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Short Communication
Characteristics of sheep flocks affected by Streptococcus dysgalactiae arthritis S.-J. Rutherford, S. Jeckel, A. Ridler IN the UK, Streptococcus dysgalactiae is the most common cause of infectious arthritis ( joint ill) in lambs aged up to four weeks (Watkins and Sharp 1998). Relatively little is known about the disease and much of this is limited to Animal Health and Veterinary Laboratories Agency – Weybridge (AHVLA - Weybridge) and Scottish Agricultural College (SAC) reports (eg Anon 2006, 2007, 2008, 2011a, b, c). The aims of this paper are to describe the characteristics of affected flocks in England and Wales, the application of treatment regimens and the antimicrobial resistance status of ovine S dysgalactiae isolates. Affected flocks were defined as having at least 2 per cent of lambs showing clinical signs consistent with joint ill from which S dysgalactiae was isolated from joint fluid from at least one lamb. During 2008, 2009 and 2010, affected flocks in England and Wales were identified via the AHVLA - Weybridge database or direct notification from veterinary surgeons or flock owners who had been encouraged to participate via rural press, word of mouth and during conference attendance. A questionnaire containing 50 questions on the general attributes of the flock, management practices during lambing and lamb disease history was administered to flock owners via post, telephone interview or farm visit. In addition, those flocks which were identified at the time of a disease outbreak were visited and flock managers were informally observed and interviewed on treatment regimens. Twenty-five S dysgalactiae isolates were subjected to antimicrobial resistance testing using methods based on those of the British Society for Antimicrobial Chemotherapy (Anon 2011d). Those tested were penicillin (1 unit), amoxicillin/clavulanate (30 μg), cephalexin (30 μg), tetracycline (10 μg), trimethoprim/ sulphonamide (25 μg), sulphamethoxanole, (25 μg), enrofloxacin (5 μg) and ciprofloxacin (5 μg). A total of 60 affected flocks from England and Wales were identified. Thirty-six flocks returned usable questionnaires and 19 of these flocks were visited. Flock characteristics and lambing management is summarised in Table 1. The farmer-reported within-flock joint ill prevalence averaged 4 per cent (range 2–20 per cent) and according to farmer estimates an average of 19 per cent of affected lambs subsequently died (range 0–75 per cent). Fourteen flocks (39 per cent) routinely gave all newborn lambs Veterinary Record (2015) S.-J. Rutherford, BSc, PhD, Department of Veterinary Clinical Sciences, Royal Veterinary College, Hawkshead Lane, Hatfield, Hertfordshire AL97TA, UK S. Jeckel, DrVetMed, MRCVS, Department of Pathology and Pathogen Biology, Royal Veterinary College, Hawkshead Lane, Hatfield, Hertfordshire AL97TA, UK
doi: 10.1136/vr.102781 A. Ridler, BVSc, PhD, DipECSRHM, Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Private Bag 11-222, Palmerston North, New Zealand E-mail for correspondence: [email protected] Provenance: Not commissioned; externally peer reviewed
injectable antimicrobials for the purpose of preventing joint ill; most commonly penicillin, amoxicillin or oxytetracycline. Seventeen flocks reported which antimicrobials were used for treatment of affected lambs. These were penicillin plus streptomycin (five flocks), penicillin (four flocks), amoxicillin (four flocks), amoxicillin plus clavulanic acid (two flocks), oxytetracycline (one flock) and tylosin (one flock). Of the 19 flocks that were visited, almost all lambs were turned out in the fields by the time cases were identified. In terms of recording treatments, two flocks had a high level of recording using electronic ear-tags and hand-held data loggers. In 14 flocks, a colour marker was sprayed onto the back of each lamb at each treatment; most lambs received one to five treatments but not necessarily on consecutive days. In three flocks, no recording was undertaken; lambs were treated on an ad hoc basis. The flocks with the highest reported lamb mortality rates due to joint ill were those where no recording was undertaken. All 25 bacterial isolates were resistant to tetracycline and two isolates from one flock were resistant to penicillin. This is the first study that has described the characteristics of flocks affected by S dysgalactiae joint ill. However, the study design and number of responses mean it is not possible to make comparisons between farms or between years. Despite several methods used to identify affected flocks in England and Wales over several years, only 60 were identified. This is likely an under-representation but nevertheless, given that there are greater than 60,000 holdings with more than 20–25 sheep in
