Anaerobic spondylodiscitis: case series and systematic review.

Background: Bacterial spondylodiscitis is rarely caused by anaerobic organisms. We describe two patients with lumbar vertebral osteomyelitis and discitis caused by anaerobic bacteria, including an unusual occurrence after an endodontic procedure, and review the salient clinical features and outcomes of 31 previously reported cases.

Methods: Case reports and review of the literature.

Results: Median age at presentation was 65 years, with a male-to-female ratio of 2:1. The most common presenting symptoms were back pain, fever, and neurologic deficits. The lumbar spine was most frequently involved (43%); an equal number of cases involved contiguous extension or hematogenous spread. Causative anaerobes were recovered from disk space or vertebrae (13), blood (4), and/or soft tissue abscess and included Bacteroides species (12), Propionibacterium acnes (7), Peptococcus species (4), Peptostreptococcus species and Clostridium species (3 each), Corynebacterium diphtheroides and Fusobacterium species (2 each), and unspecified anaerobes (3).

Conclusions: Apart from specific antibiotic selection, medical treatment and outcomes for anaerobic spondylodiscitis are similar to those for aerobic vertebral disk infection.

Key Words: anaerobic infection, infectious discitis, spondylodiscitis, vertebral osteomyelitis

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Infections of the vertebral bodies and intervening disk space are typically caused by aerobic bacteria, Mycobacterium tuberculosis, and Candida species. Bacterial spondylodiscitis is rarely caused by an anaerobic organism. (1-5) We report two cases of lumbar vertebral osteomyelitis and discitis caused by anaerobic bacteria, including an unusual occurrence after an endodontic procedure, and review the salient clinical, microbiologic, and radiographic features and outcomes for this infectious disease syndrome.

Materials and Methods

We conducted a MEDLINE search from 1906 through December 2002 and a bibliographic search of published articles to identify clearly documented cases of vertebral osteomyelitis and/or discitis (spondylodiscitis) caused by nonactinomycotic, anaerobic bacteria. To classify cases as definitive anaerobic spondylodiscitis, we required radiographic, laboratory, or clinical evidence of osteomyelitis or discitis and a documented infection based on the results of culture of a vertebral or disk biopsy specimen or a surrogate body site such as blood or soft tissue or visceral abscess specimen. We reviewed all available data, including clinical presentation, laboratory results, therapeutic interventions, and outcome.

Case Reports

Patient 1

A previously healthy 70-year-old male presented to the hospital for evaluation of severe low back pain. About 3 months previously, he had undergone an endodontic procedure and shortly thereafter began having pain in his oral cavity with radiation to his right pinna. At that same time, he noted lumbar back pain without radiation, which was exacerbated by position change and heat, and not associated with any sensory or motor symptoms. The patient's pain was initially treated with nonsteroidal anti-inflammatory drugs, and muscle relaxants were added because of lack of symptomatic response. On physical examination, the patient was clinically stable without fever, and there was tenderness to palpation over both posterior iliac spines, with decreased range of motion on lateral spine movement. There was also tenderness to deep palpation paraspinally at the L3 level. Gait was normal, and straight leg raises and internal and external hip rotation elicited no pain.

Laboratory investigations revealed an erythrocyte sedimentation rate of 62 mm/h and a normal complete blood count. Magnetic resonance imaging (MRI) of the back demonstrated erosions and contrast enhancement of the [L.sub.2-3] vertebral bodies extending into the intervening disk space consistent with infectious discitis and osteomyelitis, with paraspinous extension and involvement of the right psoas muscle (Figs. 1 and 2). Multiple blood cultures were negative, a transthoracic echocardiogram showed no vegetation or valvular abnormalities, and aspiration of the [L.sub.2-3] disk space yielded no organisms on Gram stain or culture. A second aspiration was performed 4 days later and revealed Gram-positive cocci on Gram stain, and the patient was empirically begun on intravenous vancomycin and ceftriaxone. The organisms were subsequently identified as Peptostreptococcus with resistance to penicillin G but susceptibility to ceftriaxone. The infection was eradicated with a 6-week course of intravenous ceftriaxone.

