Clinical Case Report Medicine ®

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Intestinal tuberculosis in a patient with end-stage

renal disease on hemodialysis
A case report
∗
In Hee Lee, MD, PhDa, , Seong Gyu Kim, MDa, Joong Goo Kwon, MD, PhDa, Chun-Seok Yang, MDb,
Sungmin Kang, MD, PhDc, Min-Kyung Kim, MDd, Dong Jik Ahn, MDe

Abstract
Rationale: Intestinal tuberculosis (TB) is rarely seen in patients with end-stage renal disease (ESRD). We report an intestinal TB case
with a clinical presentation similar to that of colon cancer in a patient with ESRD on hemodialysis.
Patient concerns: A 49-year-old man presented with a 3-month history of general weakness and anorexia. He had been treated
for stage 5 chronic kidney disease (CKD) due to diabetic nephropathy for the last 3 years. His blood urea nitrogen and serum
creatinine levels were 96.9 and 8.1 mg/dL, respectively, at the time of admission; azotemia was accompanied by severe anemia,
hypoalbuminemia, hyperkalemia, and metabolic acidosis. Hemodialysis was initiated for suspected exacerbation of uremia; however,
intermittent fever, night sweats, and abdominal discomfort persisted.
Diagnoses: Abdominal computed tomography (CT) and whole-body 18F-fluorodeoxyglucose positron emission tomography were
indicative of ascending colon cancer with lymph node metastases. However, colonoscopy with biopsy revealed the formation of
submucosal caseating granuloma and acid-fast bacillus.
Interventions: We initiated quadruple therapy with isoniazid, rifampicin, pyrazinamide, and ethambutol. The patient continued the
quadruple regimen for the first 2 months before switching to dual therapy and received anti-TB medications for a total of 12 months.
Outcomes: After 9 months of standard anti-TB chemotherapy, polypoid residual lesions were noted during follow-up
colonoscopy. Laparoscopy-assisted ileocecal resection was performed. No findings suggestive of recurrence of colonic TB were
observed on follow-up abdominal CT at 6 months after discontinuation of anti-TB medications.
Lessons: If non-specific uremic symptoms persist in patients with advanced CKD, the possibility of extrapulmonary TB such as
intestinal TB must be considered. Also, in patients with radiologic suspicion of colon cancer, endoscopy with biopsy should be
performed promptly to exclude colonic TB with similar clinical manifestations.
Abbreviations: AFB = acid-fast bacillus, BT = body temperature, BUN = blood urea nitrogen, CKD = chronic kidney disease, Cr
= creatinine, CT = computed tomography, EMB = ethambutol, ESRD = end-stage renal disease, FDG = fluorodeoxyglucose, HPF =
high-power field, INH = isoniazid, M = mycobacterium, PCR = polymerase chain reaction, PET = positron emission tomography,
PMC = pseudomembranous colitis, PZA = pyrazinamide, RIF = rifampicin, TB = tuberculosis, TST = tuberculin skin test, WBC =
white blood cell.
Keywords: tuberculosis, end-stage renal disease, hemodialysis, colon cancer

Editor: Maya Saranathan.

Informed written consent was obtained from the patient for publication of this case report and accompanying images.
Ethical approval: This case report was approved by the institutional review board of Daegu Catholic University Medical Center (CR-19-023-PRO-001-R).
The authors have no funding and conflicts of interest to disclose.
All data generated or analyzed during this study are included in this published article [and its supplementary information files].
a
Department of Internal Medicine, b Department of General Surgery, c Department of Nuclear Medicine, Daegu Catholic University School of Medicine, Daegu,
d
Department of Pathology, Dongguk University College of Medicine, Gyeongju, e Department of Internal Medicine, HANSUNG Union Internal Medicine Clinic and
Dialysis Center, Daegu, Republic of Korea.
∗
Correspondence: In Hee Lee, Department of Internal Medicine, Daegu Catholic University School of Medicine, 17-Gil 33, Duryugongwon-ro, Nam-gu, Daegu 42472,
Republic of Korea (e-mail: [email protected]).
Copyright © 2020 the Author(s). Published by Wolters Kluwer Health, Inc.
This is an open access article distributed under the Creative Commons Attribution License 4.0 (CCBY), which permits unrestricted use, distribution, and reproduction in
any medium, provided the original work is properly cited.
How to cite this article: Lee IH, Kim SG, Kwon JG, Yang CS, Kang S, Kim MK, Ahn DJ. Intestinal tuberculosis in a patient with end-stage renal disease on
hemodialysis: A case report. Medicine 2020;99:32(e21641).
Received: 2 December 2019 / Received in final form: 11 June 2020 / Accepted: 9 July 2020
http://dx.doi.org/10.1097/MD.0000000000021641

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1. Introduction temporary catheter for suspected exacerbation of uremia.

