DOI:10.2214/AJR.05.1088
AJR 2006; 187:873-880
© American Roentgen Ray Society
Epidemiologic, Clinical, and Imaging Findings in Brucellosis Patients with Osteoarticular Involvement
Aysin Pourbagher1,
Mir Ali Pourbagher1,
Lutfu Savas2,
Tuba Turunc3,
Yusuf Ziya Demiroglu3,
Ilknur Erol4 and
Defne Yalcintas5
1 Department of Radiology, Baskent University Adana Teaching and Medical
Research Center, Dadaloglu Mah., 39 Sok No 6, Yuregir, 01250 Adana,
Turkey.
2 Department of Infectious Diseases, Mustafa Kemal University Faculty of
Medicine, Antakya, Turkey.
3 Department of Infectious Diseases, Baskent University Adana Teaching and
Medical Research Center, Adana, Turkey.
4 Department of Pediatrics, Baskent University Adana Teaching and Medical
Research Center, Adana, Turkey.
5 Department of Biostatistics, Baskent University Adana Teaching and Medical
Research Center, Adana, Turkey.
Received June 24, 2005;
accepted after revision September 4, 2005.
Address correspondence to M. A. Pourbagher
(apourbagher{at}hotmail.com).
Abstract
OBJECTIVE. The aim of this study was to assess the epidemiologic and
clinical features, complications, imaging findings, and outcomes for
brucellosis patients with osteoarticular involvement.
SUBJECTS AND METHODS. This prospective study was performed over 4
years (December 2000-December 2004). The subjects were 251 Turkish patients
(age range, 2-77 years) who were diagnosed with brucellosis during that
period. Joint sonography, radiography, radionuclide bone scintigraphy, and MRI
were performed in all patients with osteoarticular and spinal
manifestations.
RESULTS. The disease was acute in 92 patients (36.7%), subacute in
48 patients (19.1%), and chronic in 111 patients (44.2%). Sonography of the
joints showed bursitis in 13 patients (5.2%). Radiography, MRI, and
scintigraphy revealed 71 patients (28.3%) with sacroiliitis, 26 (10.4%) with
spondylodiskitis, three (1.2%) with acute osteomyelitis, and one (0.4%) with
avascular necrosis of the femoral head. All patients received combinations of
either two or three antibiotics. Surgery was performed in three patients with
spinal instability or radiculopathy.
CONCLUSION. Brucellosis is endemic to some regions. MRI is the
method of choice for diagnosing osteoarticular and spinal complications of
human brucellosis, especially during the early phase. It is important to
differentiate tuberculous spondylodiskitis from brucellar spondylodiskitis
because proper treatment for each of these diseases can prevent complications.
The radiologic findings for these two forms of spondylodiskitis are similar,
so serologic testing for brucellosis is necessary in such cases.
Keywords: brucellosis • infectious diseases • MRI • musculoskeletal imaging • osteoarticular involvement
Introduction
Brucellosis is a zoonotic disease caused by bacteria in the organisms of
the Brucella genus. Virtually all infections occur as a result of
direct or indirect exposure to animals; the main modes of transmission are
ingestion of unpasteurized milk and milk products
[1-3].
Human-to-human transmission is unusual; however, a few cases of suspected
sexual transmission have been reported
[4]. Brucellosis exists
worldwide, with highest rates in the Mediterranean basin, the Arabian
Peninsula, the Indian subcontinent, and parts of Mexico and Central and South
America [2,
5,
6]. Brucella
melitensis and Brucella suis are usually more virulent than
Brucella abortus or Brucella canis
[2]. Human brucellosis is a
systemic infection that can affect any organ or system
[7,
8]. When involvement of a
specific organ predominates, the disease is often referred to as focal or
localized [2].
This study was conducted in Turkey. The aim of this study was to report the
clinical features, complications, imaging findings, and outcomes for a series
of brucellosis patients with osteoarticular involvement.