Patient 2

An 86-year-old female underwent vertebroplasty of the third lumbar vertebral body because of an osteoporotic compression fracture and chronic low back pain. Immediately after surgery she had noticeable relief of pain, but several days after hospital discharge she had recurrence of severe low back pain, unaccompanied by fever, chills, or night sweats. MRI scanning revealed hypodense [T.sub.1] signal in the [L.sub.3] vertebral body related to her recent surgery. An abnormal fluid collection was noted within the [L.sub.2-3] disk space, tracking into the paraspinal soft tissues bilaterally and extending into the psoas muscle on the right side. A hyperintense [T.sub.2] signal that was suspicious for infection was present within the inferior aspect of the [L.sub.2] vertebral body. The patient underwent a computed tomography-guided, closed needle aspiration of the [L.sub.2-3] disk space and adjacent paraspinal soft tissue, with removal of 2 mL of bloody fluid. Gram stains of these aspirates showed 3+ white blood cells (WBCs), but all cultures were negative. A complete blood cell count and differential was unremarkable, Westergren erythrocyte sedimentation rate was 65 mm/h, and one of two sets of blood cultures grew Staphylococcus saccharolyticus. Her pain persisted, accompanied by a low-grade fever, white blood cell count of 11,500/[mm.sup.3] with 89% neutrophils, and erythrocyte sedimentation rate of 74 mm/h. Five days later she underwent repeat needle aspiration of the disk space and surrounding soft tissue. Three milliliters of yellowish, turbid fluid was obtained, and Gram stain revealed 4+ white blood cells without organisms. Cultures from both sites grew S saccharolyticus, as did two sets of blood cultures drawn 5 days after the original positive set. Transthoracic echocardiography was performed and disclosed no significant valvular abnormalities or vegetations. In light of the patient's age and frailty, it was decided not to surgically debride the vertebroplasty site, and she was treated with 4 weeks of intravenous penicillin G in-hospital and discharged without pain on amoxicillin, to be taken for an additional 6 months.

Results

Clinical and microbiologic data for all cases are shown in Table 1. (1,3,6-17) Search of the English literature revealed 15 relevant reports describing 33 patients (including our two cases) with anaerobic spondylodiscitis (with complete or incomplete clinical details). Median and mean ages at presentation were 65 years and 55 years (range, 3 to 86 years), respectively, with a male-to-female ratio of 2:1. The most common presenting symptoms reported were back pain (9), fever (8), and motor neurologic deficits (4). Where specified, sites of vertebral involvement included lumbar (9), coccyx (6), cervical (5), thoracic (1), and unspecified (14) regions. Where accurate assessment could be made, the route of development of infection included contiguous extension (13 cases) or hematogenous spread (14 cases). Where stated, pathogenetic microorganisms were recovered disk space or vertebrae (13), blood (4), and soft tissue abscess (2). One patient had an anaerobe isolated from both bone and blood cultures. Types of anaerobic bacteria isolated are shown in Table 2. Almost all treated patients received 4 weeks or more of specific antibiotic therapy, in most cases administered parenterally. Surgical debridement or drainage of osseous or soft tissue abscesses was performed in four patients.

