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Paper
Paper Corynebacterium species nasal carriage in pigs and their farmers in Bavaria, Germany: implications for public health V. Boschert, A. Berger, R. Konrad, I. Huber, S. Hörmansdorfer, S. Zöls, M. Eddicks, M. Ritzmann, A. Sing Reports on cases of human diphtheria caused by toxigenic Corynebacterium ulcerans that were linked to occupational swine contact as well as isolation of C ulcerans from wild boars have suggested that pigs might serve as reservoir for human infections. Therefore, a prevalence study on Corynebacterium species nasal carriage in pigs and their farmers was performed between August 1 and December 31, 2009, in 41 swine farms from Bavaria, Germany. All 411 asymptomatic pigs and 29 of 30 healthy farmers were colonised with Corynebacterium strains of up to 11 different species. No potentially toxigenic Corynebacterium strain was isolated either from the pigs or from their farmers, respectively. The patterns of the species composition in the pigs and the farmers were very similar, suggesting a potential transmission of strains between animals and humans.
Introduction
Diphtheria and diphtheria-like illness in humans are caused by the three potentially toxigenic (i.e. diphtheria toxin producing) Corynebacterium species Corynebacterium diphtheriae, Corynebacterium ulcerans and Corynebacterium pseudotuberculosis. Diphtheria toxin (DT) is encoded by the tox gene that is introduced by a prophage into the genome of a toxigenic strain (Wagner and others 2012, Zakikhany and Efstratiou 2012). The historically most prominent of the three species, C diphtheriae, is mainly a human pathogen and is only sporadically found in animals: whereas most of the very rare animal C diphtheriae cases happening more than 60 years ago mainly involved horses (Parish and Okell 1926) or cattle (Greathead and Bisschop 1963), in the last two decades only five C diphtheriae animal infections from three different vertebrate species were reported: two of them were caused by toxigenic – both affecting a horse in the USA (Henricson and others 2000) and in Ireland (Leggett and others 2010), respectively, and three by non-toxigenic strains – one involving a cow in Switzerland (Corboz and others 1996) and two cats in a small outbreak in the USA caused by a novel strain (Hall and others 2010). In contrast, C ulcerans and Veterinary Record (2014) A. Berger, MD R. Konrad, PhD A. Sing, MD PhD National Consiliary Laboratory for Diphtheria, Oberschleißheim 85764, Germany V. Boschert, VetD A. Berger, MD R. Konrad, PhD I. Huber, PhD S. Hörmansdorfer, VetD A. Sing, MD PhD Bavarian Health and Food Safety Authority, Oberschleißheim 85764, Germany
doi: 10.1136/vr.102634 V. Boschert, VetD S. Zöls, VetD M. Eddicks, VetD M. Ritzmann, VetD Clinic for Swine, Ludwig-MaximiliansUniversity Munich, Oberschleißheim 85764, Germany E-mail for correspondence: [email protected] VB, AB, ME and AS contributed equally. Provenance: not commissioned; externally peer reviewed Accepted June 27, 2014
C pseudotuberculosis are considered as zoonotic. While human infections with C. pseudotuberculosis, the etiological agent of caseous lymphadenitis in several livestock species including sheep, goats and llamas, are only sporadically reported mainly among shepherds of the respective animals, farmers, abattoir workers or butchers (Peel and others 1997, Bonmarin and others 2009), diphtheria-like infections with toxigenic C ulcerans have outnumbered those caused by toxigenic C diphtheriae in many industrialised countries in the last decade (Bonmarin and others 2009, Wagner and others 2010, Wagner and others 2012, Zakikhany and Efstratiou 2012). Originally cattle were identified as the main reservoir for C ulcerans; correspondingly, human infections were most often described to be associated with consumption of raw milk and dairy products or with direct contact to cattle. In the last few years, however, C ulcerans has increasingly been isolated from domestic animals such as pet dogs and cats (Lartigue and others 2005, Hogg and others 2009, De Zoysa and others 2005). Recently, we