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Short Communication
Short Communication Actinobacillus pleuropneumoniae serotypes 3, 6, 8 and 15 isolated from diseased pigs in North America M. Gottschalk, S. Lacouture Actinobacillus pleuropneumoniae is the causative agent of porcine pleuropneumonia, an economically important swine bacterial infection (Gottschalk 2012). It affects mainly the respiratory tract of pigs and occurs in all pig-keeping countries. The clinical disease in its outbreak presentation is relatively well controlled in the USA and Canada, but it is still a significant problem in Latin American, Asian and some European countries (Gottschalk 2012). Its importance derives from the fact that it can cause pneumonia that results in death; clinical disease may also become chronic or subclinical in successive batches of pigs and cause losses due to reduced production and increased costs of medication or vaccination (Gottschalk 2012). A pleuropneumoniae strains are classified on the basis of the nicotinamide adenine dinucleotide (NAD) requirement for growth into biovar I (NAD dependent) and biovar II (NAD independent) (Pohl and others 1983). A pleuropneumoniae biotype I has been divided into 13 serotypes, and biotype II into 2 serotypes, for a total of 15 serotypes, although some exceptions occur (Gottschalk 2012). Serotyping, based on antigenic characteristics of the capsular polysaccharide (CPS), is still an important tool to epidemiologically study A pleuropneumoniae strains. The distribution of prevalent serotypes recovered from diseased animals significantly varies in different continents (Gottschalk 2012). Serotyping is traditionally performed by serological methods (Mittal and others 1992). However, several cross-reactions are usually observed. Some of these cross-reactions are due to common epitopes present at the level of the long-chain polysaccharides within the lipopolysaccharide (LPS). This is the case, for example, with serotypes 1/9/11, serotypes 4/7 and serotypes 3/6/8/15 (Gottschalk 2012). In order to circumvent these cross-reactions, monoclonal antibodies have been developed for some serotypes. However, those reacting with the LPS moiety still present cross-reactivity with more than one serotype (Lacouture and others 1997, Lebrun and others 1999). More recently, serotype-specific PCR methods (based on CPS-specific genes) have been developed for serotypes 1, 2, 3, 5, 6, 7, 8 and 12 (Angen and others 2008, Zhou and others 2008, Ito 2010). The total number of clinical cases has decreased in the last years in North America. In conventional herds, serotypes 5 and 7 are those most frequently isolated from diseased animals (Gottschalk, unpublished data). In high-health status herds, cases of swine Veterinary Record (2014) M. Gottschalk, DVM, PhD, S. Lacouture, BSc, Department of Pathology and Microbiology, Faculty of Veterinary Medicine, University of Montreal, 3200 Sicotte, Saint-Hyacinthe, Quebec, Canada J2S 2M2
doi: 10.1136/vr.102470 E-mail for correspondence: [email protected] Provenance: not commissioned; externally peer reviewed Accepted March 10, 2014
pleuropneumonia are usually associated with either serotype 12 or serogroup 3/6/8 strains. Field strains reacting with antiserotype 15, but antigenically related to the 3/6/8 group, have also been isolated (Gottschalk 2012). Using antisera, final identification of the serotype within this group is extremely difficult. In the last years, Zhou and others (2008) developed a PCR that is able to differentiate among serotypes 3, 6 and 8. Using this test, O’Neill and others (2010) have studied more than 370 field strains collected from England and Wales between 1995 and 2007. Although previous serological results had shown that serotype 3 was predominant, PCR revealed that this serotype was almost absent from that collection (only one isolate), whereas, serotype 8 was the predominant serotype in that country. The aim of the present study was to identify the actual serotype by PCR from a collection of field strains recovered from diseased pigs in Canada and the USA from 2007 to 2013. These strains had been previously serotyped by a traditional coagglutination test using serotype-specific polyclonal antibodies (Mittal and others 1992). A total of 74 field strains were isolated from acutely affected pigs with pleuropneumonia at the Diagnostic Service of the University of Montreal (Canada), or were sent for further identification from different diagnostic laboratories throughout the USA. All isolates presenting a clear reaction by the coagglutination test with antisera