Subjects and Methods
The investigation was performed with ethics committee approval. The study
involved 251 patients (180 females and 71 males; mean age, 45 years; range,
2-77 years) who were diagnosed with brucellosis and hospitalized at the same
center in Adana, Turkey, between December 2000 and December 2004. In each
patient, brucellosis was diagnosed by serologic analysis (Brucella
agglutinin titer 3 1/160) or by clinical symptoms combined with a
positive blood culture. Each patient's history was obtained and physical
examination, psychiatric consultation, and routine laboratory tests were done.
All the patients with osteoarticular involvement were tested for tuberculosis.
In addition, radiography, radionuclide bone scintigraphy, and MRI were
performed in all patients with clinical signs that suggested spondylodiskitis,
sacroiliitis, or osteomyelitis. Patients with arthralgia also underwent
sonography.
MRI was performed using a 1.5-T magnet (Vision, Siemens Medical Solutions)
with a spine coil, and all images were interpreted by a musculoskeletal
radiologist with 5 years of experience. The following spinal MR sequences were
obtained: axial and sagittal spin-echo T1-weighted images (TR/TE, 520/14),
axial and sagittal turbo spin-echo T2-weighted images (4,000/99), sagittal
fat-suppressed T2-weighted images, and contrast-enhanced axial and sagittal
spin-echo T1-weighted images (0.1 mmol/kg of gadopentetate dimeglumine
[Magnevist, Schering] administered IV). The MRI parameters were as follows:
field of view, 20-25 cm for the axial plane and 30-35 cm for the sagittal
plane; number of excitations, 2; matrix size, 256 x 132; slice
thickness, 4 mm; intersection gap, 1 mm; and echo-train length, 8.
Sonography of the joints (shoulder, elbow, wrist, knee, and ankle) was
performed using a high-definition imaging 5000 sonography machine (Philips
Medical Systems) and a 12-5-MHz linear array transducer. All sonographic
examinations were performed by a radiologist with 13 years of experience.
The data obtained were analyzed using SPSS for Windows (Microsoft), version
11.0 (Statistical Package for the Social Sciences). Chi-square and Fisher's
exact tests were used to compare clinical symptoms, laboratory findings, and
imaging findings among the groups in the three stages of disease (acute,
subacute, chronic). Values for p of < 0.05 were considered
significant.
Results
Most of the 251 brucellosis patients were middle-aged adults; relatively
few were children or elderly individuals. In 231 patients (92%), the source of
infection was unpasteurized milk and milk products, most commonly cheese.
Thirty-one (12.4%) of the infected individuals had had direct contact with
animals (sheep or cattle). One hundred forty (77.8%) of the 180 infected
females worked at domestic duties in the home. Twenty-nine (11.6%) of the 251
patients were farmers, four (1.6%) were laboratory personnel, and two (0.8%)
were veterinarians. Twenty-three patients (9.2%) had a family history of
brucellosis.
Brucella species were isolated from blood cultures in 77 cases
(30.7%). Patients were classified as having acute brucellosis (< 3 months),
subacute brucellosis (3-12 months), or chronic brucellosis (> 12 months).
Ninety-two patients (36.7%) had acute disease, 48 (19.1%) were at the subacute
stage, and 111 (44.2%) had chronic disease. Of the 140 patients who were in
the acute or subacute stage, 121 (86.4%) were admitted in the spring or
summer.
Table 1 summarizes the main
presenting clinical symptoms and the frequencies of these in the different
stages of disease. The frequencies of fatigue, fever, appetite loss, nausea,
and diarrhea were significantly higher in the acute stage than in the subacute
or chronic stages (p < 0.05 for all). Weight loss and palpitations
were significantly more frequent in the subacute stage than in the acute and
chronic stages (p < 0.05 for all), and osteoarticular
manifestations were significantly more frequent in the chronic stage than in
the acute and subacute stages (p < 0.05 for both). No significant
differences were seen among the three disease-stage groups with respect to
rates of sweating, headache, abdominal pain, psychiatric disorders, cutaneous
lesions, or pulmonary symptoms.
