Skipped vertebral spontaneous spondylodiscitis caused by Granulicatella adiacens: Case report and a systematic literature review

Skipped vertebral spontaneous spondylodiscitis caused by Granulicatella adiacens: Case report and a systematic literature review

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Skipped vertebral spontaneous spondylodiscitis caused by Granulicatella adiacens: Case report and a systematic literature review Andrea Perna a, b, 1, Luca Ricciardi a, c, *, 1, Carmelo Lucio Sturiale a, Massimo Fantoni a, d, Francesco Ciro Tamburrelli a, b, Nadia Bonfiglio a, b, Luca Proietti a, b a

Fondazione Policlinico Universitario Agostino Gemelli e IRCCS, Rome, Italy  di chirurgia vertebrale, Universita  Cattolica del Sacro Cuore, Rome, Italy Istituto di ortopedia e traumatologia, unita  Cattolica del Sacro Cuore, Rome, Italy Istituto di Neurochirurgia, Universita d  Cattolica del Sacro Cuore, Rome, Italy Istituto di Malattie infettive, Universita b c

a r t i c l e i n f o

a b s t r a c t

Article history: Received 30 May 2019 Received in revised form 23 June 2019 Accepted 11 July 2019 Available online xxx

Background: Granulicatella adiacens is a nutritional variant of streptococcus (NVS), which has been rarely reported as an etiologic agent in spondylodiscitis (SD). Material and methods: We report a case of a 51-year-old male with from chronic low-back pain associated with right sciatica and ipsilateral monoparesis. Spinal MRI showed radiological signs on L1-L2 and L5-S1 discs consistent with SD. We also performed a systematic review of the pertinent literature in order to retrieve all the key information regarding microbiological and clinical features. Results: Including our patients, seven cases with a mean age 56 ± 10.2 years were reported in English literature. Six patients were conservatively managed with antibiotic therapy (66%), whereas three with surgery in combination with antibiotics (33%). An endocarditis was associated in three cases, and a pacemaker infection in one. All patients received targeted antibiotic therapy resulting in a quick improvement of clinical symptoms with favorable outcome. Our case is the only with a skip spontaneous SD, which needed a surgical decompression due to the associated neurological symptoms. Conclusions: This incidence of SD sustained by Granulicatella adiances could be underestimated due to their particular microbiological conditions requested for their cultures. However, this infection should be suspected in cases of culture-negative SD, especially when associated with endocarditis. © 2019 Delhi Orthopedic Association. All rights reserved.

Keywords: Vertebral osteomyelitis Spondylodiscitis Streptococci Spine infection Granulicatella adiacens

1. Introduction Spinal infections are severe conditions and general guidelines are not still available.1 Among them, spondylodiscitis (SD) and vertebral osteomyelitis (VO) are uncommon and may require longlasting antibiotic therapy and, sometimes, a surgical treatment.2e4 Although usually determined by pyogenic bacteria, several agents may be also involved.5,6 Granulicatella adiacens, also known as nutritional variant Streptococcus (NVS), is a demanding pathogen

that needs vitamin B6 analogues and L-cysteine availability for growing.7 It is a microbiota commensal member of the upper respiratory, urogenital, and gastrointestinal tracts7,8; however, it can cause different infectious diseases such as endocarditis, otitis, and severe conditions affecting the eye, the periprosthetic district, and the central nervous system.7e12 In this paper, we firstly report a spontaneous skipped vertebral SD caused by Granulicatella adiacens, surgically managed, along with a systematic review of the pertinent literature. 2. Case report

Abbreviations: CRP, C-Reactive Protein; NVS, nutritional variant of Streptococcus; SD, Spondylodiscitis; VAS, visual analogue scale; VO, vertebral osteomyelitis. * Corresponding author. Department of Neurosurgery, Fondazione Policlinico  Cattolica del Sacro Cuore, Rome, Universitario Agostino Gemelli e IRCCS, Universita Italy, Largo A. Gemelli 1, 00168, Rome, Italy. E-mail address: [email protected] (L. Ricciardi). 1 These two authors contributed equally to this paper.

