Bovine and Pig Carcasses as a Source of Campylobacter in Poland: A Reservoir for Antimicrobial-Resistant Campylobacter coli

Abstract

Campylobacter is one of the most common causes of foodborne bacterial infections worldwide. Why poultry has been shown to be one of the most significant sources of these bacteria, ruminants, especially cattle, are also responsible for a high number of human Campylobacter jejuni, and to a lesser extent Campylobacter coli, infections. In this study, bovine and pig carcasses in Poland were investigated for the presence of Campylobacter and for their antimicrobial resistance. A total of 204 swabs from bovine carcasses and 355 swab samples from pig carcasses were tested during 2014–2018. Campylobacter was identified in 129 (36.3%) of the pig and in 11 (5.4%) of the bovine carcasses, respectively. The pig isolates were classified as C. coli (121; 34.1%) or C. jejuni (8; 2.3%), whereas the bovine Campylobacter were identified either as C. jejuni (8; 3.9% isolates) or C. coli (3; 1.5% strains). Resistance of the isolates (n = 140) to erythromycin, ciprofloxacin, nalidixic acid, streptomycin, and tetracycline revealed that the vast majority of C. coli was resistant to streptomycin (106 isolates; 85.5%), tetracycline (97; 78.2%), nalidixic acid (90; 72.6%), and ciprofloxacin (88; 71.0%). Among C. jejuni isolates (n = 16) the resistance rates to all antibiotics were lower than in C. coli, irrespective of the origin. A total of 74 of 121 (61.2%) C. coli isolates from the pig carcasses and one of three such isolates from the bovine samples were multiresistant. Most of the C. coli (64 isolates; 85.3%) had the ciprofloxacin+nalidixic acid+streptomycin+tetracycline resistance profile. The results suggest that pig and bovine carcasses may be an underestimated reservoir of Campylobacter, especially for C. coli in pigs. The high antimicrobial resistance rates of such strains to streptomycin, quinolones, and tetracyclines highlight the need for monitoring of these bacteria in such food and food products.

Introduction

C ampylobacter, especially Campylobacter jejuni, is among the most common causes of bacterial foodborne infections worldwide (Kaakoush et al., 2015; Tresse et al., 2017). Poultry has been shown to be the most important source of these bacteria and the main transmission route of Campylobacter to humans is the handling of contaminated food, especially of chicken meat (Humphrey et al., 2007; Kaakoush et al., 2015; Tresse et al., 2017). However, it has been described that ruminants, especially cattle, are also responsible for a high number of human C. jejuni (and to a lesser extent—Campylobacter coli) infections (Mughini Gras et al., 2012; An et al., 2018; Thépault et al., 2018).

Campylobacter has also been identified in pigs and pig carcasses that are often contaminated with feces at the slaughter and processing facilities during the evisceration process, which resulted with the presence of the bacteria in pork meat (Humphrey et al., 2007; Quintana-Hayashi and Thakur, 2012; Campos Calero et al., 2018; Rossler et al., 2019). However, compared to samples of chicken origin, the prevalence of Campylobacter on pig and bovine carcasses as well as in pork and beef meat is not broadly documented, although a high incidence of these bacteria on meat and meat products of pig and cattle origins was found (Pearce et al., 2003; Llarena et al., 2014; Wysok et al., 2015; Narvaez-Bravo et al., 2017; Signorini et al., 2018; Thépault et al., 2018).

Therefore, additional studies on the prevalence and antimicrobial resistance of Campylobacter on bovine and pig carcasses are needed to assess the risk of infection for consumers.

An increasing antimicrobial resistance among Campylobacter isolates has been observed worldwide over the last few years (Garcia-Migura et al., 2014; EFSA and ECDC, 2019). This trend is due, at least in a part, to the wide use of these substances in veterinary medicine and agriculture (Garcia-Migura et al., 2014; EMA, 2018).

