AIRP Best Cases in Radiologic- Pathologic Correlation
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1 Note: This copy is for your personal non-commercial use only. To order presentation-ready copies for distribution to your colleagues or clients, contact us at GASTROINTESTINAL IMAGING 825 AIRP Best Cases in Radiologic- Pathologic Correlation Mycobacterium avium-intracellulare Complex Enteritis 1 Editor s note Everyone who has taken the course in radiologic pathology at the Armed Forces Institute of Pathology (AFIP) remembers bringing beautifully illustrated cases for accession to the Institute. As mentioned in my October 2010 and January 2011 editorials, the long-standing and excellent AFIP course in radiologic pathology has transitioned under the auspices of the American College of Radiology to a new home in Silver Spring, Md, entitled the American Institute for Radiologic Pathology (AIRP). In recent years, the staff of the Institute has judged the course s best cases by organ system, and recognition is given to the winners on the last day of the class. With each issue of RadioGraphics, one or more of these cases are published, written by the winning resident. Radiologic-pathologic correlation is emphasized, and the causes of the imaging signs of various diseases are illustrated. Fadi Aris, MDCM Cyrille Naim, MDCM Talat Bessissow, MDCM Ramila Amre, MD Giovanni P. Artho, MD History A 43-year-old man who was positive for the human immunodeficiency virus (HIV) presented to the hospital with chronic diffuse abdominal pain, vomiting, intermittent fever, and weight loss. At presentation, his CD4 + lymphocyte count was less than /L (50/mL), and his plasma viral load was less than 50 copies per milliliter while he was receiving highly active antiretroviral therapy (HAART). At physical examination, the patient was cachectic, with normal vital signs and mild diffuse abdominal tenderness. The results of laboratory tests were an elevated white blood cell count of /L (18,800/mL), a low sodium level of 128 mmol/l, and a low albumin level of 15 g/l. Blood cultures were positive for Mycobacterium avium-intracellulare complex (MAC) that was resistant to clarithromycin therapy. Imaging Findings Computed tomography (CT) was performed for the evaluation of the chronic nonspecific abdominal symptoms and demonstrated diffuse small bowel wall thickening with mucosal hyperenhancement. Segmental dilatation of the jejunum with feculent luminal content mixed with gas bubbles (small bowel feces sign) was demonstrated proximal to a focal area of stenosis (Fig 1a, 1b). The stenotic jejunal segment appeared edematous (Fig 1b). CT showed generalized Abbreviations: HAART = highly active antiretroviral therapy, H-E = hematoxylin-eosin, HIV = human immunodeficiency virus, MAC = Mycobacterium avium-intracellulare complex, PAS = periodic acid-schiff RadioGraphics 2011; 31: Published online /rg Content Code: 1 From the Department of Radiology, McGill University Health Centre, 1650 Cedar Ave, Room C5-118, Montreal, QC, Canada H3G 1A4. Received July 12, 2010; revision requested July 22 and received September 14; accepted September 15. All authors have no financial relationships to disclose. Address correspondence to F.A. ( fadi.aris@mail.mcgill.ca). RSNA, 2011 radiographics.rsna.org
2 826 May-June 2011 radiographics.rsna.org
3 RG Volume 31 Number 3 Aris et al 827 Figure 1. (a) Contrast material enhanced coronally reformatted CT image demonstrates segmental dilatation with small bowel feces sign (*) proximal to a focal jejunal stenotic zone (arrow). Note the diffuse bowel wall mucosal hyperenhancement. (b) Axial contrast-enhanced CT image centered at the stenotic jejunal segment (arrowhead) demonstrates marked mucosal hyperemia, small bowel wall thickening, mesenteric edema (solid arrows), and a small amount of free fluid in the left paracolic gutter (open arrow). (c) Axial contrast-enhanced CT image shows engorgement of the mesenteric vessels (arrow). (d) Contrast-enhanced coronally reformatted CT image demonstrates hepatomegaly; measurement of the liver (white line) = 18.4 cm. (e) Axial contrast-enhanced CT image shows multiple small hypoattenuating areas (arrows) in the spleen. Figure 2. (a) Endoscopic image of the jejunum demonstrates small bowel fold thickening with diffuse mucosal white nodules (arrows). (b) Endoscopic image of the jejunum demonstrates a stenotic segment (arrowheads) with extensive serpentine deep ulcerations and friable, edematous borders (arrows). mild mesenteric edema and a small amount of free intraperitoneal fluid, with striking engorgement and tortuosity of the mesenteric vasculature (Fig 1c). Hepatomegaly was depicted (Fig 1d), as well as small hypoattenuating areas in the spleen (Fig 1e). There was no mesenteric or retroperitoneal lymphadenopathy. Pathologic Evaluation The patient underwent single-balloon enteroscopy for evaluation of malabsorption and the CT findings. In the second portion of the duodenum and extending into the jejunum, there were diffuse, fine white nodules (Fig 2a). Additionally, in the jejunum were multiple areas of friable and erythematous mucosa with deep ulcerations, findings that were most notable in the region of a stenotic segment (Fig 2b). At biopsy, histopathologic examination of the white nodules in the jejunum showed wellpreserved villi in some areas and focal ulceration, with several periodic acid-schiff (PAS) positive, diastase-resistant macrophages with dense fibrillar cytoplasmic material in the lamina propria (Fig 3a 3c). Acid-fast bacilli were demonstrated within the histiocytes by using the Ziehl-Neelsen stain (Fig 3d). No Tropheryma whippelii microorganisms were identified at electron microscopy.
