Population Structure and Antimicrobial Resistance in Campylobacter jejuni and C. coli Isolated from Humans with Diarrhea and from Poultry, East Africa

Abstract

Campylobacteriosis and antimicrobial resistance (AMR) are global public health concerns. Africa is estimated to have the world's highest incidence of campylobacteriosis and a relatively high prevalence of AMR in Campylobacter spp. from humans and animals. Few studies have compared Campylobacter spp. isolated from humans and poultry in Africa using whole-genome sequencing and antimicrobial susceptibility testing. We explored the population structure and AMR of 178 Campylobacter isolates from East Africa, 81 from patients with diarrhea in Kenya and 97 from 56 poultry samples in Tanzania, collected during 2006-2017. Sequence type diversity was high in both poultry and human isolates, with some sequence types in common. The estimated prevalence of multidrug resistance, defined as resistance to >3 antimicrobial classes, was higher in poultry isolates (40.9%, 95% credible interval 23.6%-59.4%) than in human isolates (2.5%, 95% credible interval 0.3%-6.8%), underlining the importance of antimicrobial stewardship in livestock systems.

Keywords: Campylobacter coli; Campylobacter jejuni; Kenya; Tanzania; antimicrobial resistance; bacteria; campylobacteriosis; east Africa; enteric infections; humans; poultry; zoonoses.

Figure 1

Location of sampling sites in study of population structure and antimicrobial resistance in Campylobacter jejuni and C. coli isolated from humans with diarrhea and from poultry, East Africa, 2006–2017. A) Data collection sites in Lwak and Kibera in Kenya and Arusha and Kilimanjao in northern Tanzania. Inset shows location of Kenya and Tanzania in East Africa. B) Poultry farm locations sampled in Arusha and Kilimanjaro regions, northern Tanzania.

Figure 2

Minimum spanning tree population structure of Campylobacter jejuni and C. coli isolated from humans with diarrhea and from poultry from Kenya and Tanzania, 2006–2017 (human) or 2016–2017 (poultry), based on core genome multilocus sequence types profiles. A) Plot colored by host (human or poultry) with CC indicated in each node; B) plot colored by CC with sequence type indicated in each node. Core-genome multilocus sequence type allele differences are indicated on each branch. CC, clonal complex; UA, unassigned.

Figure 3

Minimum spanning tree of core-genome multilocus sequence types profiles from the 4 most prevalent 7-gene multilocus sequence type–based ST isolated from poultry in Tanzania, 2016–2017, in a study of Campylobacter jejuni and C. coli, East Africa. Each color represents a different farm, with the exception of 4 ST353 isolates from human cases (dark blue). Core genome multilocus sequence type allele differences are indicated on each branch. The 2 pairs of isolates from different farms with the lowest number of allele differences, belonging to ST8043 (24 allele differences) and ST2122 (38 allele differences) (shown in brown and light pink) were from 2 farms in the same location in Luongo, Moshi. One was an intensive indigenous farm (light pink isolates), and the other was an intensive broiler farm (brown isolates). ST, sequence type.

Figure 4

Distribution of different combinations of AMR in Campylobacter jejuni and C. coli human isolates from Kenya (top, n = 81) and poultry isolates from Tanzania (bottom, n = 97) in study of population structure and AMR in C. jejuni and C. coli isolated from humans with diarrhea and from poultry, East Africa, 2006–2017. The percentage of isolates resistant to each antimicrobial is given in the table to the right of each plot. All isolates were susceptible to gentamicin. The histogram represents proportion of isolates by antimicrobial resistance pattern. Black dots represent AMR and gray dots represent absence of AMR to the specific antimicrobial agent listed. Black lines join black dots to visualize patterns of AMR. AMP, ampicillin; AMR, antimicrobial resistance; Cipro, ciprofloxacin; Eryth, erythromycin; NA, nalidixic acid; SXT, trimethoprim/sulfamethoxazole; Tet, tetracycline.

Figure 5

Circular dendrogram showing, from outer to inner rings, AST in study of population structure and antimicrobial resistance in Campylobacter jejuni and C. coli isolated from humans with diarrhea and from poultry, East Africa, 2006–2017. Colored blocks indicate resistance (all isolates were susceptible to gentamicin so this ring is not included), resistome, clonal complex (CC), sequence type (ST), Campylobacter species, poultry sample number, farm type, host and isolate ID for isolates from Kenya and Tanzania, 2006–2017 (human) or 2016–2017 (poultry). Isolates from the same poultry sample that belonged to a different ST are highlighted (samples 15, 22, 35, and 45) using colored isolate identification labels. The resistome indicates detection of resistance genes (encoding for resistance to some aminoglycosides, β-lactam antimicrobials and tetracyclines) and alleles (encoding for resistance for fluoroquinolones in the gyrase A gene, and macrolides in the 23S rRNA gene). Clustering of antimicrobial resistance phenotypes and the resistome with some CCs and STs is evident. For example, multidrug resistance is observed in C. jejuni ST2122 and C. coli ST8043 isolates. Scale bar indicates number of core-genome multilocus-sequence typing allele differences. AST, antimicrobial sensitivity.