Most Campylobacter infection cases in humans are usually self-limiting and do not need any antibiotic treatment. However, in very young or elderly patients, in pregnant women, and in infections with complications such as bacteremia, reactive arthritis, hemolytic uremic syndrome, meningitis, septicemia, and Guillain-Barré syndrome, antibiotics, especially macrolides (erythromycin) or fluoroquinolones (ciprofloxacin), are necessary (Kaakoush et al., 2015). Thus, the monitoring of antimicrobial resistance of Campylobacter isolated from food animals and food of animal origin is highly relevant to the design of control measures and the prevention of consumer’ infection with these bacteria.

The aims of the present study were (1) to test Campylobacter contamination of bovine and pig carcasses during 2014–2018 and (2) to investigate the antimicrobial resistance of the obtained Campylobacter isolates.

Materials and Methods

Samples

A total of 204 swabs from bovine carcasses and 355 samples from pig carcasses were collected during 2014–2018 by official veterinarians in commercial abattoirs. The slaughterhouses were located in 14 out of 16 voivodeships (administrative provinces) of Poland, and the number of samples was calculated based on the number of cattle and pigs slaughtered in each voivodeship according to the monitoring plan for Campylobacter established by the Polish National Reference Laboratory (Supplementary Figs. S1 and S2).

The samples were collected from fresh carcasses according to the protocol described previously (Wieczorek and Osek, 2014). In brief, the carcasses were swabbed with sponges in the brisket area (100 cm²) after exsanguination of the animals. The sterile sponges were rubbed 10 times vertically and 10 times horizontally, and then placed in plastic bags, tagged, and immediately transported to the laboratory in chilled conditions (at 1–8°C).

Campylobacter isolation

Campylobacter bacteria were isolated essentially as described previously (Wieczorek and Osek, 2014). In brief, all four sponges used for swabbing one carcass were placed together into 200 mL of Maximum Recovery Diluent (0.1% peptone, 0.85% NaCl; Oxoid, Basingstoke, United Kingdom), stomached for 3 min, and centrifuged at 1000 g for 15 min at 5°C. The pellet was resuspended in 100 mL of selective enrichment Bolton broth (Oxoid) and cultured for 48 h at 41.5°C under microaerobic conditions generated with a CampyGen Atmosphere Generation System (Oxoid). Then, the culture was plated on Karmali agar with Campylobacter selective supplement (Oxoid) and Campylobacter blood-free agar (Oxoid) with CCDA-selective supplement (Oxoid) followed by reincubation under the same conditions. The plates were examined for morphologically typical Campylobacter colonies and from each sample, one presumptive Campylobacter isolate was confirmed and identified as C. jejuni or C. coli with PCR, as described by Wang et al. (2002). The isolated bacteria from Karmali agar were stored in cryotubes (Oxoid) at −80°C for antimicrobial resistance analysis.

Antimicrobial resistance

The antimicrobial resistance of the C. jejuni and C. coli isolates was tested as recommended by the European Union Reference Laboratory for Antimicrobial Resistance (EURL-AR; www.eurl-ar.eu) and the European Commission (2013). The following antimicrobials were used: erythromycin (ERY), ciprofloxacin (CIP), nalidixic acid (NAL), streptomycin (STR), and tetracycline (TET). The analyses were performed as described previously (Wieczorek et al., 2013b). A total of 11 and 129 Campylobacter spp. from bovine and pig carcasses, respectively, were used. The number of isolates belonging to each Campylobacter species and obtained from different animal carcasses is shown in Table 1. A microbroth dilution method was used to establish the minimum inhibitory concentrations (MICs) of the Campylobacter isolates to the antimicrobials with Sensititre^® custom susceptibility plates, EUCAMP (Trek Diagnostic Systems, East Grinstead, United Kingdom). The obtained results were evaluated using a Vizion system (Trek Diagnostics). The antimicrobials and cutoff values used for the interpretation of the MIC results were in accordance with the European Committee on Antimicrobial Susceptibility Testing and the EURL-AR recommendations (Sifré et al., 2015; www.eucast.org). Multidrug resistance of the isolated Campylobacter was defined as resistance to at least three of the classes of antimicrobials used in the study (Magiorakos et al., 2012).

Table 1.

