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Review

A Review on the Prevalence of Arcobacter in Aquatic Environments

by
Rajani Ghaju Shrestha
1,2,
Yasuhiro Tanaka
3 and
Eiji Haramoto
1,*
1
Interdisciplinary Center for River Basin Environment, University of Yamanashi, 4-3-11 Takeda, Kofu 400-8511, Yamanashi, Japan
2
Division of Sustainable Energy and Environmental Engineering, Osaka University, 1-1 Yamadaoka, Suita 565-0871, Osaka, Japan
3
Department of Environmental Sciences, University of Yamanashi, 4-4-37 Takeda, Kofu 400-8510, Yamanashi, Japan
*
Author to whom correspondence should be addressed.
Water 2022, 14(8), 1266; https://doi.org/10.3390/w14081266
Submission received: 11 March 2022 / Revised: 9 April 2022 / Accepted: 11 April 2022 / Published: 13 April 2022
(This article belongs to the Special Issue Health-Related Water Microbiology and Wastewater-Based Epidemiology)
Versions Notes

Abstract

:
Arcobacter is an emerging pathogen that is associated with human and animal diseases. Since its first introduction in 1991, 33 Arcobacter species have been identified. Studies have reported that with the presence of Arcobacter in environmental water bodies, animals, and humans, a possibility of its transmission via water and food makes it a potential waterborne and foodborne pathogen. Therefore, this review article focuses on the general characteristics of Arcobacter, including its pathogenicity, antimicrobial resistance, methods of detection by cultivation and molecular techniques, and its presence in water, fecal samples, and animal products worldwide. These detection methods include conventional culture methods, and rapid and accurate Arcobacter identification at the species level, using quantitative polymerase chain reaction (qPCR) and multiplex PCR. Arcobacter has been identified worldwide from feces of various hosts, such as humans, cattle, pigs, sheep, horses, dogs, poultry, and swine, and also from meat, dairy products, carcasses, buccal cavity, and cloacal swabs. Furthermore, Arcobacter has been detected in groundwater, river water, wastewater (influent and effluent), canals, treated drinking water, spring water, and seawater. Hence, we propose that understanding the prevalence of Arcobacter in environmental water and fecal-source samples and its infection of humans and animals will contribute to a better strategy to control and prevent the survival and growth of the bacteria.

1. Introduction

The genus Arcobacter is a gram-negative, microaerophilic, nonspore-forming, motile, and spiral-shaped bacterium classified under the family Arcobacteraceae (formerly classified under Campylobacteriaceae) [1]. Arcobacter was first isolated in 1977 from bovine and pig fetuses in Belfast, UK [2]. Since then, 33 species have been recognized (Table 1), and different physiological characteristics have been identified (Table 2). Furthermore, these Arcobacter species have been isolated from humans, animals, natural and marine water environments, sewage, and septic tanks worldwide.
Arcobacter causes various diseases, such as livestock reproductive problems, mastitis, and gastric ulcers in animals, including gastroenteritis, bacteremia, peritonitis, and endocarditis in humans [3]. Furthermore, following Arcobacter infections (diarrhea and bacteremia), severe cases in humans have mainly been caused by A. butzleri, followed by A. cryaerophilus, whereas A. skirrowii and A. thereius have only been rarely reported [4]. Although the predominant transmission route is via contaminated foods, untreated water samples have also been recognized as a potential source of infection [5].
Among various Arcobacter spp., A. butzleri is one of the enteric waterborne bacterial pathogens to be considered when managing community drinking water risks [6]. During the three reported waterborne outbreaks associated with Arcobacter that occurred in Finland, Slovenia, and the US, the bacterium was isolated either from drinking water or the feces of patients with diarrhea. In all cases, their drinking water was fecally contaminated [7,8,9]. Thus, it is vital to understand the correlation between Arcobacter presence in water, food sources, and fecal contamination. This review paper describes the prevalence of Arcobacter in water, food, and fecal samples to understand its association with fecal contamination in water and food products.