A 51-year-old male patient affected by a mitral valve prolapse was admitted at our department for a persistent low back pain associated with right sciatica, which did not improve after selfmedicating with non-steroidal anti-inflammatory drugs. A written consent for medical and scientific purposes, according to the institutional guidelines, was collected. On physical examination, a

https://doi.org/10.1016/j.jcot.2019.07.002 0976-5662/© 2019 Delhi Orthopedic Association. All rights reserved.

Please cite this article as: Perna A et al., Skipped vertebral spontaneous spondylodiscitis caused by Granulicatella adiacens: Case report and a systematic literature review, Journal of Clinical Orthopaedics and Trauma, https://doi.org/10.1016/j.jcot.2019.07.002

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profuse sweating and a 3/6 systolic blowing was heard on the centrum cordis. At the neurological examination, the patient presented hypoesthesia in the right L5 and S1 territories, a motor deficit (MRC 3/5) of the ipsilateral long extensor of the hallux, tibialis anterior, and extensor of the fingers muscles, and an attenuated ipsilateral Achilles reflex. Visual analogue scale (VAS) for back and leg pain were rated 10 and 8, respectively. Laboratory investigations showed an elevated erythrocyte sedimentation rate (75 mm/h), an increased C-reactive protein (CRP, 78.7 mg/L), increased leukocytes rate (17.7 M per cm3 - NEU 14.2 M per cm3). The patient also reported multiple episodes of fever in the previous week, without any symptoms of respiratory, urogenital or gastrointestinal infections (Fig. 1). Lumbar spine MRI showed a L5-S1 and L1-L2 intervertebral discs hyperintensity on T2-weighted and STIR sequences, along with a fluid collection in the anterior epidural space at L5-S1, consistent with a skipped SD (Fig. 2). Clinical, radiological and laboratory data were suspicious for SD. Thus, the clinical status and the radiological compression were evaluated and, due to the presence of neurological symptoms,3 a decompressive surgery, consisting in a L5-S1 right laminotomy, microdiscectomy, and debulking of the purulent material was performed. Immediately after surgery, empiric antibiotic therapy with intravenous teicoplanin 1000 mg every 12 h was started for the first three administrations and then continued with 1000 mg every 24 h. Due to the diagnosis, pain and risk of deformity, a rigid brace was also prescribed.13,14 Although no microbiological agent was identified in surgical bioptic samples, postoperative (2 h after the procedure) blood cultures were positive for Granulicatella adiacens. A transesophageal echocardiogram confirmed the known mitral valve posterior flap prolapse associated with myxoid degeneration, but without presence of vegetations. After the microbial diagnosis, oral levofloxacin 750 mg every 24 h was added to the ongoing antibiotic therapy. Two days after the surgery, the neurological symptoms were significantly improved and the patient was mobilized with a rigid fiberglass brace. By the first week, the laboratory indexes showed a decreasing trend (leukocytes rate decreased from 17.7 M per cm3 at t0, to 14.8 M per cm3 the first day after surgery, to 13.4 M per cm3 the third day after surgery and 12.6 M per cm3 one week after surgery, CRP trend was shown in Fig. 1) and the pain was significantly improved (VAS-back ¼ 3; VASleg ¼ 2). The patient was discharged in good clinical and neurological conditions after 15 days of medical treatment, and oral levofloxacin (750 mg every 24 h) was continued for further 6 weeks. The rigid brace was removed 6 months later. At one-year follow-up, the patient was in good clinical conditions with no restrictions in the daily activities, and the imaging did not document segmental deformity, stenosis or radiological signs of infection (Fig. 4).