Discussion

Vertebral osteomyelitis and discitis are usually caused by aerobic bacteria such as Staphylococcus aureus, coagulase-negative staphylococci, Enterobacteriaceae and other Gramnegative bacilli, [beta]-hemolytic streptococci, Mycobacterium tuberculosis, and Candida species. (1-4) Anaerobic infection of the bony spine and disk spaces is uncommon and appears to account for less than 3% of all spinal infections. (1-3, 17) In a review by Raff and Mello, (9) only four of 201 (2.0%) cases of anaerobic osteomyelitis (excluding osteomyelitis of the foot) involved the spine. Actinomyces israelii was the first anaerobe to be implicated as a cause of vertebral osteomyelitis (18) and is the most frequently cited cause of anaerobic infection of the spine. Our review of the literature revealed only 15 previous reports with 33 cases of vertebral body and/or disk infection caused by nonactinomycotic, anaerobic microorganisms (Table 1). (1,3,6-17) The most common pathogenetic organisms isolated included Bacteroides species, Propionibacterium acnes, and Peptococcus species. Our patient 1 represents only the third instance of anaerobic vertebral osteomyelitis caused by peptostreptococci. (1,3,12)

[FIGURE 1 OMITTED]

Like aerobic infection, anaerobic spondylodiscitis can follow contiguous extension from an adjacent soft tissue or intra-abdominal or pelvic focus of infection or hematogenous seeding from a distant primary site of infection, and this appears to occur in similar frequencies, although only four cases of bacteremia with the causative organism were documented. (14-16) Our patient 1 resulted from blood-borne dissemination of peptostreptococcal organisms from a primary oropharyngeal focus after endodontic manipulation; this is the only reported case of anaerobic spondylodiscitis resulting from a dental infection or procedure. In a study examining the occurrence of bacteremia secondary to endodontic procedures, samples from all 26 root canals were found to contain anaerobic bacteria, and 11 of 26 (45%) subjects had blood cultures positive for these same organisms. (19) Although microorganisms gaining access to the blood in this setting are usually cleared by the reticuloendothelial system, they may settle and multiply in various body sites and tissues including bones. (17,18)

[FIGURE 2 OMITTED]

The clinical presentation of anaerobic spondylodiscitis is similar to aerobic infection of these structures. Insidious back pain and signs of spinal cord compression are the most common presenting signs and symptoms; fever is seen in only about 40% of cases of anaerobic infection of the vertebrae or disk space. As for aerobic infection, the lumbar region (43%) was the most commonly involved site of vertebral body or disk involvement. A number of radiographic modalities may identify destructive changes and even gas formation consistent with vertebral body or disk space infection, including plain films, radionuclide bone scanning, Gallium scanning, tomography, CT, and MRI. Of these, MRI has the most diagnostic accuracy. (20)

Blood cultures, which are useful in establishing a definitive microbiologic diagnosis in 24 to 62% cases of aerobic vertebral osteomyelitis, (1,3,11,17) were positive in four (15%) cases of anaerobic spondylodiscitis reviewed here; bacteremia was seen in 0% and 29% of instances of contiguously and hematogenously spread infection, respectively. In cases of anaerobic osteomyelitis involving nonspine sites (accounting for 98% of all anaerobic bone infections and which are largely contiguous in development), blood cultures rarely yield anaerobic organisms. (9,10)

Conclusion

Appropriate management of anaerobic spondylodiscitis is generally associated with a prognosis similar to that for aerobic infection of the spine. Prolonged courses of parenteral or oral antibiotics are generally sufficient for improvement or cure. Relapse is uncommon, and surgical debridement or drainage of spinal or paraspinal abscesses are occasionally required to optimize outcome.

Table 1. Literature cases of nonactinomycotic, anaerobic vertebral
osteomyelitis

Author(s) (year)           Age (yr)    Underlying
[ref]                      sex         risk factors           Route (a)

