Clinical management
Treatment
of acute Streptococcus equi infection
Most equids with acute strangles exhibit non-specific signs of
generalised respiratory infection with presentation depending on
challenge dose and host immunity, often responding well with only
supportive and nursing care (Rendle et al., 2021, Whitelegg and
Saunders, 2021). Acute disease can quickly deteriorate into severe
cases, emphasising the need for regular monitoring (Rendle et al.,
2021).
Nursing for an animal with strangles is vital and wide-ranging: good
nursing provision will include an environment that encourages rest,
appropriate nutrition, regular monitoring (TPR), abscess management, and
a quarantine protocol (Whitelegg and Saunders, 2021). A soft, calorific,
and palatable diet alongside water, to facilitate deglutition, both
provided from a height, can help equids with profound lymphadenopathy;
assisted nutrition may be indicated (Rendle et al., 2021). The
experience of individual equids must be considered during a strangles
outbreak, as small changes in diet and environment can aid in assuaging
the effects of infection with S. equi .
Individuals with visible lymphadenopathies require good supportive and
nursing care, with a focus on facilitating the maturation and subsequent
drainage of abscesses (Boyle et al., 2018); the use of a ‘hot pack’ can
enhance this process. Surgical drainage may be required if the abscesses
are not spontaneously rupturing, although care must be taken to ensure
the abscess is mature to enable maximal drainage (Boyle et al., 2018).
Once open, abscesses should be lavaged with saline or antiseptic
solutions, followed by daily flushing so long as discharge persists
(Rendle et al., 2021).
NSAIDs can be employed to provide analgesia and reduce pyrexia; it has
been suggested that their use can slow the development of abscesses, but
this claim lacks evidence (Rendle et al., 2021). Paracetamol has also
been recommended since it does not inhibit inflammation but possesses
anti-pyretic and analgesic actions, resulting in improved appetite and
welfare (Rendle et al., 2021). Phenylbutazone or flunixin meglumine
could also be considered (Boyle et al., 2018).
Antimicrobial therapy in strangles is controversial (Ramey, 2007): their
use is encouraged between initial exposure and abscessation (Boyle et
al., 2018). This window is not always adhered to since abscesses can
develop within days (Timoney and Kumar, 2008). Although antimicrobial
therapy can decrease the size of abscesses and should be considered in
equids with stridor, dyspnoea or dysphagia on welfare grounds, their
effects are limited following the detection of lymphadenopathy (Boyle et
al., 2018).
Penicillin is the drug of choice for S. equi infection; however,
population analysis (Morris et al., 2020) revealed that pbp2x mutations
are emerging. This mutation is in the penicillin-binding site and is
associated with penicillin resistance in Streptococcus pneumoniae(Maurer et al., 2012, Nichol et al., 2002). Penicillin resistance is
variably seen in S. equi isolates (Fonseca et al., 2020, Clark et
al., 2008, Johns and Adams, 2015) and constitutes a growing concern that
clinicians will be less able to treat severely afflicted horses in the
future. Antimicrobial therapy has a role in combatting S. equiinfections, but it must be employed judiciously on an individual
tailored basis, with careful consideration to minimise the development
of antimicrobial resistance (Jaramillo-Morales et al., 2022, Boyle et
al., 2018).
Treatment of persistentStreptococcus equi infection
Persistent infections of the guttural pouch are typically treated with
topical and prolonged systemic antimicrobial therapy (Boyle et al.,
2018). Administration of penicillin systemically and an
endoscopically-guided gelatin-penicillin mix topically, has been
regarded as broadly successful (Verheyen et al., 2000).
The removal of purulent material and chondroids from the guttural
pouches is required for the elimination of the carrier state (Boyle et
al., 2018). Endoscopic intervention is preferable to surgical
intervention due to inherent risks of general anaesthesia, surgical
dissection around vital structures, and S. equi environmental
contamination (Boyle et al., 2018). Topical application of 20%
acetylcysteine (w/v) solution can facilitate drainage of non-inspissated
mucopurulent material through the nasal passages by disrupting
disulphide bonds, thereby reducing mucus viscosity (Boyle et al., 2018).
Specific treatment methods depend on the individual presentation and the
type of material within the guttural pouches. Many carriers do not
present with empyema or chondroids, and it has been reported that the
carrier state can self-resolve without treatment (Pringle et al., 2019).
Outbreak
prevention and management
Strangles was once considered an inevitability (Solleysel, 1664), but
has since been demonstrated to be a very preventable infection (Rendle
et al., 2021). Outbreaks can be prevented by limiting exposure to the
infectious agent, through enacting rigorous biosecurity protocols, using
appropriate quarantining and screening facilities, and understanding of
the pathogenesis of S. equi (Boyle et al., 2018). Outbreaks of
strangles are controlled through the cessation of movement to and from
the farm, isolating animals that are infected and where infection is
suspected. A tiered ‘traffic light’ system with segregation based on
exposure and no mixing between groups should be adhered to (Boyle et
al., 2018). Following the outbreak, all animals should be tested for
exposure and persistent infection.
Long-term control strategies should consider the vaccination of
unexposed animals, the identification and treatment of carrier animals,
and caregiver education on clinical signs associated with acute disease
(Duran and Goehring, 2021).