1.1. Pathogenicity of Arcobacter

The complete genome sequencing and analysis of A. butzleri revealed nine putative virulence genes (cadF, cj1349, ciaB, mviN, pldA, tlyA, hecA, hecB, and irgA) [37]. These genes have received particular attention due to their homology to genes associated with pathogenicity in other microorganisms [37]. For example, some virulence determinants identified in Campylobacter jejuni homologs within A. butzleri are fibronectin-binding proteins (cadF and cj1349), the invasion protein (ciaB), the virulence factor (mviN), the phospholipase (pldA), and hemolysin (tlyA). Other putative virulence determinants irgA, hecA, and hecB present in A. butzleri have also been identified in Vibrio cholera, uropathogenic Escherichia coli, Erwinia crysthanthemi, Pseudomonas syringae, Ralstonia solanacearum, Burkholderia cepacia, and Acinetobacter [37]. After developing a polymerase chain reaction (PCR) assay to detect those nine putative virulence genes, they were primarily present in A. butzleri, A. cryaerophilus, and A. skirrowii isolates [38]. Virulence genes have also been identified in A. cibarius, A. trophiarum, A. defluvii, A. molluscorum, A. ellisii, A. bivalviorum, A. venerupis, A. suis, A. cloacae, A. faecis, and A. lanthieri, but not in A. thereius and A. mytili [39,40].
The pathogenicity of these virulence genes was also determined based on the ability of the bacteria to adhere, invade, and produce toxins on human and animal cell lines [4]. Therefore, although A. thereius and A. mytili did not possess the virulence genes as stated above, they could adhere to and invade Caco-2 cell lines [39]. Hence, these species could have some public health importance, considering that they were identified in animals (porcine abortion) and mussels, respectively [30,33]. However, an unclear association between the presence of virulence genes and the pathogenicity associated with cell lines has been observed [4]. As all species of Arcobacter might not be pathogenic, such as nitrogen-fixing A. nitrofigilis [1], more studies should be conducted regarding useful aspects, pathogenicity and virulence potentials of the Arcobacter species.

1.2. Antimicrobial Resistance of Arcobacter

Antimicrobial susceptibility tests of Arcobacter isolated from water, food-related origins, and humans have been conducted [41]. In most of these studies, the susceptibility test has been limited to three species of Arcobacter: A. butzleri, A. cryaerophilus, and A. skirrowii because of the severity of their infections in humans and animals [3]. This antimicrobial susceptibility test was conducted through various methods, i.e., agar plate dilution, broth microdilution, disk diffusion, gradient strip diffusion, and SensititreTM semiautomated [42]. Based on the treatment of Arcobacter-dependent infections, antibiotics used have included quinolones, cephalosporins, tetracyclines, macrolides, and β-lactam antibiotics combined with β-lactamase inhibitors. It has also been reported that Arcobacter was resistant to various classes of antibiotics, such as penicillins (69.3–99.2%), cephalosporins (30.5–97.4%), macrolides (10.7–39.8%), fluoroquinolones (4.3–14.0%), aminoglycosides (1.8–12.9%), and tetracyclines (0.8–7.1%). Furthermore, A. butzleri was more resistant to several antibiotics compared with other species of Arcobacter [42]. Therefore, the higher resistance rate of A. butzleri proposes that this species can act as a reservoir of genes, contributing to antimicrobial resistance dissemination through various mediums. However, the high prevalence of antimicrobial resistance can be because of Arcobacter spp. exposure to antibiotics used both in animal production and human medicine.

2. Methods for Detecting Arcobacter

2.1. Methods for Isolating and Cultivating Arcobacter

Arcobacter was first isolated from livestock abortions using an Ellinghausen–McCullough–Johnson–Harris (EMJH) Leptospira culture media [2]. Since then, various enrichment and isolation techniques have been used to isolate Arcobacter from different samples (Table 3). Therefore, isolating Arcobacter through culture mediums has been performed using enrichment media, such as EMJH, Arcobacter specific broth (ASB), Cefoperazone, amphotericin, teicoplanin (CAT) broth, Johnson–Murano broth (JMB), Arcobacter broth, and Arcobacter enrichment basal mediums supplemented with antibiotics have been used to enrich Arcobacter from meats, ground pork, broiler chicken, and poultry products. These supplementation antibiotics include 5-fluorouracil, cefoperazone, piperacillin, trimethoprim, cycloheximide, amphotericin B, teicoplanin, and novobiocin [2,43,44,45,46,47] which help in the selective growth of the bacteria with no growth of competing microorganisms. The incubation conditions varied depending upon the types of broth, mostly at 30 °C for 48–72 h under aerobic or microaerophilic conditions. After enrichment, different plating media, including Cephalotin, vancomycin, the amphotericin B (CVA) agar, Johnson–Murano (JM) agar, modified charcoal cefoperazone deoxycholate agar (mCCDA), and the Arcobacter plating medium were used with antibiotics mentioned above in enrichment media and blood agar without antibiotics [2,43,44,45,46,48], after which they were incubated at various conditions mostly at 30 °C for 48–72 h under aerobic or microaerophilic conditions as shown in Table 3. Although these enrichment and isolation techniques were developed in the 2000s, they are still widely used to isolate Arcobacter from water, animal meat, milk, rectal swab, and floor swab samples [49,50,51]. Additionally, a selective enrichment broth and a selective-differential plating medium were developed for the growth of A. butzleri, A. cryaerophilus, and A. skirrowii in food samples. The medium has 97.8% inclusivity for Arcobacter and 100% exclusivity for non-Arcobacter strains. [52]. As reported, the culture-dependent approach helps determine recovered isolates’ antibiotic susceptibilities from clinically significant samples [53]. Some studies have also proposed that a reduction in the diversity of species because of the enrichment step can also affect their direct molecular detection from enrichment broth [50,54]. However, identifying Arcobacter isolates at the species level is difficult because of insufficient biochemical tests and difficulties in phenotypic characterization of the bacterium [55]. Therefore, molecular methods are convenient for the rapid and accurate identification of Arcobacter at the species level.