3. Discussion and systematic review SD and VO sustained by Granulicatella adiacens are very rare clinical conditions. We performed a systematic review of English literature indexed in PubMed, Embase and Google Scholar databases using as search-terms “Granulicatella adiacens” AND “vertebral osteomyelitis” OR “spondylodiscitis” OR “spine infection”, and their mesh terms combinations. Two authors (A.P. and L.R.) independently screened abstracts and full-text papers, and any discordance was solved by consensus with a third author (C.L.S.). At the end of the screening of 178 manuscripts, seven papers reporting about 8 patients were included in our review, since they met our inclusion criteria. Overall, including our report, 9 patients were analyzed in this systematic review (Fig. 3).15e21 Further 4 cases of SD, 3 postsurgical and 1 in an intravenous drug user, have been found,22e25 but they were not included in this review according to the our criteria (spontaneous infection). The mean age of included patients was 56 ± 10.2 years, and the male/female ratio was 8:1. Demographic, clinical and neuroradiological information are summarized in Table 1. Overall, 6 patients were conservatively managed with antibiotic therapy (66%),15e17 whereas 3 in combination with surgery (33%).19,20 Among them, one case diagnosed for vertebral osteomyelitis was treated with a posterior decompression, a corpectomy with prosthetic replacement, and fusion,20 one case with a posterior decompression and fusion19; whereas our patient was treated with a posterior decompression only. Infectious vegetations as evidence of endocarditis were found on cardiac valves in 3 cases,15,21 and on the implanted pacemaker in one.16 In two cases (included our patient), a mitral valve myxoid degeneration without vegetations was observed.17 In one case, no heart valve degeneration or vegetation was found.21 All patients received targeted antibiotic therapy resulting in a quick improvement of clinical symptoms and a final favorable outcome. Endocarditis seemed to be the most frequent risk factor for SD by Granulicatella adiacens, being reported in 4 patients (44%),15,16,20 followed by diabetes mellitus in 2 cases (22%),19,21 and a recent dental procedures, in 1 case (11%).19 The diagnosis was based on blood cultures in 7 cases (77%),15e20 and on CT-guided discal biopsy in 2 (23%),18,21 suggesting a challenging isolation of the germ from biopsy samples. The preferred antimicrobial agents were: Gentamicin (55%),15e17,21 Penicillin (44%),15e17 Ciprofloxacin (22%),15 Vancomycin (22%),20 Ceftriaxone (22%),15 Ampicillin (11%),18 Fusidic Acid (11%),15 Amoxicillin (11%),17 Ceftazidime (11%),19 Rifampicin (11%)16 in order of percentage of use. The mean duration of the antibiotic therapy was 55.1 ± 23.76 days. All patients reported a total low back pain relief, furthermore, neurological symptoms were solved in

Fig. 1. Indexes trend. a: Graphical representation of the CRP values expressed in mg/L; b: Graphical representation of the patient's body temperature expressed in degrees Celsius, day 5 is the day the patient came to the hospital; c: Graphical representation of the values of VAS back and VAS leg.

Please cite this article as: Perna A et al., Skipped vertebral spontaneous spondylodiscitis caused by Granulicatella adiacens: Case report and a systematic literature review, Journal of Clinical Orthopaedics and Trauma, https://doi.org/10.1016/j.jcot.2019.07.002

A. Perna et al. / Journal of Clinical Orthopaedics and Trauma xxx (xxxx) xxx

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Fig. 2. Radiological findings. a,c: Sagittal cuts of lumbosacral MRI in T2-weighted sequence that show the presence of a hyper-intensity signal at the L5-S1 and L1-L2 disks. b,c: sagittal cuts of STIR sequences of MRI that highlight signal intensities at the level of the affected disks. At both levels, it is possible to observe the presence of material in the anterior epidural space. At L5-S1 level in the presacral space.

Fig. 3. Search strategy.