Vaccination
The ideal strangles vaccine should provide a high degree of protection
against S. equi , a long duration of immunity, the ability to be
administered intramuscularly safely, and permit the differentiation of
infected from vaccinated animals (DIVA) (Waller and Jolley, 2007). DIVA
capability is important since the current commercially available
enzyme-linked immunosorbent assays (ELISAs) do not differentiate between
recently exposed horses and those animals vaccinated with
live-attenuated vaccines, with implications for screening animals,
movement restrictions and disease control (Duran and Goehring, 2021).
The first strangles vaccines were developed in the 1940s, using
heat-killed bacteria, conferring a limited degree of protection but
often resulting in adverse effects, including injection site reactions
and pyrexia (Bazeley, 1940a, Bazeley, 1940b, Bazeley, 1942a, Bazeley,
1942b, Bazeley, 1943). Cell-free variations of this vaccine still exist
(Waller, 2014), although the incidence of adverse reactions and the lack
of DIVA capability have limited their use. A recent attempt to combine
the S. equi bacterin and recombinant SeM protein in a vaccine
yielded promising results in mice, with all demonstrating a humoral
response (Rosa et al., 2021); evaluation of its safety and efficacy in
horses is ongoing.
M-protein-containing extract vaccines have demonstrated some efficacy in
reducing the frequency and severity of disease; although adverse
reactions are common and they possess no DIVA capability (Hoffman et
al., 1991). In a double-blind randomised clinical trial in foals, 29%
(17/59) of vaccinates developed cervical lymphadenopathy, compared to
71% (39/55) of sham-vaccinated controls (Hoffman et al., 1991).
Commercially available options, although none are available in the UK,
include Strepvax II (Boehringer Ingelheim), Equivac S (Zoetis New
Zealand), and Strepguard (MSD Animal Health) (Duran and Goehring, 2021).
Live-attenuated vaccines have been at the forefront of strangles
prevention since the early 21st century; a 10⁹ dose of
an avirulent strain of S. equi , was shown to prevent
lymphadenopathy in 100% (5/5) and 50% (2/4) of ponies, respectively,
across two experiments conducted by Jacobs et al. (2000). The Equilis
StrepE (MSD Animal Health) is administered submucosally, and the
Pinnacle IN (Zoetis) is administered intranasally; they are commercially
available in Europe and North America, respectively, as well as other
countries intermittently (Duran and Goehring, 2021). Adverse reactions
were reported upon intramuscular administration, and these
live-attenuated vaccines possess no DIVA capability (Kemp-Symonds et
al., 2007, Borst et al., 2011, Livengood et al., 2016, Lanka et al.,
2010). Furthermore, the Equilis StrepE (MSD Animal Health) vaccine has
been linked to S. equi replication, resulting in lymph node
abscesses (Kemp-Symonds et al., 2007, Kelly et al., 2006, Mitchell et
al., 2021, Harris et al., 2015).
Strangvac (Intervacc AB) is a recombinant fusion protein vaccine that is
administered intramuscularly and has been shown to provide immunity in
up to 94% (15/16) of ponies when challenged two weeks following third
vaccination (Robinson et al., 2020). Strangvac has DIVA capability as
the vaccine does not contain live S. equi , S. equi DNA nor
the SeM and SEQ2190 antigens that are targeted by culture, PCR, or ELISA
diagnostic tests (Robinson et al., 2018). Future studies will be needed
to evaluate the utility of Strangvac (Intervacc AB) in clinical
practice.
Vaccination as a tool for outbreak prevention has been limited by
efficacy, safety, practicality, clashes with other vaccination
schedules, DIVA capability, geographical restrictions, differences in
circulating S. equi strains and owner compliance (Boyle et al.,
2018, Mitchell et al., 2021). Advancements such as the Strangvac vaccine
represent a promising development, potentially allowing vaccination to
become a more efficacious control measure. However, continued work is
required from veterinary professionals to build trust with owners and
caregivers over the use of any strangles vaccines due to past
difficulties (White et al., 2021).
Conclusion
Understanding S. equi is crucial to combatting strangles, and
much work has been carried out to characterise its evolution (Holden et
al., 2009), genome (Harris et al., 2015), epidemiology (Mitchell et al.,
2021), survivability (Durham et al., 2018), resistance profile (Fonseca
et al., 2020) and pathogenicity (Timoney and Kumar, 2008, Timoney,
2004). This increased understanding has enabled the development of more
targeted diagnostic assays (Noll et al., 2020, Webb et al., 2013, Willis
et al., 2021, Boyle et al., 2021), better outbreak prevention and
management protocols (Rendle et al., 2021) and a safe and efficacious
vaccine with DIVA capability (Robinson et al., 2020). These advances
better equip clinicians and caregivers to treat and prevent strangles.
Further research is required to investigate the role of S.
zooepidemicus as a primary respiratory pathogen in equids (Waller and
Wilson, 2021, Waller, 2017), and to better understand the growing
concern of antibiotic resistance in both S. equi and S.
zooepidemicus (Fonseca et al., 2020, Johns and Adams, 2015). The
success of S. equi as a pathogen can be attributed to the carrier
state allowing infection to spread to naïve animals. Understanding the
host and pathogenic factors that predispose equids to persistent
infection and validating a gold-standard method of diagnosis will help
prevent future outbreaks and safeguard animal welfare.
References
BANNISTER, M. F., BENSON, C. E. & SWEENEY, C. R. 1985. Rapid species
identification of group C streptococci isolated from horses. J.
Clin. Microbiol., 21, 524-6.
BAZELEY, P. L. 1940a. Studies with equine streptococci 1. Aust.
