (Cobb, Clayton, Douglas, Dekalb, Fulton, Gwinnett, Rockdale, and Newton). All 263 laboratories that were identified as serving the catchment areas participated in the study, covering an estimated population of 14,281,096 (5.4% of the estimated US population in 1996) [29].

Case selection. From 1 May 1996 through 30 April 1997, for California, Connecticut, and Minnesota, and from 1 August 1996 through 31 July 1997, for Georgia and Oregon, we identified all patients with culture-confirmed Salmonella infection. Patients infected with nontyphoidal serogroup B or D Salmonella were eligible for the main case-control study if they resided in participating catchment areas, had culture-confirmed illness, reported having diarrhea (defined as ⩾3 loose stools in a 24-h period), could remember the date of onset for their diarrhea, had diarrhea onset ⩽10 days before their stool sample was collected, spoke English, and were reachable in <16 telephone attempts. Patients were excluded if their infection had been associated with an outbreak for which a vehicle had been clearly identified by the local or state health department or if the onset of their illness was ⩽28 days after the onset of another culture-confirmed case in the same household. In Minnesota, 1 of every 2 patients with salmonellosis was considered to be potentially eligible. Within 21 days of specimen collection, we administered a standardized questionnaire to patients concerning their demographic data, the clinical course of their illness, preexisting illnesses, diet, travel history, and contact with reptiles or amphibians during the 5 days before illness onset. If the patient was <12 years of age, the questionnaire was administered to an adult member of the household. Permission from a parent or guardian was obtained prior to speaking with a case or control patient 12–18 years of age. We obtained informed consent from participants and conducted research in accordance with guidelines for human experimentation as specified by the US Department of Health and Human Services.

Patients with Salmonella infection due to serogroups other than B or D in the California site (Alameda and San Francisco counties) were contacted by telephone and administered the same 4 questions regarding reptile and amphibian exposure included in the questionnaire administered to patients with group B or D Salmonella infection. The 4 questions were as follow: (1) “In the five days before illness onset, were there any reptiles (such as snakes, turtles, iguanas, or other lizards) or any amphibians (such as frogs or salamanders) in your house?” (2) If so, “What types of reptiles or amphibians?” (3) “Did you visit a place (such as a school, pet store, or another home) where there was a reptile?” (4) “In those five days, did you touch a reptile?”

Control selection. We obtained population-based controls from the 5 sites by random-digit dialing using a sample design that results in more frequent calls to telephone bank strata with a higher probability of contacting a residential household [30]. During analysis, we accounted for differential probabilities of selection by adjusting for population characteristics of different strata. Our goal was to enroll 150 persons per month in each site. This selection method allowed us to enroll a representative selection of households in the FoodNet surveillance areas (also known as “FoodNet sites”), as well as to reliably estimate the incidence of diarrhea, associated health care-seeking practices, and population food-consumption patterns—additional interests of the study committee. We excluded non-English-speaking persons and respondents who reported having diarrhea within the 4 weeks before the interview.

Data analysis. We entered data into a computer using EpiInfo computer software, version 6.02 (CDC). We weighted data for controls using 1995 intercensal population estimates (SUDAAN, version 7.0) by their probability of selection based on household size and age- and sex-distributions within each FoodNet site. We then performed univariate and logistic regression analysis using SAS computer software, version 6.12 (SAS Institute). All risk factors associated with serogroup B or D Salmonella infection (P < .05) in univariate analysis were available for inclusion in a multivariable model. For analyses involving non-serogroup B or D Salmonella infections, only information on patients' age and sex was available and included in the multivariable model. Risks measured by multiple variables (e.g., reptile exposure in the home and touching a reptile) and those associated with exposure to specific types of reptiles were entered into separate multivariable models to avoid multicollinearity. To select variables for the final logistic regression model, we used a forward regression strategy, and to assess potential collinearity among covariates in the regression models, we used a matrix of Kendal's Tau correlation coefficients. Interaction was assessed by comparing -2 log likelihood values for the reduced and full models.

We calculated the population attributable fraction (PAF) for risk factors using adjusted ORs and the proportion of cases exposed to the risk factor [31]. Ninety-five percent CIs were computed for model-adjusted exposure-specific attributable fractions using variance estimators described by Greenland [32]. To assess the robustness of PAF estimates, we calculated the PAF for reptile and amphibian contact using a variety of models including and excluding demographic variables and risk factors known to be associated with Salmonella infection from outbreaks. These risk factors included age, sex, income, season, international travel, chronic illness, and consumption of eggs, poultry, meat, alfalfa sprouts, tomatoes, cantaloupe, and apple cider. Estimates of the annual number and percentage of reptile- and amphibian-associated cases were adjusted for the exclusion of outbreak-associated cases by subtracting the proportion of all reported cases associated with outbreaks from the estimated number of annual Salmonella infections and conservatively assuming that reptiles and amphibians were associated with no outbreaks. All P are 2-tailed.
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Results

Active surveillance. During the study period, 2157 cases of salmonellosis were ascertained. Serogrouping was performed on isolates from 2056 infected persons (93%); 1465 (73%) of these isolates were serogroup B or D. The incidence of culture-confirmed group B or D Salmonella infection in the FoodNet catchment area was 9.5 cases per 100,000 persons and varied by state, ranging from 7.2 cases per 100,000 persons in Oregon to 13.9 cases per 100,000 persons in Connecticut. Of the 1446 patients (98.7%) whose treatment information was available, 325 (22%) were hospitalized; of the 1416 (97%) with mortality data, 10 (0.7%) died. Omitting patients excluded by the selection algorithm in Minnesota, we found that 1226 patients were potential case subjects for the study.

