Seminars in Arthritis and Rheumatism ] (2016) ]]]–]]]

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Seminars in Arthritis and Rheumatism

journal homepage: www.elsevier.com/locate/semarthrit

Streptococcus bovis septic arthritis and osteomyelitis: A report of

21 cases and a literature review
María José García-País, MDa, Ramón Rabuñal, MD, PhDa,n, Victor Armesto, MDb,
Manuel López-Reboiro, MDa, Fernando García-Garrote, BD, PhDc, Amparo Coira, MD, PhDc,
Julia Pita, MDc, Ana Isabel , BD Rodríguez-Macías, BDc, María José López-Álvarez, MDa,
María Pilar Alonso, MD, PhDc, Juan Corredoira, Md, PhDa
a
Infectious Disease Unit, Hospital Universitario Lucus Augusti, Lugo, Spain
b
Department of Radiology, Hospital Universitario Lucus Augusti, Lugo, Spain
c
Department of Radiology, Hospital Universitario Lucus Augusti, Lugo, Spain

a r t i c l e in fo a b s t r a c t

Background: The Streptococcus bovis group (SBG) is a well-known cause of endocarditis, but its role in
osteoarticular infections (OAIs) has not been well described.
Keywords:
Streptococcus bovis
Methods: We analyzed all patients with OAIs by SBG diagnosed in our hospital (1988–2014). We selected
Osteomyelitis those cases with septic arthritis and osteomyelitis, as defined according to clinical, microbiological, and
Spondylitis imaging studies. Identification of the strains was performed by using the API 20 Strep and the GP card of
Arthritis, Infectious the Vitek 2 system, and confirmed the identification by molecular methods. In addition, we reviewed the
Colorectal neoplasms literature to select all cases of OAI by SBG during the period 1980–2015.
Results: From the 83 cases of OAI included in the analysis (21 from our center and 62 from the literature
review), 59 were osteomyelitis (57 of them spondylodiscitis) and 24 were arthritis (2 with associated
spondylodiscitis). The mean age was 66.9 years, and 79.2% of the patients were men. Endocarditis (IE) was
associated with 59% of the cases and this association was greater for osteomyelitis than for arthritis (78.9%
vs. 13.6%; P ¼ 0.001). OAI was a presenting symptom in 63% of the cases of IE. Colonoscopy was performed
in 64 cases, which detected colorectal neoplasm (CRN) in 46 patients (71.8%), almost all asymptomatic.
Some 69.5% of these neoplasm were carcinomas or advanced adenomas. The blood cultures were positive in
78.3% cases. In 45 cases, the S. bovis species was identified; in 82.2% of the cases the cause was Streptococcus
gallolyticus subsp. gallolyticus. The mortality was 7.2%, which in no case was attributable to the OAI.
Conclusions: OAIs are frequently the initial manifestation of IE caused by SBG. S. gallolyticus causes most of
these infections. Echocardiogram and colonoscopy are therefore mandatory, given the species’ close
association with IE and CRN.
& 2016 Elsevier Inc. All rights reserved.

Introduction caused by SBG is poorly defined, as well as the relative importance of

the various SBG species in this type of infection and their treatment.
The Streptococcus bovis group (SBG) constitutes a group of Over the course of 27 years, we followed the infections caused
bacteria that have been associated with infections in animals and by SBG, which enabled us to study OAIs in an extensive cohort of
humans. In humans, SBG has been associated with septicemia, patients. We have also reviewed the literature to jointly analyze
endocarditis (IE), meningitis, urinary tract infections, biliary infec- the characteristics of these patients.
tions, and osteoarticular infections [1–5], the latter of which have
included septic arthritis, both native and prosthetic, spondylodiscitis,
and osteomyelitis [6–9]. Although SBG alone causes a small propor-
Material and methods
tion of cases of streptococcal arthritis and spondylodiscitis [10–13],
in IE caused by SBG, osteoarticular infection (OAI) is a relatively
Study location
common complication [2,14–18]. However, the spectrum of OAIs
Our center, the Lucus Augusti Hospital, is a University Hospital,
n
Corresponding author. E-mail address: [email protected] (R. Rabuñal) with 690 beds and approximately 20,000 admissions yearly of
E-mail address: [email protected] (R. Rabuñal). adult patients. The center provides care to a predominantly rural

http://dx.doi.org/10.1016/j.semarthrit.2016.02.001
0049-0172/& 2016 Elsevier Inc. All rights reserved.
2 M.J. García-País et al. / Seminars in Arthritis and Rheumatism ] (2016) ]]]–]]]