2.2. Molecular-Based Detection Methods of Arcobacter

With several drawbacks regarding the need for a rapid, reliable, and sensitive technique for the specific detection of Arcobacter, PCR assays were developed by Bastyn et al. [57] and Harmon and Wesley [58], targeting 23S and 16S rRNA genes of Arcobacter, respectively. Therefore, these assays have been used extensively as an alternative to conventional microbiological culture methods to identify Arcobacter from drinking and environmental water, including milk, meat, clams, mussels, cattle, and fecal samples (Table 4). Furthermore, since A. butzleri, A. skirrowii, and A. cryerophilus were associated with human and animal illness [33], a multiplex PCR assay targeting the 16S and 23S rRNA was developed for the detection and identification of these three Arcobacter species [59]. This assay was extensively applied in ponds, springs, seawater, river water, wastewater, drinking water, milk, chickens, dogs, cats, cattle, meat, and feces. In addition to the three above mentioned species of Arcobacter, Pentimalli et al., [60] developed species-specific primers, targeting gyrA and 16S rRNA gene sequences of A. cibarius, including three above mentioned species of Arcobacter, as A. cibarius was isolated from the skin of broiler chicken carcasses and piggery effluents [20,61]. Subsequently, a developed PCR assay was applied to survey Arcobacter contaminations in chicken meat. Later in 2010, Douidah et al. [62] developed a multiplex PCR assay, targeting five human- and mammal-associated Arcobacter spp., to examine 16S and 23S RNA, rpoB, and gyrA genes. This multiplex PCR assay identified Arcobacter species in raw milk from vending machines in Italy [63].
In addition to these conventional PCR assays, qPCR has also been developed to evaluate their applicability to the newly discovered Arcobacter species with high specificity and sensitivity [64,65,66,67]. Similarly, fluorescent in situ hybridization (FISH) has been used to identify Arcobacter in river water and wastewater samples [49,68,69]. However, since fewer recent studies regarding pathogenicity, virulence genes, and the discovery of new Arcobacter species exist, assays targeting wide Arcobacter species should be developed. Additionally, the applicability of previously developed assays should be extended to monitor all newly discovered Arcobacter species.

3. The Specific Detection of Arcobacter in Animal Feces and Products

Although most Arcobacter species are reported as commensal in the gastrointestinal tract of animals, the feces of animals are considered a possible source of contamination [50]. Therefore, transmission routes are regarded as fecally contaminated food and water [51,86]. As summarized in Table 5, Arcobacter has been detected in various fecal samples of cows, dogs, cats, pigs, chickens, and their products [5,84,87,88,89,90]. Methods applied for detecting Arcobacter in these samples include culture and PCR, whereas methods applied for typing Arcobacter include enterobacterial repetitive intergenic consensus PCR (ERIC-PCR), multilocus sequence typing (MLST), matrix-assisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF MS) (Table 4). Moreover, studies have reported that the positive percentage of Arcobacter detected in fecal samples from humans and animals ranged from 3% to 60%. Additionally, the discharge of feces from farms with cows, pigs, horses, and sheep contains millions of bacterial cells [91]. Therefore, when discharged into the water environment, fecal pathogens serve as a potential source/reservoir of waterborne diseases and can be transferred via the food process chain and water samples.
Arcobacter has also been detected in human stool samples. In a study by Webb et al., Arcobacter was identified in the stool of diarrheic and non-diarrheic people [84]. The study identified no difference in the prevalence of Arcobacter between diarrheic and non-diarrheic stools. However, in a research study conducted by Pérez-Cataluña et al., Arcobacter detected from clinical samples contained different virulence genes, resistant to antibiotics [92]. Additionally, in Belgium and France, Arcobacter is the fourth most common bacteria isolated from patients with enteric diseases’ feces and the third most prevalent in South Africa [93].
The contamination of food with Arcobacter may result from improper hygienic practices at different stages of the food supply chain. Although the prevalence of Arcobacter in animal products varies greatly among different studies, it is found that poultry meat has a higher Arcobacter contamination ratio in comparison to red meat, raw cow milk and vegetables. In a study by Uljanovas et al., the highest contamination of Arcobacter was observed in chicken meat followed by raw milk [94]. In a study conducted by Travesera et al., milk samples intended for human consumption sold through vending machines were found positive for Arcobacter [63]. This shows that poor handling or consumption of contaminated meat or raw milk may cause adverse effects on human health. Therefore, Arcobacter might be one of the etiological factors for human gastroenteritis.