reported the isolation of an identical toxigenic C ulcerans strain (KL126) from a pig and its owner initially presenting with pharyngeal diphtheria who later developed severe systemic DT-mediated symptoms including polyneuropathy (neuralgia, diplegia of both arms, acute disability of swallowing, hoarseness) and cardiomyopathia (Schuhegger and others 2009). Their medium-sized pig-breeding farm housing 500 pigs in a nonindustrialised manner was located in a remote rural village of Northern Bavaria. Moreover, two cases of cutaneous diphtheria caused by toxigenic C ulcerans in patients with occupational pig contact have recently been reported from Germany (Berger and others 2013): one involved a 63-year-old diabetic female pig farm worker with a plantar ulcer (strain number KL241), the other a 58-year-old male farmer with a calf wound infection (strain number KL203). Interestingly, non-toxigenic, but toxpositive (non-toxigenic tox-bearing (NTTB)) C ulcerans strains have been isolated from the caseous lymph nodes or organ abscesses from 12 wild boars originating from several regions in Germany (Contzen and others 2011, Eisenberg and others 2014). These findings suggesting a potential role for pigs as a reservoir for toxigenic C ulcerans resulting in subsequent human diphtheria infections prompted us to investigate the prevalence of nasal Corynebacterium species carriage in farm pigs. September 13, 2014 | Veterinary Record
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Paper Materials and methods
The study was conducted between August 1 and December 31, 2009. Forty-one swine farms in Bavaria were included: 16 pig-producing (39 per cent), 13 finishing (32 per cent) and 12 growing to finishing farms (29 per cent). Swabs from both nasal cavities were obtained from 411 pigs of different ages. In total, 5–12 pigs per farm were investigated. All farmers were offered occupational health counselling (including a clinical and microbiological examination for Corynebacterium carriage and/or diphtheria symptoms). Nasal swabs from those 30 farmers out of 27 pig farms who requested microbiological carriage screening for themselves were examined after obtaining informed consent. Swabs were put into sterile Amies transport medium (Protagerm Amies Agar, BioMerieux, Marcy l’Etoile, France), transported within one to two hours at 8°C to the laboratory and immediately plated onto tellurite agar plates (BD Tellurite Agar, Bection Dickinson, Heidelberg, Germany). Agar plates were incubated for 48 hours at 37°C under microaerophilic conditions. From each individual plate, up to five morphologically distinguishable colonies that were suggestive to comprise coryneform bacteria were subcultivated on sheep blood agar (Oxoid, Wesel, Germany) for 24 hours at 37°C under microaerophilic conditions. All catalase-positive isolates were Gram-stained and subjected to matrix-assisted laser desorption/ionisation time-of-flight mass spectrometry (MALDI-TOF MS) analysis as reported previously (Konrad and others 2010).
Results
The Corynebacterium species nasal carriage data are shown in Table 1. A total of 796 and 52 strains were isolated from pigs and farmers, respectively. All 411 asymptomatic pigs were colonised with Corynebacterium strains (average number of strains per pig: 1.93; range: 1–7). Eleven different species were isolated from the nasal cavities of the pigs. The most prevalent species was Corynebacterium xerosis, which was found in all but one of the pigs, followed by Brevibacterium stationis, which was recently proposed to belong to the Corynebacterium genus (Bernard and others 2010) and Corynebacterium confusum. The other eight species were only prevalent in less than 5 per cent of the animals. All but one of the 30 farmers harboured at least one Corynebacterium strain (average number of strains per farmer: 1.73; range: 0–3). Nine different species were isolated from the nasal swabs with the same three species being the most prevalent as in the pigs. No strain of any of the three potentially toxigenic Corynebacterium species was isolated either from the pigs or from their farmers, respectively.