area of 230,000 inhabitants, with an advanced average age, and is and other concomitant infections, location, diagnostic methods,
the reference center for 2 regional hospitals that provide health- S. bovis biotypes or subspecies, type of malignant intestinal lesion,
care to an area of 118,000 inhabitants. comorbidities, and treatment and outcome. When the extracted
information was incomplete, we included in the denominator of
Study design the corresponding variable only those patients for whom the
required data were extracted.
Since 1988, we have an ongoing prospective study of all
episodes of SBG bacteremia, as described in previous articles Statistical analysis
[19–21]. Among these patients we selected those who had OAI
and retrospectively reviewed their medical records and imaging All data were stored in a database for analysis. SPSS statistics
tests. We also retrospectively reviewed all joint fluid and bone 17.0 (SPSS Inc.) was used for the statistical data analysis. The
samples in which SBG was isolated. All patients were monitored descriptive analysis included the mean and standard deviation for
until June 30, 2015 or until their death. quantitative variables and absolute and relative frequencies (per-
centages) for qualitative variables. Categorical variables were
Definitions compared using Pearson’s chi-squared test or Fischer’s exact test,
as appropriate. Quantitative variables were compared using either
A diagnosis of osteomyelitis was reached based on the presence Student’s t test (for normal variables) or Mann–Whitney’s U test.
of clinical picture (pain often accompanied by localized tenderness
in vertebral osteomyelitis; inflammatory signs and/or prolonged
sinus drainage in nonvertebral osteomyelitis) and positive blood Results
cultures and/or bone aspirate or biopsy and compatible CT or MRI
findings. Characteristics of our series
A diagnosis of arthritis was reached based on the presence of
clinical picture (inflamed joint with pain or limited range of Of a total of 229 cases of bacteremia caused by SBG, 20 showed
motion) and positive blood cultures and/or joint aspirate. osteoarticular involvement (SBG in synovial fluid was also isolated
Clinically significant bacteremia and IE were defined according in 2 of these 20 cases). Likewise, SBG was isolated in a bone biopsy
to a previous report [19]. We performed a colonoscopy on all in another case. A total of 21 osteoarticular infections were
patients with SBG bacteremia, except when it was contraindicated diagnosed (Table 1)—16 cases of spondylodiscitis, 1 case of osteo-
by their clinical situation or their disease prognosis. This study is myelitis, and 4 cases of septic arthritis (1 with associated spondy-
part of a series of previous studies in which we analyzed the lodiscitis). They accounted for 13.6% of spondylodiscitis and 2% of
relationship between the various SBG species and colorectal neo- septic arthritis in our center. Overall, 71% of the cases were
plasia (CRN) [21–23]. In those previous studies, we described the diagnosed in the past 10 years. The association with IE and CRN
methods used for the colonic examination. CRN was defined was 86% and 76%, respectively. S. gallolyticus subsp. gallolyticus
according to a previous report [21]. (S. gallolyticus) was the etiology in 18 cases (86%). The differences
found between these 20 patients with bacteremia and the 209
Microbiological study patients with bacteremia by SBG without OAI are listed in Table 2.
Except for 1 patient (with epidural abscess), all patients under-
Blood cultures were processed using the Bactec system (Bec- went between 4 and 6 weeks of antimicrobial therapy. Except for
ton-Dickinson Diagnostic Instrument System, Sparks, MD). Isolates 1 patient who died suddenly at 4 weeks, all patients healed
were stored in DifcoTM skim milk (Becton-Dickinson) at  701C. without relapses or osteoarticular sequelae (mean follow-up of
Phenotypic identification was performed with the API 20 Strep 49 months, range: 9–128).
system (BioMérieux, Marcy l’Etoile, France) and the Gram-positive
identification card of the Vitek 2 system (bioMérieux, Marcy
l’Etoile, France). Additional confirmation tests were performed Literature review
using conventional methods [24]. The analysis of the complete
rRNA gene sequence [3] and the polymorphism of manganese- We collected 62 cases (Table 3), 42 of which were osteomyelitis
dependent superoxide dismutase gene (sodA) [25] were used for (41 vertebral) and 19 of which were septic arthritis (1 of them with
molecular identification. The sequences obtained were compared associated spondylodiscitis).
with those of the corresponding genes available in GenBank by
using Blast sequence software (http://www.ncbi.nlm.nih.gov/). We therefore analyzed 83 cases–59 of osteomyelitis, 22 of
septic arthritis, and 2 with both types of infection.
Literature review