TABLE 1: Characteristics of 36 English and Welsh sheep flocks affected by Streptococcus dysgalactiae joint ill Flock characteristic
Response
Flock type
Lowland Upland Hill Yes No Not answered Indoors Outdoors Mix of indoor and outdoor Yes Iodine dip Iodine spray Oxytetracycline spray Other Yes No Yes No Yes No Yes No Yes No Not answered Yes No Not answered
6 (17) 31 (86) 5 (14) 26 (72) 10 (28) 13 (36) 23 (64) 29 (81) 7 (19) 8 (28) 17 (59) 4 (13) 6 (22) 20 (74) 1 (4)
Yes No Not answered Yes No Sometimes Not answered Yes No Sometimes Not answered
9 (33) 15 (56) 3 (11) 6 (17) 20 (56) 3 (8) 7 (19) 9 (25) 8 (22) 12 (33) 7 (19)
Purchase sheep (other than breeding rams) Location of lambing
Navel disinfection practised Type of navel disinfectant
Lambs tail docked Ram lambs neutered Lambs ear-tagged at less than 4 weeks of age Stomach tubes used to administer colostrum to lambs If stomach tubes used (n=29 flocks), were they disinfected between each lamb? For flocks where ewes and lambs were moved into individual pens after lambing (n=27 flocks), was bedding changed between occupations? Individual pens regularly disinfected between occupations (n=27 flocks) Gloves used when assisting lambing
Hand washing practised between assisted lambing
N. flocks (%) 19 (53) 7 (19) 10 (28) 18 (50) 13 (36) 5 (14) 23 (64) 3 (8) 10 (28) 36 (100) 19 (53) 9 (25) 2 (6)
Accepted February 8, 2015 April 25, 2015 | Veterinary Record
Downloaded from http://veterinaryrecord.bmj.com/ on July 15, 2015 - Published by group.bmj.com
Short Communication these countries (Anon 2010, 2013), it suggests prevalence of affected flocks is very low. Nevertheless joint ill can potentially have a large financial impact on affected flocks due to lamb mortalities, reduced growth rates, veterinary fees, treatment costs and extra staff hours. The potential financial impact was not quantified in this study. All affected flocks undertook the basic hygiene procedure of disinfecting lamb’s navels shortly after birth. However, only a minority practised more intensive hygiene procedures such as using gloves during assisted lambing, washing hands between assisted lambing, changing the bedding or disinfecting individual pens between occupations and disinfecting stomach tubes between lambs. Important reservoirs of S dysgalactiae are likely ewes who may carry the organism in the vagina, milk and possibly other secretions (Cornell and Glover 1925, Anon 2006, Lacasta and others 2008, Rutherford and others 2014). The organism has an in vitro survival time of up to 42 days on straw, a material commonly used in the lambing environment (Rutherford and others 2014). It is conceivable the organism could be transferred from ewe to ewe and ewe to lamb during assisted lambing, via contaminated bedding or via stomach tubes. Hence, recommendations for affected flocks that aim to limit the transmission of the pathogen, such as the procedures listed above, should be considered. However, their effectiveness at reducing the number of clinical cases is unknown. Wounds caused by tail docking, castration and ear-tagging have been implicated as possible risk factors for joint ill (Anon 2007, 2008, 2011a, b, c). In this study, most flocks practised tail docking and castration, a third ear-tagged lambs at less than four weeks of age while four flocks did not undertake any of these procedures. The possibility of the organism entering lambs via these routes cannot be discounted, but they are clearly not the only routes of infection. For example, Lacasta and others (2008) described a digestive pathway of infection. Fourteen flocks administered prophylactic antibiotics to all lambs for prevention of joint ill. However, they still had cases suggesting this was not fully effective for prevention and the level of reduction of the number of cases is unknown. It was observed that poor lamb identification and record-keeping limited the farmers’ ability to determine which lambs had been treated and when. The high level of mortality due to joint ill in some flocks emphasised the inefficacy of some treatment regimens. It is important that veterinarians work with their clients to educate them on appropriate methods of consistently and
Veterinary Record | April 25, 2015
effectively treating affected lambs. All 25 S dysgalactiae isolates were resistant to tetracycline, which should not be used for the prophylaxis or treatment of joint ill.