against serotypes 3, 6, 8 and/or 15 were included in the study. The PCR of Zhou and others (2008) was then applied to all strains. Additionally, the PCR described by Frey and others (1995) was used to identify the presence of toxin genes. By serotyping, most strains could not be easily associated with a single serotype, and none of the strains presented a clear reaction with only one antiserum. Fifty percent of the strains presented cross-reactions between serotypes 6 and 8 by coagglutination. The remaining strains presented a reaction with two or three different serotypes. The use of an additional test (immunodiffusion) did not significantly change results (data not shown). Results by PCR are shown in Table 1. A total of 53 strains (72 per cent) were shown to be serotype 8, 9 (12 per cent) serotype 6, one strain (1 per cent) presented a double reaction with serotypes 3 and 6, and the remaining 11 strains (15 per cent) did not present any reaction by PCR. No serotype 3 strains could be identified. It seems clear that for this serogroup, serotype 8 is, by far, the most frequent serotype isolated in North America, followed by serotype 6. Similar results were previously reported in England and Wales where serotype 8 was the most frequently found, and serotype 3 was seldom detected (O’Neill and others 2010). Interestingly, 11 strains presented a clear reaction with antiserotype 15 serum, additional reactions with serotypes 3 and/or 6 antisera, and a negative reaction with the PCR for serotypes 3, 6, 8. These strains were also negative in a PCR specific tests for serotypes 1/9/11, 2, 5, 7 and 12 (Angen and others 2008, Zhou and others 2008, Ito 2010, Marois-Créhan and others 2014). They were also negative when tested with monoclonal antibodies reacting with serotype 4 (Lebrun and others 1999). Finally, by coagglutination, they presented a negative reaction with antisera against serotypes 13 and 14. Although there are no gene-based typing methods for serotype 15, we can speculate that these strains probably belong to this serotype. However, the possibility that some of these strains belong to serotypes 3, 6 or 8 (cross-reacting with serotype 15), and present a negative reaction using the PCR for these serotypes, cannot be completely ruled out. In fact, it has previously been shown that some atypical Japanese serotype 3 strains may exceptionally present negative results by this PCR (Kuhnert and others 2011). Strains described in that report, however, presented an atypical toxin profile, which was not the case for any of the strains characterised in the present study. In fact, all 74 strains presented an apxIICA; apxIIICA; apxIBD; apxIIIBD gene pattern, typical of serotypes 2, 4, 6, 8 and 15, as shown in Table 1. As mentioned, one strain presented a 3/6 pattern by PCR. Very recently, Ito and others (2013) have reported the isolation of two May 3, 2014 | Veterinary Record
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Short Communication TABLE 1: Serotype distribution following PCR tests for Actinobacillus pleuropneumoniae strains recovered from diseased pigs in North America, and presenting cross-reactions by serology with antisera against serotypes 3, 6, 8 and/or 15 Serotype
Number of strains (percentage)
3 6
0 (0) 9 (12)
8
53 (72)
3, 6 Unknown
1 (1) 11 (15)
Toxine profile not done apxIICA; apxIIICA; apxIBD; apxIIIBD apxIICA; apxIIICA; apxIBD; apxIIIBD apxIICA; apxIIICA; apxIBD; apxIIIBD apxIICA; apxIIICA; apxIBD; apxIIIBD
serotype 6 strains presenting a similar pattern. When the North American strain was tested with a monoplex PCR for serotypes 3, 6 and 8, identical positive results were obtained for both serotypes 3 and 6. So, it is possible that the atypical strain identified in this study is similar to those previously reported in Japan. In conclusion, and similarly to what has been reported in the UK, A pleuropneumoniae serotype 8 is, by far, the predominant serotype, within the 3/6/8/15 cross-reacting group, isolated from diseased pigs in North America. So far, there is no clear indication of isolation of ‘true’ serotype 3 A pleuropneumoniae strains in Canada and the USA. A report of clinical disease in Canada caused by this serotype was published 30 years ago (Desrosiers and others 1984), but the serotyping techniques used and available at the time were such that it is not possible to confirm that the strain was indeed a ‘true’ serotype 3 strain. Finally, the development of primers specific for A pleuropneumoniae serotype 15 would be important to confirm the presence of this serotype among 3/6/8 PCR-negative strains from North America.