4. Specific Detection of Arcobacter in Water Samples

Water quality and human health are interrelated, as water is one of the possible bacterial transmission routes to humans and animals [3,50]. As shown in Table 5, Arcobacter has been detected in various water samples, such as groundwater, river water, wastewater, canal water, seawater, spring water, and drinking water. In this review, the quantitative data on Arcobacter showed its highest detection in sewage, with a detection percentage of >69%. Although the prevalence of Arcobacter in water samples might vary depending upon different studies, it is found that the Arcobacter detection rate was approximately 100% in most wastewater samples in tested countries, such as Italy, Spain, the UK, and the US. Nevertheless, wastewater treatment plants (WWTPs) have been developed that collect and treat wastewater. Subsequently, treated water is returned to the environment for irrigation and recreational purposes [117]. Therefore, WWTPs are unsurprisingly considered hotspots for the presence of Arcobacter since it has been detected in multiple countries through culture, qPCR, multiplex PCR, and FISH [68,110,111,112,113,114]. The presence of Arcobacter in both influent and effluent samples of WWTPs indicates the high tolerance capability of this bacteria, ultimately leading to persistence and spread. Since WWTPs are considered hotspots for the spread of antibiotic resistance genes [118], these genes might transfer to Arcobacter conducting to unsuccessful treatments of severe infections. As observed, in groundwater and river water, the positive percentage of Arcobacter ranged from 26% to 78% and 24% to 100%, respectively. However, in canals, seawater, springs, and drinking water, the positive percentage of Arcobacter was 100%, 36%, 25%, and 0%, respectively. Therefore, these results further indicate environmental water samples as popular sources for Arcobacter, which, if untreated and consumed directly or indirectly, is proposed to affect human and animal health.
The presence of Arcobacter in water samples has also been associated with waterborne outbreaks. These outbreaks occurred in Finland, Slovenia, and the US, where people experiencing acute gastroenteritis consumed water contaminated with Arcobacter [7,8,9,119]. The presence of Arcobacter in freshwater could be a potential source for the spread of infections to humans and animals as these bacteria can be consumed directly when such contaminated water is used for washing raw vegetables or indirectly by using river water for irrigation purposes or preparing foods for an animal without any treatment of Arcobacter contaminated water. Similarly, a study showed that Arcobacter could survive at different temperatures and in non-chlorinated drinking water for up to 16 days [119,120,121], showing that water sources can act as a reservoir and potential source of Arcobacter contamination to humans and animals. It also indicates the potential of Arcobacter as a waterborne pathogen. Nevertheless, another study reported that water samples treated with chlorination did not contain Arcobacter [119], suggesting the importance of chlorinating drinking water before use.

5. Microbial Community Analyses of Arcobacter in Various Samples

High-throughput sequencing technology has provided a powerful approach to improving our understanding of microbial ecology in various environments [122]. Thus, culture-independent, high-throughput sequencing of the 16S rRNA gene fragment has successfully identified Arcobacter in sediments receiving wastewater effluents, river feedback, wastewater, and groundwater samples [64,109,112,116,123,124,125,126,127,128,129]. Arcobacter was also one of the dominant pathogenic bacteria identified in groundwater, river water, and wastewater samples. Furthermore, in a study conducted by Sigala and Unc, antibiotic-resistant Arcobacter was identified through pyrosequencing [130]. Therefore, the dominance of Arcobacter among pathogenic bacterial communities illustrates the persistence of these bacteria in the environment, highlighting the importance of detecting these bacteria in other food and fecal-source samples.

