The Spectrum of Imaging Findings of Brucellosis: A Pictorial Essay

The Spectrum of Imaging Findings of Brucellosis: A Pictorial Essay

Canadian Association of Radiologists Journal 63 (2012) 5e11 www.carjonline.org  Critically Appraised Topic / Evaluation critique The Spectrum of Im...

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Canadian Association of Radiologists Journal 63 (2012) 5e11 www.carjonline.org

 Critically Appraised Topic / Evaluation critique

The Spectrum of Imaging Findings of Brucellosis: A Pictorial Essay Nizar A. Al-Nakshabandi, MD, FRCPC* Department of Radiology and Diagnostic Imaging, King Khalid University Hospital, College of Medicine, King Saud University, Riyadh, Saudi Arabia

Introduction Human brucellosis is a multisystemic disease. The disease is caused by a gram-negative coccobacilli of the genus Brucella [1]. There are 4 types of species that cause brucellosis in humans: Brucella melitensis, found in camels and sheep; Brucella abortus in cattle; Brucella canis in dogs; and Brucella suis in hogs. B. melitensis is the most virulent and invasive [1]. Brucellosis is endemic in Saudi Arabia. Morbidity in the Saudi population continues to be reported with increasing frequency from various regions of the country, particularly in the rural areas. The reported human infection range is 1.6%-2.6% [1]. The disease can present in any sex or age with varied manifestation. Any body part can be involved, but the musculoskeletal system, particularly the spine, is most commonly affected. Brucellosis remains a huge problem and a public health issue in many regions, particularly in the Mediterranean, the Middle East, parts of South and Central America, and many parts of Western Africa [2]. It has also been reported to have involved multiple organ systems in 1 patient in whom there had been Brucella hepatitis, myocarditis, acute disseminate encephalitis, and renal failure, with low attenuating, low agglutinating titers [2]. Brucellosis is an important concern in first-world countries because of issues surrounding immigration and the impact of the disease on the economy. The radiologist plays a major role in raising the suspicion of a brucellosis diagnosis in patients from high-risk demographics in nonendemic countries. Brucellosis in Saudi Arabia Morbidity in the Saudi population still continues to be reported, with human infection in the range of 1.6%e2.6% [1]. There was an increase in the rate of annual admission of brucellosis in the 1980s [1]. During this period, brucellosis in * Address for correspondence: Nizar A. Al-Nakshabandi, MD, FRCPC, Department of Radiology and Diagnostic Imaging (40), King Khalid University Hospital, College of Medicine, King Saud University, P.O. Box 7805, Riyadh 11472, Saudi Arabia. E-mail address: [email protected] (N. A. Al-Nakshabandi).

animals and humans has been thoroughly linked to the uncontrolled deportation of animals potentially infected with brucellosis, widespread animal husbandry, and the prevailing habit among the nomadic population of ingesting raw milk or its products. There has been a steady increase in the incidence of Brucella infections in animals. In 1977, the incidence of brucellosis in the southern region had been documented to be 0.8% in goats, 0.5% in sheep, 2.8% in camels, and 3.6% in cows. Ten years later, the incidence rate had gone up to 18.2% in goats, 12.3% in sheep, and 22.6% in camels, and 15.5% in cows [1]. Discussion Brucellosis can involve various body parts. The Brain In brucellosis, the central and peripheral nervous systems are involved in 3.5%e13% of patients [3]. These patients usually exhibit symptoms such as headache and neuropsychiatric complaints related to neurologic disorders [3]. Magnetic resonance (MR) spectroscopy has been used in brucellosis, because brucellosis may cause subtle cerebral alterations that are only discernible in MR spectroscopy because of its ability to detect the increased choline-to-creatine ratio, which represents an initial phase of inflammation and demyelination process of brucellosis [3]. Brucellosis in the brain has been reported to have extensive white matter changes, particularly on the fluid attenuated inversion recovery (FLAIR) sequences as well as involvement of the meninges. When gadolinium is given, the meninges and the white matter changes can be enhanced (Figure 1). Other manifestations of a neurobrucellosis range from cerebral infarction to white matter changes to peripheral nerve palsies [4,5]. The Spine Two forms of spinal brucellosis are known: the focal and the diffuse [6]. In the focal form, the organisms are