Acknowledgements
This work was funded by the Diagnostic Service of the University of Montreal.
References
ANGEN, O., AHRENS P. & JESSING, S. G. (2008) Development of a multiplex PCR test for identification of Actinobacillus pleuropneumoniae serovars 1, 7, and 12. Veterinary Microbiology 132, 312–318
Veterinary Record | May 3, 2014
DESROSIERS, R., MITTAL, K. R. & MALO, R. (1984) Porcine pleuropneumonia associated with Haemophilus pleuropneumoniae serotype 3 in Quebec. Veterinary Record 115, 628–629 FREY, J., BECK, M., VAN DEN BOSCH, J. F., SEGERS, R. P. A. M. & NICOLET, J. (1995) Development of an efficient PCR method for toxin typing of Actinobacillus pleuropneumoniae strains. Molecular and Cellular Probes 9, 277–282 GOTTSCHALK, M. (2012) Actinobacillosis. In Diseases of Swine. Ed. B. E. STRAW, J. J. ZIMMERMAN, S. D’ALLAIRE & D. J. TAYLOR. Ames, Iowa, USA: Blackwell Publishing pp 653–669 ITO, H. (2010) Development of a cps-based multiplex PCR for typing of Actinobacillus pleuropneumoniae serotypes 1, 2 and 5. Journal of Veterinary Medical Science 72, 653–655 ITO, H., KATSURAGI, K., AKAMA, S. & YUZAWA, H. (2013) Isolation of atypical genotype Actinobacillus pleuropneumoniae serotype 6 in Japan. Journal of Veterinary Medical Science. [Epub ahead of print] KUHNERT, P., ROHDE, J. & KORCZAK B. M. (2011) A new variant of Actinobacillus pleuropneumoniae serotype 3 lacking the entire apxII operon. Journal of Veterinary Diagnostic Investigation 23, 556–559 LACOUTURE, S., MITTAL, K. R., JACQUES, M. & GOTTSCHALK, M. (1997) Serotyping Actinobacillus pleuropneumoniae by the use of monoclonal antibodies. Journal of Veterinary Diagnostic Investestigation 9, 337–341 LEBRUN, A., LACOUTURE, S., CÔTÉ, D., MITTAL, K. R. & GOTTSCHALK, M. (1999) Identification of Actinobacillus pleuropneumoniae strains of serotypes 7 and 4 using monoclonal antibodies: demonstration of common LPS O-chain epitopes with Actinobacillus lignieresii. Veterinary Microbiology 65, 271–282 MAROIS-CRÉHAN, C., LACOUTURE, S., JACQUES, M., FITTIPALDI, N., KOBISCH, M. & GOTTSCHALK, M. (2014) Development of two real-time polymerase chain reaction assays to detect Actinobacillus pleuropneumoniae serovars 1-9-11 and serovar 2. Journal of Veterinary Diagnostic Investigation. 26, 146–149 MITTAL, K. R., HIGGINS, R., LARIVIERE, S. & NADEAU, M. (1992) Serological characterization of Actinobacillus pleuropneumoniae strains isolated from pigs in Quebec. Veterinary Microbiology 32, 135–148 O’NEILL, C., JONES, S. C., BOSSÉ, J. T., WATSON, C. M., WILLIAMSON, S. M., RYCROFT, A. N., KROLL, J. S. HARTLEY, H. M. & LANGFORD, H. M. (2010) Prevalence of Actinobacillus pleuropneumoniae serovars in England and Wales. Veterinary Record 167, 661–662 POHL, S., BERTSCHINGER, H. U., FREDERIKSEN, W. & MANNHEIM, W. (1983) Transfer of Haemophilus pleuropneumoniae and the Pasteurella haemolytica-like organism causing porcine necrotic pleuropneumonia to the genus Actinobacillus (Actinobacillus pleuropneumoniae comb. nov.) on the basis of phenotypic and deoxyribonucleic acid relatedness. International Journal of Systematic Bacteriology 33, 510–514 ZHOU, L., JONES, S. C., ANGEN, O., BOSSÉ, J. T., NASH, J. H., FREY, J., ZHOU, R., CHEN, H. C., KROLL, J. S., RYCROFT, A. N. & LANGFORD, P. R. (2008) Multiplex PCR that can distinguish between immunologically cross- reactive serovar 3, 6, and 8 Actinobacillus pleuropneumoniae strains. Journal of Clincial Microbiology 46, 800–803
Downloaded from http://veterinaryrecord.bmj.com/ on June 6, 2015 - Published by group.bmj.com
