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Streptococcus Zooepidemicus and Review Pathogenesis â€⢠Clinical Presentation â€â¢

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Zoonotic necrotizing myositis acquired by Streptococcus equi subsp. zooepidemicus in a farmer

  • Veronika Kuchařová Pettersen2,
  • Oddvar Oppegaard2,3,
  • Dag Harald Skutlaberg2,4,
  • Håvard Dale5,
  • Harald Thousand. Wikertwo,4 &
  • Steinar Skredeii,iii

BMC Infectious Diseases book 17, Commodity number:147 (2017) Cite this commodity

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Abstract

Background

Streptococcus equi subsp. zooepidemicus is a beta-hemolytic group C streptococcus mainly causing infections in domesticated animals. Here nosotros describe the starting time instance of zoonotic necrotizing myositis caused past this bacterium.

Example presentation

The patient was a 73-yr-old, previously good for you farmer with ii asymptomatic Shetland ponies in his stable. After close contact with the ponies while feeding them, he rapidly developed erythema of his left thigh and sepsis with multiple organ failure. The clinical course was severe and complicated, requiring repetitive surgical excision of necrotic muscle, handling with vasopressors, mechanical ventilation and continuous venovenous hemofiltration, forth with adjunctive hyperbaric oxygen therapy. The patient was discharged from infirmary at solar day 30, without obvious sequelae.

The streptococcal isolate was identified as Streptococcus equi by MALDI-ToF MS, and was later assigned subspecies identification as S. equi subsp. zooepidemicus. Multilocus sequence typing identified the strain every bit a novel sequence type (ST 364), closely related to types previously identified in horses and cattle. A focused proteomic analysis revealed that the ST 364 expressed putative virulence factors similar to that of Streptococcus pyogenes, including homologues of the G poly peptide, streptodornases, interleukin 8-protease and proteins involved in the biosynthesis of streptolysin S.

Conclusion

This case illustrates the zoonotic potential of S. equi subsp. zooepidemicus and the importance of early clinical recognition, rapid and radical surgical therapy, appropriate antibiotics and adequate supportive measures when necrotizing soft tissue infection is suspected. The expression of Streptococcus pyogenes-like putative virulence determinants in ST 364 might partially explicate the fulminant clinical picture.

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Background

Streptococcus equi subsp. zooepidemicus (Due south. zooepidemicus) is a beta-haemolytic group C streptococcus able to colonize the upper airways of horses and produce diverse clinical manifestations in domesticated animals, including respiratory tract infections, mastitis and meningitis [1–4]. South. zooepidemicus rarely causes human infection, and the mechanism is supposed to be zoonotic transmission by direct contact with infected or colonized animals or the consumption of unpasteurized milk products [five–viii]. This streptococcus has been associated with a wide range of severe human infections, including cellulitis, pericarditis, toxic shock syndrome, endovascular infections, pneumonia, septicaemia, meningitis, arthritis and spondylodiscitis [5, nine–13]. It has besides acquired a large outbreak of post-streptococcal glomerulonephritis in Brazil [14].

Necrotizing myositis is a very rare and potentially lethal infection, constituting the most severe form of necrotizing soft tissue infections (NSTI). Monomicrobial NSTI is most often caused by Streptococcus pyogenes (S. pyogenes), and often associated with septic daze and loftier mortality rates [15–17]. NSTI caused by S. zooepidemicus was recently documented in a canis familiaris shortly after subcutaneous vaccination [18], but to our knowledge, human NSTI caused by S. zooepidemicus has not been reported previously.

Here nosotros present a instance of necrotizing myositis acquired by S. zooepidemicus in a farmer who was in close contact with his two Shetland ponies prior to the infection.

Case presentation

A 73 –year-old male patient was transmitted with air ambulance from a local hospital to Haukeland Academy Hospital (HUH) in western Norway with septic shock and clinical suspicion of NSTI in his left thigh.

His previous medical history included paroxysmal atrial fibrillation, treated with flecainide, and psoriatic arthritis. He was a farmer, with two Shetland ponies in his stable. A few days prior to hospitalization, he had acquired minor abrasions and blisters on his fingers and subsequently been in directly contact with the ponies upon feeding them.

In the afternoon on day 1, he was admitted to the local hospital with acute pain in his left groin. He rapidly developed symptoms and signs of septic shock. Blood cultures were drawn, and empiric antibody therapy with penicillin Yard, clindamycin and gentamicin was initiated. Computed tomography imaging of the pelvis and left thigh showed possible necrotizing myositis or pyomyositis and he was thereupon quickly transferred to a tertiary intendance facility.