Case-control study. Of these potential case subjects, 687 (56%) were interviewed. The primary reasons for not being interviewed were not being reachable by telephone (32%), not being interviewed ⩽21 days from sample collection (26%), and being part of an outbreak (7%). Of the 687 patients who were interviewed, 463 (67%) were included in the study. The primary reasons for the 224 interviewed patients not meeting inclusion criteria were that 90 (40%) reported no diarrhea or did not remember the date of onset of diarrhea, 58 (26%) reported the onset of diarrhea >10 days before a stool sample was obtained, and 63 (28%) lived in a household with another person with a culture-confirmed case of Salmonella infection. Only 21 eligible patients (3%) who were contacted refused to participate. There were 7618 controls included in the study.

Using univariate analysis, we found that persons with Salmonella infection were more likely than controls to report having a reptile or amphibian in their home (7% vs. 4%; OR, 2.1; 95% CI, 1.5–3.0) or touching a reptile (5% vs. 3%; OR, 1.7; 95% CI, 1.1–2.5) (table 1). Salmonella infection was specifically associated with having a snake, non-iguana lizard, or amphibian in the home, but not with having a turtle or iguana. Illness was associated with “any reptile or amphibian contact,” a combination variable of having a reptile or amphibian in the home or touching a reptile (9% vs. 5%; OR, 1.8; 95% CI, 1.3–2.5). Serogroup B or D Salmonella infection was also associated with international travel, having a chronic illness, eating pink hamburger in a restaurant, and eating eggs in a restaurant.
Table 1
Table 1

Association between serogroup B or D Salmonella infection and potential risk factors.

Using multivariable analysis, we found that patients with serogroup B or D Salmonella infection were significantly more likely than controls to be younger, to be female, and to report a household income of ⩽$15,000 per year. Reptile or amphibian contact remained significantly associated with infection, with a PAF of 3%. Age was an effect modifier of the association between Salmonella infection and reptile or amphibian contact; the association was strongest for persons under the age of 21 years (OR, 2.4; 95% CI, 1.6–3.5). The association was significant and of similar magnitude for persons <11 years old and those 11–20 years old. Illness among all persons < 21 years old was associated specifically with having a snake, non-iguana lizard, or amphibian in the home (table 2). The PAF for reptile or amphibian contact in this age group was 9.5% (95% CI, 6.2%–12%), the highest for any risk factor associated with illness (the next highest being 8% for having a chronic illness, 7% for eating eggs in a restaurant, and 5% for international travel).
Table 2
Table 2

Multivariable analysis of association between serogroup B or D Salmonella infection and potential risk factors among persons aged <21 years.

Reptile or amphibian contact was associated with infection even when we restricted our analysis to patients infected with S. Enteritidis and S. Typhimurium (OR, 1.5; 95% CI, 1.0–2.3). However, this association was not statistically significant on multivariable analysis (OR, 1.4; 95% CI, 0.9–2.0).

Infection with non-serogroup B or D Salmonella. One hundred forty-one cases of non-serogroup B or D Salmonella infection were reported from the San Francisco Bay area. Fifty-three (38%) of these infections were associated with an outbreak of S. enterica serotype Montevideo and S. enterica serotype Meleagridis infections caused by the consumption of contaminated alfalfa sprouts. Answers to survey questions by 38 (43%) of the remaining cases and 1429 controls indicated that persons with non-serogroup B or D Salmonella infection more frequently reported reptile or amphibian contact than controls did (20% vs. 4%; OR, 4.2 [95% CI, 1.8–9.7]; PAF, 15.2% [95% CI, 8.8%–17.9%]) (table 3). In addition, illness was independently associated with having an amphibian, iguana, or non-iguana lizard in the home. For patients <21 years old, the PAF for reptile or amphibian contact was 23%.
Table 3
Table 3

Association between non–serogroup B or D Salmonella infection and potential risk factors among infected persons from the San Francisco Bay area.

Annual incidence of reptile- and amphibian-associated cases. Data from FoodNet indicate that an estimated 1.41 million cases of Salmonella infection occurred in the United States during the 1-year study period [1]. This is comparable with estimates made in 1987 of between 800,000 and 3.7 million annual Salmonella infections [33]. Serogroup B and serogroup D Salmonella constituted 72% of the Salmonella infections reported to FoodNet. The PAF for reptile or amphibian exposure among cases with serogroup B or D Salmonella infection was 3%, and that for those with non-serogroup B or D Salmonella infection was 15%; for patients <21 years old, the PAFs for reptile and amphibian contact were 9.5% and 23%, respectively. Assuming site homogeneity, we combined these estimates based on the proportion of Salmonella infections that was serogroup B or D and the proportion that was non-serogroup B or D in FoodNet sites. Our analysis of these combined estimates again indicated that reptile and amphibian contact was associated with 6% of all sporadic Salmonella infections and 11% of sporadic Salmonella infections among persons <21 years of age. Of all Salmonella infections in the study, 88% were not associated with known outbreaks, suggesting that ∼74,000 Salmonella infections (6% of 1.24 million non-outbreak-associated cases) may be associated with reptile and amphibian exposure in the United States annually.
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Discussion

During the 1996–1997 study period, we estimated that 74,000 Salmonella infections in the United States were associated with reptile or amphibian contact. Salmonella infection was independently associated with both touching a reptile and having a reptile or amphibian in the home. Previous reports have shown that direct reptile contact is not necessary for transmission of Salmonella; in one case series of infections with an iguana-associated serotype, only 14% of cases had direct reptile contact [15]. Other reports have also described infection from indirect contact such as visiting a babysitter who owned iguanas, cleaning an iguana's cage, sucking on pebbles from a turtle's aquarium, sharing a hospital room with a patient whose mother owned a monitor lizard, and being handled by a parent who owned black rat snakes [9, 10, 34–36].