Demographic data and clinical presentation

To identify additional cases of OAI complicating SBG infection,
we performed a MEDLINE search of articles published from
The mean age of the 83 patients was 66.9 years (range: 14–91
January 1, 1980 to June 30, 2015. The search terms used were S.
years), 61 (73.4%) patients were older than 60 years, and 79.2%
bovis, Streptococcus gallolyticus, Streptococcus pasteurianus, and
were men.
Streptococcus infantarius and “endocarditis, bacterial” and “osteo-
myelitis”, “spondylitis” and “arthritis, infectious”. Secondary refer-
ences in the retrieved articles were also reviewed. Only English, Osteomyelitis
French, and Spanish reports were considered. Of the 70 patients The locations for the 61 cases were lumbosacral [28], cervical
described, 8 were excluded due to lack of information [15,26,27]. [9], dorsal [8], and iliac [1]. The remainder had more than 1
In all, 2 patients in our series were previously published [28,29]. affected vertebral segment. The mean symptom duration before
Ultimately, we included 62 cases (4 series with 18 cases, and 44 diagnosis was 61.9 days (range: 3–180 days). Back or neck pain was
case reports) [2,6–9,30–72]. All cases reports were screened for the reported in 59 cases, and pain was the presenting symptom of the
following information: age, sex, type of osteoarticular infection disease in 73.2% of the patients. A total of 74.5% of the patients had
Table 1
Characteristics of the 21 cases of osteoarticular infection caused by Streptococcus bovis group in the Lucus Augusti hospital

Case number Age/sex Osteoarticular infection/other Endocarditisa Comorbidities Colonoscopy Microbiology Treatment Duration
infections

1 55/M Spondylodiscitis C3  4 M–Ao Adenoma S. gallolyticus Ampicillin 6 weeks

2 71/M Spondylodiscitis L3  4 M–Ao Normal S. gallolyticus Cefotaxime 8 weeks
Epidural and paravertebral abscess
3 69/M Spondylodiscitis L2  3 Ao (prosthetic) Adenoma S. gallolyticus Ceftriaxone þ gentamicin 6 þ 2 weeks

M.J. García-País et al. / Seminars in Arthritis and Rheumatism ] (2016) ]]]–]]]

4 71/M Spondylodiscitis D7  8, D10 11 Ao Diabetes mellitus Advanced adenoma S. gallolyticus Ceftriaxone 6 weeks
Paravertebral abscess
5 75/M Spondylodiscitis D8  9 Ao (prosthetic) Advanced adenoma S. gallolyticus Ceftriaxone þ gentamicin 6 þ 2 weeks
6 71/M Spondylodiscitis D10  11 M Advanced adenoma S. gallolyticus Ceftriaxone 4 weeks
Paravertebral abscess Levofloxacin 2 weeks
7 64/M Spondylodiscitis L5–S1 Ao Normal S. gallolyticus Ceftriaxone 4 weeks
8 78/M Spondylodiscitis C4  6 Ao (prosthetic) Carcinoma S. gallolyticus Ceftriaxone þ gentamicin 6 þ 2 weeks
Paravertebral abscess
9 72/M Spondylodiscitis C3  4 M–Ao Adenoma S. gallolyticus Ceftriaxone 4 weeks
10 67/M Spondylodiscitis L2  3 Ao Multiple myeloma Adenoma S. gallolyticus Ceftriaxone 4 weeks
Levofloxacin 2 weeks
11 89/F Spondylodiscitis L2  3 Ao (prosthetic) Diabetes mellitus Adenoma S. pasteurianus Ceftriaxone þ gentamicin 6 þ 2 weeks
Paravertebral abscess
12 65/M Spondylodiscitis L3  5 Ao Diabetes mellitus Adenoma S. gallolyticus Ceftriaxone 4 weeks
Paravertebral abscess Levofloxacin 2 weeks
13 85/M Spondylodiscitis L3  4 M Prostate cancer Not done S. gallolyticus Ceftriaxone 6 weeks
14 60/M Spondylodiscitis L5–S1 M–Ao Advanced adenoma S. gallolyticus Ceftriaxone 4 weeks
15 59/M Spondylodiscitis L3  5 M–Ao Bladder cancer Advanced adenoma S. gallolyticus Ceftriaxone þ gentamicin 2 þ 2 weeks
Levofloxacin 2 weeks
16 67/M Spondylodiscitis C3  4 M–T Diabetes mellitus Advanced adenoma S. gallolyticus Ceftriaxone þ gentamicin 4 þ 1 weeks
Bladder cancer
17 70/M Spondylodiscitis C5  6 Ao Adenoma S. gallolyticus Ceftriaxone 4 weeks
Paravertebral abscess
Knee arthritis
18 91/M Sternoclavicular arthritis M–Ao Carcinoma S. gallolyticus Ceftriaxone þ gentamicin 2 þ 2 weeks
Levofloxacin 2 weeks
19 58/M Knee arthritis No Cirrhosis Carcinoma S. gallolyticus Ceftriaxone 3 weeks
Surgical drainage
20 62/M Pubic symphysitis No Prostate cancer Normal S. pasteurianus Ampicillin 2 weeks
Urinary tract infection E. faecalis Amoxycillin-clavulanic 2 weeks
21 43/F Sacral osteomyelitis No Oligophrenia Not done S. infantarius Amoxycillin-clavulanic 6 weeks
Pressure ulcer S. anginosus
P. mirabilis

a
Endocarditis. Ao, aortic; M, mitral; T, tricuspid.

