Genomic Relatedness, Antibiotic Resistance and Virulence Traits of Campylobacter jejuni HS19 Isolates From Cattle in China Indicate Pathogenic Potential

Abstract

Although campylobacteriosis is a zoonotic foodborne illness, high-risk isolates from animal sources are rarely characterized, and the pathogenic potential of zoonotic strains remains an obstacle to effective intervention against human infection. HS19 has been acknowledged as a maker serotype represented by Campylobacter jejuni (C. jejuni) isolates from patients with post-infection Guillain-Barré syndrome (GBS), which is circulation in developed countries. However, a previous serotype epidemiological study of C. jejuni isolates in an animal population revealed that HS19 was also prevalent in isolates from cattle in China. In this study, to investigate the hazardous potential of zoonotic strains, 14 HS19 isolates from cattle were systematically characterized both by genotype and phenotype. The results showed that all of these cattle isolates belonged to the ST-22 complex, a high-risk lineage represented by 77.2% HS19 clinical isolates from patients worldwide in the PubMLST database, indicating that the ST-22 complex is the prominent clonal complex of HS19 isolates, as well as the possibility of clonal spread of HS19 isolates across different regions and hosts. Nevertheless, these cattle strains clustered closely with the HS19 isolates from patients, suggesting a remarkable phylogenetic relatedness and genomic similarity. Importantly, both tetracycline genes tet(O) and gyrA (T86I) reached a higher proportional representation among the cattle isolates than among the human clinical isolates. A worrying level of multidrug resistance (MDR) was observed in all the cattle isolates, and two MDR profiles of the cattle isolates also existed in human clinical isolates. Notably, although shared with the same serotype HS19 and sequence type ST-22, 35.7% of cattle isolates induced severe gastrointestinal pathology in the IL-10–/– C57BL/6 mice model, indicating that some bacteria could change due to host adaptation to induce a disease epidemic, thus the associated genetic elements deserve further investigation. In this study, HS19 isolates from cattle were first characterized by a systematic evaluation of bacterial genomics and in vitro virulence, which improved our understanding of the potential zoonotic hazard from food animal isolates with high-risk serotypes, and provided critical information for the development of targeted C. jejuni mitigation strategies.

Evidence of potential Campylobacter jejuni zooanthroponosis in captive macaque populations

“…A very high proportion of monkey isolates (95.4 %) were putatively resistant to ciprofloxacin. This is comparable to the levels observed among isolates from human infections in Taiwan (2016-2019; 91.1 %) [71] and Beijing (2017-2018; 94.50 %) [65], and livestock animals in China [30], Europe, and many other countries [72].…”

“…Increasing genomic surveillance has been informative for identifying infection sources [25][26][27][28] and describing the virulence profiles of isolates. This ranges from strains predominantly linked to asymptomatic infection [26] to those causing multidrug-resistant (MDR) infections [29,30], and serious post-infection sequelae including Guillain-Barré syndrome (GBS) [31] and irritable bowel disease [32]. Various animal infection models have been used to further understanding of Campylobacter virulence, including Galleria [33], mouse [30,34], piglet [35] and monkey systems [36].…”

Correlation between Multilocus Sequence Typing and Antibiotic Resistance, Virulence Potential of Campylobacter jejuni Isolates from Poultry Meat

“…Various studies on C. jejuni suggested the high genetic and phenotypic diversity, which indicated that not all isolates or genetic lineages pose equal risks to human health [ 14 , 15 , 16 ]. Isolates of different subgroups may exhibit diverse biological characteristics.…”

Zoonotic Transmission of Campylobacter jejuni to Caretakers From Sick Pen Calves Carrying a Mixed Population of Strains With and Without Guillain Barré Syndrome-Associated Lipooligosaccharide Loci

“…These studies have been performed in Africa [Nigeria ( Ngulukun et al, 2016 ), Ethiopia ( Nigatu et al, 2015 ; Hagos et al, 2021 ), South Africa ( Karama et al, 2020 )], Eastern Asia [China ( Ju et al, 2018 ; Zang et al, 2021a ), Japan ( Ono, 2013 ; Mori et al, 2015 ; Kiatsomphob et al, 2019 ), Malaysia ( Premarathne et al, 2017 ), South Korea ( Dong et al, 2016 ; An et al, 2018 )], Western Asia [Iraq ( Khalifa et al, 2013a , b ; Al-Edany et al, 2015 ) and India ( Rajagunalan et al, 2014 )], Europe [Austria ( Klein-Joebstl et al, 2016 ), France ( Thepault et al, 2018 ), Italy ( Bianchini et al, 2014a , b ), Latvia ( Meistere et al, 2019 ; Terentjeva et al, 2019 ), Lithuania ( Ramonaite et al, 2017 ; Aksomaitiene et al, 2019 ), Poland ( Wieczorek and Osek, 2018 ), Spain ( Ocejo et al, 2019 ), Sweden ( Hansson et al, 2021 ), New Zealand ( Rapp et al, 2012 ; Irshad et al, 2016 )], and North America [Canada ( Webb et al, 2018 ; Farfan et al, 2019 ; Inglis et al, 2020 ), and the United States ( Cha et al, 2016 ; Tang et al, 2017 )].…”

“…In addition to LOS, some heat stable (HS) Penner serotypes of C. jejuni , derived from the capsule, have been associated with the development of GBS ( Poly et al, 2011 ; Heikema et al, 2015 ; Poly et al, 2015 ; Liang et al, 2016 ). A survey by Zang et al (2021a , b) found such serotypes prevalent in livestock in China, including in cattle.…”