Prevalence of Campylobacter spp. in Pig and Bovine Carcasses Tested During the Study

Year	No. of samples positive/tested (% of positive; 95% CI)		No. of samples positive (% of total number of samples; 95% CI) for:
	Pig	Bovine	Campylobacter jejuni		Campylobacter coli
	Pig	Bovine	Pig	Bovine	Pig	Bovine
2014	27/75 (36.0; 25.2–47.9)	3/44 (6.8; 1.4–18.7)	1 (1.3; 0.0–7.2)	3 (6.8; 1.4–18.7)	26 (34.7; 24.0–46.5)	0 (0.0; 0.0–8.0)
2015	23/68 (33.8; 22.8–46.3)	0/40 (0.0; 0.0–8.8)	1 (1.5; 0.0–7.9)	0 (0.0; 0.0–8.8)	22 (32.4; 21.5–44.8)	0 (0.0; 0.0–8.8)
2016	25/70 (35.7; 24.6–48.1)	4/40 (10.0; 2.8–23.7)	2 (2.9; 0.3–9.9)	2 (5.0; 0.6–16.9)	23 (32.9; 22.1–45.1)	2 (5.0; 0.6–16.9)
2017	30/68 (44.1; 32.1–56.7)	1/39 (2.6; 0.1–13.5)	1 (1.5; 0.0–7.9)	0 (0.0; 0.0–9.0)	29 (42.6; 30.7–55.2)	1 (2.6; 0.1–13.5)
2018	24/74 (32.4; 22.0–44.3)	3/41 (7.3; 1.5–19.9)	3 (4.1; 0.8–11.4)	3 (7.3; 1.5–19.9)	21 (28.4; 18.5–40.1)	0 (0.0; 0.0–8.6)
Total	129/355 (36.3; 31.3–41.6)	11/204 (5.4; 2.7–9.4)	8 (2.3; 1.0–4.4)	8 (3.9; 1.7–7.6)	121 (34.1; 29.2–39.3)	3 (1.5; 0.3–4.2)

95% CI, 95% confidence level.

Statistical analysis

The statistical analyses based on logistic regression models and chi-square tests with the appropriate correction due to group size were performed as described previously (Wieczorek et al., 2020). The odds ratios (OR) were also calculated. The accepted significance level was alpha = 0.05. For statistical data analysis TIBCO Software Inc., Statistica (data analysis software system) v. 13 was used.

Results

Prevalence of Campylobacter

Research on the prevalence of Campylobacter-positive bovine and pig carcasses tested during 2014–2018 has shown that 5.4% and 36.3% of samples were contaminated, respectively. Campylobacter spp. was identified in 36.3% of swab samples from pig carcasses (Table 1). The prevalence of the bacteria ranged from a minimum of 32.4% in 2018 to a maximum of 44.1% in 2017, but the difference between these percentages was not statistically significant (p = 0.15; Pearson chi-square test). Various logistic regression models also did not show any statistically significant relationship between the year and the prevalence of Campylobacter spp. The Campylobacter isolates were classified as C. coli (34.1% of the total number of samples tested) or C. jejuni (2.3%) and the difference between these percentages was statistically significant (p < 0.0001; Pearson chi-square test). The calculated odds ratio (OR = 22.4) indicated a more than 22 times greater chance of obtaining a C. coli result than a C. jejuni.

At the same time, only 5.4% of bovine carcasses were contaminated with Campylobacter spp. (Table 1). The prevalence of Campylobacter spp. ranged from one isolate in 2017 to four in 2016. In 2015, none of the bovine carcass swabs was positive for Campylobacter bacteria. The bovine isolates were identified either as C. coli (1.5% of strains) or C. jejuni (3.9% of isolates), and this difference was not statistically significant (p = 0.13; V-square test).

Antimicrobial resistance

A total of 140 Campylobacter spp. from pig and bovine carcasses were tested toward antimicrobial resistance to five antimicrobials (Table 2). The results revealed that the vast majority of the C. coli was resistant to streptomycin (85.5%). Furthermore, most of such isolates of both pig and bovine carcass origin were resistant to tetracycline (78.2%), nalidixic acid (72.6%), and ciprofloxacin (71.0%), respectively (Table 2). Some of the C. coli (9.9%) recovered from pig carcasses were resistant to erythromycin, and only this group of isolates was resistant to this antimicrobial among all campylobacters tested.