The exact means of transmission for Salmonella may vary for different types of reptiles and amphibians. Lizards are frequently allowed to roam around the house, potentially contaminating objects such as rugs, table-tops, and furniture that are later touched by residents or have food prepared upon them. Salmonella survives well in the environment; it has been isolated from dried reptile stool in cages 6 months after removal of the reptile [37] and from aquarium water 6 weeks after removal of a turtle [34]. This survivability allows Salmonella to be transmitted by environmental surfaces well after a reptile has been returned to its cage. Although snakes are unlikely to be let free in the home, they are frequently handled, potentially contaminating the hands, arm, and neck of owners. Caregivers who have touched reptiles have accidentally infected infants by allowing them to suck on the caregivers' fingers [38]. Turtles and amphibians are kept in aquariums that contain water that can become contaminated with Salmonella and allow for growth of the organism [25, 27, 36, 39], creating enhanced opportunities for transmission. Because of the risk for indirect transmission, the CDC has developed guidelines for preventing reptile-associated salmonellosis that include recommendations to keep reptiles out of households containing young children or persons with weak immune systems and to not allow reptiles to roam freely throughout the house [15, 37, 40, 41]. We have adapted these guidelines to include amphibians (table 4).
Table 4
Table 4

Recommendations for preventing transmission of Salmonella from reptiles and amphibians to humans.

Reptiles and amphibians have long been known to harbor Salmonella [17, 42, 43] and to cause human infection [44]. They are asymptomatic carriers of Salmonella, and reported carriage rates from point prevalence studies have been as high as 94% [45]. It is possible that all reptiles and amphibians carry Salmonella, and that reports of <100% carriage involve intermittent shedding and variations in the sensitivity of culturing techniques. In a small study during which iguanas were repeatedly cultured for Salmonella, every iguana was found to carry the organism [46]. The high rate of colonization suggests that Salmonella may be a natural commensal organism in the gastrointestinal tract of these animals.

From the forest, field, or pond to the home, the lives of reptiles and amphibians provide them several opportunities to become infected with Salmonella. Reptiles and amphibians might initially be infected before birth while in the ovary, oviduct, or cloaca, as has been reported for turtles [26, 47, 48]. In the wild, the colonization of Salmonella in iguanas and toads may be related to the eating of feces, which typically contaminates food and water; insects, soil, and pond water have all been shown to carry Salmonella [47, 49]. In the home, reptiles and amphibians might acquire Salmonella from being fed undercooked chicken or meat or by contact with household dust, all of which have the potential to contain Salmonella [50, 51]. Attempts to permanently rid reptiles of Salmonella infection by antibiotic treatment have been unsuccessful, suggesting that the animals readily become reinfected from their environment or sequester the infection [52, 53].

In the early 1970s, pet turtles were responsible for an estimated 18% of salmonellosis among children from 1–9 years old [54, 55]. This led first to the institution of multiple local and state restrictions on the sale of turtles and then in 1975 to a federal ban on all shipments of pet turtles with a shell length <10 cm [54]. These actions resulted in a 77% reduction in the incidence of infection with “turtle-associated” Salmonella serotypes among children aged 1–9 years and a near-elimination of turtle-associated salmonellosis [54]. However, recent reports have indicated that the number of cases of reptile-associated salmonellosis has been increasing [13]. Unlike the 1970s, when turtle-associated salmonellosis especially affected young children [54, 56], information from our control population indicates that pet reptiles and amphibians are currently popular with children of all ages and young adults. With an estimated PAF of 11% among persons <21 years old, the current problem of reptile- and amphibian-associated salmonellosis is comparable with the problem of turtle-associated salmonellosis 3 decades ago.

Our larger study was designed to detect whether reptile and amphibian contact was associated with serogroup B or D salmonellosis—serotypes that are frequently associated with consumption of contaminated food. Surprisingly, among persons <21 years of age, reptile and amphibian exposure had the largest PAF for infection of any of the risk factors we assessed, including those typically thought to be the cause of salmonellosis, such as eating eggs in a restaurant and travel outside the United States. In addition, the suggestion of an association between reptile and amphibian contact and infection with S. Typhimurium and S. Enteritidis is interesting, because cultures of samples from reptiles have yielded both serotypes [8, 56], and cases of S. Typhimurium infection associated with pet snakes have recently been reported [40].

Campaigns to reduce people's risk for salmonellosis should include efforts to prevent reptile- and amphibian-associated infections, especially among persons who are considering purchasing a reptile or amphibian, those who already own one, and families who have young children. Potential venues for education might include pet stores, physician and veterinarian offices, and schools. Educational efforts to prevent turtle-associated infections did not work well in the 1970s, perhaps because of the widespread distribution of turtles: an estimated 15 million turtles were sold or given away each year in the United States, and many turtles were obtained through sources other than pet stores [56]. Currently, most of reptiles are obtained from pet stores (CDC, unpublished data), allowing for more-focused educational campaigns. In collaboration with the Pet Industry Joint Advisory Council, the CDC has developed educational posters for pet stores, and in 1999, the Council for State and Territorial Epidemiologists issued a statement that recommended pet stores be required to educate customers about the prevention of reptile-associated salmonellosis. However, if current approaches are not successful, legal restrictions on the importation or sale of reptiles and amphibians would be warranted, as was the case prior to successful governmental restrictions on turtles in the 1970s.