6. Conclusions

This review summarizes the general characteristics, pathogenicity, and methods of detecting Arcobacter. It also shows the presence of Arcobacter in various samples worldwide, including its persistence in the environment. Arcobacter has been detected in several water bodies and other animal feces, including animal products. The inter-relationship between water quality, human health, and fecal-source samples shows that Arcobacter plays an essential role in these three parameters. Furthermore, Arcobacter in water and fecal samples can be regarded as a potential risk for human and animal health. Therefore, it is necessary to identify and treat the bacteria present in environmental samples to decrease the risk of exposure and reduce their effects on humans and animals. Data concerning the potential relationship between Arcobacter in fecal and water samples remain unavailable, but such data are necessary to understand the potential risks of waterborne pathogens better. Thus, a more extensive and rigorous surveillance system should be implemented to obtain these data. Additionally, studies providing molecular epidemiology and reliable risk assessments of Arcobacter infections in humans should be conducted.

Author Contributions

Conceptualization, R.G.S. and E.H.; formal analysis, R.G.S.; funding acquisition, E.H.; investigation, R.G.S.; resources, E.H.; supervision, Y.T. and E.H.; validation, Y.T. and E.H.; visualization, R.G.S.; writing—original draft preparation, R.G.S.; writing—review and editing, Y.T. and E.H.; All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported the Japan Society for the Promotion of Science (JSPS) through the Fund for the Promotion of Joint International Research (Fostering Joint International Research (B)) (grant number JP18KK0297), the Japan Science and Technology Agency (JST) through the Accelerating Social Implementation for SDGs Achievement (aXis) (grant number JPMJAS2005), and JST and the Japan International Cooperation Agency (JICA) through the Science and Technology Research Partnership for Sustainable Development (SATREPS) program entitled “Hydro-microbiological Approach for Water Security in Kathmandu Valley, Nepal”.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Table
Table 1. List of Arcobacter species with their sources and countries of origin.
Table 1. List of Arcobacter species with their sources and countries of origin.
SpeciesSourcesCountryReferences
A. acticolaSeawaterKorea[10]
A. anaerophilusEstuarine sedimentIndia[11]
A. antarcticusAntartic intertidal sedimentAntartica[12,13]
A. aquimarinusSeawaterSpain[14]
A. arenosusMarine sedimentKorea[13,15]
A. bivalviorumShellfishSpain[16]
A. butzleriFeces (humans with diarrhea)USA[17]
A. caeniReclaimed waterSpain[18]
A. canalisWater canalSpain[19]
A. cibariusBroiler carcassBelgium[20]
A. cloacaeSewageSpain[21]
A. cryaerophilusAnimal abortionsIreland[1]
A. defluviiSewageChile[22]
A. ebronensisMusselsSpain[14]
A. ellisiiMusselsSpain[23]
A. faecisSeptic tankCanada[24]
A. halophilusHypersaline lagoonUSA[25]
A. lacusReclaimed waterSpain[18]
A. lanthieriPig and dairy cattle manureCanada[26]
A. lekinthochrousPecten maximus larvae and tank seawaterNorway[27]
A. marinusDokdo islandKorea[28]
A. molluscorumShellfishSpain[29]
A. mytiliMusselsSpain[30]
A. nitrofigilisRoots of Spartina alternifloraUSA[1]
A. pacificusSeawaterChina[31]
A. parvusSquidKorea[13,32]
A. skirrowiiFeces (humans with diarrhea)USA[17]
A. suisPork meatSpain[21]
