Swine Dysentery: Re-Emergence in the United States and Canada
Factors relating to the environment, feeding practices, diet, host susceptibility and colonic microbiota may be responsible for the increased incidence of swine dysentery over recent years, according to Eric R. Burrough of the Department of Veterinary Diagnostic and Production Animal Medicine, College of Veterinary Medicine, Iowa State University in the US.Swine dysentery (SD) is a severe mucohaemorrhagic diarrheal disease of swine that has been recognised since the 1920s and is classically associated with infection by Brachyspira hyodysenteriae. Clinical SD is typically observed in growing and finishing pigs and often results in severe economic losses in affected herds. By the mid-1990s, the prevalence of clinical dysentery in US swine herds had fallen to such low levels that the disease was considered by many to be one of historical importance but of minimal threat to the US industry going forward. This was due, at least in part, to successful implementation of effective treatment, control and elimination methods for Brachyspira spp., specifically B. hyodysenteriae.
Incidence of Disease
United States
Since 2007, the frequency of detection of Brachyspira spp. from clinical submissions to the Iowa State University Veterinary Diagnostic Laboratory (ISU VDL) has increased (Figure 1).
During this recent time-frame, B. hyodysenteriae has been isolated from at least one case submitted to the ISU VDL from pigs placed in 13 different states (Illinois, Indiana, Iowa, Kansas, Minnesota, Mississippi, Missouri, New York, North Carolina, Ohio, Pennsylvania, South Dakota, and Virginia). While some of these isolates were from surveillance submissions in adult animals, the majority were from grow-finish pigs with clinical diarrhoea. Additionally, since the latter part of 2008, there has been a concurrent increase in the number of cases with diarrhoea and lesions suggestive of SD from which a strongly β-haemolytic spirochaete was isolated that was not identified as B. hyodysenteriae by available laboratory methods (Figure 1).
Green line: Weakly Β-haemolytic Brachyspira spp.
Red line: strongly Β-haemolytic, PCR-confirmed as B. hyodysenteriae
Black line: strongly Β-haemolytic, not identified as B. hyodysenteriae by PCR.
These strongly β-haemolytic spirochaetes have included both atypical and untypable isolates (1) and have been recovered from submissions to the ISU VDL originating from eight US States (Illinois, Iowa, Michigan, Minnesota, Missouri, North Carolina, Virginia and Wisconsin) and Canada.
Retrospective analysis of partial nox gene sequences from the majority of these atypical and untypable isolates reveals they are identical or nearly identical over the region compared to either clade I or clade II isolates of the recently proposed novel species ‘Brachyspira hampsonii’ 2).
While isolation of ‘B. hampsonii’ from pigs with mucohaemorrhagic colitis is not uncommon in diagnostic cases received at the ISU VDL, B. hyodysenteriae is still the predominant species recovered from such submissions.
Canada
Since 2009, a re-emergence of SD has been observed in western Canada, primarily from farms located in Alberta and Saskatchewan (3). Additionally, and in contrast to what has been observed in the United States, ‘B. hampsonii’ isolation from pigs with loose, bloody or mucoid diarrhoea has been reported at an approximately three-fold higher frequency than that observed for B. hyodysenteriae.
Virulence
Following the identification of several untypable strongly β-haemolytic Brachyspira spp. submitted to the ISU VDL from multiple unrelated farms, a pilot study was performed in 2009 to determine if these spirochaetes were indeed pathogenic.
The results of this pilot study revealed that these strongly β-haemolytic isolates were indeed pathogenic and produced clinical disease resembling SD associated with typical B. hyodysenteriae infection (4).
A larger study followed in 2011 where groups of pigs were inoculated with one of eight different clinical isolates of Brachyspira originating from different US herds and including several weakly β-haemolytic species, typical strongly β-haemolytic B. hyodysenteriae and multiple strongly β-haemolytic isolates identified as either Brachyspira intermedia or ‘Brachyspira sp. SASK 30446’ by PCR assays described as specific for these species at that time (5).
