Abdominal tuberculosis (ATB) is encountered infrequently by individual practitioners in developed countries, compared to countries where tuberculosis (TB) is endemic. In Western countries, patients tend to be immigrants or immunocompromised. Despite many case reports, diagnosis remains challenging, because concurrent lung disease usually is absent. We report a case in a Mexican adolescent who had lived in the United States for a decade. Diagnosis was delayed nearly 4 months by an initial diagnosis of concurrent Helicobacter pylori and apparent Crohn disease (CD).
A 16-year-old boy who immigrated to the United States from Mexico at the age of 5 was seen in the pediatric gastrointestinal clinic presenting with a several-month history of abdominal pain, 30-lb weight loss, anorexia, and vomiting. Endoscopy revealed inflammation of the gastric mucosa and necrotic-appearing ulcers in the colon (Figs. 1 and 2). H pylori was present in biopsy specimens of the gastric mucosa. Focal-surface ulceration with necrosis and granulation tissue was noted in the colon pathologically. Treatment for H pylori was initiated. In addition, mesalamine and prednisone were instituted as CD treatment.
Failure of the original symptoms to improve, along with new tenderness in the right lower quadrant (without hepatosplenomegaly) and a 5 × 5-cm mass noted on examination, prompted admission and repeat computed tomography (CT) of his abdomen. Marked mucosal thickening of the terminal ileum, cecum, and ileocecal valve was revealed (Fig. 3). In addition, multiple 3-cm necrotic lymph nodes in the right lower quadrant were noted. CT of a newly noted 3 × 4-cm right-sided cervical mass, identified on admission, revealed a necrotic lymph node measuring 2.6 cm × 3 cm × 3.7 cm in the right jugulodigastric region (Fig. 4). Initial chest radiograph at admission and several repeat chest radiographs for central-line placement were normal.
Biopsy of his cervical lymph node revealed purulent inflammatory exudate and numerous acid fast bacilli (AFB) on stain. The patient's previous colonic biopsy specimen was reexamined, this time with AFB staining, and found to have AFB (Fig. 5). Standard TST was placed but remained negative, likely related to concurrent corticosteroid use.
A possible epidemiological link was investigated related to ingestion of a homemade Mexican cheese product several months prior. The family denied contact with anyone who exhibited TB symptomatology. Therefore, standard 4-drug antituberculous therapy was initiated with the addition of ciprofloxacin to treat for both Mycobacterium bovis and M tuberculosis.
Persistent symptoms prompted follow-up CT scans. Improvement in cervical and abdominal lymphadenopathy was noted, but there was persistent ileocecal disease with suggestion of appendicitis. Ciprofloxacin was discontinued when the organism was identified as M tuberculosis. Susceptibility testing revealed no resistance to first-line antituberculous therapies. Symptoms continued despite parenteral nutrition, corticosteroid, and intravenous antituberculous therapy.
An upper-gastrointestinal exam with small-bowel follow through revealed the presence of a partial small-bowel obstruction proximal to the ileocecal valve. The patient underwent laparotomy with appendectomy 3 months into his therapeutic course, with findings of a thickened and dilated ileum, as well as a scarred and fibrotic cecum. An ileal hemicolectomy was performed with end-to-side anastomosis. AFB were present microscopically in the appendiceal wall; however, tissue was not sent for culture.
He had complete resolution of his abdominal pain and vomiting within 5 days, and was discharged home approximately 2 weeks postoperatively. In addition, he gained weight on each follow-up appointment. This clinical response reduced the likelihood of concurrent CD. His 12-month course of antituberculous therapy was completed in November 2006.
The most common presenting complaints, physical-examination findings, radiological features, and endoscopic and histological findings in patients with tuberculous colitis are nonspecific and indistinguishable from CD (1–12). Classical findings attributable to TB—such as lymphadenopathy, a positive TST, or a chest radiograph that indicates either active or old pulmonary disease—may only be present in up to 64% of cases (10,13). Despite this, a chest radiograph should be obtained on every patient in whom the diagnosis of TB is considered.
The patient's history is pertinent in the diagnosis of TB colitis, which is thought to be the direct result of either swallowing infected sputum or ingesting contaminated food (12). Symptoms in patients with TB may be either acute or chronic in nature, making it easy to overlook historical links between exposure and symptomatology. Tuberculosis should be included in the differential diagnosis of all foreign-born patients, whether they immigrated recently or many years ago. Furthermore, the diagnosis of TB also should be entertained in patients who have traveled in foreign countries or who recall ingesting unpasteurized milk products. This last piece of information may be difficult to obtain, often requiring persistence on the part of the clinician.
A detailed physical examination may aid the clinician in excluding the possibility of TB when completing the initial evaluation for suspected CD. Particular importance should be placed on the cardiovascular, pulmonary, and lymphatic portions of the examination.
In endemic countries antituberculous therapy is often initiated empirically before treatment for CD because of the difficulty in differentiating CD from TB. The diagnostic value of any individual modality is low, making it essential to combine several modalities. These may include TST, CT, endoscopic biopsy with AFB stains, culture, polymerase chain reaction, and/or the QuantiFERON-TB Gold test to confirm the diagnosis. CD and TB colitis are not mutually exclusive, but when tuberculous organisms are identified and treatment leads to complete resolution of symptoms, concurrent CD is reasonably excluded.