4 828 May-June 2011 radiographics.rsna.org Figure 3. (a) Low-power photomicrograph (original magnification, 100; hematoxylin-eosin [H-E] stain) demonstrates the surface epithelium at the top of the image, with expansion of the lamina propria by cells with pale cytoplasm. (b) Higher-power photomicrograph (original magnification, 200; H-E stain) of the same section as in a shows a large conglomerate of cells in poorly formed aggregates within the lamina propria, which represent histiocytes with eccentrically located nuclei and abundant pink cytoplasm (arrows). (c) Photomicrograph (original magnification, 200; PAS diastase stain) demonstrates PAS-positive, diastase-resistant inclusions within the histiocytes (arrowheads). (d) Photomicrograph (original magnification, 400; Ziehl-Neelsen stain) shows numerous acid-fast bacillary rods (arrowheads) within the cytoplasm of histiocytes. Discussion MAC consists of two species of acid-fast mycobacteria: Mycobacterium avium and Mycobacterium intracellulare. They are difficult to distinguish and therefore are referred to collectively as MAC. These bacteria are obligate intracellular organisms that are found ubiquitously in the environment, including hot water sources, natural water, and soil. Rates of MAC infections vary widely between developed and developing countries, as well as among geographic locations (1,2). Symptomatic infections are thought to arise from recent exposure. Unlike tuberculosis, MAC does not establish a latent infection (3). MAC can affect immunocompetent hosts, typically causing cervical adenitis or pulmonary infections. However, these mycobacterial infections do not usually involve the gastrointestinal tract in patients with intact immune systems. On the other hand, immunocompromised patients may develop disseminated MAC infections that are multiorgan infections, most commonly involving the liver, spleen, gastrointestinal tract, lymph nodes, and bone marrow. Disseminated MAC infections were first reported in AIDS patients in 1982 (4). By 1987, the Centers for Disease Control and Prevention designated extrapulmonary MAC infection as an AIDS-defining illness in patients with HIVpositive serologic findings (5). In the developed world, extrapulmonary MAC infection was one
5 RG Volume 31 Number 3 Aris et al 829 of the most frequent opportunistic bacterial infections in AIDS patients. Before the widespread use of HAART and MAC prophylaxis, 20% 40% of AIDS patients developed disseminated MAC disease (6 8). In this population, it has been reported that more than 95% of MAC infections are caused by M avium (9). If untreated, disseminated MAC infections are known to cause considerable morbidity and mortality. In patients who are receiving effective antiretroviral therapy and MAC prophylaxis and who have a CD4 + lymphocyte count greater than /L ( /mL), the current reported incidence rate is two cases per 100 person-years (9). Clinically, patients with disseminated MAC infection typically have wasting syndrome. As with our patient, they present with weight loss, abdominal pain, and vomiting. Other symptoms include fever, night sweats, malabsorption, and diarrhea. At physical examination, the patient may manifest hepatomegaly, splenomegaly, or lymphadenopathy. Laboratory findings are nonspecific and include anemia, hypoalbuminemia, elevated alkaline phosphatase, and elevated lactate dehydrogenase (5). The diagnosis is made by isolating the organisms from blood cultures. In patients who are suspected of having MAC enteritis, stool cultures and small bowel biopsy are also useful. Alternatively, biopsy of affected organs, such as the liver, spleen, or bone marrow, can be considered (5,9). The most common portals of entry of MAC are the