Discussion
We started this prevalence study on Corynebacterium species nasal carriage among farm pigs and their farmers having been alerted by several diphtheria cases or diphtheria-like infections caused by toxigenic TABLE 1: Prevalence of Corynebacterium species nasal carriage in pigs (n=411) and their farmers (n=30) Species
Pigs, n (%)
Farmers, n (%)
Corynebacterium xerosis Brevibacterium stationis* Corynebacterium confusum Corynebacterium ammoniagenes Corynebacterium casei Corynebacterium camporealensis Corynebacterium testudinoris Corynebacterium amycolatum Corynebacterium freneyi Corynebacterium flavescens Corynebacterium glutamicum Corynebacterium accolens Corynebacterium propinquum Corynebacterium pseudodiphtheriticum
410 (99.8) 260 (63) 48 (12) 31 (7.5) 18 (4.4) 12 (3) 6 (1.5) 3 (0.7) 3 (0.7) 2 (0.5) 1 (0.25) 0 0 0
26 (87) 7 (23) 7 (23) 1 (3) 0 2 (7) 0 1 (3) 0 0 0 4 (13) 3 (10) 1 (3)
*Brevibacterium stationis has recently proposed to belong to the Corynebacterium genus (Bernard and others 2010)
Veterinary Record | September 13, 2014
C ulcerans in humans with occupational swine contact (Schuhegger and others 2009, Berger and others 2013). So far, no prevalence data for coryneform bacteria in pigs have been published; only 12 sporadic cases of NTTB C ulcerans infections in wild boars have come to our knowledge (Contzen and others 2011, Eisenberg and others 2014). To date, isolation of the two other potentially DT-producing species, that is, C diphtheriae or C pseudotuberculosis, from pigs has not yet been reported. In our study, none of the 411 swabbed pigs showed nasal carriage of any of the three potentially toxigenic Corynebacterium species However, due to the very high corynebacteria carriage rate of 100 per cent with up to seven different Corynebacterium species identified per nasal swab and plenty of colonies covering the agar plates, we cannot fully exclude that single colonies hiding between a large amount of other bacterial colonies might be missed, although up to five morphologically distinguishable colonies suggestive to comprise coryneform bacteria were subcultivated and subsequently analysed by MALDITOF MS. The 100 per cent carriage rate might be explained by the close contact between the animals that is enhanced by their typical behaviour using their snouts as soil-digging tools and sensory organs. Whereas animal infections with C diphtheriae are absolute rarities – in the last 40 years reported to affect horses (two toxigenic cases; Henricson and others 2000, Leggett and others 2010), cattle (one non-toxigenic case; Corboz and others 1996), cats (two non-toxigenic cases; Hall and others 2010) and dogs (two toxigenic and two non-toxigenic cases; Kraszewska and others 1979) – and the very sporadic animal-associated human C pseudotuberculosis infections – most reports dating back more than 15 years – are mainly restricted to people professionally exposed to cattle, sheep, goats or llamas (Peel and others 1997), human C ulcerans-caused diphtheria cases – many of them associated with animal contact – are considered as emergent infections (Wagner and others 2010, Wagner and others 2012). Therefore, C ulcerans is probably the only one of the three potentially toxigenic Corynebacterium species for which animal carriage might be considered as relevant from a public health point of view. So far, C ulcerans prevalence data in asymptomatic animals are published only for shelter dogs in Osaka, Japan (Katsukawa and others 2009, Katsukawa and others 2012), and Rio de Janeiro, Brazil (Dias and others 2010), showing carriage rates of 1.5 per cent (one toxigenic strain in 65 dogs; Katsukawa and others 2012), 7.5 per cent (42 toxigenic and 3 non-toxigenic strains from 583 dogs, one of them harbouring both a toxigenic and a non-toxigenic strain; Katsukawa and others 2009) and 1.7 per cent (one non-toxigenic strain in 60 dogs; Dias and others 2010), respectively. A comparison of the corynebacteria carriage rate among the clinically healthy farmers in our study with the results of screening investigations dealing with other healthy populations suggests a significantly higher carriage rate in pig farmers of 96.7 per cent than in staff working in hospital-based environments in Germany and Switzerland (69.9 per cent; von Graevenitz and others 1998), outpatients in Italy (18.6 per cent; Bergamini and others 2000), attendants of a public health laboratory in Italy (9.9 per cent; Mencarelli and others 1992) or school children in Greece (7.8 per cent; Kalapothaki and others 1984); it should be noted that tellurite-based screening agars were used in all studies. Moreover, the carriage rate of 1.73 species per individual was higher than those observed in other studies (1.0; Bergamini and others 2000, and 1.04; Mencarelli and others 1992). While in the other three studies either commercially available, that is, the API Coryne system (Biomérieux, France) (von Graevenitz and others 1998, Bergamini and others 2000), or in-house biochemical assays (Mencarelli and others 1992) were used for final species determination, MALDI-TOF MS was applied in our study. The composition of the isolated corynebacteria species spectrum also markedly differed – both quantitatively and qualitatively – between the farmers in our study and the healthy people from the other studies (see also Table 2): the carriage rates of the six most prevalent Corynebacterium species among the farmers fairly outnumbered those found in the other available studies – with the only exception of the relatively high carriage rate of 51.3 per cent for C durum in hospital-based staff (von Graevenitz and others 1998). Of the three most prevalent species in the farmer group,