Acknowledgements
The authors thank the flock owners who were involved in this study and acknowledge the private veterinarians and veterinary staff at the AHVLA – Weybridge who assisted in identifying affected flocks. Funding The funding for this study was from a BBSRC CASE PhD studentship co-funded by Zoetis. Ethics approval This research was approved by the Royal Veterinary College Animal Ethics Committee.
References
ANON (2006) VLA surveillance report. Veterinary Record 158, 357–360 ANON (2007) VLA surveillance report. Veterinary Record 160, 783–786 ANON (2008) VLA Surveillance report. Veterinary Record 162, 639–642 ANON (2010) National statistics review of data on sheep numbers at December in England. www.gov.uk/government/uploads/system/uploads/attachment_data/ file/182276/defra-stats-foodfarm-landuselivestock-decemberdecembersheepdatasourcereview110830.pdf. Accessed July 2, 2014 ANON (2011a) VLA surveillance report. Veterinary Record 168, 201–204 ANON (2011b) SAC disease surveillance report. Veterinary Record 168, 449–452 ANON (2011c) VLA surveillance report. Veterinary Record 169, 173–176 ANON (2011d) BASC Methods for Antimicrobial Susceptibility Testing Version 10.2 May 2011. http://bsac.org.uk/wp-content/uploads/2012/02/Version-10.22011-final-May-20112.pdf. Accessed July 2, 2014 ANON (2013) Welsh agricultural statistics 2011. http://wales.gov.uk/statistics-andresearch/welsh-agricultural-statistics/?lang=en. Accessed July 2, 2014 CORNELL, R. L. & GLOVER, R. E. (1925) Joint ill in lambs. Veterinary Record 5, 833–839 LACASTA, D., FERRER, L. M., RAMOS, J. J., LOSTE, A. & BUESO, J. P. (2008) Digestive pathway of infection in Streptococcus dysgalactiae polyarthritis in lambs. Small Ruminant Research 78, 202–205 RUTHERFORD, S. J., RYCROFT, A. N. & RIDLER, A. L. (2014) Sources of Streptococcus dysgalactiae in English and Welsh sheep flocks affected by infectious arthritis ( joint ill). Veterinary Record 174, 579 WATKINS, G. H. & SHARP, M. W. (1998) Bacteria isolated from arthritic and omphalatic lesions in lambs in England and Wales. The Veterinary Journal 156, 235–238
Downloaded from http://veterinaryrecord.bmj.com/ on July 15, 2015 - Published by group.bmj.com
Characteristics of sheep flocks affected by Streptococcus dysgalactiae arthritis S.-J. Rutherford, S. Jeckel and A. Ridler Veterinary Record 2015 176: 435 originally published online February 27, 2015
doi: 10.1136/vr.102781 Updated information and services can be found at: http://veterinaryrecord.bmj.com/content/176/17/435.1
These include:
References Email alerting service
This article cites 10 articles, 7 of which you can access for free at: http://veterinaryrecord.bmj.com/content/176/17/435.1#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/
Short Communication
Characteristics of sheep flocks affected by Streptococcus dysgalactiae arthritis S.-J. Rutherford, S. Jeckel, A. Ridler IN the UK, Streptococcus dysgalactiae is the most common cause of infectious arthritis ( joint ill) in lambs aged up to four weeks (Watkins and Sharp 1998). Relatively little is known about the disease and much of this is limited to Animal Health and Veterinary Laboratories Agency – Weybridge (AHVLA - Weybridge) and Scottish Agricultural College (SAC) reports (eg Anon 2006, 2007, 2008, 2011a, b, c). The aims of this paper are to describe the characteristics of affected flocks in England and Wales, the application of treatment regimens and the antimicrobial resistance status of ovine S dysgalactiae isolates. Affected flocks were defined as having at least 2 per cent of lambs showing clinical signs consistent with joint ill from which S dysgalactiae was isolated from joint fluid from at least one lamb. During 2008, 2009 and 2010, affected flocks in England and Wales were identified via the AHVLA - Weybridge database or direct notification from veterinary surgeons or flock owners who had been encouraged to participate via rural press, word of mouth and during conference attendance. A