Avian Pathology, 2014 Vol. 43, No. 6, 498–500, http://dx.doi.org/10.1080/03079457.2014.966055
ORIGINAL ARTICLE
Prevalence of enteropathogenic bacteria in common quail (Coturnix coturnix) Ludovico Dipineto*, Tamara P. Russo, Antonio Gargiulo, Luca Borrelli, Luigi M. De Luca Bossa, Antonio Santaniello, Pasquale Buonocore, Lucia F. Menna, and Alessandro Fioretti Department of Veterinary Medicine and Animal Productions, Università di Napoli Federico II, Napoli, Italy
The study was aimed at evaluating the prevalence of enteropathogenic bacteria (i.e. Campylobacter spp., shigatoxin-producing Escherichia coli, Salmonella spp.) in common quail (Coturnix coturnix). To achieve this goal, 70 common quails were collected during the hunting season in the Campania region (southern Italy). From each bird, cloacal swab samples were collected and subjected to culture methods, polymerase chain reaction and serotyping. The results of the present study showed a prevalence of 21.4% and 5.7% for Campylobacter spp. and shigatoxin-producing E. coli, respectively. In contrast, no Salmonella spp. was isolated. These findings show that common quail, as migratory birds, may constitute an environmental carrier of these pathogens representing a source of infection for other birds, livestock and humans.
Introduction
Materials and Methods
Common quail (Coturnix coturnix) is a migratory galliformes species distributed across Eurasia during its breeding period. It should not be confused with the domesticated Japanese quail (Coturnix japonica), the eastern counterpart of common quail. In fact, even if these bird species are very similar, voice is unquestionably the best identification feature. The Japanese quail utters an abrupt chattering squawk whereas the common quail has a short rhythmic twitter. Moreover, The Japanese quail has a darker plumage than the common quail. According to Birdlife International (2004), common quail populations declined in many countries of central and northern Europe, leading to an unfavourable conservation status. Even so, the common quail is a popular game species with an important socio-economic impact. Restocking with farm-reared quails to increase hunting purposes is a very common practice in several European countries, such as Italy, Greece, The Republic of Serbia, Montenegro, Romania and Spain (Sanchez-Donoso et al., 2012). Although common quails are migratory birds, little is known about their role in the spread of zoonotic agents. The majority of studies, indeed, regard Japanese quail (C. japonica) as a “sister” species to the common quail, which is mainly distributed across eastern Asia (Yee et al., 2009; Ngulukun et al., 2010). In order to address this lack of information, the present study was undertaken with the aim to evaluate the prevalence of the most common zoonotic enteropathogenic bacteria (i.e. Campylobacter spp., shigatoxin-producing Escherichia coli [STEC], Salmonella spp.) in common quail.
Sampling. During the hunting season (September/October 2013), 70 common quails were collected in the province of Napoli and Salerno (Campania region, southern Italy). Quails were subdivided into adult (n = 51) and young (n = 19) birds and into female (n = 48) and male (n = 22) birds. Each quail was sampled three times from the cloaca using sterile cotton-tipped swabs for a total of three swab samples for each quail to detect, respectively, Campylobacter spp., STEC and Salmonella spp.
Isolation and identification of Campylobacter spp. To isolate Campylobacter spp., cloacal swab samples were inoculated into Campylobacter selective enrichment broth (Oxoid Ltd, Basingstoke, UK) and incubated at 42°C for 48 h under microaerobic conditions provided by CampyGen (Oxoid). Subsequently, each sample was streaked onto Campylobacter blood-free selective agar (CCDA; Oxoid). After incubation at 42°C for 48 h under microaerobic conditions, the plates were examined for typical Campylobacter colonies. Suspected colonies were sub-cultured on sheep blood agar (Oxoid) and finally incubated for 24 h at 42°C. Under phase contrast microscopy, colonies comprising curved or spiral motile rods were presumptively identified as Campylobacter spp. and submitted to a multiplex polymerase chain reaction (PCR). The extraction and purification of DNA from isolated colonies on sheep blood agar was performed using a Bactozol kit (Molecular Research Center, Inc., Cincinnati, OH, USA) as described previously (Gargiulo et al., 2008). All DNA extracts were examined, by a triplex PCR, for the presence of Campylobacter jejuni, Campylobacter coli and Campylobacter lari species using oligonucleotide primers ICJ-UP and ICJ-DN, ICC-UP and ICC-DN, and ICL-UP and ICLDN, respectively, as described previously (Gargiulo et al., 2008). The PCR conditions were as described by Gargiulo et al. (2008) and the products were separated by electrophoresis on 1.5% agarose gels (Gibco-BRL, Milan, Italy), stained with ethidium bromide and visualized under ultraviolet light. PCR amplified without DNA was used as negative control, whereas three reference Campylobacter strains (C. jejuni ATCC 29428, C. coli ATCC 33559 and C. lari ATCC 43675) obtained from LGC Promochem (Teddington, UK), were used as positive controls.