Vet. J., 16, 140-146.
BAZELEY, P. L. 1940b. Studies with equine streptococci 2. Aust.
Vet. J., 16, 243-259.
BAZELEY, P. L. 1942a. Studies with equine streptococci 3. Aust.
Vet. J., 18, 141-155.
BAZELEY, P. L. 1942b. Studies with equine streptococci 4. Aust.
Vet. J., 18, 189-194.
BAZELEY, P. L. 1943. Studies with equine streptococci 5. Aust.
Vet. J., 19, 62-85.
BJÖRNSDÓTTIR, S., HARRIS, S. R., SVANSSON, V., GUNNARSSON, E.,
SIGURÐARDÓTTIR, Ó. G., GAMMELJORD, K., STEWARD, K. F., NEWTON, J. R.,
ROBINSON, C., CHARBONNEAU, A. R. L., PARKHILL, J., HOLDEN, M. T. G.,
WALLER, A. S., WALKER, M. J. & DUNNY, G. M. 2017. Genomic Dissection of
an Icelandic Epidemic of Respiratory Disease in Horses and Associated
Zoonotic Cases. mBio, 8, e00826-17.
BORST, L. B., PATTERSON, S. K., LANKA, S., BARGER, A. M., FREDRICKSON,
R. L. & MADDOX, C. W. 2011. Evaluation of a commercially available
modified-live Streptococcus equi subsp equi vaccine in ponies. Am.
J. Vet. Res., 72, 1130-8.
BOYLE, A. G. 2017. Strangles and its complications. Equine Vet.
Educ., 29, 149-157.
BOYLE, A. G., BOSTON, R. C., O’SHEA, K., YOUNG, S. & RANKIN, S. C.
2012. Optimization of an in vitro assay to detect Streptococcus equi
subsp. equi. Vet. Microbiol., 159, 406-10.
BOYLE, A. G., RANKIN, S. C., O’SHEA, K., STEFANOVSKI, D., PENG, J.,
SONG, J. & BAU, H. H. 2021. Detection of Streptococcus equi subsp. equi
in guttural pouch lavage samples using a loop-mediated isothermal
nucleic acid amplification microfluidic device. J. Vet. Int.
Med., 35, 1597-1603.
BOYLE, A. G., STEFANOVSKI, D. & RANKIN, S. C. 2017. Comparison of
nasopharyngeal and guttural pouch specimens to determine the optimal
sampling site to detect Streptococcus equi subsp equi carriers by DNA
amplification. BMC Vet. Res., 13, 75.
BOYLE, A. G., SWEENEY, C. R., KRISTULA, M., BOSTON, R. & SMITH, G.
2009. Factors associated with likelihood of horses having a high serum
Streptococcus equi SeM-specific antibody titer. J. Am. Vet. Med.
Assoc., 235, 973-977.
BOYLE, A. G., TIMONEY, J. F., NEWTON, J. R., HINES, M. T., WALLER, A. S.
& BUCHANAN, B. R. 2018. Streptococcus equi Infections in Horses:
Guidelines for Treatment, Control, and Prevention of Strangles-Revised
Consensus Statement. J. Vet. Intern. Med., 32, 633-647.
CHRISTOFFERSEN, M., BAAGOE, C. D., JACOBSEN, S., BOJESEN, A. M.,
PETERSEN, M. R. & LEHN-JENSEN, H. 2010. Evaluation of the systemic
acute phase response and endometrial gene expression of serum amyloid A
and pro- and anti-inflammatory cytokines in mares with experimentally
induced endometritis. Vet. Immunol. Immunopathol., 138,95-105.
CLARK, C., GREENWOOD, S., BOISON, J. O., CHIRINO-TREJO, M. & DOWLING,
P. M. 2008. Bacterial isolates from equine infections in western Canada
(1998-2003). Can. Vet. J., 49, 153-60.
CRAIG, D. 2021. Strangles screening pre-and post-import of horses into
the United Arab Emirates: A review of 5604 horses imported between
2018-2019. Equine Vet. J., 53(SUPPL 56), 25-26.
DAVIDSON, A., TRAUB-DARGATZ, J. L., MAGNUSON, R., HILL, A., IRWIN, V.,
NEWTON, R., WALLER, A., SMITH, K., CALLAN, R. J., MEEHAN, M., OWEN, P.
& SALMAN, M. 2008. Lack of correlation between antibody titers to
fibrinogen-binding protein of Streptococcus equi and persistent carriers
of strangles. J. Vet. Diagn. Invest., 20, 457-62.
DUFFEE, L. R., STEFANOVSKI, D., BOSTON, R. C. & BOYLE, A. G. 2015.
Predictor variables for and complications associated with Streptococcus
equi subsp equi infection in horses. J. Am. Vet. Med. Assoc.,247, 1161-8.
DURAN, M. C. & GOEHRING, L. S. 2021. Equine strangles: an update on
disease control and prevention. (Special Issue: Half-Century spreading
veterinary sciences.). Austral. J. of Vet. Sci., 53,23-31.
DURHAM, A. E., HALL, Y. S., KULP, L. & UNDERWOOD, C. 2018. A study of
the environmental survival of Streptococcus equi subspecies equi.Equine Vet. J., 50, 861-864.
DURHAM, A. E. & KEMP-SYMONDS, J. 2021. Failure of serological testing
for antigens A and C of Streptococcus equi subspecies equi to identify
guttural pouch carriers. Equine Vet. J., 53, 38-43.