Tuberculin skin testing should be performed in all patients with a suspected diagnosis of CD. Negative TST results do not completely exclude the diagnosis of TB, because false-negative TST occurs in 12% to 50% of patients with intestinal TB infection (2,10,14). Furthermore, false-negative TSTs increase to >80% when immunosuppressive therapy has occurred before TST (15). This underscores TST as an essential screening aspect of patients with a new apparent diagnosis of CD, before starting immunosuppressive medicines. False-positive TST results also can occur, and are usually due to cross reaction of TST antigens in patients with prior nontuberculous mycobacterial infections, or from previous vaccination with bacille Calmette-Guérin (16,17). In areas of low prevalence, the specificity of TST ranges from 50% to 90%, making biopsy or culture confirmation important (18).
There are few imaging tools to help establish the diagnosis of ATB. Abdominal films and ultrasound are not useful (4,5,10,19–21). CT remains the most useful, and may reveal adenopathy and/or thickening of the ileocecal valve and cecum. Central necrosis of abdominal lymph nodes with rim enhancement also raises suspicion of ATB (12,22). This contrasts with CD, in that CD has uniform lesser thickening of the bowel wall and skip lesions adjacent to stricture formation (22).
Although gross endoscopic findings of intestinal TB are similar to CD, tuberculous involvement of the intestine most commonly involves the terminal ileum and cecum. The physiological stasis and the high density of lymphoid tissue in the ileocecal region create an optimal environment for infection (4–6,19). This area allows for prolonged contact between the mucosa and the AFB (6). Findings that are more suggestive of intestinal TB include: rectal sparing, linear but well-defined ulcers with surrounding erythema, inflammatory polyps, nodular friable mucosa, a severely deformed and edematous ileocecal valve, or characteristic granulomas (6,8,13). The granulomas of intestinal TB are usually large and well-defined, and commonly are located in the submucosa (23). Caseating granulomas are the hallmark of TB infection (12). However, these findings are not always present histologically, and noncaseating granulomas may be present in more than one third of patients (6,9,24). To enhance the likelihood of specific diagnostic findings, biopsies should be obtained from ulcer margins because granulomas are typically located in the submucosa (4,20,25). Multiple biopsies obtained throughout the colon also may enhance diagnostic precision (26).
Although culture remains the gold standard, it is an inefficient process requiring several weeks (9) and yields a positive result in only 45% to 70% of cases (2,10,14). Specimens that have AFB on histological stains are more likely to yield a positive culture result. Precise identification of the pathogen and subsequent susceptibilities are critical for therapeutic decisions, especially in areas of increasing mycobacterial resistance.
Polymerase chain reaction of biopsy specimens may be helpful and is more sensitive than culture (18,23). When used in conjunction with history, physical examination, radiographic findings, and TST, polymerase chain reaction may allow the correct diagnosis in a timely manner. It also may prove useful in the patient with suspected ATB who has a negative TST and inconclusive biopsy histological results.
The QuantiFERON-TB Gold test measures enzyme-linked immunosorbent assay–detected interferon-γ by combining a whole-blood specimen with synthetic proteins that are present in M tuberculosis(27). It has been shown to have similar sensitivity but improved specificity when compared with TST, and can identify latent TB in patients who have received bacille Calmette-Guérin vaccine. However, it is costly and negative results must be interpreted with caution in the immunosuppressed patient.
TREATMENT AND COMPLICATIONS
Extrapulmonary TB should be treated similarly to pulmonary TB with 4-drug therapy until susceptibility results are known (28). Steroids are an adjunct treatment of TB pericarditis and meningitis (7,29), but no convincing evidence exists regarding utility in ATB (2). Furthermore, corticosteroid therapy in the absence of appropriate antituberculous therapy can be harmful.
As treatment for CD evolves to include the use of biological therapies, it is imperative to establish an accurate diagnosis. Infliximab increases the risk of reactivating latent TB. Therefore, screening for TB with a detailed history, CXR, and TST should occur in all patients before anti-TNF therapy (30), and given our patient's course, should be considered before initiating corticosteroid therapy as well.
The typical ATB patient responds quickly to medical anti-TB therapy. If quick response is not seen, then complications or concurrent CD should be considered. Obstruction is the most common complication of intestinal TB (4). Patients who have small-bowel involvement as a part of their tuberculous disease may also develop malabsorption syndrome, necessitating parenteral nutrition and parenteral antituberculous agents (4,5).
Once a common disease, TB may have slipped from the forefront of some clinicians' thinking. This is in large part due to an improved standard of living, the advent of antituberculous therapy in the 1950s, the pasteurization of milk products, and the culling of infected cows (3). In recent years, gastrointestinal and other forms of TB have been staging a comeback (3,31), partially on the back of the HIV/AIDS epidemic and also in part due to increasing immigration from regions where TB is endemic (1,9,32,33). As we become more aware of this trend, our differential must expand to include this increasingly prevalent entity (1,2).
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