This study only included cases of salmonellosis that were not associated with a known outbreak. Foodborne outbreaks of salmonellosis can be extremely large; for example, an outbreak of ice cream–related S. Enteritidis infections in 1994 involved an estimated 220,000 people [57]. If reptiles and amphibians were less likely than contaminated food and water to cause large outbreaks of disease, we may have overestimated the PAF associated with these pets. However, outbreaks caused by reptile-associated infections have also been reported; for example, an outbreak of S. enterica serotype Weltevreden infections was caused by geckos in a water tank in Hawaii [58]; an outbreak of S. Enteritidis infections occurred among visitors to a zoo reptile exhibit [8]; and an outbreak of S. enterica serotype Poona infections was associated with eating cake at a birthday party held at a house with 2 iguanas [9]. In addition, we excluded only 3% of all serogroup B or D Salmonella infections because they were associated with an outbreak. In our study of non-serogroup B or D infections, we excluded 38% of such infections because they were associated with a single outbreak in the San Francisco Bay area. In estimating the annual number of reptile- and amphibian-associated cases, we conservatively assumed that nationally the same percentage of non-serogoup B or D Salmonella cases were associated with an outbreak (and not caused by reptile or amphibian exposure), and, thus, we may have underestimated the total number of infections associated with reptile or amphibian contact.

Although we administered the questionnaire to patients within 21 days of specimen collection to minimize recall bias, respondents may have been more likely to remember some exposures, such as international travel or having contact with a reptile or amphibian, than they were to remember recently consumed food items. If this were the case, then we might have overestimated the PAF for some of these factors. In addition, fewer than one-half of all reported cases of salmonellosis in FoodNet sites participated in these studies. The major reasons for exclusion were our contacting cases >21 days after their sample collection, our inability to reach patients by telephone, and respondents not having diarrhea or not remembering the date of diarrhea onset. Although these exclusion criteria were necessary components of the studies, they may limit the generalizability of the results.

We excluded nonindex cases from the case-control study. It is unlikely that foodborne Salmonella infections would cause more secondary infections than reptile-or amphibian-associated infections, because the shedding of nontyphoidal Salmonella in a person's stool is likely to be similar across serotypes and modes of infection. Food contamination could potentially cause more nonindex cases than reptile or amphibian sources if multiple persons in a single home were exposed to the same food. This would result in an overestimation of the proportion of all infections associated with reptile and amphibian contact. However, multiple infections associated with reptile contact in the same household are also frequently reported [37, 56].

In our case-control study of non-serogroup B or D Salmonella infection, we did not collect case information other than the patients' age and sex, their Salmonella serotype, and their history of reptile and amphibian contact. The results might have changed if information were available on other potential risk factors for Salmonella infection. However, PAF estimates in the study of serogroup B or D Salmonella infection varied little when multiple potential risk factors were included in or excluded from the regression model. The study of non-serogroup B or D Salmonella was conducted in the San Francisco Bay area, only 1 of the 5 sites included in the larger study. The 3.3% rate of reptile exposure among controls in the San Francisco Bay area may not be representative of the other 4 sites, although it was the median value among them (range, 2.7%–5.6%). In addition, although the association between the risk of salmonellosis and having a reptile or amphibian in the home was statistically significant, the PAF of 15% was based on the exposure of only a few infected patients. Finally, the 13 million people living in the 5 FoodNet sites may not be representative of the nation, and reptile and amphibian exposure may be more or less important risk factors for salmonellosis in other parts of the country.
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Conclusions

This is the first study to show an association between sporadic infection with common Salmonella serotypes and reptile exposure. It is also the first to show that exposure to amphibians, which have previously been reported to carry Salmonella organisms, is also associated with human infection. Health care practitioners and public health officials should ask specifically about reptile and amphibian exposure among persons with salmonellosis and educate all patients and the general population about how to prevent the zoonotic spread of Salmonella from their pets. Our findings emphasize the need for improved prevention efforts without which thousands of preventable cases of reptile- and amphibian-associated salmonellosis may continue to occur annually in the United States.

This is the article I wanted to find but I can't find it except PDF and I can't copy and paste that.

I don't know if you have to be in an academic environment to view it.

This article is informative in terms of how many captive reptiles are infected and how it affects their health.

Salmonellosis and arizonosis in the reptile collection at the National Zoological Park.
Cambre RC, Green DE, Smith EE, Montali RJ, Bush M.
Abstract

The prevalence of Salmonella and Arizona organisms in the reptile collection at the National Zoological Park was investigated. Culture of specimens from 311 reptiles, while live or at necropsy, yielded yielded 117 positive results, for an overall infection rate of 37%. Snakes had the highest rate, 55% (69 of 125); lizards had an intermediate rate, 36% (46 of 129); and turtles and tortoises had the lowest rate, 3% (2 of 63). Twenty-four serotypes of Salmonella enteritidis, 1 of S choleraesuis, and 39 of Arizona hinshawii were represented. While clinical illness was never directly attributed to infection with these organisms, pure cultures of Salmonella and Arizona were recovered at necropsy from some reptiles with gross and/or histologic lesions in the gastrointestinal tract, liver, spleen, and blood vessels. However, numerous other concurrent diseases and management problems were often considered the immediate cause of death, with Salmonella and Arizona being ready and significant opportunistic pathogens contributing to the demise of the reptiles.