FONSECA, J. D., MAVRIDES, D. E., MORGAN, A. L., NA, J. G., GRAHAM, P. A.
& MCHUGH, T. D. 2020. Antibiotic resistance in bacteria associated with
equine respiratory disease in the United Kingdom. Vet. Rec.,187, 189.
FORD, J. & LOKAI, M. D. 1980. Complications of Streptococcus equi
infection. Equine Pract., 2, 41-44.
GALAN, J. E., TIMONEY, J. F. & LENGEMANN, F. W. 1986. Passive transfer
of mucosal antibody to Streptococcus equi in the foal. Infect.
Immun., 54, 202-6.
GEORGE, J. L., REIF, J. S., SHIDELER, R. K., SMALL, C. J., ELLIS, R. P.,
SNYDER, S. P. & MCCHESNEY, A. E. 1983. Identification of carriers of
Streptococcus equi in a naturally infected herd. J. Am. Vet. Med.
Assoc., 183, 80-4.
GHARIEB, N. M., ALI, W. S., TARTOR, Y. H., EL-NAENAEEY, E. Y. & AMMAR,
A. M. 2019. Rapid and Precise Diagnostic Tests for S. equi: An Etiologic
Agent of Equine Strangles. Zagazig Vet. J., 47, 146-159.
HAMLEN, H. J., TIMONEY, J. F. & BELL, R. J. 1994. Epidemiologic and
immunologic characteristics of Streptococcus equi infection in foals.J. Am. Vet. Med. Assoc., 204, 768-75.
HARRIS, S. R., ROBINSON, C., STEWARD, K. F., WEBB, K. S., PAILLOT, R.,
PARKHILL, J., HOLDEN, M. T. & WALLER, A. S. 2015. Genome specialization
and decay of the strangles pathogen, Streptococcus equi, is driven by
persistent infection. Genome Res., 25, 1360-71.
HEATHER, Z., HOLDEN, M. T., STEWARD, K. F., PARKHILL, J., SONG, L.,
CHALLIS, G. L., ROBINSON, C., DAVIS-POYNTER, N. & WALLER, A. S. 2008. A
novel streptococcal integrative conjugative element involved in iron
acquisition. Mol. Microbiol., 70, 1274-92.
HOFFMAN, A. M., STAEMPFLI, H. R., PRESCOTT, J. F. & VIEL, L. 1991.
Field evaluation of a commercial M-protein vaccine against Streptococcus
equi infection in foals. Am. J. Vet. Res., 52, 589-92.
HOLDEN, M. T., HEATHER, Z., PAILLOT, R., STEWARD, K. F., WEBB, K.,
AINSLIE, F., JOURDAN, T., BASON, N. C., HOLROYD, N. E., MUNGALL, K.,
QUAIL, M. A., SANDERS, M., SIMMONDS, M., WILLEY, D., BROOKS, K.,
AANENSEN, D. M., SPRATT, B. G., JOLLEY, K. A., MAIDEN, M. C., KEHOE, M.,
CHANTER, N., BENTLEY, S. D., ROBINSON, C., MASKELL, D. J., PARKHILL, J.
& WALLER, A. S. 2009. Genomic evidence for the evolution of
Streptococcus equi: host restriction, increased virulence, and genetic
exchange with human pathogens. PLoS Pathog., 5,e1000346.
IVENS, P. A., MATTHEWS, D., WEBB, K., NEWTON, J. R., STEWARD, K.,
WALLER, A. S., ROBINSON, C. & SLATER, J. D. 2011. Molecular
characterisation of ’strangles’ outbreaks in the UK: the use of
M-protein typing of Streptococcus equi ssp. equi. Equine Vet. J.,43, 359-64.
JACOBS, A. A., GOOVAERTS, D., NUIJTEN, P. J., THEELEN, R. P., HARTFORD,
O. M. & FOSTER, T. J. 2000. Investigations towards an efficacious and
safe strangles vaccine: submucosal vaccination with a live attenuated
Streptococcus equi. Vet. Rec., 147, 563-7.
JARAMILLO-MORALES, C., GOMEZ, D. E., RENAUD, D. & ARROYO, L. G. 2022.
Streptococcus equi culture prevalence, associated risk factors and
antimicrobial susceptibility in a horse population from Colombia.J. Equine Vet. Sci., 111, 103890.
JOHNS, I. C. & ADAMS, E. L. 2015. Trends in antimicrobial resistance in
equine bacterial isolates: 1999-2012. Vet. Rec., 176,334.
JUDY, C. E., CHAFFIN, M. K. & COHEN, N. D. 1999. Empyema of the
guttural pouch (auditory tube diverticulum) in horses: 91 cases
(1977-1997). J. Am. Vet. Med. Assoc., 215, 1666-70.
KAESE, H. J., VALBERG, S. J., HAYDEN, D. W., WILSON, J. H., CHARLTON,
P., AMES, T. R. & AL-GHAMDI, G. M. 2005. Infarctive purpura
hemorrhagica in five horses. J. Am. Vet. Med. Assoc.,226, 1893-1898.
KELLY, C., BUGG, M., ROBINSON, C., MITCHELL, Z., DAVIS-POYNTER, N.,
NEWTON, J. R., JOLLEY, K. A., MAIDEN, M. C. & WALLER, A. S. 2006.
Sequence variation of the SeM gene of Streptococcus equi allows
discrimination of the source of strangles outbreaks. J. Clin.
