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Negligible Impact of Perinatal Tulathromycin Metaphylaxis on the Developmental Dynamics of Fecal Microbiota and Their Accompanying Antimicrobial Resistome in Piglets.

ABSTRACT: While the antimicrobial resistance profiles of cultured pathogens have been characterized in swine, the fluctuations in antimicrobial resistance genes (ARGs) associated with the developing gastrointestinal microbiota have not been elucidated. The objective of this study was to assess the impact of perinatal tulathromycin (TUL) metaphylaxis on the developmental dynamics of fecal microbiota and their accompanying antimicrobial resistome in pre-weaned piglets. Sixteen litters were given one of two treatments [control group (CONT; saline 1cc IM) and TUL group (TUL; 2.5 mg/kg IM)] directly after birth. Deep fecal swabs were collected at day 0 (prior to treatment), and again at days 5 and 20 post treatment. Shotgun metagenomic sequencing was performed on the extracted DNA, and the fecal microbiota structure and abundance of ARGs were assessed. Collectively, the swine fecal microbiota and their accompanying ARGs were diverse and established soon after birth. Across all samples, a total of 127 ARGs related to 19 different classes of antibiotics were identified. The majority of identified ARGs were observed in both experimental groups and at all-time points. The magnitude and extent of differences in microbial composition and abundance of ARGs between the TUL and CONT groups were statistically insignificant. However, both fecal microbiota composition and ARGs abundance were changed significantly between different sampling days. In combination, these results indicate that the perinatal TUL metaphylaxis has no measurable benefits or detriment impacts on fecal microbiota structure and abundance of ARGs in pre-weaned piglets.

SUBMITTER: Zeineldin MM

PROVIDER: S-EPMC6460945 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Bovine respiratory disease (BRD) is a leading cause of disease in feedlot and stocker calves with Mannheimia haemolytica (MH) as one of the most common etiologies. One of the most effective means of controlling BRD is through metaphylaxis, which involves administering antimicrobials to all animals at high risk of developing BRD. However, increasing prevalence of multidrug resistant (MDR) MH may reduce efficacy of metaphylaxis due to decreased susceptibility to drugs used for metaphylaxis. Primarily, this study aimed to determine the effect of tulathromycin metaphylaxis and subsequent BRD treatment on antimicrobial resistance (AMR) in MH isolated from stocker calves. Secondary objectives included evaluating the effect of metaphylaxis and treatment for BRD on animal health and comparing the genetic relationship of MH isolated. Crossbred beef heifers (n = 331, mean weight = 232, SD = 17.8 kg) at high risk for BRD were randomly assigned to receive tulathromycin metaphylaxis (META, n = 167) or not (NO META, n = 164). Nasopharyngeal swabs were collected for MH isolation, antimicrobial susceptibility testing and whole genome sequencing at arrival and 3 (WK3) and 10 (WK10) weeks later. Mixed-effects logistic regression was used to identify risk factors for isolation of MH and MDR MH (resistant to ≥3 antimicrobial drug classes) at 3 and 10 weeks, BRD morbidity, and crude mortality. Animals in the META group had higher odds of isolation of MDR MH at 3 weeks [OR (95% CI) = 13.08 (5-30.9), p < 0.0001] and 10 weeks [OR (95% CI) = 5.92 (1.34-26.14), p = 0.019] after arrival. There was no difference in risk of isolation of any MH (resistant or susceptible) between META and NO META groups at all timepoints. Animals in the NO META group had 3 times higher odds of being treated for BRD [WK3: OR (95% CI) = 3.07 (1.70-5.52), p = 0.0002; WK10: OR (95% CI) = 2.76 (1.59-4.80), p = 0.0002]. Antimicrobial resistance genes found within isolates were associated with integrative conjugative element (ICE) genes. Tulathromycin metaphylaxis increased risk of isolation of MDR MH and in this population, the increase in MDR MH appeared to be associated with ICE containing antimicrobial resistance genes for multiple antimicrobial classes. This may have important implications for future efficacy of antimicrobials for control and treatment of BRD.

Project description:Optimization of antimicrobial use in swine management systems requires full understanding of antimicrobial-induced changes on the developmental dynamics of gut microbiota and the prevalence of antimicrobial resistance genes (ARGs). The purpose of this study was to evaluate the impacts of early life antimicrobial intervention on fecal microbiota development, and prevalence of selected ARGs (ermB, tetO, tetW, tetC, sulI, sulII, and blaC TX-M) in neonatal piglets. A total of 48 litters were randomly allocated into one of six treatment groups soon after birth. Treatments were as follows: control (CONT), ceftiofur crystalline free acid (CCFA), ceftiofur hydrochloride (CHC), oxytetracycline (OTC), procaine penicillin G (PPG), and tulathromycin (TUL). Fecal swabs were collected from piglets at days 0 (prior to treatment), 5, 10, 15, and 20 post treatment. Sequencing analysis of the V3-V4 hypervariable region of the 16S rRNA gene and selected ARGs were performed using the Illumina Miseq platform. Our results showed that, while early life antimicrobial prophylaxis had no effect on individual weight gain, or mortality, it was associated with minor shifts in the composition of fecal microbiota and noticeable changes in the abundance of selected ARGs. Unifrac distance metrics revealed that the microbial communities of the piglets that received different treatments (CCFA, CHC, OTC, PPG, and TUL) did not cluster distinctly from CONT piglets. Compared to CONT group, PPG-treated piglets exhibited a significant increase in the relative abundance of ermB and tetW at day 20 of life. Tulathromycin treatment also resulted in a significant increase in the abundance of tetW at days 10 and 20, and ermB at day 20. Collectively, these results demonstrate that the shifts in fecal microbiota structure caused by perinatal antimicrobial intervention are modest and limited to particular groups of microbial taxa. However, early life PPG and TUL intervention could promote the selection of ARGs in herds. While additional investigations are required to explore the consistency of these findings across larger populations, these results could open the door to new perspectives on the utility of early life antimicrobial administration to healthy neonates in swine management systems.

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Negligible Impact of Perinatal Tulathromycin Metaphylaxis on the Developmental Dynamics of Fecal Microbiota and Their Accompanying Antimicrobial Resistome in Piglets.

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