3
4 M.J. García-País et al. / Seminars in Arthritis and Rheumatism ] (2016) ]]]–]]]

Table 2 was not removed, all were diagnosed during the infection. Only
Differences between osteoarticular bacteremia and non-osteoarticular bacteremia 4 of the patients presented suggestive symptoms or signs (rectal
caused by Streptococcus bovis group in the Lucus Augusti hospital
bleeding in 2, constipation in 1, and a palpated rectal mass in the
Osteoarticular Non-osteoarticular P other). Overall, 67% of the patients with OAI and IE had CRN
bacteremia bacteremia compared with 38.2% of the patients with OAI without IE (P ¼
0.001). In all 76% of the patients with biotype I had CRN compared
No. of cases 20 209 with 36.9% of those with biotype II or not biotyped (P ¼ 0.01).
Sex (male) 19 (95%) 152 (72.3%) 0.05
Age 69.9 69.8
Endocarditis 18 (90%) 92 (44%) o 0.001 Microbiology

Underlying illnesses The bacteriologic diagnosis was established through blood

Diabetes mellitus 4 (20%) 49 (23.4%) 0.94
cultures alone in 52 cases, through biopsy specimens or articular
Cirrhosis 1 (5%) 10 (4.7%) 0.61
Cancer 5 (25%) 45 (21.5%) 0.71 fluid in 18 cases, and through blood cultures plus biopsy speci-
mens or articular fluid in 13 cases. Joint fluid cell counts were
Colorectal neoplasia 16 (80%) 92 (44%) 0.004 specified for 10 patients, with the leukocyte count ranging
S. gallolyticus 18 (90%) 117 (56%) 0.006 between 3750 and 77,000 cells/mm3 (mean: 41,314). The joint
S. pasteurianus/ 2 (10%) 91 (44%)
S. infantarius
fluid Gram stain was positive in 4 of 11 cases. The yield of the
Polymicrobial 1 (5%) 46 (22%) 0.13 blood cultures was 89% (65 of 73 performed) and was greater for
Evolution (death) 1 (5%) 30 (14.3%) 0.4 the patients with IE [97.9% (48/49)] than in those without IE [70.8%
(17/24; P ¼ 0.001)]. The diagnostic yield was also greater for the
patients with osteomyelitis [93% (54/58)] than in the patients with
arthritis [73.3% (11/15; P ¼ 0.08)]. The yield of bone biopsies (14/
fever. Paraspinal or epidural extension was observed in 16 patients
15) and joint fluid (13/14) was also very high. The other cultures
and 5 patients had neurological involvement.
that resulted positive were urine (2 cases) and the vitreous humor,
Of the 59 patients with spondylodiscitis, 46 had associated IE.
cerebrospinal liquid, ascites fluid, splenic abscess, buttock abscess,
The differences found between the cases of spondylodiscitis with
and skin ulcer (1 case each). Only 3 patients presented polymicro-
and without IE were a longer symptom duration: 64.2 vs. 26.4 days
bial infection. Of the 45 cases in which the species or SBG biotype
(P ¼ 0.014), higher rate of positive blood cultures: 100 (46/46) vs.
was identified, 37 were S. gallolyticus, 5 were S. gallolyticus subesp
69.2% (9/13; P ¼ 0.001), and more colorectal neoplasm: 67.3 (31/
pasteurianus, 1 was S. infantarius, and 2 was biotype II. Of the
46) vs. 30.7% (4/13; P ¼ 0.04) in the former.
patients with spondylodiscitis for whom species identification was
conducted, 28 of 29 cases were S. gallolyticus (96.5%), while for the
Arthritis cases of arthritis, 8 of 14 were caused by this species (57.1%; P o
The locations for the 24 cases were knee (12 cases), hip [5], 0.001). For the patients with IE, 34 of the 35 cases (97%) in which
shoulder [5], sternoclavicular [1], and pubic symphysis [1]. Only 1 the biotype was identified involved S. gallolyticus compared with
patient presented polyarthritis, and 2 cases were associated with 9 of 16 (56.2%; P o 0.001) of the cases without IE.
spondylodiscitis. In all, 11 cases were associated with prostheses
(47.8%), which were implanted 4 months–18 years earlier (median, Treatment and outcome
23 months). In 23 of the 24 cases, the pain was the first symptom
of the disease, and 58.3% of the cases presented fever. Of the 59 patients with osteomyelitis for whom the treatment
employed was specified, the most common was a beta-lactam (56
