Kevin J. Cummings

The incidence of salmonellosis among dairy herds in the northeastern United States

Abstract The objectives of this study were to estimate the incidence of salmonellosis among a large sample of dairy herds in the northeastern United States (both at the animal level and the herd level), to describe the serotypes and antimicrobial resistance profiles of the positive samples, and to determine whether various herd-level factors were important predictors of incidence. Participating veterinarians enrolled 831 dairy herds and submitted fecal samples from 2,565 female dairy cattle for Salmonella culture because of suspicion of clinical disease. Estimates of animal-level incidence rates were calculated for each age group as the number of cases per animal time at risk, and an estimate of herd-level incidence rate was calculated as the number of positive herds per herd time at risk. Descriptive analysis of serotype data and level of antimicrobial resistance was performed, and Poisson regression analysis was used to study associations between the within-herd incidence of salmonellosis and certain predictor variables (herd size, housing type, vaccination status, and prior history of Salmonella infection). Salmonella was isolated from 576 (22.5%) samples representing 93 herds. The animal-level incidence rates for preweaned female calves, heifers, and adult cows were 8.1, 0.04, and 1.8 cases per 1,000 animal-years, respectively. The herd-level incidence rate was 8.6 positive herds per 100 herd-years. Salmonella Newport was the predominant serotype, accounting for 41% of the cases, followed by Salmonella Typhimurium. Over 68% of all isolates were resistant to 5 or more antimicrobial agents. Herd size was the only significant predictor of the incidence of salmonellosis in a multivariable model; herds with at least 400 female dairy cattle had a higher incidence rate than smaller herds. Our results shed light on the impact of salmonellosis on the dairy industry in the northeastern United States, and they help clarify the role of dairy cattle as a source of Salmonella serotypes that are also important human pathogens.

The prevalence of multidrug resistance is higher among bovine than human Salmonella enterica serotype Newport, Typhimurium, and 4,5,12:i:- isolates in the United States but differs by serotype and geographic region.

ABSTRACT Salmonella represents an important zoonotic pathogen worldwide, but the transmission dynamics between humans and animals as well as within animal populations are incompletely understood. We characterized Salmonella isolates from cattle and humans in two geographic regions of the United States, the Pacific Northwest and the Northeast, using three common subtyping methods (pulsed-field gel electrophoresis [PFGE], multilocus variable number of tandem repeat analysis [MLVA], and multilocus sequence typing [MLST]). In addition, we analyzed the distribution of antimicrobial resistance among human and cattle Salmonella isolates from the two study areas and characterized Salmonella persistence on individual dairy farms. For both Salmonella enterica subsp. enterica serotypes Newport and Typhimurium, we found multidrug resistance to be significantly associated with bovine origin of isolates, with the odds of multidrug resistance for Newport isolates from cattle approximately 18 times higher than for Newport isolates from humans. Isolates from the Northwest were significantly more likely to be multidrug resistant than those from the Northeast, and susceptible and resistant isolates appeared to represent distinct Salmonella subtypes. We detected evidence for strain diversification during Salmonella persistence on farms, which included changes in antimicrobial resistance as well as genetic changes manifested in PFGE and MLVA pattern shifts. While discriminatory power was serotype dependent, the combination of PFGE data with either MLVA or resistance typing data consistently allowed for improved subtype discrimination. Our results are consistent with the idea that cattle are an important reservoir of multidrug-resistant Salmonella infections in humans. In addition, the study provides evidence for the value of including antimicrobial resistance data in epidemiological investigations and highlights the benefits and potential problems of combining subtyping methods.

The Effect of Clinical Outbreaks of Salmonellosis on the Prevalence of Fecal Salmonella Shedding Among Dairy Cattle in New York

The objective of this study was to determine if the within-herd prevalence of fecal Salmonella shedding is higher in dairy herds with clinical outbreaks of disease, as compared to herds with subclinical infections only. Data were collected prospectively from dairy herds throughout New York that had at least 150 lactating cows and that received clinical service from participating veterinarians. After enrollment, Salmonella surveillance consisted of both environmental screening and disease monitoring within the herd. Herds positive by either environmental or fecal culture were sampled during three visits to estimate the within-herd prevalence of Salmonella. We characterized isolates by serovar and antimicrobial resistance pattern. Among 57 enrolled herds, 44 (77%) yielded Salmonella-positive samples during the study period; 27 (61%) of the positive herds had Salmonella isolated from environmental samples only, and 17 (39%) had one or more laboratory-confirmed clinical cases. The within-herd prevalence of fecal Salmonella shedding ranged from 0 to 53%. Salmonella Cerro was the predominant serovar, accounting for 56% of all isolates. Antimicrobial resistance ranged from zero to nine drugs, and 14 (32%) of the positive farms generated multidrug-resistant isolates. Herds with laboratory-confirmed clinical cases had a higher prevalence of fecal Salmonella shedding than herds that only generated positive environmental samples, as estimated by a Poisson regression model (prevalence ratio, 2.7; p = 0.01). An association between dairy herd outbreaks of salmonellosis and a higher prevalence of asymptomatic shedding should help guide strategies for reducing the public health threat of Salmonella, as the ability to recognize high-risk herds by clinical laboratory submissions presents an obvious opportunity to maximize food safety at the preharvest level. This is in contrast with other foodborne zoonotic pathogens, such as Campylobacter jejuni and Escherichia coli O157:H7, which occur widely in adult cattle without accompanying clinical disease.