Table 2.

Antimicrobial Resistance of Campylobacter Isolated from Pig and Bovine Carcasses During 2014–2018

Antimicrobial	No. (%; 95% CI) of resistant isolates
	Pig carcasses (n = 129)		Bovine carcasses (n = 11)
	Campylobacter jejuni (n = 8)	Campylobacter coli (n = 121)	C. jejuni (n = 8)	C. coli (n = 3)
CIP	2 (25.0; 3.2–65.1)	85 (70.2; 61.3–78.2)	3 (37.5; 8.5–75.5)	3 (100; 29.2–100)
NAL	2 (25.0; 3.2–65.1)	87 (71.9; 63.0–79.7)	3 (37.5; 8.5–75.5)	3 (100; 29.2–100)
STR	1 (12.5; 0.3–52.7)	104 (86.0; 78.5–91.6)	0 (0; 0–36.9)	2 (66.7; 9.4–99.2)
TET	2 (25.0; 3.2–65.1)	96 (79.3; 71.0–86.2)	1 (12.5; 0.3–52.7)	1 (33.3; 0.8–90.6)
ERY	0 (0; 0–36.9)	12 (9.9; 5.2–16.7)	0 (0; 0–36.9)	0 (0; 0–70.8)

95% CI, 95% confidence level; CIP, ciprofloxacin; ERY, erythromycin; NAL, nalidixic acid; STR, streptomycin; TET, tetracycline.

Among the C. jejuni isolates (n = 16), the antibiotic resistance rates were lower than in the C. coli (n = 124) and these differences were statistically significant to CIP (p = 0.0016; V-square test), NAL (p = 0.0009; V-square test), and STR and TET (p < 0.0001; chi-square test with Yates' correction), but not statistically significant to ERY (p = 0.4083; chi-square test with Yates' correction).

Multiresistance of Campylobacter

Among all 16 C. jejuni tested, none of the isolates displayed a multiantimicrobial resistance pattern, that is, resistance to at least three classes of antimicrobials. Altogether, 61.2% of C. coli of pig carcass origin and one isolate from bovine samples were resistant to at least three of the antimicrobials used in the study (Table 3). The vast majority of multiresistant C. coli (85.3% isolates) had the CIP+NAL+STR+TET resistance profile. Such isolates were predominant among all C. coli recovered from pig carcasses (52.1% isolates). Interestingly, 6.6% of isolates from pig carcasses were resistant to all five antimicrobials tested.

Table 3.

Antimicrobial Multiresistance Profiles of Campylobacter coli Isolated from Pig and Bovine Carcasses

Antimicrobial resistance profile	No. (%) of resistant isolates
Antimicrobial resistance profile	Pig carcasses (n = 121)	Bovine carcasses (n = 3)
ERY+STR+TET	1 (0.8%)
NAL+STR+TET	1 (0.8%)
CIP+NAL+STR+TET	63 (52.1%)	1 (33.3%)
ERY+NAL+STR+TET	1 (0.8%)
ERY+CIP+NAL+STR+TET	8 (6.6%)
Total	74 (61.2%)	1 (33.3%)

CIP, ciprofloxacin; ERY, erythromycin; NAL, nalidixic acid; STR, streptomycin; TET, tetracycline.