Blood testing revealed elevated erythrocyte sedimentation rate in 123
patients (49%), anemia (hemoglobin < 13 g/dL in males, hemoglobin < 12
g/dL in females) in 75 (29.9%), elevated serum C-reactive protein in 58
(23.1%), and elevated transaminase levels in 26 (10.4%).
Table 2 summarizes the findings
for these parameters in the subgroups of patients at the different stages of
disease. Statistical analysis revealed no significant differences among the
three groups with respect to frequencies of these hematologic and biochemical
abnormalities (p > 0.05 for all).
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TABLE 2: Main Hematologic and Biochemical Findings Suggestive of Brucellosis in
251 Patients at Different Stages of Disease
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Two hundred twelve (84.5%) of the 251 patients had arthralgia. Sonography
of the joints revealed bursitis in 13 (5.2% of the 251 total) of these
individuals. Six patients with bursitis (2.4% of the 251 total) had synovial
fluid in the suprapatellar bursa, three (1.2%) had synovial fluid in the
olecranon bursa, three (1.2%) had synovial fluid in the subacromial-subdeltoid
bursa, and one (0.4%) had synovial fluid in the bursa at the lateral
malleolus. Cultures of synovial fluid aspirates from all affected joints were
negative.
Seventy-one patients were suspected to have sacroiliitis on the basis of a
positive Patrick's test. This test is used to assess disorders in the
sacroiliac joint. The patient is placed in the supine position, the thigh and
knee of one leg are flexed, and the ankle is placed over the opposite leg so
that the lateral malleolus rests on the patella of the opposite leg. The test
is positive if depression of the knee produces pain or tenderness during
direct compression of the pelvis. Scintigraphy performed with technetium-99m
methylene diphosphonate (99mTc-MDP) showed increased uptake in the
sacroiliac joints of all 71 patients with positive Patrick's tests (28.3% of
the 251 total patients in the study) (Fig.
1). Forty-eight (67.6%) of the 71 patients had unilateral
sacroiliitis, and 23 (32.4%) were affected bilaterally. Twenty-seven (38.0%)
of the 71 patients with sacroiliitis were in the acute stage of brucellosis,
and 19 (26.8%) and 25 (35.2%) were in the subacute and chronic stages,
respectively. No significant differences were seen among the rates of
sacroiliitis in the three disease-stage groups (p > 0.05).
In 26 cases (10.4% of the 251 total), scintigraphy showed diffuse increased
uptake in the vertebral bodies and associated disks, and spinal MRI revealed
spondylodiskitis. Ten (38.5%) of these patients had acute brucellosis, 12
(46.2%) were in the subacute stage, and four (15.4%) were in the chronic
stage. In all four chronic cases and in five of the 12 patients in the
subacute stage, anteroposterior and lateral radiographs of the spine showed
narrowing of intervertebral disk spaces and irregularities in adjacent
vertebral endplates. Blood cultures were positive in 10 (38.5%) of the 26
patients with spondylodiskitis. Testing for tuberculosis was negative and
chest radiography findings were normal in all these patients.
Scintigraphy and MRI revealed spondylodiskitis in the lumbar spine in 15
patients, the thoracic spine in six patients, the cervical spine in one
patient, and both the thoracic and lumbar regions in four patients
(Table 3). The frequency of
lumbar spondylodiskitis was significantly higher than the frequencies of
thoracic and cervical spondylodiskitis (p < 0.05 for both), and
the least common site of involvement was the cervical spine. In one patient
with thoracic and lumbar spondylodiskitis, four contiguous vertebrae (T11-L2)
were affected (Figs. 2A and
2B). One patient had
involvement of T12-L1. The other two patients with both these regions affected
showed noncontiguous multifocal involvement. One of the patients with thoracic
spondylodiskitis had noncontiguous multifocal involvement (Figs.