*To whom correspondence should be addressed: Tel: +39 0812536277. Fax: +39 0812536280. E-mail: [email protected] (Received 9 June 2014; accepted 21 August 2014) © 2014 Houghton Trust Ltd
Enteropathogenic bacteria in common quail Isolation, serotyping and characterization of shigatoxin-producing E. coli. To isolate STEC, cloacal swab samples were inoculated into 10 ml modified tryptone soy broth (Oxoid) supplemented with novobiocin (Oxoid). Samples were incubated at 37°C for 12 to 18 h and then inoculated onto sorbitol MacConkey agar (Oxoid) supplemented with cefixime-tellurite (Oxoid) and onto Rainbow Agar O157 (Biolog Inc., Hayward, CA, USA). After incubation at 37°C for 18 to 24 h, suspected colonies for E. coli O157 and other STEC were selected and screened by agglutination with an E. coli O157 latex test kit (Oxoid) and anti-coli polyspecific and monospecific sera (Sifin, Berlin, Germany). Isolated E. coli serotypes were subcultured on washed sheep blood plates, incubated overnight at 37°C and then subjected to a multiplex PCR assay to determine the presence of stx (stx1 and stx2) and the E. coli attaching and effacing (eae). DNA extraction and multiplex PCR assay for stx1, stx2 and eaeA gene amplification were performed as described previously (Wang et al., 2002; Dipineto et al., 2010). The PCR products were separated by electrophoresis on 1.5% agarose gels (GibcoBRL, Milan, Italy), stained with ethidium bromide and visualized under ultraviolet light. PCR amplified without the DNA was used as negative control, whereas one reference E. coli O157 ATCC 43894 strain (LGC Promochem) was used as positive control. Isolation of Salmonella spp. To isolate Salmonella spp., cloacal swabs were inoculated into buffered peptone water (Oxoid) and incubated at 37°C for 18 h. After incubation, samples were inoculated into Rappaport– Vassiliadis Broth (Oxoid) and incubated at 42°C for 18 h. The cultures obtained were plated onto xylose–lysine–desoxycholate agar (Oxoid), incubated at 37°C and examined after 24 h. Suspected colonies were inoculated onto a second selective agar (Brilliant Green Agar; Oxoid) and incubated at 37°C for 24 h. All isolates were biochemically identified using the API20-E system (bioMérieux, Milan, Italy). Statistical analysis. The quail data (age and sex, all categorical) were analysed by univariate (Pearson’s chi-square test for independence) statistical analysis using the Campylobacter spp. and STEC status (positive/ negative) as dependent variables. Statistical analysis was performed using SPSS 13 software for Windows (SPSS Inc., Chicago, IL, USA).
Results The present study showed the presence of Campylobacter spp. in 15/70 (21.4%; 95% confidence interval = 12.9 to 33.2%) quails examined. As proved by multiplex PCR, 100% of the strains were identified as C. coli (15⁄15), and six out of the 15 (40.0%) positive samples were also positive for C. jejuni. STEC were recovered in 4/70 (5.7%; 95% confidence interval = 1.8 to 14.7%) quails and were serotyped as E. coli O128 (n = 1) and E. coli O26 (n = 3). As proved by multiplex PCR, 100% of the strains carried stx1, stx2 and eae genes. In contrast, isolation of Salmonella spp. was consistently negative. No significant difference
499
(P > 0.05) related to sex and age was recorded for each bacteria. Results are presented in Table 1.