Microbiol., 44, 480-6.
KEMP-SYMONDS, J., KEMBLE, T. & WALLER, A. 2007. Modified live
Streptococcus equi (’strangles’) vaccination followed by clinically
adverse reactions associated with bacterial replication. Equine
Vet. J., 39, 284-6.
LAING, G., CHRISTLEY, R., STRINGER, A., ASHINE, T., CIAN, F., AKLILU,
N., NEWTON, R., RADFORD, A. & PINCHBECK, G. 2021. Pathology, infectious
agents and horse- and management-level risk factors associated with
signs of respiratory disease in Ethiopian working horses. Equine
Vet. J., 53, 670-681.
LANKA, S., BORST, L. B., PATTERSON, S. K. & MADDOX, C. W. 2010. A
multiphasic typing approach to subtype Streptococcus equi subspecies
equi. J. Vet. Diagn. Invest., 22, 928-36.
LANNERGARD, J. & GUSS, B. 2006. IdeE, an IgG-endopeptidase of
Streptococcus equi ssp. equi. FEMS Microbiol. Lett.,262, 230-5.
LEADON, D., WARAN, N., HERHOLZ, C. & KLAY, M. 2008. Veterinary
management of horse transport. Vet. Ital., 44, 149-163.
LIBARDONI, F., MACHADO, G., GRESSLER, L. T., KOWALSKI, A. P., DIEHL, G.
N., DOS SANTOS, L. C., CORBELLINI, L. G. & DE VARGAS, A. C. 2016.
Prevalence of Streptococcus equi subsp. equi in horses and associated
risk factors in the State of Rio Grande do Sul, Brazil. Res. Vet.
Sci., 104, 53-7.
LINDAHL, S., BÅVERUD, V., EGENVALL, A., ASPÁN, A. & PRINGLE, J. 2013.
Comparison of sampling sites and laboratory diagnostic tests for S. equi
subsp. equi in horses from confirmed strangles outbreaks. J. Vet.
Intern. Med., 27, 542-7.
LINDMARK, H., NILSSON, M. & GUSS, B. 2001. Comparison of the
fibronectin-binding protein FNE from Streptococcus equi subspecies equi
with FNZ from S. equi subspecies zooepidemicus reveals a major and
conserved difference. Infect. Immun., 69, 3159-63.
LING, A. S., UPJOHN, M. M., WEBB, K., WALLER, A. S. & VERHEYEN, K. L.
2011. Seroprevalence of Streptococcus equi in working horses in Lesotho.Vet. Rec., 169, 72.
LIVENGOOD, J. L., LANKA, S., MADDOX, C. & TEWARI, D. 2016. Detection
and differentiation of wild-type and a vaccine strain of Streptococcus
equi ssp. equi using pyrosequencing. Vaccine, 34,3935-7.
MALLICOTE, M. 2015. Update on Streptococcus equi subsp equi infections.Vet. Clin. N. Am., Equine Pract., 31, 27-41.
MAURER, P., TODOROVA, K., SAUERBIER, J. & HAKENBECK, R. 2012. Mutations
in Streptococcus pneumoniae penicillin-binding protein 2x: importance of
the C-terminal penicillin-binding protein and serine/threonine
kinase-associated domains for beta-lactam binding. Microb. Drug
Resist., 18, 314-21.
MCGLENNON, A. 2019. Surveillance of equine strangles: a new initiative.Vet. Rec., 184, 342-344.
MEEHAN, M., LEWIS, M. J., BYRNE, C., O’HARE, D., WOOF, J. M. & OWEN, P.
2009. Localization of the equine IgG-binding domain in the
fibrinogen-binding protein (FgBP) of Streptococcus equi subsp. equi.Microbiology (Reading), 155, 2583-2592.
MITCHELL, C., STEWARD, K. F., CHARBONNEAU, A. R. L., WALSH, S., WILSON,
H., TIMONEY, J. F., WERNERY, U., JOSEPH, M., CRAIG, D., VAN MAANEN, K.,
HOOGKAMER-VAN GENNEP, A., LEON, A., WITKOWSKI, L., RZEWUSKA, M.,
STEFAŃSKA, I., ŻYCHSKA, M., VAN LOON, G., CURSONS, R., PATTY, O., ACKE,
E., GILKERSON, J. R., EL-HAGE, C., ALLEN, J., BANNAI, H., KINOSHITA, Y.,
NIWA, H., BECÚ, T., PRINGLE, J., GUSS, B., BÖSE, R., ABBOTT, Y., KATZ,
L., LEGGETT, B., BUCKLEY, T. C., BLUM, S. E., CRUZ LÓPEZ, F., FERNÁNDEZ
ROS, A., MAROTTI CAMPI, M. C., PREZIUSO, S., ROBINSON, C., NEWTON, J.
R., SCHOFIELD, E., BROOKE, B., BOURSNELL, M., DE BRAUWERE, N., KIRTON,
R., BARTON, C. K., ABUDAHAB, K., TAYLOR, B., YEATS, C. A., GOATER, R.,
AANENSEN, D. M., HARRIS, S. R., PARKHILL, J., HOLDEN, M. T. G. &
WALLER, A. S. 2021. Globetrotting strangles: the unbridled national and
international transmission of Streptococcus equi between horses.Microb Genom, 7.