gastrointestinal and respiratory tracts (7,10,11). However, in as many as 90% of disseminated MAC infections, the gastrointestinal tract is the primary route of colonization (3). MAC invades the mucosal epithelium and is engulfed by the macrophages in the lamina propria. Because macrophage activation which is essential for the destruction of the organisms is impaired in advanced AIDS, the organisms survive and proliferate in vacuoles within the macrophages. Therefore, macrophages laden with mycobacterial bacillary rods accumulate in the lamina propria, leading to the expansion of the intestinal villi that is due to lacteal vessel obstruction and bowel wall thickening. Histologically, mild signs of inflammation and rare ulcerations of the intestinal epithelium are seen, with sheets of mycobacteria-filled histiocytes in the lamina propria. The mycobacteria then spread locally into the submucosa and are eventually carried to the local lymph nodes and disseminate hematogenously (12,13). These findings correspond to the imaging appearance at barium studies, where small bowel is usually the most severely affected segment, demonstrating diffusely thickened, irregular small bowel folds with mucosal nodularities (13). Currently, CT of the abdomen and pelvis is a commonly used radiologic examination for the evaluation of symptomatic AIDS patients who are suspected of having intraabdominal disease. CT demonstrates the presence of small bowel involvement as segmental or diffuse wall thickening with mucosal hyperenhancement. These findings can be the direct result of MAC enteritis or a reflection of the hypoalbuminemic state of these patients (14,15). Cross-sectional imaging has the added advantage of the depiction and evaluation of retroperitoneal and mesenteric lymph nodes, which may be increased in number and enlarged in mycobacterial infections. It has been observed that MAC infections are associated with smaller lymph nodes, compared with those associated with Mycobacterium tuberculosis infections. Furthermore, lymph nodes in mycobacterial infections can have hypoattenuating centers secondary to necrosis. This finding is more frequently associated with M tuberculosis infections than with MAC disease. Such findings have been attributed to the fact that M tuberculosis induces a more pronounced immune response, which leads to larger lymph nodes and more frequent caseation (14,16,17). Our patient did not demonstrate mesenteric or retroperitoneal lymphadenopathy. This fact can be attributed to the patient s poor immune response secondary to the persistent low CD4 + lymphocyte count despite receiving a regimen of HAART (16). The clinical, radiologic, and histopathologic manifestations of MAC infection can be similar to those of Whipple disease, which is caused by T whippelii; hence the frequent use of the term pseudo-whipple disease to describe MAC enteritis (18,19). Electron microscopy can depict ultrastructural differences between these microorganisms, but it is the reaction to acid-fast staining that is the most important distinguishing feature, with MAC being acid-fast stain positive and T whippelii being acid-fast stain negative (17 19). In multiorgan disseminated MAC disease, the reticuloendothelial system commonly is involved, with infiltration of the liver and spleen with noncaseating and/or poorly formed granulomas. Findings at gross pathologic examination include organ enlargement and yellowish pigmented foci that are due to mycobacteria-laden swollen macrophages (3,20). These histopathologic findings manifest radiologically as hepatomegaly and/or splenomegaly. Additionally, focal hypoattenuating areas may be identified in the liver and/or spleen that correspond to the granulomas.
