Salmonella Phage CKT1 Effectively Controls the Vertical Transmission of Salmonella Pullorum in Adult Broiler Breeders

SIMPLE SUMMARY: Salmonella enterica serovar Gallinarum biovar Pullorum (S. Pullorum), a septicemic pathogenic bacterium of poultry due to high mortality of chicks or poults, could not only result in a high mortality rate among embryos and chicks, but also lead to persistent infection and transmission to eggs or progeny in adult chickens during the carrier state. Diseases caused by Salmonella infection via vertical transmission continue to pose a highly significant threat to both human and animals; however, research on phage therapy regarding the vertical transmission of Salmonella is currently lacking. In this study, we evaluated the effect of Salmonella phage CKT1 on controlling the vertical infection of S. Pullorum by detecting the bacterial load in the reproductive system, eggshells and liquid whole eggs of adult broiler breeders. The results showed that the oral use of phage CKT1 could effectively reduce the colonization level of S. Pullorum in various organs including liver, spleen, heart, ovary and oviduct of adult breeders. More importantly, phage treatment significantly decreased the Salmonella-specific IgG level in serum of infected chickens, and reduced the bacterial load in eggshells and liquid whole eggs, thus decreasing the probability of vertical transmission of S. Pullorum in poultry. In addition, the total bacterial load in the poultry breeding environment was also significantly reduced after phage therapy, probably due to the decrease in the Salmonella load in cecal contents and restoration of the intestinal microbiome in chickens. ABSTRACT: Phage therapy is widely being reconsidered as an alternative to antibiotics for the treatment of multidrug-resistant bacterial infections, including salmonellosis caused by Salmonella. As facultative intracellular parasites, Salmonella could spread by vertical transmission and pose a great threat to both human and animal health; however, whether phage treatment might provide an optional strategy for controlling bacterial vertical infection remains unknown. Herein, we explored the effect of phage therapy on controlling the vertical transmission of Salmonella enterica serovar Gallinarum biovar Pullorum (S. Pullorum), a poultry pathogen that causes economic losses worldwide due to high mortality and morbidity. A Salmonella phage CKT1 with lysis ability against several S. enterica serovars was isolated and showed that it could inhibit the proliferation of S. Pullorum in vitro efficiently. We then evaluated the effect of phage CKT1 on controlling the vertical transmission of S. Pullorum in an adult broiler breeder model. The results demonstrated that phage CKT1 significantly alleviated hepatic injury and decreased bacterial load in the liver, spleen, heart, ovary, and oviduct of hens, implying that phage CKT1 played an active role in the elimination of Salmonella colonization in adult chickens. Additionally, phage CKT1 enabled a reduction in the Salmonella-specific IgG level in the serum of infected chickens. More importantly, the decrease in the S. Pullorum load on eggshells and in liquid whole eggs revealed that phage CKT1 effectively controlled the vertical transmission of S. Pullorum from hens to laid eggs, indicating the potential ability of phages to control bacterial vertical transmission.