PMID:
7451315
[PubMed - indexed for MEDLINE]

The Changing Epidemiology of Salmonella: Trends in Serotypes Isolated from Humans in the United States, 1987–1997

Sonja J. Olsen1,2,
Richard Bishop3,
Frances W. Brenner1,
Thierry H. Roels1,
Nancy Bean3,
Robert V. Tauxe1 and
Laurence Slutsker1

+ Author Affiliations

1Foodborne and Diarrheal Diseases Branch, Division of Bacterial and Mycotic Diseases, National Center for Infectious Diseases,
2Epidemic Intelligence Service, Division of Applied Public Health Training, Epidemiology Program Office, and
3Biostatistics and Information Management Branch, Division of Bacterial and Mycotic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia

Reprints or correspondence: Dr. Sonja J. Olsen, Centers for Disease Control and Prevention, Foodborne and Diarrheal Diseases Branch, 1600 Clifton Rd., MS A-38, Atlanta, GA 30333 ([email protected])


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Abstract

Salmonellosis is a major cause of illness in the United States. To highlight recent trends, data for 1987–1997 from the National Salmonella Surveillance System were analyzed. A total of 441,863 Salmonella isolates were reported, with the highest age-specific rate among infants (159/100,000 infants at 2 months). Annual isolation rates decreased from 19 to 13/100,000 persons; however, trends varied by serotype. The isolation rate of Salmonella serotype Enteritidis increased until 1996, whereas declines were noted in Salmonella serotypes Hadar and Heidelberg. Overall, serotypes that increased in frequency were significantly more likely than those that decreased to be associated with reptiles (P=.008). Salmonella infections continue to be an important cause of illness, especially among infants. Recent declines in food-associated serotypes may reflect changes in the meat, poultry, and egg industries that preceded or anticipated the 1996 implementation of pathogen-reduction programs. Additional educational efforts are needed to control the emergence of reptile-associated salmonellosis

Salmonellosis is an important cause of diarrheal illness in humans, causing ∼1.4 million illnesses and 600 deaths annually in the United States [1]. Much of what is known about the epidemiology of salmonellosis comes from outbreak investigations. These investigations have determined that most human infections result from the ingestion of foods of animal origin that are contaminated with Salmonella species [2–5]. Other vehicles, including nonanimal foods, such as fresh fruits and vegetables [6], water [7], reptiles [8–13], and direct person-to-person transmission [14–16], also have been implicated. However, most Salmonella infections do not occur in recognized outbreaks, but rather as sporadic infections [17]

There are 2449 known serotypes of Salmonella [18]. Serotyping is a useful classification scheme that allows for trends in Salmonella surveillance data to be followed over time. For example, from the late 1800s to the mid-1900s, Salmonella serotype Typhi was the leading cause of Salmonella infection in the United States [19]. Improvements in sanitation nearly eliminated Salmonella Typhi infections, and in the 1950s, nontyphoidal Salmonella infections began to increase in importance. More recently, specific serotypes have been linked with certain foods or exposures. For example, outbreaks of Salmonella serotype Enteritidis have been repeatedly associated with raw or undercooked eggs [2, 3, 20–22], and Salmonella serotype Marina infection has been associated with exposure to reptiles [12, 23]

Surveillance for Salmonella species in the United States began in 1962 and is conducted jointly by the Council of State and Territorial Epidemiologists, the Association of Public Health Laboratories, and the Centers for Disease Control and Prevention (CDC). The objectives of the surveillance system are fourfold: to define endemic patterns of salmonellosis, to identify trends in disease transmission, to detect outbreaks, and to moni-tor control efforts. These surveillance data are periodically summarized and published; the last report reviewed data from 1984 through 1986 [24]. This report reviews the trends in Salmonella infections in the United States from 1987 through 1997
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Materials and Methods

Salmonella surveillance system.Salmonella surveillance is a passive, laboratory-based surveillance system conducted in all 50 states and the District of Columbia. Clinical laboratories are requested (and, in some states, required) to forward clinical isolates of Salmonella species to their state public health department laboratory for serotyping. The state health department completes a report that contains information on patient sex, age, race, and county and state of residence, as well as the specimen source, serotype, and date of collection. Because additional clinical or epidemiologic information is not included in the report, we do not know the proportion of isolates that are cultured from persons without gastrointestinal symptoms; however, we suspect that it is low, because only ∼10% of specimens are from sources other than stool samples. Reports are then sent to the CDC. Since 1994, reports from all states have been sent electronically through the Public Health Information System. Summaries of the reported isolates are tabulated annually (available at http://www.cdc.gov/ncidod/dbmd/phlisdata/salmonella.htm)

Exact duplicate entries are discarded on a weekly basis. When the data are closed out for a given calendar year, all entries for a given name within a state are compared (except for Oklahoma, which provides initials only). Duplicate entries for a name that also match on age, state, and specimen date within the same or 2 consecutive months are discarded. Entries that match on these criteria but differ in the specimen source are not discarded; however, because most specimens were obtained from stool samples, this number should be small. For Salmonella Typhi, only the first occurrence in a year for a person is kept

A reptile-associated serotype was defined as a Salmonella serotype in the non-human Salmonella database (National Veterinary Services Laboratory, Ames, IA) that was isolated from reptiles in ⩾50% of the isolates tested. The nonhuman Salmonella database was begun in 1981 and has >20,000 isolates. In addition, all Salmonella subspecies II, III, IV, V, or VI were considered to be reptile associated, because reptiles have historically been the source in >50% of these isolates reported to the CDC [25]

SerotypingIsolates are serotyped according to the Kauffman and White scheme, using somatic (O) and flagellar (H) antigens [18]. Most clinical laboratories use only the O antigen to serogroup salmonellae. Complete serotyping is available through state public health laboratories. The National Salmonella Reference Laboratory is located at CDC