Comorbidities and predisposing factors cases), accompanied by an aminoglycoside (23 cases) and/or a
quinolone (8 cases). The treatment duration in the 53 cases in
In 31 (37.3%) patients, 1 or more following immunosuppressive which it was specified varied between 2 and 35 weeks, and in 25
diseases were found: diabetes mellitus (18%), malignancies (12%), cases the parenteral treatment was completed orally. Short treat-
and cirrhosis (10.8%) were the most frequent. In 4 patients, the ments ( r6 weeks) were employed for 33 patients, with 1 recur-
infection was related to manipulation [spinal injection (2 patients), rence. Long treatments ( 46 weeks) were employed for 20
intra-articular injection (1), and prostate biopsy (1)]. patients with no recurrence. Surgical drainage was performed in
5 cases (1 case of short treatment and 4 cases of long treatment).
Concomitant infectious processes and presumed sources of infection The patients with arthritis were treated with beta-lactam as the
main treatment in 14 cases. The treatment duration varied
The main associated infections were as follows: IE (49 cases), between 3 and 12 weeks, with 2 patients undergoing suppressive
splenic abscess (3 cases), meningitis (2 cases), and hepatic abscess, treatment indefinitely. All but 1 patient with peripheral arthritis
spontaneous bacterial peritonitis, urinary tract infection, endoph- underwent some type of drainage, generally surgical. For the
thalmitis, pressure ulcer, and myositis (1 case each). IE was more patients with prosthesis, the implant was removed in 7 cases,
common among the patients with spondylodiscitis than among another prosthesis was implanted in 6 cases (5 two-stage oper-
the patients with arthritis (78.9% vs. 13.6%; P ¼ 0.001). The IE was ations and 1 one-stage operation), and arthrodesis was performed
bivalvular in an appreciable percentage—32.6% (16/49), and in only in another case. In 4 cases, drainage was performed with retention
10/41 (24%) there was previous predisposing heart disease. The of the implant.
SBG OAI was healthcare associated in 5 cases (6%). Overall, 6 patients died (7.2%) but none from osteoarticular
A hematogenous spread was the presumed source of infection, complications. In all, 4 of these patients (with endocarditis) died
except in 6 cases—4 of them after manipulation, 1 due to sacral from heart failure [2], cerebral embolism [1], and other patient
osteomyelitis secondary to a pressure ulcer and 1 due to prosthetic with ischemic heart disease died suddenly at the end of the
arthritis, which was a late postsurgical infection. The colon was antimicrobial therapy (Table 3 [2,30], and Table 1, case 11).
examined through colonoscopy in 64 of the 83 patients, with 46 Another patient (with cirrhosis) died of septic shock (Table 3)
tumors detected—30 adenomas (16 of them advanced) and 16 [58] other died of cancer metastasis (Table 3) [38]. There was only
carcinomas. Except for 1 case that was diagnosed a year earlier and 1 reported recurrence in a patient with spondylodiscitis (Table 3)
Table 3
Characteristics of the 62 cases of osteoarticular infection caused by Streptococcus bovis group of the review of the literature

References Age/sex Osteoarticular infection/other Endocarditisa Comorbidities and Colonoscopy Microbiology Treatment Duration
infections predisposing factors

Spondylodiscitis with endocarditis

[2] 59/M Spondylodiscitis M–Ao Not done S. gallolyticus Ampicillin þ gentamicin 4 þ 2 weeks
Quinolone 6 weeks
[2] 57/F Spondylodiscitis M–Ao Advanced adenoma S. gallolyticus Ampicillin þ gentamicin 4 þ 2 weeks
Quinolone 6 weeks
[2] 64/M Spondylodiscitis M–Ao Adenoma S. gallolyticus Ampicillin þ gentamicin 4 þ 2 weeks
Quinolone 6 weeks
[2] 55/M Spondylodiscitis M–Ao Cirrhosis Normal S. gallolyticus Ampicillin þ gentamicin 4 þ 2 weeks
Quinolone 6 weeks
[2] 47/M Spondylodiscitis Ao–T Advanced adenoma S. gallolyticus Ampicillin þ gentamicin 4 þ 2 weeks
Quinolone 6 weeks