Salmonella enterica serotype Cerro among dairy cattle in New York: an emerging pathogen?

The focus of this study was Salmonella enterica serotype Cerro, a potentially emerging pathogen of cattle. Our objectives were to document the within-herd prevalence of Salmonella Cerro among a sample of New York dairy herds, to describe the antimicrobial resistance patterns and pulsed-field gel electrophoresis types of the isolates, and to elucidate the status of this serotype as a bovine pathogen. Data were collected prospectively from dairy herds throughout New York that had at least 150 lactating cows and that received clinical service from participating veterinarians. Following enrollment, Salmonella surveillance consisted of both environmental screening and disease monitoring within the herd. Herds positive by either environmental or fecal culture were sampled during three visits to estimate the within-herd prevalence of Salmonella. Among 57 enrolled herds, 44 (77%) yielded Salmonella-positive samples during the study period. Of these, 20 herds (46%) were positive for Salmonella Cerro. Upon follow-up sampling for estimation of prevalence, Cerro was identified in 10 of the 20 herds; the median within-herd Cerro prevalence was 17%, with a maximum of 53%. Antimicrobial resistance ranged from zero to nine drugs, and eight (40%) of the Cerro-positive farms generated drug-resistant isolates. Eight XbaI pulsed-field gel electrophoresis types were represented among 116 isolates tested, although 89% of these isolates shared the predominant type. Among herds with clinical cases, cattle that had signs consistent with salmonellosis were more likely to test positive for Cerro than apparently healthy cattle, as estimated by a logistic regression model that controlled for herd as a random effect (odds ratio: 3.9). There is little in the literature concerning Salmonella Cerro, and published reports suggest an absence of disease association in cattle. However, in our region there has been an apparent increase in the prevalence of this serotype among cattle with salmonellosis. Other Salmonella serotypes important to bovine health have emerged to become leading causes of human foodborne disease, and close monitoring of Cerro is warranted.

Antimicrobial Resistance Trends Among Salmonella Isolates Obtained from Dairy Cattle in the Northeastern United States, 2004–2011

Monitoring antimicrobial resistance trends among bacteria isolated from food animals and people is necessary to inform public policy regarding appropriate antimicrobial use. Our objectives were to describe the antimicrobial resistance status of Salmonella isolates from dairy cattle in the northeastern United States and to identify trends in resistance to various antimicrobial agents over time. Data were collected retrospectively for all bovine Salmonella isolates that were obtained from samples submitted to Cornell Universitys Animal Health Diagnostic Center between January 1, 2004 and December 31, 2011. Temporal trends in the prevalence of resistant Salmonella were investigated for each antimicrobial agent using the Cochran-Armitage trend test. Antimicrobial susceptibility testing was performed on 2745 bovine Salmonella isolates from clinical samples submitted during the study period. Overall resistance to each antimicrobial agent ranged from 0% (amikacin, ciprofloxacin, and nalidixic acid) to 72.0% (sulfadimethoxine). There was evidence of a significantly decreasing trend in prevalence of resistance to most agents: amoxicillin/clavulanic acid (AUG), ampicillin (AMP), cefoxitin (FOX), ceftiofur (TIO), ceftriaxone (AXO), chloramphenicol (CHL), chlortetracycline (CTET), florfenicol (FFN), kanamycin (KAN), neomycin (NEO), oxytetracycline (OXY), spectinomycin (SPE), streptomycin (STR), sulfadimethoxine (SDM), sulfisoxazole (FIS), and tetracycline (TET). Among the 265 isolates that were tested using the National Antimicrobial Resistance Monitoring System (NARMS) panel, the most common resistance patterns were pansusceptible (54.0%), AUG-AMP-FOX-TIO-AXO-CHL-KAN-STR-FIS-TET (18.1%), and AUG-AMP-FOX-TIO-AXO-CHL-STR-FIS-TET (12.1%). Increasing prevalence of S. enterica serovar Cerro over the course of the study period presumably had an impact on the observed resistance trends. Nevertheless, these results do not support the notion that the current level of antimicrobial use in dairy cattle is driving an increase in the emergence and dissemination of drug-resistant Salmonella in the region served by the laboratory.

Farm Animal Contact as Risk Factor for Transmission of Bovine-associated Salmonella Subtypes

Salmonellosis prevention should focus on safe animal contact as well as food safety.