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Figure 1. (A, B) Axial T1- and T2-weighted image in a 32-year-old woman, showing high signal intensity in the right posterior aspect of right parietal lobe. (C) Fluid attenuated inversion recovery sequence, showing focal high signal intensity in the same region. (D) Axial T1 after gadolinium infusion, showing focal enhancement in the white matter and the meninges (arrows).

transferred by the hematogenous route and localized in the anterior aspect of the superior end plate, which is known for its rich blood supply. The disks and paraspinal soft tissues at the level of focal disease are usually within normal limits. Late changes will be definitely identified on bone scans and MR imaging (Figure 2). In diffuse disease, the infection is usually more severe and involves the epidural space at times; even in severe cases, the changes are not usually seen on plain radiographs. MR is usually needed to identify these changes, which are identified by areas of loss of signal intensity on T1-weighted images that become hyperintense on T2-weighted magnetic resonance imaging (MRI) sequences when using a low, long TR and TE, and, after gadolinium administration, avid enhancement usually occurs (Figure 3) [6,7].

Bone scans are an important diagnostic tool for detecting spinal involvement of brucellosis. However, MRI is the method of choice for diagnosing Brucella spondylodiscitis and gives the added benefit of seeing paraspinal or epidural abscess involvement, particularly when cord or nerve compression is in question [7]. Diffusion weighted imaging (DWI) has a valuable role in detecting vertebral brucellar spondylodiscitis. DWI is a sensitive and fast sequence that can differentiate acute from chronic forms of spondylodiscitis, which is at times crucial in imaging the spine [8]. The acute form of brucellosis of the vertebral bodies and end plates will be hyperintense, whereas it will be hypointense in the chronic form on DWI [9]. The issue of differentiating brucellar spondylitis from tuberculo-spondylitis remains a conundrum. However,

Figure 2. Focal form of spinal brucellosis in a 26-year-old woman with systemic brucellosis and low back pain. (A) Radiograph, showing loss of disk height between L4-L5 and an anterior osteophyte (arrow), sclerosis. (B) Scintigram, showing focal increased uptake in the bodies of L4 and L5. This was seen only on the anterior view. (C) Fat-suppressed T1-weighted magnetic resonance image (TR was 500 msec; TE was 18 msec [500/18]) obtained after administration of gadolinium, showing focal enhancement of the anterior aspect of the superior end plate of L4 and L5 (arrows). Also note the enhancement of the anterior aspect of the L4 and L5 disks (arrow). (Case courtesy of Dr Fatima Abdulla, Manama General Hospital, Manama, Kingdom of Bahrain.)

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Figure 3. A 60-year-old woman with neck pain and a diffuse form of brucellosis. (A) Sagittal turbo spin echo image, showing destruction of the C5 and C6, and involvement of the disk space (arrow). (B) Sagittal T1-weighted image with intravenous gadolinium, showing an enhancing mass with destruction of the vertebral bodies of C5 and C6 as well as enhancement of the disk space (arrow). (C) Coronal weighted image with intravenous gadolinium, showing an enhancing mass with destruction of the vertebral bodies of C5 and C6 as well as enhancement of the disk space (arrow).

multiple reports claim that involvement of the multiple vertebral bodies with the involvement of the disk space and Gibbus deformity usually suggests tuberculo-spondylitis [8]. In addition, brucellar serology, in most cases by using the agglutination test, is positive in brucellar spondylodiscitis and not often the case in tuberculo-spondylitis.

along the mammary ducts, with abscess formation (Figure 4A). MR elegantly demonstrates this oedema and abscess formation, which demonstrates avid contrast enhancement (Figure 4B).

The Breast

Any joint can be involved, with affinity to large joints, but all joints have been involved, including sternoclavicular joints and sacroiliac joints. Brucella has also been reported to cause avascular nephrosis in the femoral head in longstanding and neglected cases [11,12]. Joints involved in a great majority of patients show an increased uptake on

There are at least 7 published cases of brucellar mastitis in the literature [9]. Brucellar mastitis is not seen primarily in women who are lactating but can be seen in women with breast implants [10]. It is seen on ultrasound as oedema

The Musculoskeletal System

Figure 4. (A) A 38-year-old non-pregnant woman with right breast redness, tenderness, and a positive Brucella titer. Ultrasound by using a 10-MHz probe, showing oedema of the breast consistent with diffuse mastitis and a complex mass (arrow). (B) The same patient in (A). Fat sat fast spoiled echo gradient (FSPGR) with gadolinium infusion, showing avid enhancement of the oedematous tissue and mass, extending to the nipple (arrow).