Discussion The findings of the present study suggest the occurrence of Campylobacter spp. and STEC in living common quails with a prevalence of 21.4% and 5.7%, respectively. Comparative data on the prevalence of campylobacteriosis in common quails are limited and the majority refers to Japanese quails. A study conducted by Ngulukun et al. (2010) in Nigeria isolated Campylobacter spp., with a predominance of C. jejuni, from 42/135 (31.1%) Japanese quail caecal samples. A similar study performed by Vashin & Stoyanchev (2005) in Bulgaria isolated Campylobacter spp. from 29/180 (16.1%) viscera collected from three Japanese quail flocks, with C. jejuni as the predominant species. Finally, a study conducted by Dogra & Ayyagari (1988) in India detected C. jejuni spp. from 4/23 (17.4%) domestic quails examined. Our results are in line with those reported by the previous authors although C. coli was the predominant Campylobacter species identified in our study. It was difficult to speculate on these differences, but similar studies conducted in other game birds (i.e. pheasant, partridge) showed that C. coli is frequently isolated with a prevalence higher than C. jejuni (Dipineto et al. 2008, 2009). With respect to STEC, our results show the occurrence of E. coli O128 and E. coli O26 serotypes in one quail and three quails, respectively. It was hard to compare our results because no comparative data on the presence of STEC in quails are available in the literature. It was not possible to make assumptions regarding the source of STEC infections in the present study because the common quail populations arriving in Italy come from an area stretching from Spain and Ukraine, with a few birds from northern Africa, and very little is known of those periods when quails are presumably in these areas. Negative results for Salmonella spp. are in line with those recorded in a study conducted by McCrea et al. (2006) in which no Salmonella was isolated from quail flocks examined. Our results suggest the common quail to be a potential carrier of enteropathogenic bacteria for other animals and for humans who during the hunting season utilize this avian species as a game bird. Finally, common quails, as migratory birds, may spread pathogens over a wide range, thus enhancing their carrier role.
Table 1. Prevalence of Campylobacter spp., STEC and Salmonella spp. isolated from 70 common quails stratified by sex (male/female), and age (young/adult).
Number of positive quails (% positive) Quail data Sex Male Female Age group Young Adult Total
Number of quails tested
Campylobacter
a
STEC
b
P value (chi-square) Campylobacter
STEC
22 48
6 (27.3) 9 (18.7)
1 (4.6) 3 (6.3)
0.419
0.775
19 51 70
2 (10.5) 13 (25.5) 15 (21.4)
1 (5.3) 3 (5.9) 4 (5.7)
0.175
0.921
a Campylobacter spp. were identified as C. coli (n = 15) and C. jejuni (n = 6). This latter species was isolated from mixed infections. bSTEC were serotyped as E. coli O26 (n = 3) and E. coli O128 (n = 1).
500
L. Dipineto et al.
References BirdLife International. (2004). Birds in Europe: Population Estimates, Trends and Conservation Status. BirdLife Conservation Series No. 12. Cambridge: Birdlife International. Dipineto, L., Gargiulo, A., De Luca Bossa, L.M., Rinaldi, L., Borrelli, L., Menna, L.F. & Fioretti, A. (2008). Prevalence of thermotolerant Campylobacter in pheasants (Phasianus colchicus). Avian Pathology, 37, 507–508. Dipineto, L., Gargiulo, A., De Luca Bossa, L.M., Rinaldi, L., Borrelli, L., Santaniello, A., Menna, L.F. & Fioretti, A. (2009). Prevalence of thermotolerant Campylobacter in partridges (Perdix perdix). Letters in Applied Microbiology, 49, 351–353. Dipineto, L., Gargiulo, A., Russo, T.P., De Luca Bossa, L.M., Borrelli, L., d’Ovidio, D., Sensale, M., Menna, L.F. & Fioretti, A. (2010). Survey of Escherichia coli O157 in captive frogs. Journal of Wildlife Diseases, 46, 944–946. Dogra, M.S.C. & Ayyagari, A. (1988). Isolation of Campylobacter jejuni from quails: an initial report. The British Veterinary Journal, 144, 411–412. Gargiulo, A., Rinaldi, L., D’Angelo, L., Dipineto, L., Borrelli, L., Fioretti, A. & Menna, L.F. (2008). Survey of Campylobacter jejuni in stray cats in southern Italy. Letters in Applied Microbiology, 46, 267–270.