questionnaire containing 50 questions on the general attributes of the flock, management practices during lambing and lamb disease history was administered to flock owners via post, telephone interview or farm visit. In addition, those flocks which were identified at the time of a disease outbreak were visited and flock managers were informally observed and interviewed on treatment regimens. Twenty-five S dysgalactiae isolates were subjected to antimicrobial resistance testing using methods based on those of the British Society for Antimicrobial Chemotherapy (Anon 2011d). Those tested were penicillin (1 unit), amoxicillin/clavulanate (30 μg), cephalexin (30 μg), tetracycline (10 μg), trimethoprim/ sulphonamide (25 μg), sulphamethoxanole, (25 μg), enrofloxacin (5 μg) and ciprofloxacin (5 μg). A total of 60 affected flocks from England and Wales were identified. Thirty-six flocks returned usable questionnaires and 19 of these flocks were visited. Flock characteristics and lambing management is summarised in Table 1. The farmer-reported within-flock joint ill prevalence averaged 4 per cent (range 2–20 per cent) and according to farmer estimates an average of 19 per cent of affected lambs subsequently died (range 0–75 per cent). Fourteen flocks (39 per cent) routinely gave all newborn lambs Veterinary Record (2015) S.-J. Rutherford, BSc, PhD, Department of Veterinary Clinical Sciences, Royal Veterinary College, Hawkshead Lane, Hatfield, Hertfordshire AL97TA, UK S. Jeckel, DrVetMed, MRCVS, Department of Pathology and Pathogen Biology, Royal Veterinary College, Hawkshead Lane, Hatfield, Hertfordshire AL97TA, UK
doi: 10.1136/vr.102781 A. Ridler, BVSc, PhD, DipECSRHM, Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Private Bag 11-222, Palmerston North, New Zealand E-mail for correspondence: [email protected] Provenance: Not commissioned; externally peer reviewed
injectable antimicrobials for the purpose of preventing joint ill; most commonly penicillin, amoxicillin or oxytetracycline. Seventeen flocks reported which antimicrobials were used for treatment of affected lambs. These were penicillin plus streptomycin (five flocks), penicillin (four flocks), amoxicillin (four flocks), amoxicillin plus clavulanic acid (two flocks), oxytetracycline (one flock) and tylosin (one flock). Of the 19 flocks that were visited, almost all lambs were turned out in the fields by the time cases were identified. In terms of recording treatments, two flocks had a high level of recording using electronic ear-tags and hand-held data loggers. In 14 flocks, a colour marker was sprayed onto the back of each lamb at each treatment; most lambs received one to five treatments but not necessarily on consecutive days. In three flocks, no recording was undertaken; lambs were treated on an ad hoc basis. The flocks with the highest reported lamb mortality rates due to joint ill were those where no recording was undertaken. All 25 bacterial isolates were resistant to tetracycline and two isolates from one flock were resistant to penicillin. This is the first study that has described the characteristics of flocks affected by S dysgalactiae joint ill. However, the study design and number of responses mean it is not possible to make comparisons between farms or between years. Despite several methods used to identify affected flocks in England and Wales over several years, only 60 were identified. This is likely an under-representation but nevertheless, given that there are greater than 60,000 holdings with more than 20–25 sheep in
TABLE 1: Characteristics of 36 English and Welsh sheep flocks affected by Streptococcus dysgalactiae joint ill Flock characteristic
Response
Flock type
Lowland Upland Hill Yes No Not answered Indoors Outdoors Mix of indoor and outdoor Yes Iodine dip Iodine spray Oxytetracycline spray Other Yes No Yes No Yes No Yes No Yes No Not answered Yes No Not answered
6 (17) 31 (86) 5 (14) 26 (72) 10 (28) 13 (36) 23 (64) 29 (81) 7 (19) 8 (28) 17 (59) 4 (13) 6 (22) 20 (74) 1 (4)