M.J. García-País et al. / Seminars in Arthritis and Rheumatism ] (2016) ]]]–]]]

[2] 74/F Spondylodiscitis M–Ao Adenoma S. gallolyticus Ampicillin þ gentamicin 4 þ 2 weeks
Quinolone 6 weeks
[2] 58/M Spondylodiscitis Ao Cirrhosis Carcinoma S. gallolyticus Ampicillin þ gentamicin 4 þ 2 weeks
Spleen abscess Quinolone 6 weeks
[30] 72/M Spondylodiscitis L3  4 M–Ao Adenoma S. bovis Penicillin þ gentamicin 6 þ 2 weeks
Amoxicillin 6 weeks
[30] 79/M Spondylodiscitis D9  12 Ao Advanced adenoma S. bovis Penicillin 6 weeks
Amoxicillin 6 weeks
[30] 67/M Spondylodiscitis C4 5 M–Ao Not done S. bovis Penicillin þ gentamicin 3 days
[30] 72/M Spondylodiscitis L3  4 Ao Metastatic cancer Not done S. bovis Ampicillin þ gentamicin 4 weeks
[30] 49/M Spondylodiscitis D12–L1 Ao Not done S. bovis Penicillin þ aminoglycoside 7 weeks
Amoxicillin 28 weeks
[30] 70/M Spondylodiscitis L5–S1 Ao Not done S. bovis Penicillin þ gentamicin 12 weeks
[31] 84/F Spondylodiscitis D–L Ao Leukemia Advanced adenoma S. gallolyticus Antibiotics ?
[33] 81/M Spondylodiscitis D12–L1 Ao Carcinoma S. bovis Ampicillin þ gentamicin 6 weeks
Paraspinal and epidural abscess
[35] 78/F Spondylodiscitis L2  3 Ao Not done S. bovis Ceftriaxone þ gentamicin 6 þ 2 weeks
Epidural abscess
[39] 71/F Spondylodiscitis L4  5 Septal Normal S. bovis Imipenem þ streptomycin 2 weeks
Vancomycin þ streptomycin 2 weeks
[40] 72/M Spondylodiscitis C2, C4  6, Ao Cirrhosis Normal S. bovis Cefotaxime þ metronidazole 1 weeks
D8  10, L4  5
Liver abscess Amoxycillin-clavulanic 24 weeks
[42] 57/F Spondylodiscitis L2  3 Ao Normal S. bovis Penicillin þ streptomycin 12 þ 2 weeks
[43] 68/M Spondylodiscitis D2, D10  11 Ao Carcinoma S. gallolyticus Penicillin þ gentamicin 2 weeks
Spleen abscess Amoxicillin þ clindamicin 4 weeks
[44] 79/M Spondylodiscitis D9  10 M Advanced adenoma S. bovis Penicillin þ gentamicin 6 þ 1 weeks
Paraspinal abscess Amoxicillin 6 weeks
[45] 53/M Spondylodiscitis D9  10 Ao Not done S. bovis Penicillin þ aminoglycoside ?
[49] 84/F Spondylodiscitis D12–L1 Ao Myelodisplastic syndrome Advanced adenoma S. gallolyticus Penicillin þ gentamicin 6 þ 2 weeks
Ciprofloxacin þ rifampicin 4 weeks
[50] 65/F Spondylodiscitis L3  5 M Carcinoma S. bovis Ceftizoxime 6 weeks
[51] 77/M Spondylodiscitis L2  3 Ao Adenoma S. bovis Penicillin þ gentamicin 6 weeks
[52] 61/M Spondylodiscitis L3  4 Ao Carcinoma S. bovis Beta-lactamic ?
[53] 72/M Spondylodiscitis C5 6 M Diabetes mellitus Carcinoma S. bovis Penicillin þ gentamicin 4 weeks þ 6 days
Meningitis
[54] 52/M Spondylodiscitis L4  5 M–Ao Not done S. bovis Penicillin þ streptomycin 4 weeks
Amoxicillin 8 weeks
[56] 64/M Spondylodiscitis L4  5 M Carcinoma S. gallolyticus Penicillin 12 weeks
Paraspinal and epidural abscess Amoxicillin 8 weeks
Surgery