McCrea, B.A., Tonooka, K.H., VanWorth, C., Boggs, C.L., Atwill, E.R. & Schrader, J.S. (2006). Prevalence of Campylobacter and Salmonella species on farm, after transport, and at processing in specialty market poultry. Poultry Science, 85, 136–143. Ngulukun, S.S., Oboegbulem, S.I., Fagbamila, I.O., Emennaa, P.E., Ankeli, P.I., Ardzard, S.S., Okeke, L.A., Ajayi, O.T., Usman, M., Muhammed, M.J., Odugbo, M.O. & Okewole, P.A. (2010). Isolation of thermophilic Campylobacter species from Japanese quails (Coturnix coturnix) in Vom, Nigeria. The Veterinary Record, 166, 147–148. Sanchez-Donoso, I., Vilà, C., Puigcerver, M., Butkauskas, D., Caballero de la Calle, J.R., Morales-Rodríguez, P.A. & Rodríguez-Teijeiro, J.D. (2012). Are farm-reared quails for game restocking really common quails (Coturnix coturnix)? a genetic approach. PLoS One, 7, e39031. Vashin, I. & Stoyanchev, T. (2005). Presence of Campylobacter spp. in meat and internal organs of Japanese quail (Coturnix coturnix). Trakia Journal of Sciences, 3, 23–25. Wang, G., Clark, C.G. & Rodgers, F.G. (2002). Detection in Escherichia coli of the genes encoding the major virulence factors, the genes defining the O157:H7 serotype, and components of the type 2 Shiga toxin family by multiplex PCR. Journal of Clinical Microbiology, 40, 3613–3619. Yee, K.S., Cardona, C.J. & Carpenter, T.E. (2009). Transmission of lowpathogenicity avian influenza virus of subtype H6N2 from chickens to Pekin ducks and Japanese quail (Coturnix coturnix japonica). Avian Pathology, 38, 59–64.
Copyright of Avian Pathology is the property of Taylor & Francis Ltd and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
ORIGINAL ARTICLE
Prevalence of enteropathogenic bacteria in common quail (Coturnix coturnix) Ludovico Dipineto*, Tamara P. Russo, Antonio Gargiulo, Luca Borrelli, Luigi M. De Luca Bossa, Antonio Santaniello, Pasquale Buonocore, Lucia F. Menna, and Alessandro Fioretti Department of Veterinary Medicine and Animal Productions, Università di Napoli Federico II, Napoli, Italy
The study was aimed at evaluating the prevalence of enteropathogenic bacteria (i.e. Campylobacter spp., shigatoxin-producing Escherichia coli, Salmonella spp.) in common quail (Coturnix coturnix). To achieve this goal, 70 common quails were collected during the hunting season in the Campania region (southern Italy). From each bird, cloacal swab samples were collected and subjected to culture methods, polymerase chain reaction and serotyping. The results of the present study showed a prevalence of 21.4% and 5.7% for Campylobacter spp. and shigatoxin-producing E. coli, respectively. In contrast, no Salmonella spp. was isolated. These findings show that common quail, as migratory birds, may constitute an environmental carrier of these pathogens representing a source of infection for other birds, livestock and humans.
Introduction
Materials and Methods
Common quail (Coturnix coturnix) is a migratory galliformes species distributed across Eurasia during its breeding period. It should not be confused with the domesticated Japanese quail (Coturnix japonica), the eastern counterpart of common quail. In fact, even if these bird species are very similar, voice is unquestionably the best identification feature. The Japanese quail utters an abrupt chattering squawk whereas the common quail has a short rhythmic twitter. Moreover, The Japanese quail has a darker plumage than the common quail. According to Birdlife International (2004), common quail populations declined in many countries of central and northern Europe, leading to an unfavourable conservation status. Even so, the common quail is a popular game species with an important socio-economic impact. Restocking with farm-reared quails to increase hunting purposes is a very common practice in several European countries, such as Italy, Greece, The Republic of Serbia, Montenegro, Romania and Spain (Sanchez-Donoso et al., 2012). Although common quails are migratory birds, little is known about their role in the spread of zoonotic agents. The majority of studies, indeed, regard Japanese quail (C. japonica) as a “sister” species to the common quail, which is mainly distributed across eastern Asia (Yee et al., 2009; Ngulukun et al., 2010). In order to address this lack of information, the present study was undertaken with the aim to evaluate the prevalence of the most common zoonotic enteropathogenic bacteria (i.e. Campylobacter spp., shigatoxin-producing Escherichia coli [STEC], Salmonella spp.) in common quail.