Yes No Not answered Yes No Sometimes Not answered Yes No Sometimes Not answered
9 (33) 15 (56) 3 (11) 6 (17) 20 (56) 3 (8) 7 (19) 9 (25) 8 (22) 12 (33) 7 (19)
Purchase sheep (other than breeding rams) Location of lambing
Navel disinfection practised Type of navel disinfectant
Lambs tail docked Ram lambs neutered Lambs ear-tagged at less than 4 weeks of age Stomach tubes used to administer colostrum to lambs If stomach tubes used (n=29 flocks), were they disinfected between each lamb? For flocks where ewes and lambs were moved into individual pens after lambing (n=27 flocks), was bedding changed between occupations? Individual pens regularly disinfected between occupations (n=27 flocks) Gloves used when assisting lambing
Hand washing practised between assisted lambing
N. flocks (%) 19 (53) 7 (19) 10 (28) 18 (50) 13 (36) 5 (14) 23 (64) 3 (8) 10 (28) 36 (100) 19 (53) 9 (25) 2 (6)
Accepted February 8, 2015 April 25, 2015 | Veterinary Record
Downloaded from http://veterinaryrecord.bmj.com/ on July 15, 2015 - Published by group.bmj.com
Short Communication these countries (Anon 2010, 2013), it suggests prevalence of affected flocks is very low. Nevertheless joint ill can potentially have a large financial impact on affected flocks due to lamb mortalities, reduced growth rates, veterinary fees, treatment costs and extra staff hours. The potential financial impact was not quantified in this study. All affected flocks undertook the basic hygiene procedure of disinfecting lamb’s navels shortly after birth. However, only a minority practised more intensive hygiene procedures such as using gloves during assisted lambing, washing hands between assisted lambing, changing the bedding or disinfecting individual pens between occupations and disinfecting stomach tubes between lambs. Important reservoirs of S dysgalactiae are likely ewes who may carry the organism in the vagina, milk and possibly other secretions (Cornell and Glover 1925, Anon 2006, Lacasta and others 2008, Rutherford and others 2014). The organism has an in vitro survival time of up to 42 days on straw, a material commonly used in the lambing environment (Rutherford and others 2014). It is conceivable the organism could be transferred from ewe to ewe and ewe to lamb during assisted lambing, via contaminated bedding or via stomach tubes. Hence, recommendations for affected flocks that aim to limit the transmission of the pathogen, such as the procedures listed above, should be considered. However, their effectiveness at reducing the number of clinical cases is unknown. Wounds caused by tail docking, castration and ear-tagging have been implicated as possible risk factors for joint ill (Anon 2007, 2008, 2011a, b, c). In this study, most flocks practised tail docking and castration, a third ear-tagged lambs at less than four weeks of age while four flocks did not undertake any of these procedures. The possibility of the organism entering lambs via these routes cannot be discounted, but they are clearly not the only routes of infection. For example, Lacasta and others (2008) described a digestive pathway of infection. Fourteen flocks administered prophylactic antibiotics to all lambs for prevention of joint ill. However, they still had cases suggesting this was not fully effective for prevention and the level of reduction of the number of cases is unknown. It was observed that poor lamb identification and record-keeping limited the farmers’ ability to determine which lambs had been treated and when. The high level of mortality due to joint ill in some flocks emphasised the inefficacy of some treatment regimens. It is important that veterinarians work with their clients to educate them on appropriate methods of consistently and
Veterinary Record | April 25, 2015
effectively treating affected lambs. All 25 S dysgalactiae isolates were resistant to tetracycline, which should not be used for the prophylaxis or treatment of joint ill.