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Paper TABLE 2: Prevalence of Corynebacterium spp. nasal carriage in different human populations Species Corynebacterium xerosis Brevibacterium stationis† Corynebacterium confusum Corynebacterium accolens Corynebacterium propinquum Corynebacterium camporealensis Corynebacterium pseudodiphtheriticum Corynebacterium amycolatum Corynebacterium ammoniagenes Corynebacterium durum Corynebacterium group G Corynebacterium jeikeium Corynebacterium spp. Corynebacterium argentoratense Corynebacterium minutissimum Corynebacterium group F-1 Corynebacterium matruchotii Corynebacterium urealyticum Corynebacterium ulcerans Corynebacterium striatum Corynebacterium group A-4
Present study, n (%) n=30
von Graevenitz and others (1998) n (%) n=113
26 (87) 7 (23) 7 (23) 4 (13) 3 (10) 2 (7) 1 (3) 1 (3) 1 (3)
1 (0.9)
Bergamini and others (2000), n (%) n=500
Mencarelli and others (1992) *, n (%) n=515
24 (4.8)
8 (1.6)
2 (1.8)
58 (51.3) 7 (6.2) 4 (3.5) 4 (3.5) 1 (0.9) 1 (0.9) 1 (0.9)
15 (3.0)
6 (1.2)
10 (2.0)
9 (1.7) 4 (0.8) 9 (1.8) 6 (1.2) 10 (2.0)
12 (2.3)
7 (1.4) 14 (2.7)
*Only cystinase-producing Corynebacterium spp. lacking urease activity were intended to be included in this study. However, during the study obviously also cystinasenegative, urease-positive strains were added (Mencarelli and others 1992) †Brevibacterium stationis has recently been proposed to belong to the Corynebacterium genus (Bernard and others 2010)
only one species, C xerosis, ranked among the three most prevalent species found in any of the other groups – although at a much lower rate of 4.8 per cent vs. 87 per cent. The species ranking among the three most common isolates found in at least two of the other studies, that is, Corynebacterium pseudodiphtheriticum, Corynebacterium matruchotii, Corynebacterium minutissimum, Corynebacterium striatum and Corynebacterium jeikeium, were either absent or were very rare in the farmer group. Interestingly, among these C pseudodiphtheriticum and C striatum were the two most often isolated Corynebacterium species in consecutively obtained swabs from the upper respiratory tract in symptomatic patients within a hospital setting (Riegel and others 1996). Interestingly, human nasal or throat carriage of nontoxigenic C ulcerans seems to be rare and was found in 1.2 per cent of healthy adults in Italy (Bergamini and others 2000) and in 0.01 per cent of people of all ages with sore throat in the UK (Wagner and others 2011), respectively. Taken together, the composition of the corynebacteria flora in the farmer group very much resembled that of the pigs in our study and profoundly differed from the species distribution isolated from healthy humans in other studies. This correlation might suggest the potential of transmission of the respective corynebacteria between pigs and farmers. So far, direct proof of transmission of toxigenic C ulcerans between animal and human by isolation of an identical strain from both an animal and its owner is documented only in four instances, two of them involving dogs (Lartigue and others 2005, Hogg and others 2009), two a cat (Berger and others 2011, Yoshimura and others 2014) and one a pig (Schuhegger and others 2009), respectively. Moreover, as mentioned above, NTTB C ulcerans strains have been isolated from 12 wild boars in Germany (Contzen and others 2011, Eisenberg and others 2014) and from one pig connected to a human diphtheria case (toxigenic; (Schuhegger and others 2009)), respectively.
Conclusion
In conclusion, although we were not able to find any of the three potentially toxigenic Corynebacterium species in our prevalence study among pigs, the – although only sporadic – isolation of tox-positive C ulcerans from pigs, the report of three pig-linked cases of human diphtheria (Schuhegger and others 2009, Berger and others 2013), as well as the similarity of the corynebacteria carriage pattern in pigs and their farmers in our study suggest that pigs might be a rare source for toxigenic C ulcerans infections in humans having prolonged and close contact with these animals.
Acknowledgements
We thank the farmers who volunteered to participate in this study. We also thank Wolfgang Schmidt, Karola Grünwald, Marzena Maggipinto and Daniela Sebah for cultivation, microbiological and molecular characterisation of the corynebacteria. Funding The study was partly supported by the Bavarian State Ministry of the Environment and Public Health and by the German Federal Ministry of Health via the Robert Koch-Institute and its National Reference Laboratories Network (09-47, FKZ 1369-359 and FKZ 415).