The risk of Mycobacterium tuberculosis (M tuberculosis) Regular hemodialysis was conducted three times a week, and
infection is high in patients with chronic kidney disease (CKD) an autologous arteriovenous fistula was created on the 10th
because of suppressed cell-mediated immunity resulting from hospital day. During hemodialysis on the 14th day of hospitali-
various causes, such as advanced age, hypoalbuminemia, zation, high fever with a BT of 38.3°C was noted. With suspicion
malnutrition, uremia, and immunosuppressive therapy.[1] The of catheter-related infection, we exchanged the catheter used for
prevalence of active tuberculosis (TB) in patients with end-stage vascular access for hemodialysis and administered cefazolin (2.0
renal disease (ESRD) undergoing dialysis is 6 to 25 times higher g, three times per week) after each hemodialysis. Methicillin-
than that in the general population, which may increase the sensitive Staphylococcus epidermidis was isolated from blood
mortality rate of these patients.[2] Extrapulmonary TB is a disease cultures. On the 25th day of hospitalization, the patient presented
in which M tuberculosis invades many different organs other than with intermittent low-grade fever, abdominal pain, and watery
the lung parenchyma, and patients with CKD infected with M diarrhea. Polymerase chain reaction (PCR) for Clostridium
difficile toxins in stool specimens detected the toxin B-positive
tuberculosis more commonly present non-specific symptoms
because the frequency of extrapulmonary TB is higher than that strain. On the diagnosis of pseudomembranous colitis (PMC), we
of pulmonary TB.[3] Extrapulmonary TB mainly involves the discontinued the administration of cefazolin and administered
oral metronidazole (1500 mg/day). However, the patient’s
lymph nodes, bones, peritoneum, and bone marrow in patients
with ESRD, but intestinal TB has been rarely reported.[4,5] abdominal discomfort, fever (BT, 37.5–38.3°C), and night
Therefore, we report the case of a 49-year-old male patient who sweats persisted. Because the origin of fever was not clear,
abdominal computed tomography (CT) performed on the 28th
was on hemodialysis for ESRD secondary to diabetic nephropa-
thy and was misdiagnosed with colon cancer before being hospital day revealed masses with irregular walls in the proximal
confirmed as colonic TB via endoscopic biopsy. portion of the ascending colon near the ileocecal valve and
adjacent lymphadenopathy (Fig. 1A); an increase in 18F-
Fluorodeoxyglucose (FDG) uptake was also noted in the
2. Case report
corresponding region on whole-body positron emission tomog-
A 49-year-old male patient was admitted to our hospital with a 3- raphy (PET)/CT scan (Fig. 2). The radiologic diagnosis was colon
month history of general weakness and anorexia. The patient had cancer with lymph node metastases. Colonoscopy with biopsy for
been treated for stage 5 CKD secondary to diabetic nephropathy histopathologic diagnosis was performed. A fungating circum-
at the nephrology division for the last 3 years. The patient’s blood ferential mass with hypertrophic ulcerations, which mimicked a
urea nitrogen (BUN) level was 57.2 mg/dL and creatinine (Cr) colonic tumor, was found in the ascending colon (Fig. 3A).
level was 6 mg/dL at 3 months before admission, and he reported However, microscopic examination demonstrated chronic case-
worsening of uremic symptoms, such as malaise, weight loss, ating granulomatous inflammation and positive Ziehl-Neelsen
anorexia, nausea, and vomiting. After his diagnosis of type 2 stain for acid-fast bacillus (AFB), consistent with colonic TB
diabetes mellitus 20 years before admission, the patient was on (Fig. 4A and B). PCR analysis of the colonic lesions was negative
combination therapy including oral hypoglycemic agents and for M. tuberculosis. The patient’s tuberculin skin test (TST) result
insulin. He had no past history of pulmonary TB and viral was also negative, and tumor markers, such as carcinoembryonic
hepatitis. At the time of admission, his blood pressure, pulse rate, antigen and carbohydrate antigen 19-9, were all normal. We
respiration rate, and body temperature (BT) were 109/53 mm Hg, recommended surgical intervention including hemi-colectomy in
80 beats/min, 20 breaths/min, and 37.3 °C, respectively. His view of the morphologic characteristics of the colonic lesions, but
consciousness was clear, and no murmur or crackles were the patient refused surgery. Accordingly, we initiated quadruple
detected on chest auscultation, although both conjunctivae were therapy (HRZE): isoniazid (INH; 300 mg/day), rifampicin (RIF;
pale. No signs of a mass, organomegaly, and nearby tenderness 600 mg/day), pyrazinamide (PZA; 30 mg/kg, three times per
were observed on the abdominal examination. A peripheral week), and ethambutol (EMB; 15 mg/kg, three times per week).
blood test on admission revealed the following: white blood cell The patient was discharged from the hospital on the 45th day of
(WBC) count, 7000/mL (neutrophils, 72%); hemoglobin, 5.2 g/ admission after complete resolution of systemic symptoms. Anti-
dL; platelets, 374,000/mL; and erythrocyte sedimentation rate, TB quadruple therapy was applied for the first 2 months;
44 mm/h. Serum biochemical examination revealed the follow- thereafter, it was switched to dual combination therapy (HR) of
ing: glucose, 267 mg/dL; total protein, 6.2 g/dL; albumin, 2.6 g/ INH and RIF. Three months after the administration of anti-TB
dL; BUN, 96.9 mg/dL; Cr, 8.1 mg/dL (estimated glomerular medications, follow-up colonoscopy showed improvement in
filtration rate, 8 mL/min); aspartate aminotransferase, 7 IU/L; colonic lesions. However, 9 months after the initiation of
alanine aminotransferase, 18 IU/L; Na+/K+/Cl /total CO2, 130/ quadruple therapy, a second follow-up abdominal CT and
6.0/100/14 mEq/L; calcium, 7.6 mg/dL; phosphorus, 6.2 mg/dL; colonoscopy showed polypoid residual lesions in the ascending
uric acid, 13.4 mg/dL; and C-reactive protein, 14.6 mg/L. On colon (Figs. 1B and 3B) and we conducted laparoscopy-assisted
urinalysis, 2+ was observed for albumin and 1+ for occult blood, ileocecal resection. Anti-TB chemotherapy was maintained for a
and microscopic urinary sediment evaluation revealed 1 to 3 total of 12 months. Progression of lymphadenopathy in the
WBCs per high-power field (HPF) and 3 to 5 red blood cells per abdominal cavity or recurrence of colonic TB was not noted on
HPF. Serum immunological tests showed the following: iron, follow-up abdominal CT performed at 6 months after discontin-
14 mg/dL; total iron binding capacity, 199 mg/dL; ferritin, 172 ng/ uation of anti-TB medications.
mL; and HbA1C, 8%. A 24-h urine examination revealed a
urinary protein excretion level of 1156 mg/day and Cr clearance
of 8.8 mL/min/1.73 m2. The patient’s chest radiograph did not 3. Discussion
reveal pulmonary infiltrates in either lung field. On admission, As renal function declines, immune deficiencies deteriorate in
hemodialysis was initiated after insertion of a dual-lumen patients with CKD because of various clinical factors, such as