Acknowledgements
The authors thank the flock owners who were involved in this study and acknowledge the private veterinarians and veterinary staff at the AHVLA – Weybridge who assisted in identifying affected flocks. Funding The funding for this study was from a BBSRC CASE PhD studentship co-funded by Zoetis. Ethics approval This research was approved by the Royal Veterinary College Animal Ethics Committee.
References
ANON (2006) VLA surveillance report. Veterinary Record 158, 357–360 ANON (2007) VLA surveillance report. Veterinary Record 160, 783–786 ANON (2008) VLA Surveillance report. Veterinary Record 162, 639–642 ANON (2010) National statistics review of data on sheep numbers at December in England. www.gov.uk/government/uploads/system/uploads/attachment_data/ file/182276/defra-stats-foodfarm-landuselivestock-decemberdecembersheepdatasourcereview110830.pdf. Accessed July 2, 2014 ANON (2011a) VLA surveillance report. Veterinary Record 168, 201–204 ANON (2011b) SAC disease surveillance report. Veterinary Record 168, 449–452 ANON (2011c) VLA surveillance report. Veterinary Record 169, 173–176 ANON (2011d) BASC Methods for Antimicrobial Susceptibility Testing Version 10.2 May 2011. http://bsac.org.uk/wp-content/uploads/2012/02/Version-10.22011-final-May-20112.pdf. Accessed July 2, 2014 ANON (2013) Welsh agricultural statistics 2011. http://wales.gov.uk/statistics-andresearch/welsh-agricultural-statistics/?lang=en. Accessed July 2, 2014 CORNELL, R. L. & GLOVER, R. E. (1925) Joint ill in lambs. Veterinary Record 5, 833–839 LACASTA, D., FERRER, L. M., RAMOS, J. J., LOSTE, A. & BUESO, J. P. (2008) Digestive pathway of infection in Streptococcus dysgalactiae polyarthritis in lambs. Small Ruminant Research 78, 202–205 RUTHERFORD, S. J., RYCROFT, A. N. & RIDLER, A. L. (2014) Sources of Streptococcus dysgalactiae in English and Welsh sheep flocks affected by infectious arthritis ( joint ill). Veterinary Record 174, 579 WATKINS, G. H. & SHARP, M. W. (1998) Bacteria isolated from arthritic and omphalatic lesions in lambs in England and Wales. The Veterinary Journal 156, 235–238
Downloaded from http://veterinaryrecord.bmj.com/ on July 15, 2015 - Published by group.bmj.com
Characteristics of sheep flocks affected by Streptococcus dysgalactiae arthritis S.-J. Rutherford, S. Jeckel and A. Ridler Veterinary Record 2015 176: 435 originally published online February 27, 2015
doi: 10.1136/vr.102781 Updated information and services can be found at: http://veterinaryrecord.bmj.com/content/176/17/435.1
These include:
References Email alerting service
This article cites 10 articles, 7 of which you can access for free at: http://veterinaryrecord.bmj.com/content/176/17/435.1#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/