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Corynebacterium species nasal carriage in pigs and their farmers in Bavaria, Germany: implications for public health V. Boschert, A. Berger, R. Konrad, I. Huber, S. Hörmansdorfer, S. Zöls, M. Eddicks, M. Ritzmann and A. Sing Veterinary Record 2014 175: 248 originally published online July 18, 2014
doi: 10.1136/vr.102634 Updated information and services can be found at: http://veterinaryrecord.bmj.com/content/175/10/248
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Paper Corynebacterium species nasal carriage in pigs and their farmers in Bavaria, Germany: implications for public health V. Boschert, A. Berger, R. Konrad, I. Huber, S. Hörmansdorfer, S. Zöls, M. Eddicks, M. Ritzmann, A. Sing Reports on cases of human diphtheria caused by toxigenic Corynebacterium ulcerans that were linked to occupational swine contact as well as isolation of C ulcerans from wild boars have suggested that pigs might serve as reservoir for human infections. Therefore, a prevalence study on Corynebacterium species nasal carriage in pigs and their farmers was performed between August 1 and December 31, 2009, in 41 swine farms from Bavaria, Germany. All 411 asymptomatic pigs and 29 of 30 healthy farmers were colonised with Corynebacterium strains of up to 11 different species. No potentially toxigenic Corynebacterium strain was isolated either from the pigs or from their farmers, respectively. The patterns of the species composition in the pigs and the farmers were very similar, suggesting a potential transmission of strains between animals and humans.
Introduction
Diphtheria and diphtheria-like illness in humans are caused by the three potentially toxigenic (i.e. diphtheria toxin producing) Corynebacterium species Corynebacterium diphtheriae, Corynebacterium ulcerans and Corynebacterium pseudotuberculosis. Diphtheria toxin (DT) is encoded by the tox gene that is introduced by a prophage into the genome of a toxigenic strain (Wagner and others 2012, Zakikhany and Efstratiou 2012). The historically most prominent of the three species, C diphtheriae, is mainly a human pathogen and is only sporadically found in animals: whereas most of the very rare animal C diphtheriae cases happening more than 60 years ago mainly involved horses (Parish and Okell 1926) or cattle (Greathead and Bisschop 1963), in the last two decades only five C diphtheriae animal infections from three different vertebrate species were reported: two of them were caused by toxigenic – both affecting a horse in the USA (Henricson and others 2000) and in Ireland (Leggett and others 2010), respectively, and three by non-toxigenic strains – one involving a cow in Switzerland (Corboz and others 1996) and two cats in a small outbreak in the USA caused by a novel strain (Hall and others 2010). In contrast, C ulcerans and Veterinary Record (2014) A. Berger, MD R. Konrad, PhD A. Sing, MD PhD National Consiliary Laboratory for Diphtheria, Oberschleißheim 85764, Germany V. Boschert, VetD A. Berger, MD R. Konrad, PhD I. Huber, PhD S. Hörmansdorfer, VetD A. Sing, MD PhD Bavarian Health and Food Safety Authority, Oberschleißheim 85764, Germany
doi: 10.1136/vr.102634 V. Boschert, VetD S. Zöls, VetD M. Eddicks, VetD M. Ritzmann, VetD Clinic for Swine, Ludwig-MaximiliansUniversity Munich, Oberschleißheim 85764, Germany E-mail for correspondence: [email protected] VB, AB, ME and AS contributed equally. Provenance: not commissioned; externally peer reviewed Accepted June 27, 2014
C pseudotuberculosis are considered as zoonotic. While human infections with C. pseudotuberculosis, the etiological agent of caseous lymphadenitis in several livestock species including sheep, goats and llamas, are only sporadically reported mainly among shepherds of the respective animals, farmers, abattoir workers or butchers (Peel and others 1997, Bonmarin and others 2009), diphtheria-like infections with toxigenic C ulcerans have outnumbered those caused by toxigenic C diphtheriae in many industrialised countries in the last decade (Bonmarin and others 2009, Wagner and others 2010, Wagner and others 2012, Zakikhany and Efstratiou 2012). Originally cattle were identified as the main reservoir for C ulcerans; correspondingly, human infections were most often described to be associated with consumption of raw milk and dairy products or with direct contact to cattle. In the last few years, however, C ulcerans has increasingly been isolated from domestic animals such as pet dogs and cats (Lartigue and others 2005, Hogg and others 2009, De Zoysa and others 2005). Recently, we reported the isolation of an identical toxigenic C ulcerans strain (KL126) from a pig and its owner initially presenting with pharyngeal diphtheria who later developed severe systemic DT-mediated symptoms including polyneuropathy (neuralgia, diplegia of both arms, acute disability of swallowing, hoarseness) and