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Figure 5. A 12-year-old boy with left-sided limping and pain, with positive Brucella titer. (A) Plain radiograph, showing subtle femoral head erosion (arrow). (B) T2-weighted image, showing a left hip joint effusion and debris in it as well as bone marrow oedema (arrow). (C) Diffuse synovial enhancement is seen after gadolinium infusion (arrow).

Figure 6. A 44-year-old woman with lower back pain that radiated to the left side and a positive Brucella titer. (A) Plain radiograph, showing widening of the left sacroiliac (SI) joint with erosions and sclerosis on the iliac side (arrow). (B) Computed tomography, elegantly demonstrating widening of the left SI joint, with erosions and sclerosis on the iliac side (arrow). (C) Axial T1-weighted image, showing low signal on both sides of the SI joint along with widening (arrow). (D) Axial T1 postgadolinium infusion, showing avid enhancement of the SI joint, bone, and muscles consistent with brucellar septic arthritis and osteomyelitis (arrow).

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Figure 7. A 39-year-old woman with fever, positive Brucella titer, and a newly diagnosed murmur. Long-axis transesophageal echo, showing vegetations on the ventricular surface of the aortic valve (arrow), an aortic regurgitation, and chamber enlargement as a result. (Case courtesy of Dr Rajaa Mestady, Riyadh, Saudi Arabia.)

Figure 8. A 50-year-old man with a positive Brucella titer was having abdominal pain and pulsating abdominal mass. (A) A computed tomography (CT) of the aorta at the level of a destructed L3, with erosions of the body and extension of the inflammatory process into the aorta, which caused a mycotic aneurysm (arrow). (B) Sagittal CT of the same patient, elegantly showing the extent of destruction and aneurysm formation (arrow). (C, D) Coronal T2-weighted image of the lumbar spine, showing destruction of the disk space between L3 and L4, with spread of the phlegmon to the abdominal aorta, which caused a mycotic aneurysm (arrow). (Case courtesy of Dr Khalid Alismail, King Faisal Specialist Hospital, Riyadh, Saudi Arabia.)

Figure 9. A 27-year-old man with brucellosis and abdominal pain. (A) Plain abdominal radiograph, showing an enlarged liver shadow (arrow). (B) Coronal T2-weighted image, confirming the plain radiograph suspicion of hepatomegaly (arrow).

bone scans. In addition, an increase of synovial fluid is evident on MRI, with evidence of bone marrow oedema (Figure 5). The joints are presumed to have only a synovial disease [6]. However, aspiration of the joints almost always

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culture, along with visualization of vegetations on a cardiac valve [14]. In addition, direct spread of the spinal brucellar phlegmon can encase the major vessels, for example, the aorta, and cause mycotic aneurysms (Figure 8). The Gastrointestinal System Brucella can cause local infections in the gastrointestinal system, for example, hepatitis that leads to hepatomegaly (Figure 9), cholecystitis, and pancreatitis [15]. Colitis, spontaneous bacterial peritonitis, and adenopathy (Figure 10) have also been reported with Brucella [15]. The Genitourinary System Figure 10. A 33-year-old woman with severe diarrhoea and abdominal pain after drinking unpasteurized milk. (Arrow A) points to dilated severely inflamed loop of bowel. (Arrow B) points to ascites and nodular peritonitis. (Arrow C) points to reactive lymphadenopathy.

Scrotal infections are generally diagnosed by clinical features. Ultrasound and Doppler are helpful in confirming the diagnoses and detecting complications such as abscesses or testicular torsion [16]. The imaging features of heterogeneity

Figure 11. A 29-year-old man with testicular pain and a high Brucella titer. (A) Transverse sonogram of the testis, showing an enlarged and predominantly hypoechoic epididymis, with a reactive hydrocele in a patient with acute epididymitis. (B, C) Colour-flow sonogram, showing increased vascularity in the epididymis. An enlarged epididymis with increased vascularity in the appropriate clinical setting is diagnostic of acute epididymitis. This figure is available in colour online at http://carjonline.org/.