Actinobacillus pleuropneumoniae serotypes 3, 6, 8 and 15 isolated from diseased pigs in North America M. Gottschalk and S. Lacouture Veterinary Record 2014 174: 452 originally published online April 1, 2014
doi: 10.1136/vr.102470 Updated information and services can be found at: http://veterinaryrecord.bmj.com/content/174/18/452.2
These include:
References Email alerting service
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Short Communication
Short Communication Actinobacillus pleuropneumoniae serotypes 3, 6, 8 and 15 isolated from diseased pigs in North America M. Gottschalk, S. Lacouture Actinobacillus pleuropneumoniae is the causative agent of porcine pleuropneumonia, an economically important swine bacterial infection (Gottschalk 2012). It affects mainly the respiratory tract of pigs and occurs in all pig-keeping countries. The clinical disease in its outbreak presentation is relatively well controlled in the USA and Canada, but it is still a significant problem in Latin American, Asian and some European countries (Gottschalk 2012). Its importance derives from the fact that it can cause pneumonia that results in death; clinical disease may also become chronic or subclinical in successive batches of pigs and cause losses due to reduced production and increased costs of medication or vaccination (Gottschalk 2012). A pleuropneumoniae strains are classified on the basis of the nicotinamide adenine dinucleotide (NAD) requirement for growth into biovar I (NAD dependent) and biovar II (NAD independent) (Pohl and others 1983). A pleuropneumoniae biotype I has been divided into 13 serotypes, and biotype II into 2 serotypes, for a total of 15 serotypes, although some exceptions occur (Gottschalk 2012). Serotyping, based on antigenic characteristics of the capsular polysaccharide (CPS), is still an important tool to epidemiologically study A pleuropneumoniae strains. The distribution of prevalent serotypes recovered from diseased animals significantly varies in different continents (Gottschalk 2012). Serotyping is traditionally performed by serological methods (Mittal and others 1992). However, several cross-reactions are usually observed. Some of these cross-reactions are due to common epitopes present at the level of the long-chain polysaccharides within the lipopolysaccharide (LPS). This is the case, for example, with serotypes 1/9/11, serotypes 4/7 and serotypes 3/6/8/15 (Gottschalk 2012). In order to circumvent these cross-reactions, monoclonal antibodies have been developed for some serotypes. However, those reacting with the LPS moiety still present cross-reactivity with more than one serotype (Lacouture and others 1997, Lebrun and others 1999). More recently, serotype-specific PCR methods (based on CPS-specific genes) have been developed for serotypes 1, 2, 3, 5, 6, 7, 8 and 12 (Angen and others 2008, Zhou and others 2008, Ito 2010). The total number of clinical cases has decreased in the last years in North America. In conventional herds, serotypes 5 and 7 are those most frequently isolated from diseased animals (Gottschalk, unpublished data). In high-health status herds, cases of swine Veterinary Record (2014) M. Gottschalk, DVM, PhD, S. Lacouture, BSc, Department of Pathology and Microbiology, Faculty of Veterinary Medicine, University of Montreal, 3200 Sicotte, Saint-Hyacinthe, Quebec, Canada J2S 2M2
doi: 10.1136/vr.102470 E-mail for correspondence: [email protected] Provenance: not commissioned; externally peer reviewed Accepted March 10, 2014