Upon access at HUH 24-hour interval 2 the patient was intubated and maintained an adequate blood force per unit area of 139/61 mmHg on a low-dose noradrenaline-infusion (0.03 μg/kg/min). His temperature was 38.7 ° C and the pulse rate was 108 per minute. A relatively sharply demarcated erythema in the left thigh was observed, just neither bulla, ecchymosis or skin necrosis was present. Blood cultures and initial claret chemistry analyses were obtained. Further diagnostic and therapeutic strategies were discussed in a multidisciplinary team consisting of an orthopaedic and plastic surgeon, infectious disease consultant and anaesthesiologist. A preoperative magnetic resonance tomography was rapidly performed, revealing probable necrotizing fasciitis and myositis primarily involving the adductor muscles and musculus pectineus in the left thigh. The patient was then transmitted to the operation theatre with a apace spreading erythema and a fulminant septic stupor, now requiring high-dose noradrenaline infusion (0.3 μg/kg/min). Initial blood chemical science results were as follows, with normal range values in parentheses:

C-reactive protein 129 mg/l (<5 mg/l); leucocytes i.5 × xix/fifty (three.5 × ten9/l to 11.0 × 109/l); neutrophils one.two × 109/fifty (i.7 × ten9/50 to 8.2 × 109/l); haemoglobin 12.4 g/dl (13.4 to 17.0 g/dl); thrombocytes 85 × 109/l (145 × 109/l to 348 × 109/l); creatinine 63 μmol/l (lx μmol/l to 105 μmol/l); myoglobin ten,323 μmol/50 (<70 μmol/fifty), creatine kinase 9550 U/l (40 U/l to eighty U/l); bilirubin 20 μmol/l (<19 μmol/l); activated partial thromboplastin time 47 s (thirty to 44 south); International Normalized Ratio ane.3 (<one.1), lactate 4.8 mmol/l (0.nine mmol/l to ane.seven mmol/fifty), procalcitonin 23.2 μg/50 (<0.1 μg/l).

At the starting time surgical exploration all-encompassing muscle necrosis was establish, requiring excision of m. adductor longus, along with the anterior part of one thousand. adductor magnus. Profound subcutaneous exudation ("dishwater fluid"), simply not frank pus, was besides observed, compatible with the diagnosis necrotizing myositis. Perioperative tissue and fluid samples (n = 8) were obtained for microbiological and histopathological analyses, and a rapid microscopic evaluation of a Gram stained smear from the site of infection revealed Gram positive diplo- and streptococci. The patient was transmitted to the intensive care unit of measurement, with a tentative diagnosis of streptococcal necrotizing myositis.

On mean solar day 3 cultures from blood, tissue and fluid grew beta-haemolytic colonies on blood agar. Species identification of the bacterial isolate every bit Streptococcus equi was performed using matrix-assisted light amplification by stimulated emission of radiation desorption ionization-fourth dimension of flight mass spectrometry (MALDI-ToF MS), using Microflex™ with the MALDI Biotyper database (Bruker Daltonik, Bremen, Germany) and after group C carbohydrate specificity was determined using a slide agglutination exam (Oxoid, Cambridge, United Kingdom). The group C streptococcus was fully susceptible to all tested antibiotics, with the following MIC-values: penicillin Thousand 0.016 mg/l, ceftriaxone 0.064 mg/l and clindamycin 0.25 mg/l. In order to obtain a correct subspecies identification, the streptococcal isolate was sent to the national reference laboratory at the Norwegian Veterinary Constitute in Oslo for further analyses.

The patient withal required treatment with vasopressors and mechanical ventilation, and continuous venovenous hemofiltration was started due to an elevated level of creatinine, oliguria and hyperkalaemia. Gentamicin was discontinued, and therapy with penicillin G and clindamycin was sustained. A 2d surgical revision was performed, revealing progressive necrosis of the subcutaneous tissue and muscle of the left thigh that was treated with a resection of nearly the unabridged m. adductor magnus and brevis, m. pectineus and m. gracilis.

The farther clinical course was severe and complicated, characterized past a need for repeated surgical excision of necrotic tissue, hyperbaric oxygen (HBO) therapy and sustained intensive intendance treatment of gradually resolving organ dysfunctions and a nosocomial soft tissue superinfection probably acquired past Pseudomonas aeruginosa, which grew from a wound specimen upon clinical deterioration on handling with penicillin G and clindamycin.