Retrospective analysis of partial nox gene sequences from these strongly β-haemolytic isolates identified as B. intermedia and ‘B. sp. SASK 30446&sdquo; revealed they are identical or nearly identical over the region compared to clade I and clade II isolates of ‘B. hampsonii’, respectively.
In this study, infection with strongly β-haemolytic spirochaetes, regardless of their molecular identification, induced diarrhoea and lesions similar to those associated with B. hyodysenteriae infection whereas weakly β-haemolytic isolates were poorly pathogenic.
This is consistent with what is reported clinically in affected herds in the United States where typical SD is described in association with either B. hyodysenteriae or ‘B. hampsonii’ infection and there appears to be no appreciable difference in virulence in naïve herds.
Additionally, a recent experimental study described disease indistinguishable from SD in pigs following infection with a Canadian isolate of ‘B. hampsonii’ (6).
Diagnostic Trends
Given the specialised growth requirements and prolonged incubation period required for routine isolation of Brachyspira spp. from clinical samples, many veterinary diagnostic laboratories have favoured rapid culture-independent methods for detection of these spirochaetes, particularly PCR.
Published PCR assays often target the two well-characterized pathogenic species of swine, B. hyodysenteriae and Brachyspira pilosicoli (7). Unfortunately, such PCR assays, while highly specific, are not sufficiently sensitive to identify all potentially pathogenic Brachyspira spp. and negative results in cases suggestive of Brachyspira-associated disease should be interpreted with caution.
The emergence of ‘B. hampsonii’ in North America is case in point for the importance of such caution as commonly used PCR assays for B. hyodysenteriae will not detect ‘B. hampsonii’ and, without concurrent microbial culture, the resultant lapse in pathogen identification may ultimately contribute to the spread of novel agents.
At the ISU VDL, the current standard practice for identification of Brachyspira spp. from clinical samples is selective anaerobic culture followed by a genus-level nox gene PCR from primary cultures with sequence-based speciation. As more broadly specific PCR assays and other culture-independent methods are developed and described, these likely will be incorporated into routine diagnostic and surveillance practices; however, selective microbial culture should remain a key component of any diagnostic protocol in cases suggestive of SD, particular from index farm situations.
Conclusions – Expanding the Definition
The precise mechanisms underlying the re-emergence of SD in the United States and Canada have not been fully elucidated at the present time. While the emergence of a novel species likely contributed to the problem, particularly in Canada where ‘B. hampsonii&rsdquo; is now a predominant species isolated, this does not fully explain the situation as B. hyodysenteriae isolations have also increased in the United States over this same period.
Together, these findings suggest that one or more factors relating to the environment, feeding practices, diet, host susceptibility and colonic microbiota likely play a significant role in the increased incidence of SD over the last several years.
The classical definition of SD, as described in most textbooks, is severe diarrhoea with mucus and blood from which B. hyodysenteriae is detected by anaerobic culture or culture-independent means. Given the multiple recent experimental reproductions of disease indistinguishable from SD following oral inoculation of pigs with strongly β-haemolytic spirochaetes that are not B. hyodysenteriae, it seems appropriate that the definition of SD be expanded to include all cases of mucohaemorrhagic diarrhoea from which a strongly β-haemolytic Brachyspira spp. is isolated by culture.
References
- Clothier et al., 2011. J Vet Diagn Invest. 23: 1140-1145.
- Chander et al., 2012. J Vet Diagn Invest. 24: 903-910.
- Harding et al., 2013. Adv Pork Prod; Banff Seminar, Proc. 24: 175-179.
- Schwartz et al., 2010. 41st Annual AASV Meeting, Proc. 77-79.
- Burrough et al., 2012. J Vet Diagn Invest. 24: 1025-1034.
- Rubin et al., 2013. PLoS One. 8: e57146.
- La et al., 2003. J Clin Microbiol. 41: 3372-3375.
The paper was presented at the 6th International Conference on Colonic Spirochaetes in Animals and Humans 2013, University of Surrey, UK. 5-6 September 2013.
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October 2013