Fig. 4. Radiological follow-up. The images collected 1 year after the surgical procedure did not show signs of segmental deformity (aeb) or stenosis (ced) at the involved segments.

Please cite this article as: Perna A et al., Skipped vertebral spontaneous spondylodiscitis caused by Granulicatella adiacens: Case report and a systematic literature review, Journal of Clinical Orthopaedics and Trauma, https://doi.org/10.1016/j.jcot.2019.07.002

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Table 1 Systematic review data. Author and year

Sex Age Risk Factors (Year)

Heath CH M et al., 1998 M

Symptoms

Level Pathogen involved

Complication Antibiotic treatment

not reported IV PCN þ GENT 4 w, IV PCN 2 w, PO CLIN 2w L3-L4,- Abiotrophia not reported PO CPF and FA 12 w L5 adiacens (empiric), IV PCN þ GENT 2w, IV CTX 2w T10-T11 Granulicatella not reported PCN þ GENT þ RIF Back pain, fever, TEE: Adiacens (no duration or vegetation adjacent to the type of PM lead administration) IV PCN þ GENTf4 Granulicatella Mitral Back pain, fever TEE: no L3-L4 Adiacens valvoplasty w, PO AMOX (no vegetation, mixoid in 107 days duration reported) degeneration Back pain, fever, weakness L3-L4- Abiotrophia not reported IV AMP 6 w in the right toe L5 adiacens L2-L3,L4

Abiotrophia adiacens

Outcome

Blood

None

Cured

Blood

None

Cured

Blood

None

Cured

Blood

None

Cured

Blood and Disc Blood

Needle biopsy of the L3- Cured 4 disc

45

not reported

50

not reported

Rosenthal M O et al., 2002

68

DM, IHD, coronary stenosis, PM

M

73

HT,HL

F

48

PD

M

62

HT

Back pain, fever, TEE: heart valve vegetation

M

46

Back and lower extremity L2 pain, lower extremity weakness, numbness, saddle anesthesia

Granulicatella not reported IV VM and CFZ 1 w, Blood Adiacens IV VM 6 w

Sandhu R M et al., 2017. Present M case

61

DM, Smoker, dental procedure one month prior DM, HT

L3-L4 Back pain, TEE: no vegetation, non valve degeneration L1-L2, Back pain, fever, neurological deficits. TEE: L5-S1 no vegetation, mixoid degeneration

Granulicatella not reported IV CTX þ GENT 6 w Disc Adiacens

needle biopsy of the L3-4 Cured disc

Granulicatella not reported IV TPL þ PO CPF 2 Adiacens w, PO CPF 6 w

L5-S1 t laminotomy, pus Cured drenage, disc biopsy

Fukuda R et al., 2010 Uehara K et al., 2013 Shiferaw B et al., 2015. York J et al., 2016

51

Mitral valve prolaps, HT

Back pain, fever, mitral regurgitation, TEE: mitral vegetation Back pain, aortic regurgitation, TEE: aortic vegetation

Culture Surgery

T10Abiotrophia T11-T12 adiacens

not reported IV VM 6 w

Blood

Cured L2 posterior decompression and fixation T9 to L2 Cured L2 corpectomy, interbody cage, posterior decompression and fixation from L1 to L3

AMOX: amoxicillin; AMP: ampicillin; CFZ: Ceftazidime; CLIN: clindamycin; CPF: ciprofloxacin; CTX: ceftriaxone; DM: diabetes mellitus; FA: fusidic acid; GENT: gentamicin; HT: hypertension, HL: hyperlipidemia; IHD: ischemic heart disease; IV: intravenous administration; PCN: penicillin; PD: Parkinson's disease; PM: pacemaker; PO: oral administration; RIF: rifampicin; TPL: teicoplanin; TEE: Transesophageal echocardiogram; VM: vancomycin; W: weeks.

