Genomic analysis of group B Streptococcus from milk demonstrates the need for improved biosecurity: a cross-sectional study of pastoralist camels in Kenya

Abstract

Background Streptococcus agalactiae (Group B Streptococcus, (GBS)) is the leading cause of mastitis (inflammation of the mammary gland) among dairy camels in Sub-Saharan Africa, with negative implications for milk production and quality and animal welfare. Camel milk is often consumed raw and presence of GBS in milk may pose a public health threat. Little is known about the population structure or virulence factors of camel GBS. We investigated the molecular epidemiology of camel GBS and its implications for mastitis control and public health. Results Using whole genome sequencing, we analysed 65 camel milk GBS isolates from 19 herds in Isiolo, Kenya. Six sequence types (STs) were identified, mostly belonging to previously described camel-specific STs. One isolate belonged to ST1, a predominantly human-associated lineage, possibly as a result of interspecies transmission. Most (54/65) isolates belonged to ST616, indicative of contagious transmission. Phylogenetic analysis of GBS core genomes showed similar levels of heterogeneity within- and between herds, suggesting ongoing between-herd transmission. The lactose operon, a marker of GBS adaptation to the mammary niche, was found in 75 % of the isolates, and tetracycline resistance gene tet(M) in all but two isolates. Only the ST1 isolate harboured virulence genes scpB and lmb, which are associated with human host adaptation. Conclusions GBS in milk from Kenyan camel herds largely belongs to ST616 and shows signatures of adaptation to the udder. The finding of similar levels of within- and between herd heterogeneity of GBS in camel herds, as well as potential human-camel transmission highlights the need for improved internal as well as external biosecurity to curb disease transmission and increase milk production.

Investigation of extramammary sources of Group B Streptococcus reveals its unusual ecology and epidemiology in camels

“…The phylogenetic analysis revealed distinct herd clusters, reflecting how ranches are relatively closed management systems in comparison to traditional pastoral herds. This outcome is quite distinct from previous results for milk isolates from traditional pastoralist herds, where highly similar strains were identified in multiple herds [39]. Camel herdsmen working on ranches visit each other and ranch camel herds and other local sedentary camel herds in Laikipia are not strictly separated from each other.…”

“…We found a high prevalence of GBS on the nasal mucosa of apparently healthy animals (27%), similar to the findings by Younan and Bornstein [13], but in contrast to the low prevalence described in a different study in northern Kenya [38]. Furthermore, isolates from the nasal mucosa showed a high level of genetic diversity, with isolates belonging to all STs identified in the study, with the exception of ST616, an ST which is significantly associated with the mammary gland [14,39]. These findings suggest that nasal colonisation of GBS in healthy camels is common, in contrast to the situation in humans and cattle.…”

“…Only four of ten GBS milk isolates belonged to ST616, which has previously been associated with mastitis [14,39]. The remaining milk isolates belonged to STs that were predominantly found in extramammary sources.…”

“…The association between specific GBS types and intramammary infection was thought to be due to the presence of the lactose operon (Lac.2), both in cattle [25,47,49] and in camels [39]. In a study on camels from a different region in Kenya and with a different production system, more than 80% of GBS isolates from milk harboured Lac.2 [39].…”

The landscape of antimicrobial resistance in the neonatal and multi-host pathogen group B Streptococcus: review from a One Health perspective

“…In the medical literature, host adaptation is mostly considered in the context of host age, i.e., pediatric vs. adult GBS ( Raabe and Shane, 2019 ; Watkins et al, 2019 ), but GBS is also a cause of infectious diseases among food-producing animals, including cattle ( Pinto et al, 2013 ; Cobo-Angel et al, 2019 ), fishes ( Delannoy et al, 2013 ; Leal et al, 2019 ) and camels ( Fischer et al, 2013 ; Seligsohn et al, 2021b ) and it has been detected in companion animals ( Maeda et al, 2022 ), laboratory animals ( Bodi Winn et al, 2018 ), and wildlife ( Bowater et al, 2012 ). There is evidence for GBS transmission between humans and animals from evolutionary ( Barkham et al, 2019 ; Richards et al, 2019 ; Crestani et al, 2021 ) as well as epidemiological studies ( Kalimuddin et al, 2017 ; Sørensen et al, 2019 ; Seligsohn et al, 2021a ) with transmission via multiple routes and in both directions ( Botelho et al, 2018a ; Crestani et al, 2021 ). The frequency of such transmission events, whether through direct contact, food, or the environment, is poorly known ( Botelho et al, 2018a ).…”