5
Spondylodiscitis without endocarditis

6
[8] 79/M Spondylodiscitis C5 6 No Advanced adenoma S. bovis Cefazoline 7 weeks
Epidural abscess Surgery
[31] 73/F Spondylodiscitis D–L No Diabetes mellitus Advanced adenoma S. gallolyticus Antibiotics ?
[32] 79/M Spondylodiscitis L2  3 No Normal S. bovis Penicillin 6 weeks
Surgery
[34] 57/F Spondylodiscitis C3 4 No Spinal injection Not done S. bovis Vancomycin 10 weeks
Epidural abscess Surgery
[36] 64/M Spondylodiscitis C6 7, D9  10 No Advanced adenoma S. bovis Penicillin 6 weeks
[37] 41/F Spondylodiscitis L4  5 No Epidural anesthesia Not done S. bovis Vancomycin 6 weeks
[38] 78/F Spondylodiscitis L1  2 No Diabetes mellitus Carcinoma S. bovis Penicillin 6 weeks
Epidural abscess
Meningitis
[41] 77/M Spondylodiscitis L1  2 No Not done S. gallolyticus Penicillin 24 weeks
[46] 24/F Spondylodiscitis D12–L1 No Diabetes mellitus Not done S. bovis Piperacillin 4 weeks
Paraspinal abscess Lung transplantation Amoxicillin 4 weeks
[47] 70/M Spondylodiscitis L4  5 No Cirrhosis Normal S. gallolyticus Vancomycin þ Rifampicin ?
[48] 76/M Spondylodiscitis No Liver cancer Not done S. bovis Meropenem 2 weeks

M.J. García-País et al. / Seminars in Arthritis and Rheumatism ] (2016) ]]]–]]]

Endophthalmitis
[55] 72/M Spondylodiscitis D7  8 No Diabetes mellitus Normal S. bovis Penicillin 6 weeks
Epidural and paravertebral abscess Amoxicillin 6 weeks

Spondylodiscitis with arthritis

[57] 47/M Spondylodiscitis L4  5 No Normal S. bovis Penicillin 6 weeks
Shoulder arthritis Surgery

Osteomyelits
[9] 14/M Ileum osteomyelitis No Normal S. bovis Penicillin 3 weeks
Buttock abscess Amoxicillin 3 weeks
Surgery

Native arthritis
[6] 70/M Knee arthritis No Normal S. bovis II Vancomycin þ gentamicin 2 weeks
Penicillin 10 days
Surgery
[31] 50/M Hip arthritis No Diabetes mellitus Adenoma S. gallolyticus Antibiotics ?
[58] 55/M Knee arthritis No Cirrhosis. HIV.Splenectomy Not done S. pasteurianus Vancomycin þ moxifloxacin 1 day
Spontaneous bacterial peritonitis þ gentamicin þ
[59] 69/M Knee arthritis No Cirrhosis Normal S. bovis Ceftriaxone 24 days
Intra-articular injection Arthroscopy
[60] 61/M Shoulder arthritis No Diabetes mellitus Diverticula S. gallolyticus Antibiotics ?
Alcoholism Surgery
Cirrhosis
[61] 67/M Shoulder arthritis M Diabetes mellitus Advanced adenoma S. bovis Penicillin þ gentamicin 4 þ 2 weeks
Splenic abscess
[62] 73/M Shoulder arthritis No Cirrhosis Not done S. bovis Penicillin 5 weeks
Surgery
[72] 84/M Shoulder arthritis No Normal S. bovis II Penicillin þ metronidazol 4 weeks
Veillonella dispar Arthroscopy

Prosthetic arthritis
[7] 51/M Prosthetic hip arthritis No Diabetes mellitus Adenoma S. gallolyticus Antibiotics ?
Surgery
[63] 76/M Prosthetic knee arthritis No Carcinoma S. bovis Ampicillin 6 weeks
Surgery
[64] 76/M Prosthetic knee arthritis No Multiple myeloma Diverticula S. bovis Penicillin 6 weeks
Steroids Amoxicillin LLSTb
Surgery
[65] 72/M Prosthetic hip arthritis No Carcinoma S. bovis Vancomycin 12 weeks
Surgery
 M.J. García-País et al. / Seminars in Arthritis and Rheumatism ] (2016) ]]]–]]] 7

[56], which required a new antimicrobial cycle and surgical

18 days þ 3 days
drainage. None of the cases reported permanent osteoarticular or
neurological sequelae.
12 weeks

12 weeks

6 weeks
4 weeks
LLSTb

Discussion
?