Discussion

The analogous previous studies performed in Poland revealed that from 11.7% to 14.7% and from 26.0% to 30.4% of bovine and pig carcasses were positive for Campylobacter bacteria, respectively (Wieczorek and Osek, 2014, 2018). Identification of the bacterial species revealed that C. jejuni was present in from 57.1% to 59.5% of bovine and from 13.7% to 24.7% of pig positive samples, respectively (Wieczorek and Osek, 2014, 2018). Some of these C. jejuni isolates recovered from the carcasses during 2014–2016 were also used in the present investigation toward antimicrobial resistance (Wieczorek and Osek, 2018). In the current study, it was found that pig carcasses were much more often contaminated with C. coli than with C. jejuni (93.8% and 6.2% of Campylobacter-positive samples, respectively). However, in the investigation performed during 2009–2016, pig carcasses were only tested toward C. jejuni; therefore, it was not possible to compare the C. coli-positive rates during both periods (Wieczorek and Osek, 2018). In the case of the bovine carcasses tested in the current period, only 11 samples were Campylobacter-positive, mainly for C. jejuni (8 carcasses; 3.9% of total samples tested), whereas during the years 2009–2013 and 2009–2016, the prevalence rates of such C. jejuni-positive carcasses were 8.4% and 6.9%, respectively (Wieczorek and Osek, 2014, 2018). In relationship to C. coli, such values for bovine carcasses were 1.5% (current study) and 6.3% (previous investigation), respectively (Wieczorek and Osek, 2014). In our earlier studies on the prevalence of Campylobacter along the beef food chain only 11 out of 406 (2.7%) bovine carcasses were positive, either for C. jejuni (7 isolates) or C. coli (4 samples) (Wieczorek et al., 2013a). It seems that pig and bovine carcasses in Poland have been contaminated with Campylobacter during recent years at a relatively high rate, especially from pig origin. This may be due to the fact that none of the official Campylobacter control programs in pigs and cattle nor in their carcasses was applied during this period.

There are no other similar studies on the prevalence of Campylobacter on pig and bovine carcasses in Poland performed by other authors. Recently, Andrzejewska et al. (2019) identified 10.9% of Campylobacter-positive samples from pork and 12.7% from beef meat samples. Furthermore, Korsak et al. (2015) found that 10.6% and 10.1% of pork and beef meat samples at the retail level, respectively, were contaminated with these bacteria. However, it is hard to compare these results with the percentages of the positive respective carcasses obtained in the present study.

There are also rather few studies on the prevalence of Campylobacter on pig and bovine carcasses performed in other countries. Pearce et al. (2003) identified in the United States 20.5% of swine carcasses contaminated with Campylobacter, mainly with C. coli (73.5% of positive samples). Abley et al. (2012) found 100% of pig carcasses contaminated with Campylobacter in the same country, with a rather high level of 1.7 × 10³ colony-forming unit of the bacteria per half carcass.

In a survey in Belgium, 3.3% of 60 beef carcasses were positive for Campylobacter, with C. jejuni being the predominant species (75.0% of positive samples) (Ghafir et al., 2007). A much lower contamination rate of bovine carcasses with Campylobacter was identified in Tanzania where 24 out of 253 (9.5%) were positive for these bacteria, mainly for C. coli (62.5% of positive samples) (Kashoma et al., 2016).

It has been previously shown that hides and feces of food-producing animals were the major sources of bacterial pathogens during slaughter and processing (Abley et al., 2012; An et al., 2018; Thépault et al., 2018; Inglis et al., 2020). The differences in the prevalence of Campylobacter found among various studies may result from differences in the study size, sampling and bacterial detection methods, geographical region, and time of the year (Stanley et al., 1998; Shange et al., 2019). The results of the present and other studies clearly indicate that pork and beef may be contaminated with Campylobacter and so play a role as a potential source of these bacteria for consumers. On the contrary, such bacterial sources, especially pig carcasses and pork meat, are often more positive for C. coli than for C. jejuni, which was also identified in the current investigation (Mughini Gras et al., 2012; An et al., 2018; Thépault et al., 2018; Rossler et al., 2019). It has been previously described that C. coli seems to be less pathogenic for humans compared to C. jejuni, but it can also be a cause of human infections (Gillespie et al., 2002; Janssen et al., 2008; Burnham and Hendrixson, 2018). According to a recent EFSA zoonotic report, only 719 confirmed campylobacteriosis cases were noted in Poland in 2019; however, the Campylobacter species were not determined (EFSA, 2019). One can speculate whether such a low number of infections in our country was due to the less pathogenic C. coli which was currently found to be predominant in pig carcasses.