A. thereiusPigs and ducksBelgium[33]
A. trophiarumPigsBelgium[34]
A. vandammeiPorcine intestineBelgium[35]
A. venerupisShellfishSpain[16]
A. vitoriensisWastewaterSpain[13,36]
Table
Table 2. Differential physiological characteristics of all identified genus Arcobacter species.
Table 2. Differential physiological characteristics of all identified genus Arcobacter species.
Characteristics123456789101112131415161718192021222324252627282930313233
Growth in/on:
Air at 37 °C−−−++++−+−+++−+++++−+++−+*+−−−+−+
CO2 at 37 °C*−*++++−+++++−+++++−+++−+*+−−−+++
CO2 at 42 °C*−*−*−+−+−−−+−+−−+−*−++−−*−−−−−−−
4% (w/v) NaCl−++−++−−+−−−−−−−+−−−+++++++−−−−−−
1% (w/v) Glycine*+*−−−−−−−−−−−−−+−+−+−+−**−−+−−−−
MacConkey agar**+−*+−+v++−−−++−++−+++−−+−+−+*++
CCDA**−+*+++−−+++−++−++−−−−−**+−−+*++
Enzyme activity:
Urease−−−−−−−−−−−−++−−−−−−−−−+−*−−−−−+*
Catalase+−*+−++++−+++−++−+++−++++*+++++++
Esterase−****++**+*+−*+++*+−++++−−+*−+**+
Hippurate hydrolysis*****−−**−*−−*+−−*−*−−−−*+−*−−***
Alkaline phosphatase*****++**−*+−*−−−*−−+++−−+−*−−**−
Voges-Proskauer test*****−−**−*−−*−+−*+−+−−−**−*−−**+
Na-succinate assimilation*****+−**−*+−*−−+*−*−−−−**−*−+***
Nitrate reduction−+*+−−++−−+++−+++++++++++++++−−++
Nitrite production−****−−**−*+−*−−−*+*−−−−**−*−−***
TTC reduction*****−+−−+*−−*−++−++−−+−*w−*−−−*+
Indoxyl acetate hydrolysis*+*+*+++−++++++++++*+−−+++++++++*
Resistance to cefoperazone (64 mg/L)*−*−*−++−+−++−−−−++−−+−−+*+−++*−+
Strains/species: 1, A. acticola; 2, A. anaerophilus; 3, A. antarcticus; 4, A. aquimarinus; 5, A. arenosus; 6, A. bivalviorum; 7, A. butzleri; 8, A. caeni; 9, A. canalis; 10, A. cibarius; 11, A. cloacae; 12, A. cryaerophilus; 13, A. defluvii; 14, A. ebronensis; 15, A. ellisii; 16, A. faecis; 17, A. halophilus; 18, A. lacus; 19, A. lanthieri; 20, A. lekinthochrous; 21, A. marinus; 22, A. molluscorum; 23, A. mytili; 24, A. nitrofigilis; 25, A. pacificus; 26, A. parvus; 27, A. skirrowii; 28, A. suis; 29, A. thereius; 30, A. trophiarum; 31, A. vandammei; 32, A. venerupis; 33, A. vitoriensis. Data for Arcobacter species were obtained from sources of [10,11,12,14,15,18,19,24,26,27,31,32,35,36]. “+”, Positive. “−“, Negative. “*”, Not determined. V, 12–94% strains positive. W, weakly positive.
Table
Table 3. Isolation and cultivation methods for Arcobacter.
Table 3. Isolation and cultivation methods for Arcobacter.
EnrichmentIsolationReferences
Formulation
Antibiotics Used (mg/L)		Incubation ConditionsPlating Medium
Antibiotics Used (mg/L)		Incubation Conditions
EMJH
5-Fluorouracil (100)		30 °C, 48–72 h, mO2Blood agar
No antibiotics		30 °C, 48–72 h, mO2, and O2[2]
ASB
Cefoperazone (32)
Piperacillin (75)
Trimethoprim (20)
Cycloheximide (100)		24 °C, 48 h, O2ASM
Cefoperazone (32),
Piperacillin (75)
Trimethoprim (20)
Cycloheximide (100)		24 °C, 48–72 h, O2[45]
EMJH
5-Fluorouracil (200)		30 °C, 9 days, O2CVA agar
Cephalothin (20)
Vancomycin (10)
Amphotericin B (5)		30 °C, up to 7
days, O2		[44]
CAT broth
Cefoperazone (8)
Amphotericin B (10)
Teicoplanin (5)		30 °C, 48 h,
mO2		Blood agar
No antibiotics
Membrane filtration		30 °C, up to 7
days, O2		[43]
JM broth
Cefoperazone (16),
5-Fluorouracil (200)		30 °C, 48 h,
O2		JM agar
Cefoperazone (32)		30 °C, 48 h, O2[46]
--modified charcoal cefoperazone deoxycholate agar (mC-
CDA)
Cefoperazone (32)		37°C, 48 h, mO2[48]
Arcobacter broth
Cefoperazone (16),
Amphotericin B (10)
5-Fluorouracil (100)
Novobiocin (32)
Trimethoprim (64)		28 °C, 48 h,
mO2		Arcobacter plating
medium
Cefoperazone (16),