?
Amoxycillin-clavulanic þ Clindamicin

To our knowledge, this is the largest series of OAI by SBG

reported in the literature. This series also includes some types of
OAI caused by SBG that have not previously been reported, such as
sternoclavicular arthritis, sacral osteomyelitis, and pubic symphy-
Vancomycin þ rifampicin

sitis. This study also provides a detailed description of the various

associations of the different species of S. bovis with OAI and CRN.
Our experience and literature review suggest that OAI is a
relatively common complication of SBG endocarditis, with an
Levofloxacin
Vancomycin

Arthroscopy

Arthroscopy
Amoxicillin

Antibiotics

Cefditoren

incidence that varies between 9% and 23% [2,14–18]. When SBG

Penicillin
Surgery

Surgery

Surgery

Surgery

Surgery

bacteremic infections are considered, the rate of OAIs range

between 3.4% and 6.4% [4,73]. In our center, OAIs caused by SBG
represent approximately 4.6 cases/100,000 admissions, and their
incidence appears to be increasing, as has already been reported
S. pasteurianus

S. pasteurianus

for other streptococcal OAIs [12,13]. Factors such as the aging of the
S. gallolyticus

S. gallolyticus

population and the increasingly routine use of MRI could be

S. bovis

S. bovis

S. bovis

contributing to this incidence.

Signs and symptoms of SBG OAI do not appear to differ from
those of previous reports of OAI caused by other micro-organisms.
However, there are 2 characteristic facts of OAIs associated with
Nonspecific ulcers

SBG—a high association with spondylodiscitis and IE. This associ-

ation contrasts with S. aureus, S. pneumoniae, and other pyogenic
Carcinoma

Carcinoma

Carcinoma

streptococci, which are often associated with arthritis and are

Adenomas

Not done

Normal

rarely associated with IE [11,12,74]. This association with spondy-

lodiscitis is also greater than that of streptococci from the viridans
group [2,16–18]. In these studies, however, the patients with SBG
infection had a significantly older mean age, and this factor is
associated with spondylodiscitis [75,76].
Musculoskeletal symptoms are common in IE, and back pain is
a frequent manifestation, especially in IE caused by SBG, with an
Diabetes mellitus

incidence of 15–29% [26,77]. Vertebral osteomyelitis, however, is

an uncommon complication, ranging between 2% and 6% [26,77].
This percentage was higher in our cases. Of the 110 cases of
endocarditis caused by SBG in our hospital, 19 patients had back
pain as the prominent symptom (17.2%), and 17 of them had
spondylodiscitis (15.4%). These differences with earlier studies
[26,27,77] could be due to the fact that MRI was performed early
in almost all of our cases. MRI is the most sensitive diagnostic
method to date, even in very early stages of the disorder [11,75,76].
No

No

No

No

No

No
Ao

Joint involvement in patients with SBG septic arthritis was

similar to that in adults with septic arthritis caused by other
organisms. Septic arthritis is an uncommon condition and affects
the large joints; knee involvement was the most common location.
Unlike other bacteria [78], polyarticular septic arthritis is excep-
Prosthetic knee arthritis

Prosthetic knee arthritis

Prosthetic knee arthritis

Prosthetic knee arthritis

Prosthetic knee arthritis

tional [58]. A striking fact of this review is that of the 23 cases of

Endocarditis. Ao, aortic; M, Mitral; T, tricuspid.
Prosthetic hip arthritis

Prosthetic hip arthritis

arthritis, 11 (47.8%) involved prostheses. In other series with

streptococcal arthritis, the percentage of prosthetic arthritis was
much lower [10,13]. Although publication bias cannot be ruled out,
LLST, lifelong suppressive therapy.

the affinity of SBG for forming biofilms [79] could be one of the
causes of this greater association. Unlike spondylodiscitis, most
cases of arthritis caused by SBG are not associated with IE [6,7,57–
72], and its association with biotype I was not so significant.
Diabetes mellitus, cirrhosis, and cancer were the most common
comorbidities. It is worth noting that 62.7% of the patients had no
78/M

75/M

73/M
76/M
70/?

79/F
73/F

underlying immunosuppressive disease, and most of the cases

with IE had no previously known valvular heart disease.
In the cases in which the species was identified, the species was
mostly S. gallolyticus (82.2%), both in the cases of arthritis and
[65]

[66]

[68]

[69]
[67]

[70]

[71]

especially in the cases of spondylodiscitis. In those cases in which

b
a

the species was not identified, we assume that an appreciable

8 M.J. García-País et al. / Seminars in Arthritis and Rheumatism ] (2016) ]]]–]]]

percentage of cases were probably also caused by S. gallolyticus, colonoscopy, even in the absence of symptoms. The treatment in
given the high association in these cases with IE (50%) and CRN most of the cases associated with IE should probably be no
(42%), raising this percentage to 64% if we only included the different from that of IE without OAI. The prognosis is good,
patients who underwent colonoscopy. It is know that S. gallolyticus without permanent sequelae or mortality attributable to OAI.
is associated with IE and CRN [1,2,19,21,79–82]. S. pasteurianus and
S. infantarius are mainly associated with abdominal and urinary
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