The Campylobacter isolates from pig and bovine carcasses origin identified in the current study were most commonly resistant to streptomycin (76.4% of all isolates) followed by tetracycline (71.4%), nalidixic acid (67.9%), and ciprofloxacin (66.4%). High resistance rates of Campylobacter, especially of C. coli, to these antimicrobials were previously found by many authors (Smith and Fratamico, 2010; Ge et al., 2013; Iovine, 2013; Garcia-Migura et al., 2014). Other studies also indicated that Campylobacter of pig and cattle origin (isolated either from live animals or carcasses) were highly resistant to (fluoro)quinolones and, to a lesser extent, to tetracycline (Quintana-Hayashi and Thakur, 2012; Kashoma et al., 2016; Cha et al., 2017; Karikari et al., 2017; Kempf et al., 2017; Premarathne et al., 2017; Andrzejewska et al., 2019; Meistere et al., 2019; Ocejo et al., 2019). Our own previous research on the antimicrobial resistance of C. jejuni from pig and bovine carcasses revealed that such isolates were resistant to quinolones and tetracycline, either at a lower (1.5% resistant to TET) or a higher level (52.3% to CIP and 31.8% to TET) (Wieczorek et al., 2013a; Wieczorek and Osek, 2018). It was suggested that the prevalence of quinolone- and tetracycline-resistant Campylobacter isolates may be due to the broad use of these antimicrobials in food animal production for therapeutic purposes (Iovine, 2013). As shown in a recent European Medicines Agency (EMA) report, in Poland, 9.7 mg of fluoroquinolones per population correction unit (PCU) were sold for veterinary use; a much higher amount than the average for 30 other European countries (2.7 mg/PCU) (EMA, 2018). In the case of tetracycline, the corresponding values were similar, that is, 41.5 mg/PCU in Poland and 40.3 mg/PCU in other European countries, respectively.

During the present study 9.9% of C. coli of pig carcass origin were resistant to erythromycin—one of the drugs of choice used for the treatment of Campylobacter infections in humans. Erythromycin-resistant C. coli were also identified in other countries with the mean rate of 15.6% as reported in the recent European Union antimicrobial report (EFSA and ECDC, 2019). Identification of resistant Campylobacter spp., especially C. coli, in food animals (cattle and pigs) was also noted in several European countries. According to the recent EFSA report, 52.3% of such isolates from fattening pigs were resistant to ciprofloxacin and nalidixic acid (EFSA and ECDC, 2019). Furthermore, 9.7% of C. coli from the same animals displayed simultaneous resistance to the two most important therapeutic compounds, CIP and ERY. In the present study, 6.6% of such resistant isolates were identified among C. coli of pig carcass origin. The presence of such isolates along the food chain is important from a public health point of view because erythromycin is one of the two critically important antimicrobials for the treatment of Campylobacter infections in humans (WHO, 2019). Furthermore, it has been noted that C. coli is being increasingly isolated from people with Campylobacter infection cases (10.5% of such strains in 2018) (EFSA, 2019).

Conclusions

The results of the present study show a relatively high level of contamination of pig and, to a lesser extent, bovine carcasses with Campylobacter, especially with C. coli. This suggests that these food animals may be an underestimated reservoir for Campylobacter. However, C. coli seems to be less pathogenic for humans than C. jejuni with the result being that most detected campylobacteriosis cases worldwide are due to C. jejuni, which is contrary to the results obtained from food isolates. On the contrary, the high resistance rates of C. coli strains to streptomycin, quinolones, and tetracyclines highlight the need for monitoring of this Campylobacter species in bovine and pig carcasses and their food products. The identification of C. coli resistant to erythromycin, the drug of choice for the treatment of Campylobacter infections in humans, calls for implementation of specific control monitoring procedures to determine the risk factor for the emergence of erythromycin-resistant C. coli.

Footnotes

Acknowledgments

The authors thank Beata Lachtara for technical assistance in laboratory analyses.

Disclosure Statement

No competing financial interests exist.

Funding Information

This study was financed by the Polish Government under the multiannual monitoring program, Decision 229/2013 of December 31, 2013.

Supplementary Material

Supplementary Figure S1

Supplementary Figure S2

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