Amphotericin B (10)
5-Fluorouracil (100)
Novobiocin (32)
Trimethoprim (64)		30 °C, 24–72 h,
mO2		[56]
Nguyen-Restaino-Juárez (NRJ) broth
Cefsulodin (6), vancomycin (4), and moxalactam (10)		30 °C, 48 h, O2NRJ medium
cefsulodin (10), vancomycin
(1), novobiocin (1), and moxalactam (10)		30 °C, 48 h, O2[52]
EMJH, Ellinghausen–McCullough–Johnson–Harris semisolid medium; ASB, Arcobacter selective broth; CAT, Cefoperazone, amphotericin, teicoplanin broth; JM, Johnson–Murano; ASM, Arcobacter selective medium; CVA, cephalotin, vancomycin and amphotericin B agar; mO2, microaerobic conditions; O2, aerobic conditions.
Table
Table 4. Specific detection of Arcobacter using molecular-based methods.
Table 4. Specific detection of Arcobacter using molecular-based methods.
MethodsGenes TargetedSpecies IdentifiedReferences
RFLP, Southern blotting16S rRNA, 23S rRNAA. butzleri[70]
PCR-hybridizationglyAA. butzleri[71]
Real time PCRgyrAA. butzleri, A. cryaerophilus, A. cibarius, A. nitrofigilis[72]
Real time PCR
Multiplex PCR		rpoBC, 23S rRNA
rpoBC, 23S rRNA		A. butzleri, A. cryaerophilus
A. butzleri, A. cryaerophilus		[73]
MALDI-TOF MSProteinsA. butzleri, A. cryaerophilus, A. skirrowi,[74]
PCR23S rDNAArcobacter spp.[57]
Multiplex PCR16S rRNA, 23S rRNAArcobacter spp., A. butzleri[75]
PCR-RFLP16S rRNAA.butzleri[76]
PCR-RFLP23S rRNAA. butzleri, A. nitrofigilis[77]
In situ hybridization16S rRNAArcobacter spp.[69]
PCR-RFLP16S rRNAA. butzleri, A. cryaerophilus, A. skirrowii[78]
PCR-culture16S rRNAArcobacter spp.[65]
Multiplex PCR16S rRNA, 23S rRNAA. butzleri, A. cryaerophilus, A. skirrowii[59]
Multiplex PCR23S rRNAA. butzleri, A. cryaerophilus, A. skirrowii[79]
PCR-RFLPgroELA. butzleri[80]
PCR-RFLP16S rRNA, 23S rRNAA. butzleri[81]
PCR-DGGE16S rRNAA. cryaerophilus, A. nitrofigilis[82]
PCR-RFLP16S rRNAA. butzleri, A. cryaerophilus, A. skirrowii, A. cibarius, A. nitrofigilis, A. halophilus, A. cibarius, A. mytili[83]
PCRgyrA, 16S rRNAA. butzleri, A. cryaerophilus, A. skirrowii, A. cibarius[60]
Multiplex PCR23S rRNA, gyrAA. butzleri, A. cryaerophilus, A. skirrowii, A. cibarius, A. thereius[62]
PCRhsp60A. trophiarum[34]
PCR16S rRNAArcobacter spp.[66]
PCR16S rRNAA. butzleri[84]
MPN-qPCRhsp60Arcobacter spp.[85]
qPCR16S rRNAArcobacter spp.[64]
RFLP, restriction fragment length polymorphism; DGGE, denaturing gradient gel electrophoresis; MALDI-TOF MS, matrix-associated laser desorption ionization-time-of-flight mass spectrometry; MPN-qPCR, most probable number-qPCR.
Table
Table 5. Various samples from which Arcobacter was detected and isolated.
Table 5. Various samples from which Arcobacter was detected and isolated.
Sample TypeNo. of Positive Samples/No. of Samples Tested (%)CountriesArcobacter spp. IdentifiedReferences
Fecal samplesHuman stool360/4636 (8)GermanyA. butzleri, A. cryaerophilus, A. lanthieri[5]
892/1596 (60)CanadaA. butzleri[84]
20/1200 (1.7)LithuaniaA. butzleri[94]
Cattle feces20/51 (39)BelgiumA. butzleri, A. cryaerophilus, A. skirrowii[95]
12/332 (4)JapanA. butzleri, A. cryaerophilus[89]
14/200 (7)TurkeyA. butzleri, A. cryaerophilus, A. skirrowii[96]
240/1682 (14)USAArcobacter spp.[90]
Pig feces36/82 (44)BelgiumA. butzleri, A. cryaerophilus[95]
25/250 (10)JapanA. butzleri, A. cryaerophilus, A. skirrowii[89]
Sheep feces10/62 (16)BelgiumA. butzleri, A. cryaerophilus[95]
Horse feces2/13 (15)BelgiumA. butzleri[95]
Dog feces5/267 (2)BelgiumA. butzleri, A. cryaerophilus[88]
Cat feces0/61 (0)BelgiumNot detected[88]