The duration of fecal Salmonella shedding following clinical disease among dairy cattle in the northeastern USA

The objectives of this study were to determine the duration of fecal Salmonella shedding among dairy cattle in the northeastern United States following laboratory-confirmed clinical disease and to evaluate whether age group or serotype was associated with either shedding period or mortality. Study farms included 22 dairy herds that had at least two previous salmonellosis cases confirmed by fecal culture. Veterinarians continued to submit culture samples from clinical suspects following herd enrollment, and fecal samples from positive cattle were collected monthly until three sequential negative results were obtained or until loss to follow-up. There were 357 culture-positive clinical cases that each involved a single serotype during the shedding period. The Kaplan-Meier median duration of fecal Salmonella shedding was 50 days, and the maximum was 391 days. S. Newport was the predominant serotype, accounting for 51% of the cases. Age group and serotype were not significant predictors of Salmonella shedding duration in a Cox proportional hazards model, when stratifying by herd. However, the proportion of adult cows shedding for at least two consecutive monthly samples was significantly greater than the proportion of female calves shedding for this duration (Fishers exact test p-value<0.01). Age group was also associated with mortality in this study; calves with salmonellosis were more likely to die than cows as estimated by a logistic regression model which controlled for herd as a random effect (p-value=0.04).

Evaluation of dietary energy intake and physical activity in dogs undergoing a controlled weight-loss program

OBJECTIVE To quantify physical activity and dietary energy intake in dogs enrolled in a controlled weight-loss program and assess relationships between energy intake and physical activity, sex, age, body weight, and body condition score (BCS). DESIGN Prospective clinical study. ANIMALS 35 client-owned obese dogs (BCS > 7/9). PROCEDURES Dogs were fed a therapeutic diet with energy intake restrictions to maintain weight loss of approximately 2%/wk. Collar-mounted pedometers were used to record the number of steps taken daily as a measure of activity. Body weight and BCS were assessed at the beginning of the weight-loss program and every 2 weeks thereafter throughout the study. Relationships between energy intake and sex, age, activity, BCS, and body weight at the end of the study were assessed via multivariable linear regression. Variables were compared among dogs stratified post hoc into inactive and active groups on the basis of mean number of steps taken (< or > 7,250 steps/d, respectively). RESULTS Mean ± SD daily energy intake per unit of metabolic body weight (kg(0.75)) of active dogs was significantly greater than that of inactive dogs (53.6 ± 15.2 kcal/kg(0.75) vs 42.2 ± 9.7 kcal/kg(0.75), respectively) while maintaining weight-loss goals. In regression analysis, only the number of steps per day was significantly associated with energy intake. CONCLUSIONS AND CLINICAL RELEVANCE Increased physical activity was associated with higher energy intake while maintaining weight-loss goals. Each 1,000-step interval was associated with a 1 kcal/kg(0.75) increase in energy intake.

Subtype analysis of Salmonella isolated from subclinically infected dairy cattle and dairy farm environments reveals the presence of both human- and bovine-associated subtypes

While it is well established that clinically ill livestock represent a reservoir of Salmonella, the importance of subclinical shedders as sources of human salmonellosis is less well defined. The aims of this study were to assess the subtype diversity of Salmonella in healthy dairy cattle and farm environments and to compare the subtypes isolated from these sources with the Salmonella subtypes associated with clinical human cases in the same geographic area. A total of 1349 Salmonella isolates from subclinical dairy cattle and farm environments (46 farms) were initially characterized by traditional or molecular serotyping and tested for antimicrobial susceptibility. A set of 381 representative isolates was selected for further characterization by pulsed-field gel electrophoresis (PFGE); these isolates represented unique combinations of sampling date, serovar, antimicrobial resistance pattern, farm of origin, and source, to avoid overrepresentation of subtypes that were re-isolated from a given source. These 381 isolates represented 26 Salmonella serovars; the most common serovars were Cerro [(38.8%, 148/381) isolated from 21 farms], Kentucky [16.3%; 10 farms], Typhimurium [9.4%; 7 farms], Newport [7.6%; 8 farms], and Anatum [6.3%; 6 farms]. Among the 381 isolates, 90 (23.6%) were resistant to between 1 and 11 antimicrobial agents, representing 50 different antimicrobial resistance patterns. Overall, 61 XbaI-PFGE types were detected among these 381 isolates, indicating considerable Salmonella diversity on dairy farms. Fourteen PFGE types, representing 12 serovars, exactly matched PFGE types from human isolates, suggesting that subclinically infected dairy cattle could be sources of human disease-associated Salmonella.

Salmonella Cerro isolated over the past twenty years from various sources in the US represent a single predominant Pulsed-Field Gel Electrophoresis type

Salmonella Cerro prevalence in US dairy cattle has increased significantly during the past decade. Comparison of 237 Salmonella isolates collected from various human and animal sources between 1986 and 2009 using pulsed-field gel electrophoresis, antimicrobial resistance typing, and spvA screening, showed very limited genetic diversity, indicating clonality of this serotype. Improved subtyping methods are clearly needed to analyze the potential emergence of this serotype. Our results thus emphasize the critical importance of population-based pathogen surveillance for the detection and characterization of potentially emerging pathogens, and caution to critically evaluate the adequacy of diagnostic tests for a given study population and diagnostic application.