Beigelman and Rantz        45/M        Neck abscess           C
  (1949) [5]
Ambrose (1966) [6]         70/F        NS (b)                 H
                            3/F        NS                     H
Felner and Dowel           NS          NS                     NS
  (1971) [7]
Newman and Mitchell        75/M        NS                     H
  (1975) [8]
Raff and Mello (1978) [9]  37/M        Abdominal gunshot      C
                                         wound
Lewis et al (1978) [10]    10 pts (c)  NS                     H (4)
                                                              C (6)
Sapico and Montgomeric     18/M        Abdominal gunshot      C
  (1979) [1]                             wound
Hall et al (1983) [11]      4 pts      Vertebral fractures    C
Papasian (1986) [12]       70/M        TURP, inguinal         H
                                         herniorraphy
Incavo (1988) [13]         77/F        NS                     H
Perrone (1994) [3]         NS          NS                     NS
Bilgrami (1995) [14]       65/M        Metastatic prostate    H
                                         cancer to spine
Torda et al (1995) [15]    69/M        Biliary sepsis, liver  H
                                         abscess
Honan et al (1996) [16]    54/F        None                   H
                           54/M        Benign prostatic       NS
                                         hypertrophy
                           41/M        None                   NS
McHenry et al (2002) [17]  NS/NS       NS                     NS
                           NS/NS       NS                     NS
Present case (2003)        77/M        Endodontic             H
                                         procedure
Present case (2003)        86/F        Vertebroplasty         H

Author(s) (year)           Site of
[ref]                      involvement  Organism

Beigelman and Rantz        Cervical     Bacteroides sp.
  (1949) [5]
Ambrose (1966) [6]         Thoracic     Corynebacterium diphtheroides
                           Lumbar       C diphtheroides
Felner and Dowel           NS           Fusobacterium necrophorum
  (1971) [7]
Newman and Mitchell        Cervical     Proprionobacterium sp.
  (1975) [8]
Raff and Mello (1978) [9]  Lumbar       Peptococcus sp. Bacteroides sp.,
                                          Escherichia coli
Lewis et al (1978) [10]    Coccyx (6),  Bacteroides melaninogenicus (6
                             NS (4)       isolates) Fusobacterium sp.
                                          (1), Bacteroides sp (1),
                                          unspecified anaerobe (3)
Sapico and Montgomeric     Lumbar       Bacteroides fragilis,
  (1979) [1]                              Peptostreptococcus magnus,
                                          Proprionibacterium sp.,
                                          betahemolytic streptococci,
                                          Staphylococcus epidermidis
Hall et al (1983) [11]     NS           Peptococcus, Bacteroides, and
                                          Clostridium spp. (c)
Papasian (1986) [12]       Lumbar       Peptosreptococcus micros
Incavo (1988) [13]         Lumbar       Clostridium difficile
Perrone (1994) [3]         NS           Peptostreptococcus sp.
Bilgrami (1995) [14]       Lumbar       Bacteroides fragilis
Torda et al (1995) [15]    Lumbar       Clostridium perfringens
                                          Escherichia coli.
                                          Streptococcus adjacens
Honan et al (1996) [16]    Cervical     Propionibacterium acnes
                           Cervical     Propionibacterium acnes
                           Cervical     Propionibacterium acnes
McHenry et al (2002) [17]  NS           Propionobacterium sp.
                           NS           Propionobacterium sp.
Present case (2003)        Lumbar       Peptostreptococcus sp.
Present case (2003)        Lumbar       Staphylococcus (peptococcus)
                                          saccharolyticus

Author(s) (year)           Source of
[ref]                      recovery          Treatment

Beigelman and Rantz        Spine             Sulfonamide
  (1949) [5]
Ambrose (1966) [6]         Spine             NS
                           Spine             NS
Felner and Dowel           NS                NS
  (1971) [7]
Newman and Mitchell        Soft tissue mass  Penicillin G
  (1975) [8]
Raff and Mello (1978) [9]  Paravertebral     NS
                             abscess
Lewis et al (1978) [10]    NS                NS
Sapico and Montgomeric     Spine             Clindamycin +
  (1979) [1]                                   gentamicin
Hall et al (1983) [11]     Spine (4)         NS
Papasian (1986) [12]       Spine             Clindamycin
Incavo (1988) [13]         Spine             Metronidazole
Perrone (1994) [3]         NK (f)            NS
Bilgrami (1995) [14]       Blood             Metronidazole
Torda et al (1995) [15]    Blood             Ticarcillin/clavulanate;
                                               then ciprofloxacin;
                                               then clindamycin +
                                               trimethoprim
Honan et al (1996) [16]    Blood             Clindamycin
                           Spine             Vancomycin
                           Spine             Vancomycin
McHenry et al (2002) [17]  NS                NS
                           NS                NS
Present case (2003)        Spine             Clindamycin
Present case (2003)        Spine, blood      Clindamycin