3A,
3B, and
3C). The patient with cervical
spondylodiskitis exhibited contiguous involvement of the C5-C7 vertebrae
(Figs. 4A and
4B).
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Fig. 2A —MRI of 55-year-old woman with brucellosis and
spondylodiskitis in contiguous thoracic and lumbar vertebrae. Sagittal
spin-echo T1-weighted image shows decreased signal intensity in bodies of
T11-L2 vertebrae.
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Fig. 2B —MRI of 55-year-old woman with brucellosis and
spondylodiskitis in contiguous thoracic and lumbar vertebrae. Turbo spin-echo
T2-weighted image shows increased signal intensity in bodies of affected
vertebrae (arrows) and abnormal signal extending across disk
space.
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Fig. 3A —MRI of 55-year-old man with brucellosis and noncontiguous
multifocal thoracic spondylodiskitis. Sagittal spin-echo T1-weighted image
shows decreased signal intensity in T6-T7 and T9-T10 vertebral bodies
(arrows).
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Fig. 3B —MRI of 55-year-old man with brucellosis and noncontiguous
multifocal thoracic spondylodiskitis. Sagittal turbo spin-echo T2-weighted
image shows increased signal intensity in affected vertebrae with irregular
vertebral body endplates and narrowing of intervertebral disk spaces
(arrowheads).
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Fig. 3C —MRI of 55-year-old man with brucellosis and noncontiguous
multifocal thoracic spondylodiskitis. Sagittal gadolinium-enhanced T1-weighted
image shows areas of enhancement in affected vertebral bodies (open
arrows) and disks (solid arrows).
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Fig. 4A —MRI of 63-year-old man with brucellosis and cervical
spondylodiskitis. Sagittal spin-echo T1-weighted images show decreased signal
of contiguous involvement of C5-C7 vertebra (A) and heterogeneously
increased signal (B) after IV injection of gadolinium in affected
vertebrae with irregular vertebral body endplates.
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Fig. 4B —MRI of 63-year-old man with brucellosis and cervical
spondylodiskitis. Sagittal spin-echo T1-weighted images show decreased signal
of contiguous involvement of C5-C7 vertebra (A) and heterogeneously
increased signal (B) after IV injection of gadolinium in affected
vertebrae with irregular vertebral body endplates.
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Fig. 5 —34-year-old man with brucellosis. Transverse T1-weighted
spin-echo MR image obtained after IV injection of gadolinium shows
heterogeneous enlargement of soft tissue to right of patient's spine
(arrows). Abscess is area of low signal intensity in mid portion of
inflamed muscle (arrowheads).
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On MRI of the patients with spondylodiskitis, sagittal T1-weighted images
of the spine showed low signal intensity in the bodies of involved vertebrae
and T2-weighted images showed high signal intensity at these sites (Figs.
2A and
2B). After gadolinium
administration, sagittal T1-weighted images showed high signal intensity in
the bodies of affected vertebrae and disks
(Fig. 3C). Eight patients had
paraspinal or epidural abscesses (Fig.
5). None of the 26 patients with spondylodiskitis showed
subligamentous spread or involvement of the posterior portions of vertebrae.
In three patients with thoracic spondylodiskitis, MRI showed vertebral
destruction and cord and root compression similar to the findings in
tuberculous spondylodiskitis (Pott's disease) (Figs.
6A,
6B, and
6C). All the patients with
paraspinal or epidural abscesses and vertebral destruction were in the acute
or subacute stage of spondylodiskitis.
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Fig. 6A —MRI of 66-year-old man with brucellosis and T7-T8
spondylodiskitis. Sagittal spin-echo T1-weighted image (A), sagittal
turbo spin-echo T2-weighted image (B), and sagittal spin-echo
T1-weighted image after IV injection of gadolinium (C) show T8
vertebral collapse and cord and root compression. These are also features of
tuberculous spondylodiskitis (Pott's disease).