Statistical analysisWe calculated annual isolation rates, using US Census Bureau data and intercensal population estimates. To calculate age-specific isolation rates by month of age for infants <1 year old, we used a denominator of one-twelfth the total population of infants. To calculate isolation rates by geographic region, we grouped states into the 9 divisions established by the US Census Bureau. To examine annual trends among serotypes with ⩾100 reports per year, we performed least squares regression and calculated a 95% confidence interval around the slope, using SAS software (version 6.12; SAS Institute). To compare the proportion of reptile-associated serotypes among those serotypes that were significantly increasing or decreasing in frequency over time, we calculated 2-tailed Fisher’s exact P values, using Epi Info (version 6; CDC)
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Results

From 1987 to 1997, 441,863 Salmonella isolates were reported to CDC; 92% had a known serotype (table 1). The number of isolates with an unknown serotype increased from 3.3% in 1987 to 7.3% in 1991 and then decreased to a low of 1.1% in 1997. The annual isolation rate was highest in 1987 (19.1/100,000 persons) and decreased to a low of 12.9/100,000 persons in 1997; this decrease occurred in all age groups. During the entire 11-year surveillance period, the top 5 reported Salmonella serotypes (Salmonella Typhimurium, Salmonella Enteritidis, Salmonella Heidelberg, Salmonella Newport, and Salmonella Hadar) accounted for 66% of all isolates with a known serotype

During the study period, Salmonella Typhimurium was the most frequently reported Salmonella serotype, accounting for 24% (100,713) of all isolates with a known serotype. The annual incidence of Salmonella Typhimurium remained fairly stable over the study period, as did the proportion of isolates that were Salmonella Typhimurium

The next most frequently reported serotype was Salmonella Enteritidis, accounting for 22% (91,280) of all isolates with a known serotype. From 1994 to 1996, Salmonella Enteritidis was the most frequently reported serotype in the United States. The annual incidence rate rose from 2.9/100,000 persons in 1987 to 3.9/100,000 persons in 1995. In addition, from 1987 to 1997, the proportion of all Salmonella isolates with a known serotype that were Salmonella Enteritidis increased from 16% in 1987 to 27% in 1994 and remained >20% through 1997. Data from 1996 and 1997 suggest that Salmonella Enteritidis infections are decreasing. Between 1996 and 1997, the annual isolation rates decreased from 3.6 to 3.0/100,000 persons

Salmonella Heidelberg was the third most common serotype during the 11-year surveillance period; this serotype&ranked third each year, except in 1995, when it&ranked fourth. The total number of reported Salmonella Heidelberg isolates, 35,840, accounted for 9% of all isolates with a known serotype. The proportion of isolates with a known serotype that were Salmonella Heidelberg decreased steadily over the study period. In 1987, this proportion was 13%, and by 1997 it had decreased to 6%

Age and sexInformation on patient age was available for 83% of reported isolates. The highest incidence rate was for infants, at 121.7/100,000 persons per year; this rate peaked at 159.5/100,000 persons in the second month of life (figure 1). Rates decreased abruptly after infancy, remained relatively constant through the adult years, and increased slightly among persons ⩾70 years old. Boys <15 years old had a slightly higher age-specific isolation rate than did girls (data not shown). In contrast, the isolation rate for women (10.2/100,000 persons per year) exceeded that for men (8.8/100,000 persons per year) between the ages of 20 and 74 years. The age- and sex-specific isolation rates for Salmonella Typhimurium and Salmonella Heidelberg were similar to that for all serotypes combined, whereas the rate of Salmonella Enteritidis infection was higher among adults than were those of other serotypes
Figure 1
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Figure 1

Isolation rates by age and sex of patient and year for all Salmonella and Salmonella serogroups Typhimurium, Enteritidis, and Heidelberg in the United States, 1987–1997. Inset is isolation rate for all Salmonella species among infants, by month of age and sex

For isolates from patients with known age, 15% were from infants, 33% were from children 1–19 years old, 34% were from persons 20–49 years old, 15% were from persons 50–79 years old, and 3% were from persons ⩾80 years old (table 2). Persons with Salmonella Typhimurium infection were most likely to be 1–19 years old. In contrast, persons with Salmonella Enteritidis or Salmonella Typhi infection were more likely to be 20–49 years old
Figure 2
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Figure 2

Percentage of reported Salmonella isolates by month of specimen collection and selected serotype in the United States, 1987–1997penta center-figure-legend>
Figure 3
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Figure 3

Isolation rate of all Salmonella species (A) and of Salmonella serotypes Typhimurium (B) and Enteritidis (C) by geographic region in the United States, 1987–1997
Figure 4
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Figure 4

Number of human isolates by year among selected animal-associated serotypes of Salmonella in the United States, 1987–1997. A, Salmonella Marina (reptile associated). B, Salmonella Kentucky and Salmonella Heidelberg (broiler chicken associated). C, Salmonella Hadar and Salmonella Heidelberg (turkey associated). D, Salmonella Derby and Salmonella Typhimurium (swine associated)
Table 1
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Table 1

Annual number of reported Salmonella isolates from humans and their&ranking: 15 most frequent serotypes, United States, 1987–1997
Table 2
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Table 2

Distribution, by age group and serotype, of the 15 most frequently reported serotypes of Salmonella isolates from humans, United States, 1987–1997

SeasonalityOverall, the largest percentages of isolates were reported in August (12%) and September (12%), and the smallest percentage was reported in February (5.5%; figure 2). Although this general pattern was consistent for most serotypes of Salmonella some serotypes demonstrated slight variations (e.g., Salmonella Hadar peaked earlier). Salmonella Newport exhibited the greatest seasonal variation. The trend toward more isolations in late summer did not vary by age group (data not shown)