every case. No cases of death were recorded, so that SD sustained by Granulicatella adiacens seems to be less fatal than those mediated by other agents, such as the drug-resistant Staphylococcus (1.7%e 11%).6,26e28 However, this data is biased by the small patients sample included in this review. The pathogenesis of SD recognizes three main pathways: haematogenous spreading, direct inoculation (iatrogenic), and diffusion from adjacent sites.2,3,6,13 However, the first mechanism is the most reported.6 In fact, in about 12% of cases, the SD is determined by endocarditis.17 Nonetheless, in the case we reported, we were not able to demonstrate the presence of endocarditis, according to Duke's criteria, despite the isolation of a microbial agent in the peripheral blood. Staphylococcus aureus represents the most frequent etiologic agent of spondylodiscitis, followed by Escherichia coli and Streptococcus species.5,6,26,29 Granulicatella adiacens, firstly reported by Frenkel and Hirsch in 1961,8 is often responsible for endocarditis with negative blood cultures. In fact, its growth is particularly difficult in standard microbiological culture plates, which do not contain analogues of vitamin B6, essential for the Granulicatella metabolism.7 Nowadays, only 8 previous cases of spontaneous spondylodiscitis caused by Granulicatella adiacens have been reported.15e21 Among them, Heath et al., in 1998 described 2 cases of SD involving multiple adjacent intervertebral discs.15 Accordingly, this is the first case of a skip (L1-L2 and L5-S1) vertebral SD. The clinical onset of SD may be various, making the diagnosis challenging.2,3,6 An intense and long-lasting low back pain associated with fever, unresponsive to anti-inflammatory drugs, should be considered as suspicious for a SD, although, on the other hand,

the low back pain represents one of the most common pathological condition in the general population.2,3,6,30 SD-related pain has usually mechanical characteristics, getting worse with the axial load, and may be associated with neurological symptoms.3 To complete the diagnosis, the identification of the pathogen is required, from blood cultures or biopsy.4,6 A CT-guided percutaneous biopsy is the procedure of choice in the majority of the cases.3 Nonetheless, an open biopsy may be preferred when a direct decompression is necessary for the presence of neurologic symptoms.3,31 The possibility for percutaneous endoscopic techniques, as reported for lumbar discectomy, should be also considered in case of need for both sampling and decompression. Although biopsy samples are often negative, diagnosis may be achieved by the peri-operative blood cultures, due to a transient bacteremia caused by the surgical procedure.3,4,6 Antibiotic therapy should be started as soon as possible,3,4 starting with intravenous drugs, and administered for up to six weeks, except in specific cases.3,4,25,32

4. Conclusions A single or multiple levels SD sustained by Granulicatella adiances represents a rare condition, even though its incidence may be underestimated, due to technical difficulties. This agent should be investigated in culture negative SD, especially when associated with endocarditis, being the targeted therapy a possibility for complete recovery. Our case is the firstly reported skip vertebral spontaneous spondylodiscitis determined by Granulicatella adiacens, managed with a posterior decompression, without any instrumentation, and

Please cite this article as: Perna A et al., Skipped vertebral spontaneous spondylodiscitis caused by Granulicatella adiacens: Case report and a systematic literature review, Journal of Clinical Orthopaedics and Trauma, https://doi.org/10.1016/j.jcot.2019.07.002

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medical therapy. This systematic review results showed the diagnostic strategy along with its technical limitations, the most preferred drugs combinations, and patients outcomes. Patient consent The patient has consented to the submission of this case report to the journal.

13.

14.

15.

Funding statement 16.

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

17.

Appendix A. Supplementary data

18.

Supplementary data to this article can be found online at https://doi.org/10.1016/j.jcot.2019.07.002.

19.

20.

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Please cite this article as: Perna A et al., Skipped vertebral spontaneous spondylodiscitis caused by Granulicatella adiacens: Case report and a systematic literature review, Journal of Clinical Orthopaedics and Trauma, https://doi.org/10.1016/j.jcot.2019.07.002