cardiomyopathia (Schuhegger and others 2009). Their medium-sized pig-breeding farm housing 500 pigs in a nonindustrialised manner was located in a remote rural village of Northern Bavaria. Moreover, two cases of cutaneous diphtheria caused by toxigenic C ulcerans in patients with occupational pig contact have recently been reported from Germany (Berger and others 2013): one involved a 63-year-old diabetic female pig farm worker with a plantar ulcer (strain number KL241), the other a 58-year-old male farmer with a calf wound infection (strain number KL203). Interestingly, non-toxigenic, but toxpositive (non-toxigenic tox-bearing (NTTB)) C ulcerans strains have been isolated from the caseous lymph nodes or organ abscesses from 12 wild boars originating from several regions in Germany (Contzen and others 2011, Eisenberg and others 2014). These findings suggesting a potential role for pigs as a reservoir for toxigenic C ulcerans resulting in subsequent human diphtheria infections prompted us to investigate the prevalence of nasal Corynebacterium species carriage in farm pigs. September 13, 2014 | Veterinary Record
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Paper Materials and methods
The study was conducted between August 1 and December 31, 2009. Forty-one swine farms in Bavaria were included: 16 pig-producing (39 per cent), 13 finishing (32 per cent) and 12 growing to finishing farms (29 per cent). Swabs from both nasal cavities were obtained from 411 pigs of different ages. In total, 5–12 pigs per farm were investigated. All farmers were offered occupational health counselling (including a clinical and microbiological examination for Corynebacterium carriage and/or diphtheria symptoms). Nasal swabs from those 30 farmers out of 27 pig farms who requested microbiological carriage screening for themselves were examined after obtaining informed consent. Swabs were put into sterile Amies transport medium (Protagerm Amies Agar, BioMerieux, Marcy l’Etoile, France), transported within one to two hours at 8°C to the laboratory and immediately plated onto tellurite agar plates (BD Tellurite Agar, Bection Dickinson, Heidelberg, Germany). Agar plates were incubated for 48 hours at 37°C under microaerophilic conditions. From each individual plate, up to five morphologically distinguishable colonies that were suggestive to comprise coryneform bacteria were subcultivated on sheep blood agar (Oxoid, Wesel, Germany) for 24 hours at 37°C under microaerophilic conditions. All catalase-positive isolates were Gram-stained and subjected to matrix-assisted laser desorption/ionisation time-of-flight mass spectrometry (MALDI-TOF MS) analysis as reported previously (Konrad and others 2010).
Results
The Corynebacterium species nasal carriage data are shown in Table 1. A total of 796 and 52 strains were isolated from pigs and farmers, respectively. All 411 asymptomatic pigs were colonised with Corynebacterium strains (average number of strains per pig: 1.93; range: 1–7). Eleven different species were isolated from the nasal cavities of the pigs. The most prevalent species was Corynebacterium xerosis, which was found in all but one of the pigs, followed by Brevibacterium stationis, which was recently proposed to belong to the Corynebacterium genus (Bernard and others 2010) and Corynebacterium confusum. The other eight species were only prevalent in less than 5 per cent of the animals. All but one of the 30 farmers harboured at least one Corynebacterium strain (average number of strains per farmer: 1.73; range: 0–3). Nine different species were isolated from the nasal swabs with the same three species being the most prevalent as in the pigs. No strain of any of the three potentially toxigenic Corynebacterium species was isolated either from the pigs or from their farmers, respectively.
Discussion
We started this prevalence study on Corynebacterium species nasal carriage among farm pigs and their farmers having been alerted by several diphtheria cases or diphtheria-like infections caused by toxigenic TABLE 1: Prevalence of Corynebacterium species nasal carriage in pigs (n=411) and their farmers (n=30) Species
Pigs, n (%)
Farmers, n (%)
Corynebacterium xerosis Brevibacterium stationis* Corynebacterium confusum Corynebacterium ammoniagenes Corynebacterium casei Corynebacterium camporealensis Corynebacterium testudinoris Corynebacterium amycolatum Corynebacterium freneyi Corynebacterium flavescens Corynebacterium glutamicum Corynebacterium accolens Corynebacterium propinquum Corynebacterium pseudodiphtheriticum
410 (99.8) 260 (63) 48 (12) 31 (7.5) 18 (4.4) 12 (3) 6 (1.5) 3 (0.7) 3 (0.7) 2 (0.5) 1 (0.25) 0 0 0
26 (87) 7 (23) 7 (23) 1 (3) 0 2 (7) 0 1 (3) 0 0 0 4 (13) 3 (10) 1 (3)
*Brevibacterium stationis has recently proposed to belong to the Corynebacterium genus (Bernard and others 2010)
Veterinary Record | September 13, 2014