Site of isolationA known clinical source was reported for 384,266 isolates (87%; table 3). Of these, 89% were isolated from stool samples. Among the top 15 serotypes, except for Salmonella Typhi, the most frequent site of isolation was stool samples, ranging from a high of 94% for serotypes Salmonella Newport, Salmonella Braenderup, and Salmonella Muenchen to a low of 83% for Salmonella Oranienburg. Of all isolates, 22,979 (6.0%) were from blood, 10,750 (2.8%) were from urine, and 258 (<1%) were from cerebrospinal fluid. Of those serotypes with >100 isolates reported from 1987 to 1997, those most commonly isolated from blood were Salmonella Paratyphi A (442 [64%] of 694), Salmonella Choleraesuis (467 [63%] of 736), Salmonella Typhi (2565 [62%] of 4147), and Salmonella Dublin (350 [52%] of 671). The isolation rate of Salmonella species from sterile sites (i.e., blood or cerebrospinal fluid) was 6.5/100,000 infants, 0.5/100,000 persons 1–19 years old and 20–49 years old, 0.6/100,000 persons 50–79 years old, and 1.5/100,000 persons ⩾80 years old. Serotypes most commonly isolated from urine were Salmonella Cubana (63 [18%] of 355), Salmonella Tennessee (185 [12%] of 1509), Salmonella Meleagridis (42 [11%] of 393), and Salmonella Senftenberg (141 [9%] of 1598)
Table 3
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Table 3

Reported number of Salmonella isolates from humans, by source of isolation and serotype: 15 most frequent serotypes, United States, 1987–1997

Regional distributionFrom 1987 to 1997, the rates of isolation of Salmonella species were highest in the New England states (figure 3A). Rates of Salmonella Typhimurium were also highest in New England, except from 1991 to 1993, when the rates in the Pacific region surpassed those in New England (figure 3B). In the early 1990s, rates of Salmonella Enteritidis (figure 3C) nearly doubled in a single year in both New England (5.7/100,000 persons in 1992 to 10.2 in 1993) and the Pacific region (3.2/100,000 persons in 1993 to 6.7 in 1994). In the Mountain region, rates of Salmonella Enteritidis increased more gradually, from 1.2/100,000 persons in 1992 to 4.5 in 1996. In contrast, in the Mid-Atlantic region, rates of Salmonella Enteritidis decreased 49% from a high in 1989 of 10.5/100,000 persons to a low of 5.4/100,000 in 1997. These decreases were also seen in the Pacific (34% decline from 1994–1997) and New England (57% from 1995–1997) regions. In all other regions, the rate of Salmonella Enteritidis remained relatively stable over time

Animal-associated serotypesWe examined trends in serotypes known to be associated with animals, including the reptile-associated serotype Salmonella Marina [12], as well as the top 2 serotypes identified by a 1998–1999 US Department of Agriculture (USDA) survey of broiler plants (Salmonella Kentucky and Salmonella Heidelberg), turkey plants (Salmonella Hadar and Salmonella Heidelberg), and swine plants (Salmonella Derby and Salmonella Typhimurium) [26]. Fewer than 10 human isolates of Salmonella Marina were reported until 1991, at which time there was a dramatic increase, which peaked at 81 isolates in 1996 and then decreased to 36 in 1997 (figure 4A). The number of reported Salmonella Kentucky isolates from humans decreased from 66 in 1987 to 31 in 1992, generally increased to reach 80 in 1995, and then decreased to 60 by 1997 (figure 4B). Salmonella Heidelberg steadily decreased from 6107 isolates in 1987 to 2104 in 1997 (figure 4B). The number of human isolates of Salmonella Hadar peaked at 2442 in 1988 and then steadily decreased to 543 in 1997 (figure 4C). Overall, the number of Salmonella Derby isolates recovered from humans declined over time from 412 in 1987 to 152 in 1997, and the number of Salmonella Typhimurium isolates decreased from 10,719 in 1987 to a low of 7950 in 1992 and then increased to 9116 in 1997 (figure 4D)

Emerging serotypesThe serotype with the greatest average annual increase in the number of isolates from 1987 to 1997 was Salmonella Stanley, followed by Salmonella Paratyphi B, and S. Marina (table 4). Of the top 20 increasing serotypes, 7 (35%) were common reptile-associated Salmonella serotypes (Salmonella Marina, Salmonella Flint, Salmonella Kintambo, Salmonella Wassenaar, Salmonella Ealing, Salmonella Carrau, and Salmonella Abaetetuba), compared with none of the 20 decreasing serotypes (P=.008, 2-tailed Fisher’s exact test). During the same period, the serotypes with the greatest average annual decreases in the number of isolates were Salmonella Heidelberg, Salmonella Hadar, and Salmonella Infantis (table 4)
Table 4
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Table 4

Top 20 increasing and decreasing Salmonella serotypes, United States, 1987–1997
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Discussion

For the 11-year period, 1987–1997, 441,863 culture-confirmed Salmonella infections were reported to CDC, a mean of 40,169 each year. During this period, the isolation rate decreased from 19.1 to 12.9/100,000 persons, a decrease of ∼30%. This is in marked contrast to the earlier trend seen from 1976 to 1986, when the isolation rate increased from 10.7 to 18.1/100,000 persons, an increase of ∼70% [24]