pleuropneumonia are usually associated with either serotype 12 or serogroup 3/6/8 strains. Field strains reacting with antiserotype 15, but antigenically related to the 3/6/8 group, have also been isolated (Gottschalk 2012). Using antisera, final identification of the serotype within this group is extremely difficult. In the last years, Zhou and others (2008) developed a PCR that is able to differentiate among serotypes 3, 6 and 8. Using this test, O’Neill and others (2010) have studied more than 370 field strains collected from England and Wales between 1995 and 2007. Although previous serological results had shown that serotype 3 was predominant, PCR revealed that this serotype was almost absent from that collection (only one isolate), whereas, serotype 8 was the predominant serotype in that country. The aim of the present study was to identify the actual serotype by PCR from a collection of field strains recovered from diseased pigs in Canada and the USA from 2007 to 2013. These strains had been previously serotyped by a traditional coagglutination test using serotype-specific polyclonal antibodies (Mittal and others 1992). A total of 74 field strains were isolated from acutely affected pigs with pleuropneumonia at the Diagnostic Service of the University of Montreal (Canada), or were sent for further identification from different diagnostic laboratories throughout the USA. All isolates presenting a clear reaction by the coagglutination test with antisera against serotypes 3, 6, 8 and/or 15 were included in the study. The PCR of Zhou and others (2008) was then applied to all strains. Additionally, the PCR described by Frey and others (1995) was used to identify the presence of toxin genes. By serotyping, most strains could not be easily associated with a single serotype, and none of the strains presented a clear reaction with only one antiserum. Fifty percent of the strains presented cross-reactions between serotypes 6 and 8 by coagglutination. The remaining strains presented a reaction with two or three different serotypes. The use of an additional test (immunodiffusion) did not significantly change results (data not shown). Results by PCR are shown in Table 1. A total of 53 strains (72 per cent) were shown to be serotype 8, 9 (12 per cent) serotype 6, one strain (1 per cent) presented a double reaction with serotypes 3 and 6, and the remaining 11 strains (15 per cent) did not present any reaction by PCR. No serotype 3 strains could be identified. It seems clear that for this serogroup, serotype 8 is, by far, the most frequent serotype isolated in North America, followed by serotype 6. Similar results were previously reported in England and Wales where serotype 8 was the most frequently found, and serotype 3 was seldom detected (O’Neill and others 2010). Interestingly, 11 strains presented a clear reaction with antiserotype 15 serum, additional reactions with serotypes 3 and/or 6 antisera, and a negative reaction with the PCR for serotypes 3, 6, 8. These strains were also negative in a PCR specific tests for serotypes 1/9/11, 2, 5, 7 and 12 (Angen and others 2008, Zhou and others 2008, Ito 2010, Marois-Créhan and others 2014). They were also negative when tested with monoclonal antibodies reacting with serotype 4 (Lebrun and others 1999). Finally, by coagglutination, they presented a negative reaction with antisera against serotypes 13 and 14. Although there are no gene-based typing methods for serotype 15, we can speculate that these