C ulcerans in humans with occupational swine contact (Schuhegger and others 2009, Berger and others 2013). So far, no prevalence data for coryneform bacteria in pigs have been published; only 12 sporadic cases of NTTB C ulcerans infections in wild boars have come to our knowledge (Contzen and others 2011, Eisenberg and others 2014). To date, isolation of the two other potentially DT-producing species, that is, C diphtheriae or C pseudotuberculosis, from pigs has not yet been reported. In our study, none of the 411 swabbed pigs showed nasal carriage of any of the three potentially toxigenic Corynebacterium species However, due to the very high corynebacteria carriage rate of 100 per cent with up to seven different Corynebacterium species identified per nasal swab and plenty of colonies covering the agar plates, we cannot fully exclude that single colonies hiding between a large amount of other bacterial colonies might be missed, although up to five morphologically distinguishable colonies suggestive to comprise coryneform bacteria were subcultivated and subsequently analysed by MALDITOF MS. The 100 per cent carriage rate might be explained by the close contact between the animals that is enhanced by their typical behaviour using their snouts as soil-digging tools and sensory organs. Whereas animal infections with C diphtheriae are absolute rarities – in the last 40 years reported to affect horses (two toxigenic cases; Henricson and others 2000, Leggett and others 2010), cattle (one non-toxigenic case; Corboz and others 1996), cats (two non-toxigenic cases; Hall and others 2010) and dogs (two toxigenic and two non-toxigenic cases; Kraszewska and others 1979) – and the very sporadic animal-associated human C pseudotuberculosis infections – most reports dating back more than 15 years – are mainly restricted to people professionally exposed to cattle, sheep, goats or llamas (Peel and others 1997), human C ulcerans-caused diphtheria cases – many of them associated with animal contact – are considered as emergent infections (Wagner and others 2010, Wagner and others 2012). Therefore, C ulcerans is probably the only one of the three potentially toxigenic Corynebacterium species for which animal carriage might be considered as relevant from a public health point of view. So far, C ulcerans prevalence data in asymptomatic animals are published only for shelter dogs in Osaka, Japan (Katsukawa and others 2009, Katsukawa and others 2012), and Rio de Janeiro, Brazil (Dias and others 2010), showing carriage rates of 1.5 per cent (one toxigenic strain in 65 dogs; Katsukawa and others 2012), 7.5 per cent (42 toxigenic and 3 non-toxigenic strains from 583 dogs, one of them harbouring both a toxigenic and a non-toxigenic strain; Katsukawa and others 2009) and 1.7 per cent (one non-toxigenic strain in 60 dogs; Dias and others 2010), respectively. A comparison of the corynebacteria carriage rate among the clinically healthy farmers in our study with the results of screening investigations dealing with other healthy populations suggests a significantly higher carriage rate in pig farmers of 96.7 per cent than in staff working in hospital-based environments in Germany and Switzerland (69.9 per cent; von Graevenitz and others 1998), outpatients in Italy (18.6 per cent; Bergamini and others 2000), attendants of a public health laboratory in Italy (9.9 per cent; Mencarelli and others 1992) or school children in Greece (7.8 per cent; Kalapothaki and others 1984); it should be noted that tellurite-based screening agars were used in all studies. Moreover, the carriage rate of 1.73 species per individual was higher than those observed in other studies (1.0; Bergamini and others 2000, and 1.04; Mencarelli and others 1992). While in the other three studies either commercially available, that is, the API Coryne system (Biomérieux, France) (von Graevenitz and others 1998, Bergamini and others 2000), or in-house biochemical assays (Mencarelli and others 1992) were used for final species determination, MALDI-TOF MS was applied in our study. The composition of the isolated corynebacteria species spectrum also markedly differed – both quantitatively and qualitatively – between the farmers in our study and the healthy people from the other studies (see also Table 2): the carriage rates of the six most prevalent Corynebacterium species among the farmers fairly outnumbered those found in the other available studies – with the only exception of the relatively high carriage rate of 51.3 per cent for C durum in hospital-based staff (von Graevenitz and others 1998). Of the three most prevalent species in the farmer group,