Although the recent overall downward trend in rates of Salmonella infections is encouraging, it should be noted that this trend varies by serotype. Our findings document a general continued increase in Salmonella Enteritidis infections in the United States during the first 10 years of the reporting period that is consistent with previous studies both in the United States [24, 27] and Europe [27–30]. Furthermore, from 1988 to 1996, the percentage of Salmonella outbreaks that were caused by Salmonella Enteritidis increased from 47% to 55%, and Salmonella Enteritidis was the most common cause of all foodborne disease outbreaks in the United States during this same period [5, 17]. Many of these outbreaks have been epidemiologically linked to the consumption of undercooked eggs [2–5]. Case-control studies of sporadic Salmonella Enteritidis infections have also implicated raw or undercooked eggs [31–34] and, to a lesser extent, chicken [34, 35] as vehicles for transmission. In the early 1990s, efforts were made to control the spread of Salmonella Enteritidis through eggs by traceback of eggs implicated in outbreaks and diversion of infected eggs to pasteurization [36]. In addition, the egg industry implemented quality-assurance programs in several states, in an effort to reduce Salmonella Enteritidis in eggs and flocks [37]. The recent decline in the number of human Salmonella Enteritidis isolates in 1996 and 1997 may reflect these improvements; data from 1998 suggest that this decline has continued [38]

Salmonella isolation rates were highest for infants <1 year old. Although there may be some detection bias because of a greater likelihood that samples from an ill infant would be cultured, this most likely reflects a real increased rate among infants. The reasons for this are largely unknown but may include host susceptibility and exposure differences. The finding that infants have a 4–13-fold higher rate of invasive disease than do other age groups is intriguing and highlights the need for prevention

Salmonellosis demonstrated a marked pattern of seasonality, increasing in the warm summer months. This pattern is similar to other foodborne pathogens, such as Escherichia coli O157:H7 [39]. The reasons for this pattern are not entirely known; however, it may be related to infection trends in animal hosts or to holding food at an insufficiently cool temperature and food mishandling during the warmer months

Several O serogroups, A, C1, and D1, more commonly cause invasive infection and are frequently isolated from blood. Although Salmonella virulence factors are not well understood, differences in the O-side chain of the lipopolysaccharide appear to be important [40, 41]. Similar to findings from a recent study in California [42], the serotypes most frequently isolated from urine included O serogroups G, C1, E1, and E4

Overall, the rate of Salmonella species isolation was greatest in the New England states. This high rate is largely driven by the high rate of Salmonella Enteritidis, which persisted in this region until 1995. High rates of Salmonella Enteritidis in New England, the Mid-Atlantic region, and later in the Pacific region, probably reflect high infection rates among chicken flocks in these areas [43]

Although some serotypes, such as Typhimurium, are common in many different animal species, a number of Salmonella serotypes have specific animal reservoirs that are thought to contribute to disease in humans. For example, the animal reservoir for Salmonella Marina is a marine iguana that has become increasingly popular as a pet [12]. Salmonella Marina and other reptile-associated serotypes appear to be increasing over time. The recent decline of Salmonella Marina infections beginning in 1997 may reflect increased edu-cation for pediatricians, veterinarians, and pet store owners about the risk of reptile-associated salmonellosis [11, 44]

In 1996, the USDA implemented a rule, the Pathogen Reduction and Hazard Analysis and Critical Control Point (HACCP) Systems, aimed at reducing pathogens in our food. As part of this system, in 1998, USDA began routine testing for Salmonella species in large, federally inspected raw meat and poultry plants [26]. Of interest, 2 of the serotypes most commonly isolated from poultry demonstrated significant decreases in the number of human isolations from 1987 to 1997. During this same period, per capita consumption of chicken and turkey increased (chicken, from 39.1 to 50.9 lbs; turkey, from 11.6 to 13.9 lbs), and consumption of swine decreased from 47.7 to 45.6 lbs [45]. Although the decreases seen in human illness preceded the formal implementation of the HACCP system, industry-wide changes had been taking place for a number of years. For example, in the late 1980s, turkey manufacturers began providing chlorinated drinking water to turkeys to improve overall health (Peter Poss, poultry consultant, Wilmar, MN; personal communication). These changes may have contributed to the precipitous decline in the number of human isolates of 2 poultry-associated serotypes, Salmonella Hadar and Salmonella Heidelberg

From 1987 to 1997, there was a steady increase in the number of Salmonella Stanley isolations, and a peak occurred in 1995 during a large outbreak associated with alfalfa spouts [6]. Another serotype that increased during this period was Salmonella Paratyphi B, which is difficult to distinguish from Salmonella Java; the primary biochemical difference between Salmonella Paratyphi B and Salmonella Java is tartrate (positive in Salmonella Java), and a test for this is not routinely done in most state public health laboratories. Although the reasons for these increases are not known, both Salmonella Stanley and Salmonella Java have been found in reptiles [46]

The completeness of data reported through this system appears to be increasing. The percentage of isolates with an unknown serotype decreased from 6.2% in 1992 to 1.1% in 1997, which suggests that state public health laboratories may have improved serotyping capability. Furthermore, compared with previous years, patient age was more frequently reported on the surveillance forms (79% in 1984–1986 [24] vs. 85% in 1987–1997). Despite improvements, these data have several limitations. This surveillance system is a passive system that relies on clinical laboratories to send Salmonella isolates to the state laboratory. Only persons who were ill, sought care, had a stool culture, and had the Salmonella isolate forwarded to the state could have been captured in this system. For these reasons, it is recognized that the burden of illness caused by salmonellosis is greatly underreported in the United States [1]

Future surveillance will be enhanced by 2 new tools, the Salmonella outbreak detection algorithm [47] and PulseNet [48]. As described in detail elsewhere, these 2 tools will greatly aid epidemiologists in the detection of outbreaks. Serotyping remains an important laboratory tool that helps public health researchers better understand and define the epidemiology of salmonellosis in the United States. Measuring trends in serotypes over time can provide information about emerging serotypes and about the efficacy of prevention and control measures