strains probably belong to this serotype. However, the possibility that some of these strains belong to serotypes 3, 6 or 8 (cross-reacting with serotype 15), and present a negative reaction using the PCR for these serotypes, cannot be completely ruled out. In fact, it has previously been shown that some atypical Japanese serotype 3 strains may exceptionally present negative results by this PCR (Kuhnert and others 2011). Strains described in that report, however, presented an atypical toxin profile, which was not the case for any of the strains characterised in the present study. In fact, all 74 strains presented an apxIICA; apxIIICA; apxIBD; apxIIIBD gene pattern, typical of serotypes 2, 4, 6, 8 and 15, as shown in Table 1. As mentioned, one strain presented a 3/6 pattern by PCR. Very recently, Ito and others (2013) have reported the isolation of two May 3, 2014 | Veterinary Record
Downloaded from http://veterinaryrecord.bmj.com/ on June 6, 2015 - Published by group.bmj.com
Short Communication TABLE 1: Serotype distribution following PCR tests for Actinobacillus pleuropneumoniae strains recovered from diseased pigs in North America, and presenting cross-reactions by serology with antisera against serotypes 3, 6, 8 and/or 15 Serotype
Number of strains (percentage)
3 6
0 (0) 9 (12)
8
53 (72)
3, 6 Unknown
1 (1) 11 (15)
Toxine profile not done apxIICA; apxIIICA; apxIBD; apxIIIBD apxIICA; apxIIICA; apxIBD; apxIIIBD apxIICA; apxIIICA; apxIBD; apxIIIBD apxIICA; apxIIICA; apxIBD; apxIIIBD
serotype 6 strains presenting a similar pattern. When the North American strain was tested with a monoplex PCR for serotypes 3, 6 and 8, identical positive results were obtained for both serotypes 3 and 6. So, it is possible that the atypical strain identified in this study is similar to those previously reported in Japan. In conclusion, and similarly to what has been reported in the UK, A pleuropneumoniae serotype 8 is, by far, the predominant serotype, within the 3/6/8/15 cross-reacting group, isolated from diseased pigs in North America. So far, there is no clear indication of isolation of ‘true’ serotype 3 A pleuropneumoniae strains in Canada and the USA. A report of clinical disease in Canada caused by this serotype was published 30 years ago (Desrosiers and others 1984), but the serotyping techniques used and available at the time were such that it is not possible to confirm that the strain was indeed a ‘true’ serotype 3 strain. Finally, the development of primers specific for A pleuropneumoniae serotype 15 would be important to confirm the presence of this serotype among 3/6/8 PCR-negative strains from North America.
Acknowledgements
This work was funded by the Diagnostic Service of the University of Montreal.
References
ANGEN, O., AHRENS P. & JESSING, S. G. (2008) Development of a multiplex PCR test for identification of Actinobacillus pleuropneumoniae serovars 1, 7, and 12. Veterinary Microbiology 132, 312–318
Veterinary Record | May 3, 2014
DESROSIERS, R., MITTAL, K. R. & MALO, R. (1984) Porcine pleuropneumonia associated with Haemophilus pleuropneumoniae serotype 3 in Quebec. Veterinary Record 115, 628–629 FREY, J., BECK, M., VAN DEN BOSCH, J. F., SEGERS, R. P. A. M. & NICOLET, J. (1995) Development of an efficient PCR method for toxin typing of Actinobacillus pleuropneumoniae strains. Molecular and Cellular Probes 9, 277–282 GOTTSCHALK, M. (2012) Actinobacillosis. In Diseases of Swine. Ed. B. E. STRAW, J. J. ZIMMERMAN, S. D’ALLAIRE & D. J. TAYLOR. Ames, Iowa, USA: Blackwell