Animal productsBeef meat6/100 (6)TurkeyA. butzleri, A. cryaerophilus[53]
39/148 (26)MalaysiaA. butzleri, A. cryaerophilus, A. skirrowii[51]
13/45 (29)USAA. butzleri, A. skirrowii[97]
37/108 (34)Northern IrelandA. butzleri, A. cryaerophilus, A. skirrowii[98]
7/32 (22)AustraliaA. butzleri[99]
2/90 (2)JapanA. butzleri[100]
5/97 (5)TurkeyA. butzleri[96]
1/68 (1)The NetherlandsArcobacter spp.[45]
Pork meat7/100 (7)JapanA. butzleri, A. cryaerophilus[100]
64/200 (32)USAArcobacter spp.[101]
1/27 (4)ItalyA. butzleri[102]
35/101 (35)Northern IrelandA. butzleri, A. cryaerophilus, A. skirrowii[98]
23/45 (51)USAA. butzleri, A. cryaerophilus, A. skirrowii[97]
Sheep meat2/13 (15)AustraliaA. butzleri[99]
Chicken livers and carcasses29/32 (91)SpainA. butzleri, A. cryaerophilus, A. skirrowii[87]
89/170 (52)GermanyA. butzleri[103]
Chicken meat30/51 (59)Japan and ThailandA. butzleri[104]
36/42 (86)SpainA. butzleri, A. cryaerophilus[60]
53/220 (24)The NetherlandsArcobacter spp.[45]
23/100 (23)JapanA. butzleri, A. cryaerophilus, A. skirrowii[100]
6/15 (40)USAA. butzleri, A. skirrowii[97]
16/22 (73)AustraliaA. butzleri[99]
58/94 (62)Northern IrelandA. butzleri, A. cryaerophilus, A. skirrowii[98]
119/331 (36)LithuaniaA. butzleri, A. cryaerophilus[94]
Turkey meat303/395 (77)USAA. butzleri, Arcobacter spp.[105]
Duck carcass8/10 (80)UKA. butzleri, A. cryaerophilus, A. skirrowii[106]
Buccal cavity of dogs2/267 (0.8)BelgiumA. cryaerophilus[88]
Buccal cavity of cats0/61 (0)BelgiumNot detected[88]
Chicken cloacal swabs34/234 (15)JapanA. butzleri, A. cryaerophilus, A. skirrowii[89]
Cow’s rectal swabs8/120 (7)MalaysiaA. butzleri, A. skirrowii[51]
Cow milk64/484 (13)ItalyA. butzleri[107]
6/105 (6)MalaysiaA. butzleri, A. cryaerophilus, A. skirrowii[51]
8/37 (22)ItalyA. butzleri[63]
26/104 (25)LithuaniaA. butzleri[94]
Water samplesSurface water13/25 (52)Czech RepublicA. butzleri[108]
10/10 (100)SpainArcobacter spp.[68]
4/17 (24)JapanA. butzleri[104]
14/18 (78)NepalArcobacter spp.[109]
36/128 (28)LithuaniaA. butzleri, A. cryaerophilus[94]
Wastewater (Influent and effluent water)9/9 (100)UKA. butzleri, A. cryaerophilus[110]
44/44 (100)SpainArcobacter spp.[111]
30/30 (100)SpainArcobacter spp.[68]
43/48 (90)USArcobacter spp.[112]
29/30 (97)ChileA. butzleri, A. cloacae, A. cryaerophilus, A. defluvii, A. ellisii, A. nitrofigilis, A. skirrowii, A. thereius[113]
61/88 (69)ItalyA. butzleri[114]
5/50 (10)ItalyArcobacter spp.[115]
Canal7/7 (100)JapanA. butzleri[104]
Treated drinking water2/18 (11)MalaysiaA. butzleri, A. skirrowii[51]
Sewage24/66 (36)Czech RepublicA. butzleri[108]
Spring water4/16 (25)Czech RepublicA. butzleri, Arcobacter spp.[108]
Drinking water0/8 (0)Czech RepublicNot detected[108]
Groundwater13/47 (26)NepalArcobacter spp.[64]
99/286 (35)NepalArcobacter spp.[116]
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Ghaju Shrestha, R.; Tanaka, Y.; Haramoto, E. A Review on the Prevalence of Arcobacter in Aquatic Environments. Water 2022, 14, 1266. https://doi.org/10.3390/w14081266

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Ghaju Shrestha R, Tanaka Y, Haramoto E. A Review on the Prevalence of Arcobacter in Aquatic Environments. Water. 2022; 14(8):1266. https://doi.org/10.3390/w14081266

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Ghaju Shrestha, Rajani, Yasuhiro Tanaka, and Eiji Haramoto. 2022. "A Review on the Prevalence of Arcobacter in Aquatic Environments" Water 14, no. 8: 1266. https://doi.org/10.3390/w14081266

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