Intensive antibiotic treatment of sows with parenteral crystalline ceftiofur and tulathromycin alters the composition of the nasal microbiota of their offspring

Abstract

The nasal microbiota plays an important role in animal health and the use of antibiotics is a major factor that influences its composition. Here, we studied the consequences of an intensive antibiotic treatment, applied to sows and/or their offspring, on the piglets' nasal microbiota. Four pregnant sows were treated with crystalline ceftiofur and tulathromycin (CT_sows) while two other sows received only crystalline ceftiofur (C_sows). Sow treatments were performed at D-4 (four days pre-farrowing), D3, D10 and D17 for ceftiofur and D-3, D4 and D11 for tulathromycin. Half of the piglets born to CT_sows were treated at D1 with ceftiofur. Nasal swabs were taken from piglets at 22-24 days of age and bacterial load and nasal microbiota composition were defined by 16 s rRNA gene qPCR and amplicon sequencing. Antibiotic treatment of sows reduced their nasal bacterial load, as well as in their offspring, indicating a reduced bacterial transmission from the dams. In addition, nasal microbiota composition of the piglets exhibited signs of dysbiosis, showing unusual taxa. The addition of tulathromycin to the ceftiofur treatment seemed to enhance the deleterious effect on the microbiota diversity by diminishing some bacteria commonly found in the piglets' nasal cavity, such as Glaesserella, Streptococcus, Prevotella, Staphylococcus and several members of the Ruminococcaceae and Lachnospiraceae families. On the other hand, the additional treatment of piglets with ceftiofur resulted in no further effect beyond the treatment of the sows. Altogether, these results suggest that intensive antibiotic treatments of sows, especially the double antibiotic treatment, disrupt the nasal microbiota of their offspring and highlight the importance of sow-to-piglet microbiota transmission.

Keywords: Nasal microbiota; antibiotics; bacterial transmission; piglets; sows.

Figure 1

Quantitative PCR of 16S rRNA gene in nasal swabs. A 16S rRNA gene quantity (pg) detected by qPCR in nasal swabs taken from sows before (Pre-antibiotic, in yellow) and after (Post-antibiotic, in purple) first administration of their respective antibiotic treatments: crystalline ceftiofur + tulathromycin sows (CT_sows) and crystalline ceftiofur sows (C_sows). Each dot corresponds to one animal. B 16S rRNA gene quantity (pg) detected by qPCR in nasal swabs from piglets of the groups under study: non-treated piglets born to ceftiofur + tulathromycin treated sows (CT_sowN_piglet, red); ceftiofur treated piglets born to ceftiofur + tulathromycin treated sows (CT_sowC_piglet, green); non-treated piglets born to ceftiofur treated sows (C_sowN_piglet, blue); and the reference group of age-matched farm piglets (grey). Each dot corresponds to one animal. Significant P values are shown in upper bars.

Figure 2

Comparison of the most abundant taxa in the study groups and healthy farms. Relative abundances (log scaled) of the top 15 most prevalent genera found in nasal cavities of piglets from the different groups of this study and in age-matched animals from farms from the studies of Correa-Fiz et al. [5, 8]. Genera have been labelled as found between the most abundant in farms, this study groups, or both. Farms are labelled withs their original ID from their respective studies. Abundances in samples from this study are shown per group: non-treated piglets born to ceftiofur + tulathromycin treated sows (CT_sowN_piglet); ceftiofur treated piglets born to ceftiofur + tulathromycin treated sows (CT_sowC_piglet); non-treated piglets born to ceftiofur treated sows (C_sowN_piglet).

Figure 3

Alpha and beta diversity analysis of the groups under study. Non-treated piglets born to ceftiofur + tulathromycin treated sows (CT_sowN_piglet, red); ceftiofur treated piglets born to ceftiofur + tulathromycin treated sows (CT_sowC_piglet, green); non-treated piglets born to ceftiofur treated sows (C_sowN_piglet, blue). A Alpha diversity boxplots estimated with Chao1 and Shannon indexes. Each dot represents a sample. Dots corresponding to outlier simples are coloured in black. B Beta diversity PCoA analysis computed with Bray–Curtis dissimilarity index, of the groups under study. Each dot represents a sample. Ellipses of confidence are calculated using Euclidean distances within the samples of each group.

Figure 4

Differently abundant ASVs between CT_sow and C_sow piglets. Top 5 most relatively abundant ASVs within all the differentials found with ANCOM-BC and DSFDR when comparing non-treated piglets born to ceftiofur + tulathromycin treated sows (CT_sowN_piglet, red) and non-treated piglets born to ceftiofur treated sows (C_sowN_piglet, blue). The abundances of these ASVs in ceftiofur treated piglets born to ceftiofur + tulathromycin treated sows (CT_sowC_piglet) are shown too (green). Dots corresponding to outlier samples are coloured in black. All the differently abundant ASVs are listed in Additional file 6.