Sampling. During the hunting season (September/October 2013), 70 common quails were collected in the province of Napoli and Salerno (Campania region, southern Italy). Quails were subdivided into adult (n = 51) and young (n = 19) birds and into female (n = 48) and male (n = 22) birds. Each quail was sampled three times from the cloaca using sterile cotton-tipped swabs for a total of three swab samples for each quail to detect, respectively, Campylobacter spp., STEC and Salmonella spp.
Isolation and identification of Campylobacter spp. To isolate Campylobacter spp., cloacal swab samples were inoculated into Campylobacter selective enrichment broth (Oxoid Ltd, Basingstoke, UK) and incubated at 42°C for 48 h under microaerobic conditions provided by CampyGen (Oxoid). Subsequently, each sample was streaked onto Campylobacter blood-free selective agar (CCDA; Oxoid). After incubation at 42°C for 48 h under microaerobic conditions, the plates were examined for typical Campylobacter colonies. Suspected colonies were sub-cultured on sheep blood agar (Oxoid) and finally incubated for 24 h at 42°C. Under phase contrast microscopy, colonies comprising curved or spiral motile rods were presumptively identified as Campylobacter spp. and submitted to a multiplex polymerase chain reaction (PCR). The extraction and purification of DNA from isolated colonies on sheep blood agar was performed using a Bactozol kit (Molecular Research Center, Inc., Cincinnati, OH, USA) as described previously (Gargiulo et al., 2008). All DNA extracts were examined, by a triplex PCR, for the presence of Campylobacter jejuni, Campylobacter coli and Campylobacter lari species using oligonucleotide primers ICJ-UP and ICJ-DN, ICC-UP and ICC-DN, and ICL-UP and ICLDN, respectively, as described previously (Gargiulo et al., 2008). The PCR conditions were as described by Gargiulo et al. (2008) and the products were separated by electrophoresis on 1.5% agarose gels (Gibco-BRL, Milan, Italy), stained with ethidium bromide and visualized under ultraviolet light. PCR amplified without DNA was used as negative control, whereas three reference Campylobacter strains (C. jejuni ATCC 29428, C. coli ATCC 33559 and C. lari ATCC 43675) obtained from LGC Promochem (Teddington, UK), were used as positive controls.
*To whom correspondence should be addressed: Tel: +39 0812536277. Fax: +39 0812536280. E-mail: [email protected] (Received 9 June 2014; accepted 21 August 2014) © 2014 Houghton Trust Ltd
Enteropathogenic bacteria in common quail Isolation, serotyping and characterization of shigatoxin-producing E. coli. To isolate STEC, cloacal swab samples were inoculated into 10 ml modified tryptone soy broth (Oxoid) supplemented with novobiocin (Oxoid). Samples were incubated at 37°C for 12 to 18 h and then inoculated onto sorbitol MacConkey agar (Oxoid) supplemented with cefixime-tellurite (Oxoid) and onto Rainbow Agar O157 (Biolog Inc., Hayward, CA, USA). After incubation at 37°C for 18 to 24 h, suspected colonies for E. coli O157 and other STEC were selected and screened by agglutination with an E. coli O157 latex test kit (Oxoid) and anti-coli polyspecific and monospecific sera (Sifin, Berlin, Germany). Isolated E. coli serotypes were subcultured on washed sheep blood plates, incubated overnight at 37°C and then subjected to a multiplex PCR assay to determine the presence of stx (stx1 and stx2) and the E. coli attaching and effacing (eae). DNA extraction and multiplex PCR assay for stx1, stx2 and eaeA gene amplification were performed as described previously (Wang et al., 2002; Dipineto et al., 2010). The PCR products were separated by electrophoresis on 1.5% agarose gels (GibcoBRL, Milan, Italy), stained with ethidium bromide and visualized under ultraviolet light. PCR amplified without the DNA was used as negative control, whereas one reference E. coli O157 ATCC 43894 strain (LGC Promochem) was used as positive control. Isolation of Salmonella spp. To isolate Salmonella spp., cloacal swabs were inoculated into buffered peptone water (Oxoid) and incubated at 37°C for 18 h. After incubation, samples were inoculated into Rappaport– Vassiliadis Broth (Oxoid) and incubated at 42°C for 18 h. The cultures obtained were plated onto xylose–lysine–desoxycholate agar (Oxoid), incubated at 37°C and examined after 24 h. Suspected colonies were inoculated onto a second selective agar (Brilliant Green Agar; Oxoid) and incubated at 37°C for 24 h. All isolates were biochemically identified using the API20-E system (bioMérieux, Milan, Italy). Statistical analysis. The quail data (age and sex, all categorical) were analysed by univariate (Pearson’s chi-square test for independence) statistical analysis using the Campylobacter spp. and STEC status (positive/ negative) as dependent variables. Statistical analysis was performed using SPSS 13 software for Windows (SPSS Inc., Chicago, IL, USA).
Results The present study showed the presence of Campylobacter spp. in 15/70 (21.4%; 95% confidence interval = 12.9 to 33.2%) quails examined. As proved by multiplex PCR, 100% of the strains were identified as C. coli (15⁄15), and six out of the 15 (40.0%) positive samples were also positive for C. jejuni. STEC were recovered in 4/70 (5.7%; 95% confidence interval = 1.8 to 14.7%) quails and were serotyped as E. coli O128 (n = 1) and E. coli O26 (n = 3). As proved by multiplex PCR, 100% of the strains carried stx1, stx2 and eae genes. In contrast, isolation of Salmonella spp. was consistently negative. No significant difference
499
(P > 0.05) related to sex and age was recorded for each bacteria. Results are presented in Table 1.
Discussion The findings of the present study suggest the occurrence of Campylobacter spp. and STEC in living common quails with a prevalence of 21.4% and 5.7%, respectively. Comparative data on the prevalence of campylobacteriosis in common quails are limited and the majority refers to Japanese quails. A study conducted by Ngulukun et al. (2010) in Nigeria isolated Campylobacter spp., with a predominance of C. jejuni, from 42/135 (31.1%) Japanese quail caecal samples. A similar study performed by Vashin & Stoyanchev (2005) in Bulgaria isolated Campylobacter spp. from 29/180 (16.1%) viscera collected from three Japanese quail flocks, with C. jejuni as the predominant species. Finally, a study conducted by Dogra & Ayyagari (1988) in India detected C. jejuni spp. from 4/23 (17.4%) domestic quails examined. Our results are in line with those reported by the previous authors although C. coli was the predominant Campylobacter species identified in our study. It was difficult to speculate on these differences, but similar studies conducted in other game birds (i.e. pheasant, partridge) showed that C. coli is frequently isolated with a prevalence higher than C. jejuni (Dipineto et al. 2008, 2009). With respect to STEC, our results show the occurrence of E. coli O128 and E. coli O26 serotypes in one quail and three quails, respectively. It was hard to compare our results because no comparative data on the presence of STEC in quails are available in the literature. It was not possible to make assumptions regarding the source of STEC infections in the present study because the common quail populations arriving in Italy come from an area stretching from Spain and Ukraine, with a few birds from northern Africa, and very little is known of those periods when quails are presumably in these areas. Negative results for Salmonella spp. are in line with those recorded in a study conducted by McCrea et al. (2006) in which no Salmonella was isolated from quail flocks examined. Our results suggest the common quail to be a potential carrier of enteropathogenic bacteria for other animals and for humans who during the hunting season utilize this avian species as a game bird. Finally, common quails, as migratory birds, may spread pathogens over a wide range, thus enhancing their carrier role.
Table 1. Prevalence of Campylobacter spp., STEC and Salmonella spp. isolated from 70 common quails stratified by sex (male/female), and age (young/adult).