Publishing pp 653–669 ITO, H. (2010) Development of a cps-based multiplex PCR for typing of Actinobacillus pleuropneumoniae serotypes 1, 2 and 5. Journal of Veterinary Medical Science 72, 653–655 ITO, H., KATSURAGI, K., AKAMA, S. & YUZAWA, H. (2013) Isolation of atypical genotype Actinobacillus pleuropneumoniae serotype 6 in Japan. Journal of Veterinary Medical Science. [Epub ahead of print] KUHNERT, P., ROHDE, J. & KORCZAK B. M. (2011) A new variant of Actinobacillus pleuropneumoniae serotype 3 lacking the entire apxII operon. Journal of Veterinary Diagnostic Investigation 23, 556–559 LACOUTURE, S., MITTAL, K. R., JACQUES, M. & GOTTSCHALK, M. (1997) Serotyping Actinobacillus pleuropneumoniae by the use of monoclonal antibodies. Journal of Veterinary Diagnostic Investestigation 9, 337–341 LEBRUN, A., LACOUTURE, S., CÔTÉ, D., MITTAL, K. R. & GOTTSCHALK, M. (1999) Identification of Actinobacillus pleuropneumoniae strains of serotypes 7 and 4 using monoclonal antibodies: demonstration of common LPS O-chain epitopes with Actinobacillus lignieresii. Veterinary Microbiology 65, 271–282 MAROIS-CRÉHAN, C., LACOUTURE, S., JACQUES, M., FITTIPALDI, N., KOBISCH, M. & GOTTSCHALK, M. (2014) Development of two real-time polymerase chain reaction assays to detect Actinobacillus pleuropneumoniae serovars 1-9-11 and serovar 2. Journal of Veterinary Diagnostic Investigation. 26, 146–149 MITTAL, K. R., HIGGINS, R., LARIVIERE, S. & NADEAU, M. (1992) Serological characterization of Actinobacillus pleuropneumoniae strains isolated from pigs in Quebec. Veterinary Microbiology 32, 135–148 O’NEILL, C., JONES, S. C., BOSSÉ, J. T., WATSON, C. M., WILLIAMSON, S. M., RYCROFT, A. N., KROLL, J. S. HARTLEY, H. M. & LANGFORD, H. M. (2010) Prevalence of Actinobacillus pleuropneumoniae serovars in England and Wales. Veterinary Record 167, 661–662 POHL, S., BERTSCHINGER, H. U., FREDERIKSEN, W. & MANNHEIM, W. (1983) Transfer of Haemophilus pleuropneumoniae and the Pasteurella haemolytica-like organism causing porcine necrotic pleuropneumonia to the genus Actinobacillus (Actinobacillus pleuropneumoniae comb. nov.) on the basis of phenotypic and deoxyribonucleic acid relatedness. International Journal of Systematic Bacteriology 33, 510–514 ZHOU, L., JONES, S. C., ANGEN, O., BOSSÉ, J. T., NASH, J. H., FREY, J., ZHOU, R., CHEN, H. C., KROLL, J. S., RYCROFT, A. N. & LANGFORD, P. R. (2008) Multiplex PCR that can distinguish between immunologically cross- reactive serovar 3, 6, and 8 Actinobacillus pleuropneumoniae strains. Journal of Clincial Microbiology 46, 800–803
Downloaded from http://veterinaryrecord.bmj.com/ on June 6, 2015 - Published by group.bmj.com
Actinobacillus pleuropneumoniae serotypes 3, 6, 8 and 15 isolated from diseased pigs in North America M. Gottschalk and S. Lacouture Veterinary Record 2014 174: 452 originally published online April 1, 2014
doi: 10.1136/vr.102470 Updated information and services can be found at: http://veterinaryrecord.bmj.com/content/174/18/452.2
These include:
References Email alerting service
This article cites 12 articles, 4 of which you can access for free at: http://veterinaryrecord.bmj.com/content/174/18/452.2#BIBL Receive free email alerts when new articles cite this article. Sign up in the box at the top right corner of the online article.
Notes
To request permissions go to: http://group.bmj.com/group/rights-licensing/permissions To order reprints go to: http://journals.bmj.com/cgi/reprintform To subscribe to BMJ go to: http://group.bmj.com/subscribe/