Table 1 highlights important aspects of the clinical course and summarizes the major microbiological findings, and Fig. 1 shows the muscular necrosis, infiltration of granulocytes and streptococci found upon histopathological analyses.

Tabular array one Summary of the clinical, microbiological and histopathological findings

Total size table

Fig. 1
figure 1

Histological preparation of muscle biopsy (Hematoxylin-eosin staining, × 40), showing infiltration of neutrophil granulocytes (rightward arrows) and aggregates of streptococcal bacteria (downward arrows), surrounded by necrotic muscular tissue

Full size epitome

On day 11, the tracheostomy was removed. The patient was then transferred from the ICU to the infectious illness ward at HUH and further on to the local hospital at 24-hour interval 20. He was treated with penicillin and ciprofloxacin until solar day 30, and was discharged without whatsoever signs of systemic organ dysfunction.

Thereafter, he received physiotherapy on an outpatient basis for a short period and speedily regained adequate muscular function. Twelve months after discharge from hospital he was feeling well, worked full-fourth dimension and went hiking in the local mountains on a regular ground.

Molecular analyses

The strain was identified as S. zooepidemicus according to standard microbiological procedures at the Norwegian Veterinarian Institute [19]. In society to farther identify the strain on a molecular level we performed multilocus sequence typing (MLST), every bit previously described, with primer pairs targeting seven housekeeping genes [twenty]. The sequence analyses showed that this particular strain belonged to a new sequence type of S. zooepidemicus, ST 364, closely related to sequence types previously recovered from horses and cattle (http://pubmlst.org/szooepidemicus).

In guild to explore potential virulence determinants of ST 364, a proteomic analysis based on liquid chromatography-tandem mass spectrometry (LC-MS/MS) was performed (Additional files 1 and 2). The analysis was primarily based on a selection of putative virulence factors identified in the only published South. zooepidemicus genome associated with human infection [21], with a particular focus on a search for homologues of selected well-known virulence factors in Due south. pyogenes.

The proteomic analysis identified altogether 18 proteins linked to S. zooepidemicus virulence (Tabular array 2). For all of these proteins we had derived their relative amounts by employing the proteomic software MaxQuant, which allows for proteins label-free quantification (LFQ) [22]. As a reference poly peptide served elongation factor TU, which is one of the near abundant proteins in most bacterial cells [23]. A number of virulence factors were detected at relatively high levels in ST 364 under in vitro culturing condition. These were cell-surface Chiliad-like protein SzM, streptodornase SdzB, serine protease ScpC/CepA, and several proteins involved in streptolysin S biosynthesis (SagCDG). In add-on, the analysis identified iii other proteins engaged in streptolysin S biosynthesis (SagBHI), a putative peptidoglycan hydrolase (GbpB/SagA/PcsB), several surface-anchored proteins (MlpZ, Fbp, SpaZ and Szp) and enzymes that aid in breaking down the host connective tissue (HylZ) and activate plasminogen (Skc_1, Skc_2).

Table 2 Identification of Streptococcus equi subsp. zooepidemicus ST 364 putative virulence factors by proteomic analysis

Full size tabular array

Discussion

This showtime written report of zoonotic necrotizing myositis caused by S. zooepidemicus illustrates the crucial role of a multidisciplinary approach at access, rapid clinical identification, early on and repeated surgery, acceptable supportive measures and appropriate antibiotics in the treatment of NSTI. The findings from a previous written report on 89 cases of NSTI showed that time to surgery is an important prognostic factor [24], and it is likely that early surgery and meticulous surgical follow-upward was a prerequisite for therapeutic success in our case. The empiric antibiotic treatment consisted of penicillin, clindamycin and gentamicin, in accordance with the national antibiotic guidelines in Norway (http://sites.helsedirektoratet.no/sites/antibiotikabruk-i-sykehus/Sider/default.aspx).

When the bacterial cause was identified and the antibiotic susceptibility design was confirmed, the patient was further treated with a combination of penicillin and clindamycin. Clindamycin has been shown to be superior to beta-lactam-antibiotics in two observational studies on streptococcal NSTI, and furthermore, to reduce mortality of astringent GAS infections including toxic stupor and NSTI [25–28]. Hence, although ST 364 did not belong to South. pyogenes, the combination of penicillin and clindamycin appeared to be the most sensible antibiotic regimen, in line with the recommendations for treatment of beta-haemolytic NSTI in the IDSA-guidelines [29].

