4| DISCUSSION
To the best of the authors’ knowledge, this is the first description of an outbreak of abomasal bloat (emphysematous abomasitis) in a dairy goat flock in Latin America. Likewise, based on an epidemiological investigation combined with pathological, microbiological, and molecular diagnosis, it was possible to identify the agents and associated factors involved. Therefore, we emphasize the importance of a broad diagnostic approach in order to elucidate and resolve health conflicts within rural establishments.
According to Panciera et al. (2007) and reviewed by Burgstaller, Wittek, and Smith (2017), abomasal bloat syndrome can be multifactorial, and the pathophysiology primarily involves excess fermentation of high-energy gastrointestinal contents in the abomasum (from milk, milk replacer, or high-energy OES), as well as bacterial activity releasing fermentative enzymes leading to gas production and bloat. In addition, such a progression would also be enhanced by any factor that slowed abomasal emptying or caused paralytic ileus. Regarding the bacterial etiology, in agreement with the current report, the most frequently isolated bacterial pathogens include C. perfringens type A andC. ventriculi species (DeBey et al., 1996; Vatn et al., 2000; Edwards et al., 2008; Van Kruiningen et al., 2009; Leite Filho et al., 2016). Additional bacterial pathogens isolated from calves affected with abomasal bloat include α streptococci, other streptococci species,E. coli , C. fallax , and C. sordellii (Roeder et al., 1987; Vatn et al., 2000).
The pathogenic role of C. perfringens type A was first demonstrated by intraruminal inoculation of such bacteria in neonatal calves, resulting in anorexia, depression, abomasal bloat, diarrhea, and death (Roeder et al., 1988). Clinical severity is associated with the production of lethal toxins as the major cause, namely alpha (CPA; necrotizing and hemolytic action), although other toxins such as enterotoxin (CPE; enterotoxic), beta2 toxin (CPB2; enterotoxic and cytotoxic) and beta-like toxin (NetB; enterotoxic and cytotoxic) can also be produced by this agent (Freedman et al., 2015). Interestingly, this agent has also been reported in cases of gas gangrene in horses and, more recently, in cattle (Peek et al., 2003; Pires et al., 2017). Lastly, Khan et al. (2020) reported a greater prevalence of pathogenic C. perfringens type A in kid goats when compared to B and D types.
While C. perfringens has been associated with food poisoning in humans, the role of C. ventriculi as a primary agent in gastrointestinal disorders (e.g., emphysematous gastritis) is well-described in humans (Freedman et al., 2015; de Meij et al., 2017; Singh, 2019). In addition, it is found in patients with gastric ulcers and delayed gastric emptying, but it is also considered a normal commensal microbiota, and it was also found in our control kids in the current report. Therefore, it is considered to be opportunistic when the environment becomes conducive to its growth (Crowther, 1971; Al Rasheed and Senseng, 2016). Although the pathogenic role of C. ventriculiis not clear, the local accumulation of acetaldehyde and ethanol formed from carbohydrate fermentation by the organism could induce stomach and duodenal injuries. Furthermore, the carbon dioxide production from glucose fermentation and pyruvate metabolism results in abdominal distention, as previously reported in some human patients (Tolentino et al., 2003).
Regarding the diagnosis, confirmation of C. ventriculi infection is feasible by molecular or histology/cytology methods, since this microorganism cannot be detected by classical culture techniques, which in most cases reveal negative results (DeBey et al., 1996; Vatn et al., 2000; Edwards et al., 2008; Lam-Himlin et al., 2011; de Meij et al., 2017). In this sense, concerning C. ventriculi detection, it is important to highlight two facts. Firstly, the diagnosis of such an agent must be associated with pathological findings, as its finding by chance does not point toward a clinical risk to the animal. Secondly, the smears evaluation in combination with histopathology of the abomasum is a strongly suggestive diagnostic method, as carried out in this study. Morphologically, the main differential diagnosis in this case is the presence of bacteria of the Micrococcus genus; these are smaller (0.5 μm) and tend to form tightly packed clusters, a feature not seen with C. ventriculi (Lam-Himlin et al., 2011).
