A number of studies have described the prevalence and/or risk factors for fecal Salmonella
shedding among dairy cattle (Kabagambe, et al., 2000
; Warnick, et al., 2001
; Huston, et al., 2002
; Fossler, et al., 2004
), but few have examined the duration of shedding in either subclinical or clinical cases. This study had the particular advantage of involving a large number of clinically affected animals from multiple herds. Over 350 cattle with laboratory-confirmed salmonellosis were tested via fecal culture at approximately monthly intervals until three sequential negative results were obtained or until loss to follow-up.
Although we obtained data on a large number of cattle, the relatively small number of enrolled herds (22) may have introduced a degree of selection bias into this study. These herds were all located in either New York (15) or Vermont (7) and may not be representative of all dairy operations in the northeastern USA. These herds were also quite homogeneous with respect to a number of important covariates of interest in this study, thus precluding analysis; for example, all 22 herds utilized free-stall housing, and only one used a flush water system to remove manure from alleys. It is possible that additional selection bias may have arisen from our requirement that study herds had to have had at least two previous laboratory-confirmed Salmonella cases in order to be eligible. Perhaps the pattern of Salmonella shedding is different among those herds with sporadic cases of disease in individual animals, although we found no significant correlation between the number of cases per herd and the maximum duration of fecal Salmonella shedding within that herd. Finally, the issue of informative censoring must be addressed, particularly in light of the high percentage of censored cases in this study. It is conceivable that those cattle that were right-censored due to death or sale would have had an extended duration of fecal Salmonella shedding on account of disease severity. However, our sensitivity analysis led us to decide that even if our assumption of independent censoring was not met, we would have reached the same conclusions. Furthermore, loss of an animal due to death or culling is, in practical terms, a means of bringing an end to that animal’s shedding of Salmonella into the dairy farm environment. One could argue that these outcomes be considered as legitimate endpoints of fecal Salmonella shedding duration on the dairy farm.
In this study, fecal Salmonella
shedding exceeded one year in two animals, with the maximum duration (391 days) being seen in an adult cow infected with the Newport serotype. This is more than twice the maximum shedding time (190 days) reported in a study involving two dairy herds that had experienced clinical outbreaks of Salmonella
Newport (Cobbold, et al., 2006
). Prolonged periods of shedding could lead to extensive environmental contamination and an increased risk of within-herd transmission and spread to other herds. As evidenced in this study, shedding often persists well beyond the typical duration of clinical signs in cattle with salmonellosis. Furthermore, extended survival of the organism in the environment is possible; one study found that S
. Newport could survive in manure for at least six months over the course of winter (Clegg, et al., 1983
). Despite the fact that multiple Salmonella
serotypes are common in the dairy farm environment (Wells, et al., 2001
; Edrington, et al., 2004
), over 91% of the cattle with multiple positive samples in this study had the same serotype isolated from all of them. This is consistent with true bacterial colonization rather than organisms simply passing through the gastrointestinal tract. However, we cannot rule out either re-infection from the environment or a pass-through effect as contributing to repeated positive samples in some cattle.
Adult cows tended to shed Salmonella in their feces longer than calves did, in part because affected calves often died early in the course of their disease. In fact, the odds of mortality were significantly higher among calves in a logistic regression model controlling for herd as a random effect. Of the 34 calves lost to follow-up for known reasons, death was the cause in 33 of them. Dairy herd outbreaks that involve calves represent an important concern for producers because of high case fatality. On the other hand, infected cows are more likely to have an extended duration of shedding, which can result in significant public health consequences in addition to potential transmission to other cattle.
Serotype was not a significant predictor of Salmonella
shedding duration in this study, according to a Cox proportional hazards model. It may be that host (immune status) and environmental factors (herd management and hygiene practices) play a more prominent role in determining the length of shedding. Alternatively, other pathogen factors such as dose of inoculum may have a significant effect on shedding duration. One study found that periparturient cows and cows designated as sick by farm personnel were more likely than other cattle to be shedding Salmonella
in their feces (Fossler, et al., 2005
). According to another study, cows in early lactation (≤ 60 DIM) were more likely to be shedding Salmonella
than cows in late lactation (Fitzgerald, et al., 2003
). Therefore, it seems logical that physiologic stress and concurrent illness could predispose to prolonged fecal shedding among dairy cattle. A number of studies have reported large herd size as a risk factor for fecal Salmonella
shedding in dairy herds (Kabagambe, et al., 2000
; Huston, et al., 2002
; Blau, et al., 2005
; Fossler, et al., 2005
). Large herds tend to be housed in free-stalls, which present considerable challenges when combating manure-transmitted pathogens, and they may have a greater likelihood of purchasing cattle from outside sources. It is conceivable that these factors could lead to increased duration of fecal Salmonella
shedding among individual cattle as well. Manure management could also play a role in shedding; one study found that farms where manure was removed from alleys via a flush water system were more likely to have Salmonella
shedders than farms that employed a different system (Kabagambe, et al., 2000
). Again, it is possible that a similar mechanism could also lead to prolonged shedding among individual animals.
Newport was clearly the major serotype in this study, accounting for over half the cases. This is particularly noteworthy since Newport is also an increasingly important human pathogen and has generally been multidrug-resistant among cattle in recent years (Cummings, et al., In Press
). According to CDC FoodNet data from 2006, the annual incidence of foodborne S
. Newport infections in the U.S. had increased by 42% over the average annual incidence for 1996–1998 (Centers for Disease Control and Prevention (CDC), 2007
). Multidrug resistance is also on the rise; the prevalence of the most common MDR S
. Newport phenotype increased from 1% of human Newport isolates tested by the National Antimicrobial Resistance Monitoring System (NARMS) in 1998 to 21% of isolates tested in 2003. This phenotype, Newport-MDRAmpC, is characterized by resistance to at least nine antimicrobial agents (ampicillin, amoxicillin-clavulanic acid, cefoxitin, ceftiofur, cephalothin, chloramphenicol, streptomycin, sulfamethoxazole/sulfisoxazole, and tetracycline). It also displays decreased susceptibility to ceftriaxone, a crucial drug used for treating invasive Salmonella
infections in children. This serotype undoubtedly represents an important threat to public health. Reported risk factors for Newport-MDRAmpC infection in people include direct exposure to a dairy farm (Gupta, et al., 2003
), consumption of uncooked ground beef (Varma, et al., 2006
), and consumption of unpasteurized dairy products (Centers for Disease Control and Prevention (CDC), 2008
); these examples illustrate the key role that dairy cattle play as a source of MDR Salmonella