The potential effect of HBO - therapy in NSTI has mainly been evaluated in small, retrospective studies, including patients with varying disease severity and a wide range of different bacteriological aetiologies, and the results are diverging [30–32]. The findings from a recent investigation, yet, indicate that the well-nigh severely affected NSTI-patients might do good the nigh from HBO-therapy [33]. Our patient had life-threatening sepsis with multiorgan-dysfunction and extensive muscle necrosis, and received HBO-therapy on two sequent days. We believe that prompt and radical surgery along with appropriate antibiotics were the handling cornerstones in this case, but it is believable that HBO-therapy might have contributed to the relatively rapid improvement of the infection.

Zoonotic transmission to man from asymptomatic horses colonized with Due south. zooepidemicus in the upper airways has previously been described [eight]. Unfortunately, nasopharyngeal swabs were not obtained from the healthy ponies in the present case. The patient developed sores and abrasions on his fingers prior to the infection, was in direct contact with the ponies while feeding them, and had no direct contact with other animals before and effectually the time of infection. Hence, a direct manual of ST 364 from pony to human is suspected and too supported the close genetic relationship between ST 364 and other S. zooepidemicus sequence types from horses, namely ST twoscore, ST 138 and ST 214 (http://pubmlst.org/szooepidemicus).

According to a genomic report on animal isolates of Streptococcus equi subspecies equi and zooepidemicus, the former probably has evolved from an ancestral S. zooepidemicus into a specialized pathogen primarily responsible for strangles in horses [34]. Furthermore, although S. zooepidemicus is able to cause significant respiratory tract infections in horse, they are occasionally associated with asymptomatic nasopharyngeal carriage [1, 35]. Both S. equi subsp. equi and zooepidemicus share extensive homology with South. pyogenes, and lateral genetic substitution betwixt these three streptococcal species has been inferred [34]. In a genomic written report on a Due south. zooepidemicus strain responsible for an outbreak of post-streptococcal glomerulonephritis, the majority of the putative virulence determinants were Due south. pyogenes-homologues [21]. Moreover, like S. pyogenes, S. zooepidemicus causing human infection tend exist associated with a wide range of severe clinical manifestations [five, 9–13].

Knowledge on virulence determinants of severe S. zooepidemicus-infections is scarce, particularly in humans. In the aforementioned genomic report by Beres et al., approximately 100 genes homologous to putative or proven virulence factors in other bacteria, primarily Southward. pyogenes, were identified, including genes encoding factors involved in adhesion, immune response evasion, host jail cell cytotoxicity, bacterial dissemination and mitogenicity [21]. The highlighted proteomic data on ST 364 presented in this study, indicate a marked expression of homologues of virulent determinants (shown in parenthesis) known to play a part in the pathogenesis of beta-haemolytic streptococcal NSTI, namely the Chiliad protein (SzM), streptodornases (SdzB), interleukin eight-protease (SCpC/CepA), and proteins involved in the streptolysin S biosynthesis (sag C/D/Grand) [36–39]. Notably, we could non notice evidence for superantigen activity in ST 364, in concordance with in a recent written report on horses, where just 50% of the S. zooepidemicus-isolates independent superantigen-encoding genes [40].

Our molecular data does not allow for business firm conclusions on the virulence properties of ST 364, and call for a more thorough genetic and proteomic autopsy of this item strain. Furthermore, although our patient did not have any obvious susceptibility for astringent streptococcal affliction, the clinical effect was probably a result of a complex interplay between host factors and bacterial virulence.

Taken together, we speculate that this case story matches the available microbiological, molecular and clinical information on S. zooepidemicus quite well:

Nosotros suspect that a S. zooepidemicus-strain, perhaps non fit do produce clinically significant nasopharyngeal infection in the ponies, but potentially armed with virulence properties homologous to those of S. pyogenes, was transmitted to a human without known predisposition to infection, causing a severe Southward. pyogenes-similar clinical picture.

Determination

This starting time example written report on necrotizing myositis caused past Southward. equi subsp. zooepidemicus illustrates the zoonotic potential and clinical versatility of this beta-haemolytic streptococcus. It is as well a reminder of the fulminant course streptococcal NSTI can pursue, requiring prompt recognition, extensive surgery, advisable antibiotics and supportive treatment in the intensive care unit.