MORRIS, E. R. A., BOYLE, A. G., RIIHIMÄKI, M., ASPÁN, A., ANIS, E.,
HILLHOUSE, A. E., IVANOV, I., BORDIN, A. I., PRINGLE, J. & COHEN, N. D.
2021. Differences in the genome, methylome, and transcriptome do not
differentiate isolates of Streptococcus equi subsp. equi from horses
with acute clinical signs from isolates of inapparent carriers.PLoS One, 16, e0252804.
MORRIS, E. R. A., HILLHOUSE, A. E., KONGANTI, K., WU, J., LAWHON, S. D.,
BORDIN, A. I. & COHEN, N. D. 2020. Comparison of whole genome sequences
of Streptococcus equi subsp. equi from an outbreak in Texas with
isolates from within the region, Kentucky, USA, and other countries.Vet. Microbiol., 243, 108638.
MUHKTAR, M. M. & TIMONEY, J. F. 1988. Chemotactic response of equine
polymorphonuclear leucocytes to Streptococcus equi. Res. Vet.
Sci., 45, 225-9.
NEWTON, J. R., WOOD, J. L., DUNN, K. A., DEBRAUWERE, M. N. & CHANTER,
N. 1997a. Naturally occurring persistent and asymptomatic infection of
the guttural pouches of horses with Streptococcus equi. Vet.
Rec., 140, 84-90.
NEWTON, J. R., WOOD, J. L. N. & CHANTER, N. 1997b. Strangles: Long term
carriage of Streptococcus equi in horses. Equine Vet. Educ.,9, 98-102.
NICHOL, K. A., ZHANEL, G. G. & HOBAN, D. J. 2002. Penicillin-binding
protein 1A, 2B, and 2X alterations in Canadian isolates of
penicillin-resistant Streptococcus pneumoniae. Antimicrob. Agents
Chemother., 46, 3261-4.
NOLL, L. W., STOY, C. P. A., WANG, Y., PORTER, E. G., LU, N., LIU, X.,
BURKLUND, A., PEDDIREDDI, L., HANZLICEK, G., HENNINGSON, J., CHENGAPPA,
M. M. & BAI, J. 2020. Development of a nested PCR assay for detection
of Streptococcus equi subspecies equi in clinical equine specimens and
comparison with a qPCR assay. J. Microbiol. Methods,172, 172.
PAILLOT, R., LOPEZ-ALVAREZ, M. R., NEWTON, J. R. & WALLER, A. S. 2017.
Strangles: A modern clinical view from the 17th century. Equine
Vet. J., 49, 141-145.
PARKHILL, J., SEBAIHIA, M., PRESTON, A., MURPHY, L. D., THOMSON, N.,
HARRIS, D. E., HOLDEN, M. T., CHURCHER, C. M., BENTLEY, S. D., MUNGALL,
K. L., CERDENO-TARRAGA, A. M., TEMPLE, L., JAMES, K., HARRIS, B., QUAIL,
M. A., ACHTMAN, M., ATKIN, R., BAKER, S., BASHAM, D., BASON, N.,
CHEREVACH, I., CHILLINGWORTH, T., COLLINS, M., CRONIN, A., DAVIS, P.,
DOGGETT, J., FELTWELL, T., GOBLE, A., HAMLIN, N., HAUSER, H., HOLROYD,
S., JAGELS, K., LEATHER, S., MOULE, S., NORBERCZAK, H., O’NEIL, S.,
ORMOND, D., PRICE, C., RABBINOWITSCH, E., RUTTER, S., SANDERS, M.,
SAUNDERS, D., SEEGER, K., SHARP, S., SIMMONDS, M., SKELTON, J., SQUARES,
R., SQUARES, S., STEVENS, K., UNWIN, L., WHITEHEAD, S., BARRELL, B. G.
& MASKELL, D. J. 2003. Comparative analysis of the genome sequences of
Bordetella pertussis, Bordetella parapertussis and Bordetella
bronchiseptica. Nat. Genet., 35, 32-40.
PRESCOTT, J. F., SRIVASTAVA, S. K., DEGANNES, R. & BARNUM, D. A. 1982.
A mild form of strangles caused by an atypical Streptococcus equi.J. Am. Vet. Med. Assoc., 180, 293-9.
PRINGLE, J., ASP..N, A. & RIIHIM..KI, M. 2022. Repeated nasopharyngeal
lavage predicts freedom from silent carriage of Streptococcus equi after
a strangles outbreak. J. Vet. Int. Med., 36, 787-791.
PRINGLE, J., STORM, E., WALLER, A. & RIIHIMAKI, M. 2020a. Influence of
penicillin treatment of horses with strangles on seropositivity to
Streptococcus equi ssp. equi-specific antibodies. J. Vet. Intern.
Med., 34, 294-299.
PRINGLE, J., VENNER, M., TSCHESCHLOK, L., BÄCHI, L. & RIIHIMÄKI, M.
2019. Long term silent carriers of Streptococcus equi ssp. equi
following strangles; carrier detection related to sampling site of
collection and culture versus qPCR. Vet. J., 246, 66-70.
PRINGLE, J., VENNER, M., TSCHESCHLOK, L., WALLER, A. S. & RIIHIMAKI, M.
2020b. J. Vet. Int. Med. Journal of Veterinary Internal Medicine,34, 2751-2757.
PUSTERLA, N., BARNUM, S. M. & BYRNE, B. A. 2021. Investigation of a
24-Hour Culture Step to Determine the Viability of Streptococcus equi
Subspecies equi Via Quantitative Polymerase Chain Reaction in Nasal
Secretions From Horses With Suspected Strangles. J. Equine Vet.