yields sterile serosanguineous fluid. The sacroiliac joint is another favorite location for brucellar septic arthritis and osteomyelitis. Sacroiliac joint involvement can extend to bone and muscle involvement in the region [8]. One of the hallmarks of Brucella septic arthritis is that it affects both joint spaces in the sacroiliac joint and causes erosive and bony destruction of the sacroiliac joint, with enhancement (Figure 6). This feature is similarly seen in psoriatic gout and arthropathy [13]. The Cardiovascular System Brucella endocarditis is a rare manifestation of brucellosis [14]; in imaging, usually thickening of the myocardium as well as vegetation on valves can be seen in cases of endocarditis (Figure 7) and thickening of the pericardium in cases of pericarditis, with a pericardial effusion. Brucella endocarditis is a diagnosis based on a positive titer and blood

differences in the testicle and thickening of the scrotum as well as hydrocele and enlargement of the epididymal head are seen on ultrasound. In addition, Doppler interrogation usually demonstrates an increase in flow to the inflamed regions in patients who have a positive Brucella titer (Figure 11). Summary Brucellosis remains a major health and economic problem in some parts of the world. The radiologist plays a major role in its diagnosis and management. Brucellosis is an important concern in first-world countries because of issues surrounding immigration and the impact of the disease on the economy. References [1] Al Eissa YA. Brucellosis in Saudi Arabia: past, present and future. Ann Saudi Med 1999;19:403e4.

Imaging findings of brucellosis / Canadian Association of Radiologists Journal 63 (2012) 5e11 [2] Khorvash F, Keshteli AH, Behati M, et al. An unusual presentation of brucellosis, involving multiple organ systems, with low agglutinating titers: a case report. J Med Case Reports 2007;1:53. [3] Kayabas U, Alkan A, Kemat FA, et al. Magnetic resonance spectroscopy features of normal-appearing white matter in patients with acute brucellosis. Eur J Radiol 2008;65:417e20. [4] Al-Sous MW, Bohlega S, Al-Kawi MZ, et al. Neurobrucellosis: clinical and neuroimaging correlation. Am J Neuroradiol 2004;25: 395e401. € [5] Ozkavukcu E, Tuncay Z, Selcuk F, et al. An unusual case of neurobrucellosis presenting with unilateral abducens nerve palsy: clinical and MRI findings. Diagn Interv Radiol 2009;15:236e8. [6] Al-Shahed MS, Sharif HS, Haddad MC, et al. Imaging features of musculoskeletal brucellosis. Radiographics 1994;14:333e48. [7] Pourbagher A, Pourbagher MA, Savas L, et al. Epidemiologic, clinical, and imaging findings in brucellosis patients with osteoarticular involvement. AJR Am J Roentgenol 2006;187:873e80. [8] Jung NY, Jee WH, Ha KY, et al. Discrimination of tuberculous spondylitis from pyogenic spondylitis on MRI. AJR Am J Roentgenol 2004; 182:1405e10.

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[9] Oztekin O, Calli C, Adibelli Z, et al. Brucellar spondylodiscitis: magnetic resonance imaging features with conventional sequences and diffusion weighted imaging. Radiol Med 2010;115:794e803. [10] Jensenius M, Hermansen N, Jahr G, et al. Brucellar mastitis: presentation of a case and review of the literature. Int J Infect Dis 2008;12:98e113. [11] Benjamin B, Khan MR. Hip involvement in childhood brucellosis. J Bone Joint Surg Br 1994;76:544e7. [12] Gedalia A, Howard C, Einhom M. Brucellosis induced avascular necrosis of the femoral head in a 7 year old child. Ann Rheum Dis 1992;51:404e6. [13] Dayan L, Deyev S, Palma L, et al. Long standing, neglected sacroiliitis with remarked sacro-iliac degenerative changes as a result of Brucella spp. infection. Spine J 2009;9:e1e4. [14] Yildiz A, Tufekcioglu O, Aras D, et al. Myocardial noncompaction presenting with Brucella endocarditis. Int J Cardiol 2009;131:e87e9. [15] Aziz S, Al-Anazi A, Al-Aska A. A review of gastrointestinal manifestations of Brucellosis. Saudi J Gastroenterol 2005;11:20e7. [16] Ozturk A, Ozturk E, Zeyrek F, et al. Comparison of brucella and nonspecific epididymorchitis: gray scale and color Doppler ultrasonographic features. Eur J Radiol 2005;56:256e62.