The strain ST 364 belonged to a new sequence type closely related to Due south. zooepidemicus-strains previously identified in horses, and expressed S. pyogenes-like putative virulence determinants.

Key points

  • South. zooepidemicus is primarily an animate being pathogen, but occasionally fit to produce astringent zoonotic infections, including the exceedingly rare manifestation necrotizing myositis

  • Necrotizing myositis requires prompt clinical recognition along with adequate surgical, antibody and supportive therapy

  • The S. pyogenes-like, fulminant grade of necrotizing myositis acquired by Due south. zooepidemicus might exist partially explained by homologous virulence properties

Abbreviations

CVVHF:

Continuous venovenous hemofiltration

HBO:

Hyperbaric oxygen

HUH:

Haukeland Academy Hospital

LC-MS/MS:

Liquid chromatography-tandem mass spectrometry

LFQ:

Label-free quantification

MALDI-ToF MS:

Matrix-assisted laser desorption ionization-time of flight mass spectrometry

MIC:

Minimal inhibitory concentration

MLST:

Multilocus sequence typing

NA:

Noradrenaline

NSTI:

Necrotizing soft tissue infections

Southward. pyogenes :

Streptococcus pyogenes

S.zooepidemicus :

Streptococcus equi subsp. zooepidemicus

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Acknowledgements

We sincerely give thanks Anne Bang Nordstoga for information nearly species identification of ST 364 performed at the Norwegian Veterinary Found, Oslo, Norway, along with Ellen Berget for preparing the picture show of histopathological findings from musculus biopsy performed at the Department of Pathology at Haukeland University Hospital.

Funding

This study received back up from the University of Bergen, and the European Union (FP7/2007-2013) under the grant agreement 305340.

Availability of data and materials

All data generated or analysed during this report are included in this published article and its supplementary information files.

Authors' contribution

BRK drafted the manuscript, performed a literature review and was involved in the design of the molecular analyses, VKP designed and performed the proteomic analyses and revised the manuscript, OO was involved in clinical care, performed the MLST analysis and revised the manuscript, DHS was involved in the microbiological analyses and revised the manuscript, HD was involved in clinical care, obtained surgical samples for microbiological analyses and revised the manuscript, HGW was involved in the blueprint of the proteomic analyses and revised the manuscript SS was involved in clinical care, the design of molecular analyses and revised the manuscript. All authors read and approved the concluding manuscript.

Competing interests

The authors declare that they have no competing interests.

Consent for publication

Written informed consent was obtained from the patient for publication of this case report, including images and any potentially identifying information.

Ideals approval and consent to participate

Not applicable.

Author information

Affiliations

  1. Section of Medicine, Haraldsplass Deaconess Hospital, Bergen, Kingdom of norway

    Bård Reiakvam Kittang

  2. The Gade Research Group for Infection and Amnesty, Department of Clinical Science, University of Bergen, Bergen, Norway

    Veronika Kuchařová Pettersen, Oddvar Oppegaard, Dag Harald Skutlaberg, Harald One thousand. Wiker & Steinar Skrede

  3. Section of Medicine, Haukeland University Hospital, Bergen, Kingdom of norway

    Oddvar Oppegaard & Steinar Skrede

  4. Department of Microbiology, Haukeland University Hospital, Bergen, Norway

    Dag Harald Skutlaberg & Harald G. Wiker

  5. Department of Orthopaedic Surgery, Haukeland University Hospital, Bergen, Norway

    Håvard Dale

Corresponding author

Correspondence to Bård Reiakvam Kittang.

Boosted files

Additional file 1:

Proteomic assay – materials and methods. Methodology of sample training for LC-MS/MS analysis and the MS/MS information analysis. (Md 40 kb)

Additional file 2:

Data sheets – Proteins and Peptides. Results from the proteomic analysis; Streptococcus equi subsp. zooepidemicus proteins detected at 1% FDR and corresponding peptide sequences detected at 1% FDR. (XLSX 45 kb)

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Kittang, B.R., Pettersen, V.G., Oppegaard, O. et al. Zoonotic necrotizing myositis caused by Streptococcus equi subsp. zooepidemicus in a farmer. BMC Infect Dis 17, 147 (2017). https://doi.org/10.1186/s12879-017-2262-7

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  • DOI : https://doi.org/10.1186/s12879-017-2262-vii

Keywords

  • Instance study
  • Zoonosis
  • Streptococcus equi subsp. zooepidemicus
  • Necrotizing myositis

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