Number of positive quails (% positive) Quail data Sex Male Female Age group Young Adult Total
Number of quails tested
Campylobacter
a
STEC
b
P value (chi-square) Campylobacter
STEC
22 48
6 (27.3) 9 (18.7)
1 (4.6) 3 (6.3)
0.419
0.775
19 51 70
2 (10.5) 13 (25.5) 15 (21.4)
1 (5.3) 3 (5.9) 4 (5.7)
0.175
0.921
a Campylobacter spp. were identified as C. coli (n = 15) and C. jejuni (n = 6). This latter species was isolated from mixed infections. bSTEC were serotyped as E. coli O26 (n = 3) and E. coli O128 (n = 1).
500
L. Dipineto et al.
References BirdLife International. (2004). Birds in Europe: Population Estimates, Trends and Conservation Status. BirdLife Conservation Series No. 12. Cambridge: Birdlife International. Dipineto, L., Gargiulo, A., De Luca Bossa, L.M., Rinaldi, L., Borrelli, L., Menna, L.F. & Fioretti, A. (2008). Prevalence of thermotolerant Campylobacter in pheasants (Phasianus colchicus). Avian Pathology, 37, 507–508. Dipineto, L., Gargiulo, A., De Luca Bossa, L.M., Rinaldi, L., Borrelli, L., Santaniello, A., Menna, L.F. & Fioretti, A. (2009). Prevalence of thermotolerant Campylobacter in partridges (Perdix perdix). Letters in Applied Microbiology, 49, 351–353. Dipineto, L., Gargiulo, A., Russo, T.P., De Luca Bossa, L.M., Borrelli, L., d’Ovidio, D., Sensale, M., Menna, L.F. & Fioretti, A. (2010). Survey of Escherichia coli O157 in captive frogs. Journal of Wildlife Diseases, 46, 944–946. Dogra, M.S.C. & Ayyagari, A. (1988). Isolation of Campylobacter jejuni from quails: an initial report. The British Veterinary Journal, 144, 411–412. Gargiulo, A., Rinaldi, L., D’Angelo, L., Dipineto, L., Borrelli, L., Fioretti, A. & Menna, L.F. (2008). Survey of Campylobacter jejuni in stray cats in southern Italy. Letters in Applied Microbiology, 46, 267–270.
McCrea, B.A., Tonooka, K.H., VanWorth, C., Boggs, C.L., Atwill, E.R. & Schrader, J.S. (2006). Prevalence of Campylobacter and Salmonella species on farm, after transport, and at processing in specialty market poultry. Poultry Science, 85, 136–143. Ngulukun, S.S., Oboegbulem, S.I., Fagbamila, I.O., Emennaa, P.E., Ankeli, P.I., Ardzard, S.S., Okeke, L.A., Ajayi, O.T., Usman, M., Muhammed, M.J., Odugbo, M.O. & Okewole, P.A. (2010). Isolation of thermophilic Campylobacter species from Japanese quails (Coturnix coturnix) in Vom, Nigeria. The Veterinary Record, 166, 147–148. Sanchez-Donoso, I., Vilà, C., Puigcerver, M., Butkauskas, D., Caballero de la Calle, J.R., Morales-Rodríguez, P.A. & Rodríguez-Teijeiro, J.D. (2012). Are farm-reared quails for game restocking really common quails (Coturnix coturnix)? a genetic approach. PLoS One, 7, e39031. Vashin, I. & Stoyanchev, T. (2005). Presence of Campylobacter spp. in meat and internal organs of Japanese quail (Coturnix coturnix). Trakia Journal of Sciences, 3, 23–25. Wang, G., Clark, C.G. & Rodgers, F.G. (2002). Detection in Escherichia coli of the genes encoding the major virulence factors, the genes defining the O157:H7 serotype, and components of the type 2 Shiga toxin family by multiplex PCR. Journal of Clinical Microbiology, 40, 3613–3619. Yee, K.S., Cardona, C.J. & Carpenter, T.E. (2009). Transmission of lowpathogenicity avian influenza virus of subtype H6N2 from chickens to Pekin ducks and Japanese quail (Coturnix coturnix japonica). Avian Pathology, 38, 59–64.
Copyright of Avian Pathology is the property of Taylor & Francis Ltd and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