Concerning the presence of S. cerevisiae in the milk replacer used to feed the kid goats, S. cerevisiae fermentation products have been extensively used in the dairy industry with beneficial effects on production parameters (Poppy et al., 2012), modulation of the immune system (Zaworski et al., 2014), improvement in rumen fermentation, stability of the gut microbiota (Brewer et al., 2014), and reduction of diarrhea in calves (Alugongo et al., 2017). Although there are several positive arguments regarding the introduction of such yeast into the ruminant diet, disturbances in gastric emptying associated with milk accumulation may have provided an opportunistic and deleterious growth of the S. cerevisiae within the kids’ abomasum. They also ferment sugars, releasing ethyl alcohol and carbon dioxide similar to C. ventriculi . Corroborating this line of thought, there was a lot of yeast in the cytological smears of the kids affected by abomasal bloat. Therefore, more attention should be paid when adding yeasts to the diet of young ruminants.
Regarding the possible associated factors with the occurrence of abomasal bloat, our results are in agreement with the findings from most worldwide reports, where high infection rates were related to microbiota imbalances and poor hygiene. All environment/food samples (100.0%; 7/7) collected in this case were positive for the 16S rRNA gene related toClostridium spp. Likewise, the use of a milk substitute instead of natural goat milk can be closely related to the disturbance in abomasal emptying. The large volume of milk ingested in a short time, high osmolarity, and the high temperature of the milk replacer associated with kid management are other strong reasons already verified in previous reports (DeBey et al., 1996; Van Kruiningen et al., 2009; Burgstaller et al., 2017).
Other important management findings highlighted is this study is the offering of ad libitum concentrate to the kids and their behavior to look for such food immediately after milking management. This can have favored the development of an environment with a large amount of milk and soluble carbohydrates contained within the abomasum. As already known, a high protein and carbohydrate concentration in the gut triggers the growth of C. perfringens , increasing the risk of enterotoxemia (Riddell and Kong, 1992; Roberfroid et al., 2010). Quinnet al . (2011) also described various predisposing factors for the occurrence of enterotoxemia, like changes in diet, low proteolytic efficiency in neonates, trypsin inhibitors in colostrum, malnutrition, inefficient pancreatic secretion, no established intestinal flora, carbohydrates engorgement, and intestinal hypomotility (Sato et al., 1978).
Few reports on treatments of abomasal bloat have been described. However, most therapies included antibiotics (primarily penicillin and ampicillin), rumen “tonics” (including a wide variety of medicaments), non-steroidal anti-inflammatories (primarily flunixin meglumine), relieving the distension via a tube or trocar, Clostridial antitoxin, and fluid therapy as reviewed by Shoemaker et al . (2008). In the authors’ experience, the earlier the clinical signs (abomasal bloat) are identified, the better the animal’s prognosis.
Lastly, regarding prophylaxis, the high frequency of C. perfringens type A detection in several reports on abomasal bloat and gas gangrene in ruminants, reinforces that such an agent should be part of the routine clostridial vaccines. Reversed genetics have demonstrated that alpha toxin is the main virulence factor for C. perfringenstype A causing gas gangrene, and that vaccination with alpha toxoid could protect animals against this agent (Awad et al., 1995). Unfortunately, only a few vaccines against clostridial diseases for ruminants contain C. perfringens alpha toxoid in Brazil (Pires et al., 2017). Therefore, it is important to look for this information at the time of purchase and immunization of the flock. In the current report, pregnant goats were vaccinated with a commercial vaccine containing alpha toxin, so it is believed that since there was no colostrum management program, the kid goats could be receiving low quality colostrum and immunization was not occurring efficiently. In this sense, the importance of quality plans for colostrum management in dairy farms is also emphasized.
In conclusion, an outbreak of abomasal bloat affected a dairy goat farm throughout the kidding season. The disease affected suckling kid goats among one and three months old with an acute clinical course of 6–12 hours until death. There was a mortality rate of 30% (66/221), and the agents C. perfringens type A and C. ventriculi were identified as the main ones involved with possible participation ofS. cerevisiae . Among the possible associated factors, the erroneous use of milk replacer associated with errors in kid management favored decreases in abomasal emptying with local dysbiosis and clinical signs. Among the prophylactic measures, hygiene care, proper use of milk replacer, vaccination plan containing C. perfringens alpha toxoid associated with a good colostrum management were suggested.