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Fig. 6B —MRI of 66-year-old man with brucellosis and T7-T8
spondylodiskitis. Sagittal spin-echo T1-weighted image (A), sagittal
turbo spin-echo T2-weighted image (B), and sagittal spin-echo
T1-weighted image after IV injection of gadolinium (C) show T8
vertebral collapse and cord and root compression. These are also features of
tuberculous spondylodiskitis (Pott's disease).
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Fig. 6C —MRI of 66-year-old man with brucellosis and T7-T8
spondylodiskitis. Sagittal spin-echo T1-weighted image (A), sagittal
turbo spin-echo T2-weighted image (B), and sagittal spin-echo
T1-weighted image after IV injection of gadolinium (C) show T8
vertebral collapse and cord and root compression. These are also features of
tuberculous spondylodiskitis (Pott's disease).
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On scintigraphy, one patient with right leg pain showed increased uptake in
the tibia, one with hip pain showed increased uptake in the iliac bones, and
one with pain and swelling at the left sternoclavicular junction showed
increased uptake at the junction. On MRI, all three of these patients were
diagnosed with acute osteomyelitis on the basis of the low signal intensity on
T1-weighted images and high signal intensity on T2-weighted images (Figs.
7A,
7B,
8A,
8B,
9A, and
9B). Needle aspiration biopsy
confirmed the diagnoses. None of the patients who underwent scintigraphy
exhibited uptake in regions that were nonpainful.
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Fig. 7A —MRI of 6-year-old boy with brucellosis and osteomyelitis of
tibia. Coronal spin-echo T1-weighted (A) and turbo spin-echo
T2-weighted (B) images show involvement of metaphysis and epiphysis
(arrows).
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Fig. 7B —MRI of 6-year-old boy with brucellosis and osteomyelitis of
tibia. Coronal spin-echo T1-weighted (A) and turbo spin-echo
T2-weighted (B) images show involvement of metaphysis and epiphysis
(arrows).
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Fig. 8A —MRI of 20-year-old woman with brucellosis and osteomyelitis
of right iliac bone. Transverse spin-echo T1-weighted image shows region of
low signal intensity (arrowheads) in wing of right iliac bone.
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Fig. 9A —MRI of 49-year-old woman with brucellosis and osteomyelitis
and abscess formation at left sternoclavicular junction. Coronal spin-echo
T1-weighted image shows low signal intensity at junction and in soft tissue
(arrows).
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Fig. 9B —MRI of 49-year-old woman with brucellosis and osteomyelitis
and abscess formation at left sternoclavicular junction. Transverse turbo
spin-echo T2-weighted image shows high signal intensity in these same zones
and evidence of abscess formation (arrow).
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A 9-year-old boy who was diagnosed with subacute brucellosis presented with
pain and limited range of motion in the right hip. Radiographs of the joint
revealed an extensive subchondral fracture and collapse of the femoral head,
and these findings were interpreted as avascular necrosis of the right hip
(Fig. 10).
All 251 patients with brucellosis were treated with either two- or
three-drug combinations of antibiotics (ciprofloxacin, tetracycline,
rifampicin, streptomycin). The median duration of therapy was 45 days. In four
cases (1.6%), the infection did not respond to therapy; serum titers were
still abnormal after 2 months. Nine patients (3.6%) relapsed after the start
of treatment (six individuals at 3 months, one at 6 months, and two at 12
months). Three of these nine patients relapsed again 4 months after they
started their second round of treatment. Surgery was performed in three
patients with spinal instability or radiculopathy.
Discussion
Brucellosis remains an important public health problem in certain
Mediterranean regions, including Turkey. This disease can cause serious
complications, and early diagnosis is necessary to avoid these problems.