Author(s) (year)
[ref]                      Outcome

Beigelman and Rantz        Died
  (1949) [5]
Ambrose (1966) [6]         Recovery
                           Recovery
Felner and Dowel           NS
  (1971) [7]
Newman and Mitchell        Recovery
  (1975) [8]
Raff and Mello (1978) [9]  NS
Lewis et al (1978) [10]    Died (5 pts) (d),
                             Recovered (3 pts)
                           NS (4 pts)
Sapico and Montgomeric     Recovery
  (1979) [1]
Hall et al (1983) [11]     NS
Papasian (1986) [12]       Recovery
Incavo (1988) [13]         Improved
Perrone (1994) [3]         NS
Bilgrami (1995) [14]       Improved
Torda et al (1995) [15]    Recovery
Honan et al (1996) [16]    Recovery
                           Recovery
                           Recovery
McHenry et al (2002) [17]  NS
                           NS
Present case (2003)        Improved
Present case (2003)        Recovery

(a) C, contiguous extension; H, hematogenous spread.
(b) Not stated.
(c) Mean patient age, 52 years; sex not stated.
(d) Four of five patients were from the pre-antibiotic era.
(e) All patients had mixed aerobic-anaerobic infection.
(f) Not known.

Table 2. Anaerobic bacteria isolated from 33 literature cases of
spondylodiscitis

                                            No. of isolates (a)

Gram positive
  Peptococcus spp.                           3
  Staphylococcus saccharolyticus (formerly   1
    Peptococcus saccharolyticus)
  Peptostreptococcus spp.                    3
  Clostridium perfringens                    1
  Clostridium difficile                      1
  Other Clostridium sp.                      1
  Corynebacterium diphtheroides              2
  Propionibacterium acnes                    7
  Unspecified anaerobe                       3
Total                                       22
Gram negative
  Bacteroides fragilis                       2
  Bacteroides melaninogenicus                6
  Other Bacteroides spp.                     4
  Fusobacterium necrophorum                  1
  Fusobacterium spp.                         1
Total                                       14
Total                                       36

(a) Some patients had polymicrobial infection with two or more anaerobic
organisms isolated.

Accepted February 8, 2004.

References

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RELATED ARTICLE: Key Points

* The most frequent pathogenetic organisms isolated in anaerobic spondylodiscitis include Bacteroides species, Propionibacterium acnes, and Peptococcus species.

* The most common sites of vertebral involvement, in decreasing order of incidence, include lumbar, sacrococcygeal, cervical, and thoracic regions.

* Anaerobic spondylodiscitis typically presents with back pain, fever, and motor neurologic deficits.

* Of all the radiographic modalities, magnetic resonance imaging has the most diagnostic accuracy.

* Anaerobic spondylodiscitis is generally treated in the same fashion as aerobic infection, with 4 weeks or more of parenteral antibiotic therapy.

Musab U. Saeed, MD, Paul Mariani, MD, Candelaria Martin, MD, Raymond A. Smego Jr, MD, MPH, Anil Potti, MD, Robert Tight, MD, and David Thiege, MD

From the Department of Medicine, University of North Dakota School of Medicine and Health Sciences, Fargo, ND.

Reprint requests to Dr. Musab U. Saeed. Department of Medicine, University of North Dakota, 720 4th St North, Route 170. Fargo, ND 58122. Email: [e-mail]