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Paper TABLE 2: Prevalence of Corynebacterium spp. nasal carriage in different human populations Species Corynebacterium xerosis Brevibacterium stationis† Corynebacterium confusum Corynebacterium accolens Corynebacterium propinquum Corynebacterium camporealensis Corynebacterium pseudodiphtheriticum Corynebacterium amycolatum Corynebacterium ammoniagenes Corynebacterium durum Corynebacterium group G Corynebacterium jeikeium Corynebacterium spp. Corynebacterium argentoratense Corynebacterium minutissimum Corynebacterium group F-1 Corynebacterium matruchotii Corynebacterium urealyticum Corynebacterium ulcerans Corynebacterium striatum Corynebacterium group A-4
Present study, n (%) n=30
von Graevenitz and others (1998) n (%) n=113
26 (87) 7 (23) 7 (23) 4 (13) 3 (10) 2 (7) 1 (3) 1 (3) 1 (3)
1 (0.9)
Bergamini and others (2000), n (%) n=500
Mencarelli and others (1992) *, n (%) n=515
24 (4.8)
8 (1.6)
2 (1.8)
58 (51.3) 7 (6.2) 4 (3.5) 4 (3.5) 1 (0.9) 1 (0.9) 1 (0.9)
15 (3.0)
6 (1.2)
10 (2.0)
9 (1.7) 4 (0.8) 9 (1.8) 6 (1.2) 10 (2.0)
12 (2.3)
7 (1.4) 14 (2.7)
*Only cystinase-producing Corynebacterium spp. lacking urease activity were intended to be included in this study. However, during the study obviously also cystinasenegative, urease-positive strains were added (Mencarelli and others 1992) †Brevibacterium stationis has recently been proposed to belong to the Corynebacterium genus (Bernard and others 2010)
only one species, C xerosis, ranked among the three most prevalent species found in any of the other groups – although at a much lower rate of 4.8 per cent vs. 87 per cent. The species ranking among the three most common isolates found in at least two of the other studies, that is, Corynebacterium pseudodiphtheriticum, Corynebacterium matruchotii, Corynebacterium minutissimum, Corynebacterium striatum and Corynebacterium jeikeium, were either absent or were very rare in the farmer group. Interestingly, among these C pseudodiphtheriticum and C striatum were the two most often isolated Corynebacterium species in consecutively obtained swabs from the upper respiratory tract in symptomatic patients within a hospital setting (Riegel and others 1996). Interestingly, human nasal or throat carriage of nontoxigenic C ulcerans seems to be rare and was found in 1.2 per cent of healthy adults in Italy (Bergamini and others 2000) and in 0.01 per cent of people of all ages with sore throat in the UK (Wagner and others 2011), respectively. Taken together, the composition of the corynebacteria flora in the farmer group very much resembled that of the pigs in our study and profoundly differed from the species distribution isolated from healthy humans in other studies. This correlation might suggest the potential of transmission of the respective corynebacteria between pigs and farmers. So far, direct proof of transmission of toxigenic C ulcerans between animal and human by isolation of an identical strain from both an animal and its owner is documented only in four instances, two of them involving dogs (Lartigue and others 2005, Hogg and others 2009), two a cat (Berger and others 2011, Yoshimura and others 2014) and one a pig (Schuhegger and others 2009), respectively. Moreover, as mentioned above, NTTB C ulcerans strains have been isolated from 12 wild boars in Germany (Contzen and others 2011, Eisenberg and others 2014) and from one pig connected to a human diphtheria case (toxigenic; (Schuhegger and others 2009)), respectively.
Conclusion
In conclusion, although we were not able to find any of the three potentially toxigenic Corynebacterium species in our prevalence study among pigs, the – although only sporadic – isolation of tox-positive C ulcerans from pigs, the report of three pig-linked cases of human diphtheria (Schuhegger and others 2009, Berger and others 2013), as well as the similarity of the corynebacteria carriage pattern in pigs and their farmers in our study suggest that pigs might be a rare source for toxigenic C ulcerans infections in humans having prolonged and close contact with these animals.
Acknowledgements
We thank the farmers who volunteered to participate in this study. We also thank Wolfgang Schmidt, Karola Grünwald, Marzena Maggipinto and Daniela Sebah for cultivation, microbiological and molecular characterisation of the corynebacteria. Funding The study was partly supported by the Bavarian State Ministry of the Environment and Public Health and by the German Federal Ministry of Health via the Robert Koch-Institute and its National Reference Laboratories Network (09-47, FKZ 1369-359 and FKZ 415).
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Corynebacterium species nasal carriage in pigs and their farmers in Bavaria, Germany: implications for public health V. Boschert, A. Berger, R. Konrad, I. Huber, S. Hörmansdorfer, S. Zöls, M. Eddicks, M. Ritzmann and A. Sing Veterinary Record 2014 175: 248 originally published online July 18, 2014
doi: 10.1136/vr.102634 Updated information and services can be found at: http://veterinaryrecord.bmj.com/content/175/10/248
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