Sci., 97, 103328.
PUSTERLA, N., LEUTENEGGER, C. M., BARNUM, S. M. & BYRNE, B. A. 2018.
Use of quantitative real-time PCR to determine viability of
Streptococcus equi subspecies equi in respiratory secretions from horses
with strangles. Equine Vet. J., 50, 697-700.
RAMEY, D. 2007. Does early antibiotic use in horses with ‘strangles’
cause metastatic Streptococcus equi bacterial infections? Equine
Vet. Educ., 19, 14-15.
RENDLE, D., BRAUWERE, N. D., HALLOWELL, G., IVENS, P., MCGLENNON, A.,
NEWTON, R., WHITE, J. & WALLER, A. 2021. Streptococcus equi infections:
current best practice in the diagnosis and management of ’strangles’.U.K. Vet. Equine, 5, S3-S15.
RIIHIMÄKI, M., PRINGLE, J. P., BÅVERUD, V., NYMAN, A. K. & GRÖNDAHL, G.
2016. Correlation between endoscopic findings and real-time PCR analysis
for Streptococcus equi subsp. equi DNA of guttural pouches in recovered
strangles cases. J. Equine Vet. Sci., 39, S96.
ROBINSON, C., FRYKBERG, L., FLOCK, M., GUSS, B., WALLER, A. S. & FLOCK,
J. I. 2018. Strangvac: A recombinant fusion protein vaccine that
protects against strangles, caused by Streptococcus equi.Vaccine, 36, 1484-1490.
ROBINSON, C., STEWARD, K. F., POTTS, N., BARKER, C., HAMMOND, T. A.,
PIERCE, K., GUNNARSSON, E., SVANSSON, V., SLATER, J., NEWTON, J. R. &
WALLER, A. S. 2013. Combining two serological assays optimises
sensitivity and specificity for the identification of Streptococcus equi
subsp. equi exposure. Vet. J., 197, 188-91.
ROBINSON, C., WALLER, A. S., FRYKBERG, L., FLOCK, M., ZACHRISSON, O.,
GUSS, B. & FLOCK, J. I. 2020. Intramuscular vaccination with Strangvac
is safe and induces protection against equine strangles caused by
Streptococcus equi. Vaccine, 38, 4861-4868.
ROSA, M. C., CONRAD, N. L., MORAES, C. M. & LEITE, F. P. L. 2021.
Immunogenicity of Streptococcus equi subsp. equi recombinant SeM protein
and bacterin in mice. Pesqui. Vet. Bras., 41.
RUFFO, G. 1256. De Medicina Equorum. Italy.
SCHÜTZ, J. W. 1888. The Streptococcus of Strangles. J. Comp.
Pathol. Ther., 1, 191-208.
SHEORAN, A. S., SPONSELLER, B. T., HOLMES, M. A. & TIMONEY, J. F. 1997.
Serum and mucosal antibody isotype responses to M-like protein (SeM) of
Streptococcus equi in convalescent and vaccinated horses. Vet.
Immunol. Immunopathol., 59, 239-51.
SLOVIS, N. M., BROWNE, N. & BOZORGMANESH, R. 2020. Point-of-Care
Diagnostics in Equine Practice. Vet. Clin. N. Am., Equine Pract.,36, 161-171.
SOLLEYSEL, J. 1664. e parfait mareschal qui enseigne a connoistre
la beauté, la bonté, & les deffauts des chevaux, Paris, Gervais
Clousier.
SPONSELLER, B. T., VALBERG, S. J., TENNENT-BROWN, B. S., FOREMAN, J. H.,
KUMAR, P. & TIMONEY, J. F. 2005. Severe acute rhabdomyolysis associated
with Streptococcus equi infection in four horses. J. Am. Vet. Med.
Assoc., 227, 1800-7, 1753-4.
SPOORMAKERS, T. J., ENSINK, J. M., GOEHRING, L. S., KOEMAN, J. P., TER
BRAAKE, F., VAN DER VLUGT-MEIJER, R. H. & VAN DEN BELT, A. J. 2003.
Brain abscesses as a metastatic manifestation of strangles:
symptomatology and the use of magnetic resonance imaging as a diagnostic
aid. Equine Vet. J., 35, 146-151.
STEWARD, K. F., ROBINSON, C., MASKELL, D. J., NENCI, C. & WALLER, A. S.
2017. Investigation of the Fim1 putative pilus locus of Streptococcus
equi subspecies equi. Microbiology (Reading), 163,1217-1228.
ŠTRITOF, Z., MITCHELL, C., TURK, N., HABUŠ, J., HAĐINA, S., PERHARIĆ, M.
& WALLER, A. S. 2021. Seroprevalence of Streptococcus equi subspecies
equi in Croatia - Short communication. Acta Vet. Hung.,68, 361-363.
SVONNI, E., ANDREASSON, M., FERNSTROM, L. L., RYDEN, A., PRINGLE, J. &
RIIHIMAKI, M. 2020. Potential for residual contamination by
Streptococcus equi subspp equi of endoscopes and twitches used in
diagnosis of carriers of strangles. Equine Vet. J., 52,884-890.
SWEENEY, C. R., TIMONEY, J. F., NEWTON, J. R. & HINES, M. T. 2005.
Streptococcus equi infections in horses: guidelines for treatment,
control, and prevention of strangles. J. Vet. Intern. Med.,19, 123-34.