6 830 May-June 2011 radiographics.rsna.org The management of MAC disease in HIV-positive patients is primarily focused on chemoprophylaxis, which is recommended in HIV-positive patients who have CD4 + lymphocyte counts of less than /L (50/mL). Clarithromycin or azithromycin is the preferred antibiotic. Prophylaxis may be discontinued if there is a good response to HAART, which is indicated by CD4 + lymphocyte counts rising to more than /L (100/mL) for at least 3 months. MAC disease should be treated aggressively with at least two antimycobacterial agents to avoid the development of drug resistance. Clarithromycin and ethambutol are the recommended combination. Other regimens are considered in cases of drug interactions, drug resistance, high mycobacterial loads, or the lack of HAART (9). Unfortunately, our patient had developed multidrug-resistant MAC infection, which was treated with rifabutin, ciprofloxacin, ethambutol, cycloserine, and ethionamide. Despite all of this therapy, he presented to the hospital 1 month later with worsening respiratory status, and in keeping with the patient s wishes, he was given comfort care and died peacefully. References 1. Horsburgh CR Jr, Schoenfelder JR, Gordin FM, Cohn DL, Sullam PM, Wynne BA. Geographic and seasonal variation in Mycobacterium avium bacteremia among North American patients with AIDS. Am J Med Sci 1997;313(6): Fordham von Reyn C, Arbeit RD, Tosteson AN, et al. The international epidemiology of disseminated Mycobacterium avium complex infection in AIDS: International MAC Study Group. AIDS 1996;10 (9): Mandell GL, Douglas RG, Bennett JE, Dolin R. Mandell, Douglas, and Bennett s principles and practice of infectious diseases. 7th ed. Philadelphia, Pa: Churchill Livingstone/Elsevier, Greene JB, Sidhu GS, Lewin S, et al. Mycobacterium avium-intracellulare: a cause of disseminated life-threatening infection in homosexuals and drug abusers. Ann Intern Med 1982;97(4): Centers for Disease Control (CDC). Revision of the CDC surveillance case definition for acquired immunodeficiency syndrome: Council of State and Territorial Epidemiologists, AIDS Program, Center for Infectious Diseases. MMWR Morb Mortal Wkly Rep 1987;36(suppl 1):1S 15S. 6. Chaisson RE, Moore RD, Richman DD, Keruly J, Creagh T. Incidence and natural history of Mycobacterium avium-complex infections in patients with advanced human immunodeficiency virus disease treated with zidovudine: the Zidovudine Epidemiology Study Group. Am Rev Respir Dis 1992;146(2): Benson C. Disseminated Mycobacterium avium complex disease in patients with AIDS. AIDS Res Hum Retroviruses 1994;10(8): Nightingale SD, Byrd LT, Southern PM, Jockusch JD, Cal SX, Wynne BA. Incidence of Mycobacterium avium-intracellulare complex bacteremia in human immunodeficiency virus-positive patients. J Infect Dis 1992;165(6): Kaplan JE, Benson C, Holmes KH, Brooks JT, Pau A, Masur H. Guidelines for prevention and treatment of opportunistic infections in HIV-infected adults and adolescents: recommendations from CDC, the National Institutes of Health, and the HIV Medicine Association of the Infectious Diseases Society of America. MMWR Recomm Rep 2009; 58(RR-4): Damsker B, Bottone EJ. Mycobacterium avium- Mycobacterium intracellulare from the intestinal tracts of patients with the acquired immunodeficiency syndrome: concepts regarding acquisition and pathogenesis. J Infect Dis 1985;151(1): Roth RI, Owen RL, Keren DF, Volberding PA. Intestinal infection with Mycobacterium avium in acquired immune deficiency syndrome (AIDS): histological and clinical comparison with Whipple s disease. Dig Dis Sci 1985;30(5): Horsburgh CR Jr. The pathophysiology of disseminated Mycobacterium avium complex disease in AIDS. J Infect Dis 1999;179(suppl 3):S461 S Reeders JW, Yee J, Gore RM, Miller FH, Megibow AJ. Gastrointestinal infection in the immunocompromised (AIDS) patient. Eur Radiol 2004;14 (suppl 3):E84 E Radin DR. Intraabdominal Mycobacterium tuberculosis vs Mycobacterium avium-intracellulare infections in patients with AIDS: distinction based on CT findings. AJR Am J Roentgenol 1991;156(3): Macari M, Megibow AJ, Balthazar EJ. A pattern approach to the abnormal small bowel: observations at MDCT and CT enterography. AJR Am J Roentgenol 2007;188(5): Nalaboff KM, Rozenshtein A, Kaplan MH. Imaging of Mycobacterium avium-intracellulare infection in AIDS patients on highly active antiretroviral therapy: reversal syndrome. AJR Am J Roentgenol 2000; 175(2): Koh DM, Burn PR, Mathews G, Nelson M, Healy JC. Abdominal computed tomographic findings of Mycobacterium tuberculosis and Mycobacterium avium intracellulare infection in HIV seropositive patients. Can Assoc Radiol J 2003;54(1): Gillin JS, Urmacher C, West R, Shike M. Disseminated Mycobacterium avium-intracellulare infection in acquired immunodeficiency syndrome mimicking Whipple s disease. Gastroenterology 1983;85(5): Vincent ME, Robbins AH. Mycobacterium aviumintracellulare complex enteritis: pseudo-whipple disease in AIDS. AJR Am J Roentgenol 1985;144 (5): Robbins SL, Cotran RS, Kumar V. Robbins and Cotran pathologic basis of disease. 8th ed. Philadelphia, Pa: Saunders Elsevier, 2010.
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