Brucellosis is widely recognized as an occupational risk among adults
[2] and is more common in males
[1]. However, in our series of
251 brucellosis patients from Adana, Turkey, only 13.9% (29 farmers, four
laboratory personnel, and two veterinarians) had occupational risk, and there
were many more women than men (71.7% vs 28.3%, respectively). The main mode of
transmission in our patients was the ingestion of unpasteurized milk and milk
products.
Brucellosis most often affects young or middle-aged adults, with low
incidence rates in children and the elderly
[9]. It is not rare to observe
outbreaks of the disease within families, especially when a common food source
is involved [10]. In our
series, 9.2% of the patients had a family history of brucellosis. The first
signs of Brucella infection usually appear 2-4 weeks after
inoculation [5]. As noted, any
organ or body system can be affected. The symptoms of brucellosis are
nonspecific (osteoarticular complaints, fatigue, sweating, prolonged fever,
anxiety or depression, hepatobiliary or gastrointestinal abnormalities). In
our series, osteoarticular complaints were the most common symptoms.
Reportedly, the erythrocyte sedimentation rate is of minimal diagnostic value
in brucellosis [11]; however,
the main hematologic abnormalities we observed in our 251 patients were
elevated erythrocyte sedimentation rate, anemia, elevated serum C-reactive
protein, and elevated transaminase levels.
Osteoarticular complications of brucellosis are common
[9,
12], and 114 (45.4%) of our
251 patients exhibited this form of involvement. The lumbar region is the most
frequent site of spondylodiskitis in brucellosis patients
[13]. In our series,
sacroiliitis was the most common osteoarticular complication of brucellosis,
followed by spondylodiskitis, bursitis, and osteomyelitis. In accordance with
the literature, we found that the lumbar spine was the most frequent site of
spondylodiskitis (57.7%). The cervical spine was the region least affected
with this condition (3.8%). In cases of brucellar spondylodiskitis, initial
radiographs may show completely normal findings, and early diagnosis is often
difficult because of the long latency period with spondylodiskitis
[14].
Radionuclide bone scintigraphy is an important diagnostic tool for
detecting osteoarticular sites affected by brucellosis. MRI is the method of
choice for diagnosing brucellar spondylodiskitis, paraspinal or epidural
abscesses, and cord or root compression related to brucellosis, especially in
the early phase of spondylodiskitis. Signal changes in vertebral bodies
without morphologic changes and enhancement of facet joints after gadolinium
injection have been identified as specific MRI features of brucellar
spondylitis [15]. However, we
also detected vertebral destruction that appeared similar to tuberculous
spondylodiskitis in three of our patients, which has not been reported
previously, to our knowledge, in cases of human brucellosis. Multiple reports
claim that involvement of multiple vertebral bodies and skip lesions suggests
tuberculous spondylodiskitis
[16-19].
In our series, some patients with spondylodiskitis exhibited involvement of
contiguous vertebrae, whereas others showed noncontiguous involvement.
Avascular necrosis secondary to brucellosis is extremely rare. To our
knowledge, only two such cases have been reported previously, and the femoral
head was the site affected in both instances
[20,
21]. One (0.4% of the 251
total) of our patients had avascular necrosis of the femoral head.
In conclusion, brucellosis is hyperendemic in Turkey, where the disease is
transmitted mainly by unpasteurized milk and milk products. Thus, prevention
depends on eliminating the disease from domestic animals and educating people
to use pasteurized products. Brucellosis should be included in the
differential diagnosis of any patient with arthralgia or symptoms of
osteomyelitis or spondylodiskitis. The index of suspicion should be high in
regions where the disease is endemic. Scintigraphy and MRI are the methods of
choice for investigating osteoarticular and spinal complications of human
brucellosis. If vertebral destruction or collapse, multiple vertebral
involvement, or skip lesions are detected, it is important to differentiate
tuberculous spondylodiskitis from brucellar spondylodiskitis because
appropriate treatment for each of these diseases can prevent complications.
The radiologic findings for these two forms of spondylodiskitis are similar,
so serologic testing for brucellosis is necessary in such cases.
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Abstract
Introduction