SWEENEY, C. R., WHITLOCK, R. H., MEIRS, D. A., WHITEHEAD, S. C. &
BARNINGHAM, S. O. 1987. Complications associated with Streptococcus equi
infection on a horse farm. J. Am. Vet. Med. Assoc., 191,1446-8.
TIMONEY, J. F. 2004. The pathogenic equine streptococci. Vet.
Res., 35 397–409.
TIMONEY, J. F., ARTIUSHIN, S. C. & BOSCHWITZ, J. S. 1997. Comparison of
the sequences and functions of Streptococcus equi M-like proteins SeM
and SzPSe. Infect. Immun., 65, 3600-5.
TIMONEY, J. F. & KUMAR, P. 2008. Early pathogenesis of equine
Streptococcus equi infection (strangles). Equine Vet. J.,40, 637-42.
TIMONEY, J. F., SHEORAN, A. & ARTIUSHIN, S. 1998. Detection of
strangles carriers. Vet. Rec., 142, 648.
TIWARI, R., QIN, A., ARTIUSHIN, S. & TIMONEY, J. F. 2007. Se18.9, an
anti-phagocytic factor H binding protein of Streptococcus equi.Vet. Microbiol., 121, 105-15.
TODD, T. G. 1910. Strangles. J. Comp. Path. Therap., 23,212–229.
TSCHESCHLOK, L., VENNER, M., STEWARD, K., BOSE, R., RIIHIMAKI, M. &
PRINGLE, J. 2018. Decreased Clinical Severity of Strangles in Weanlings
Associated with Restricted Seroconversion to Optimized Streptococcus
equi ssp equi Assays. J. Vet. Intern. Med., 32, 459-464.
VALBERG, S. J., BULLOCK, P., HOGETVEDT, W., AMES, T., HAYDEN, D. W. &
OTT, K. 1996. Myopathies associated with Streptococcus equi infections
in horses. Proc. Am. Assoc. Equine Pract., 42, 292–293.
VAN DE KOLK, J. H. & KROEZE, E. J. B. V. 2013. Infectious
Diseases of the Horse : Diagnosis, Pathology, Management, and Public
Health, London, Manson Publishing/The Veterinary Press.
VAN MAANEN, K., GRONDAHL, G., PRINGLE, J., RIIHIMAKI, M., DE BRAUWERE,
N. & WALLER, A. 2021. Streptococcus equi subspecies equi avidity ELISA:
A useful tool to detect carriers? Equine Vet. J., 53(SUPPL
56), 24-25.
VERHEYEN, K., NEWTON, J. R., TALBOT, N. C., DE BRAUWERE, M. N. &
CHANTER, N. 2000. Elimination of guttural pouch infection and
inflammation in asymptomatic carriers of Streptococcus equi.Equine Vet. J., 32, 527-32.
WALLER, A. & WILSON, H. Streptococcus zooepidemicus: commensal or
pathogen? 67th Annual Convention of the American Association of Equine
Practitioners, 4-8 December 2021 2021 Nashville, Tennessee. Lexington,
319-326
WALLER, A. S. 2014. New perspectives for the diagnosis, control,
treatment, and prevention of strangles in horses. Vet. Clin. N.
Am., Equine Pract., 30, 591-607.
WALLER, A. S. 2016. Strangles: a pathogenic legacy of the war horse.Vet. Rec., 178, 91-2.
WALLER, A. S. 2017. Science-in-brief: Streptococcus zooepidemicus: a
versatile opportunistic pathogen that hedges its bets in horses.Equine Vet. J., 49, 146-148.
WALLER, A. S. & JOLLEY, K. A. 2007. Getting a grip on strangles: recent
progress towards improved diagnostics and vaccines. Vet. J.,173, 492-501.
WALLER, A. S., PAILLOT, R. & TIMONEY, J. F. 2011. Streptococcus equi: a
pathogen restricted to one host. J. Med. Microbiol., 60,1231-1240.
WALLER, A. S. & ROBINSON, C. 2013. Streptococcus zooepidemicus and
Streptococcus equi evolution: the role of CRISPRs. Biochem. Soc.
Trans., 41, 1437-43.
WEBB, K., BARKER, C., HARRISON, T., HEATHER, Z., STEWARD, K. F.,
ROBINSON, C., NEWTON, J. R. & WALLER, A. S. 2013. Detection of
Streptococcus equi subspecies equi using a triplex qPCR assay.Vet. J., 195, 300-4.
WHITE, J., PRESCOTT, K. & ROGERS, S. 2021. Applying the science of
behaviour change to the management of strangles. U.K. Vet.
Equine, 5, 110-114.
WHITELEGG, H. & SAUNDERS, T. 2021. Nursing a horse with strangles.U.K. Vet. Equine, 5, 225-230.
WHITLOCK, F. M., NEWTON, J. R. & WALLER, A. S. 2019. Metastatic
abscessation and other potential complications following strangles.Equine Vet. Educ., 31, 539-542.
WILLIS, A. T., BARNUM, S. & PUSTERLA, N. 2021. Validation of a
point-of-care polymerase chain reaction assay for detection of
Streptococcus equi subspecies equi in rostral nasal swabs from horses
with suspected strangles. Can. Vet. J., 62, 51-54.
WOOLCOCK, J. B. 1974. The capsule of Streptococcus equi. J. Gen.
Microbiol., 85, 372-5.