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Figure 1. Abdominal computed tomography (CT) findings. (A) Initial abdominal CT scan shows a mass which is located just distal to ileocecal valve (arrows), with
the formation of adjacent multiple lymphadenopathy. (B) Abdominal CT obtained at 9 months after antituberculous chemotherapy shows marked resolution of
colonic tuberculosis (arrow). CT = computed tomography.

oxidative stress, chronic inflammation, 25(OH)-vitamin D anorexia, vomiting, and chronic anemia, were also often
deficiency, malnutrition, and secondary hyperparathyroidism.[6] reported.[9]
In particular, patients with CKD have a higher TB risk, increased Gastrointestinal TB comprises 3% to 5% of the total
reactivation of latent TB, and worse progression of active TB than extrapulmonary TB cases in the general population,[10] but
the general population owing to the impairment of the cell- intestinal TB is rare in patients with CKD.[5] Intestinal TB can be
mediated immune system, which is involved in eliminating caused by the reactivation of a primary infection. In addition,
intracellular microorganisms such as M tuberculosis.[7] Old age, patients with active pulmonary TB may develop intestinal TB
male sex, diabetes mellitus, hypoalbuminemia, low body mass through various routes, such as swallowing infected sputum,
index, chronic anemia, ischemic heart disease, and smoking have hematogenous dissemination of AFB in patients with active
been reported as significant independent risk factors for the pulmonary or miliary TB, consumption of food or milk
development of TB in patients with ESRD on hemodialysis.[8] TB contaminated with M tuberculosis, and spreading of infection
is most commonly seen at the early stage of dialysis, particularly directly from infected adjacent organs or lymph nodes.[10]
within 1 year after hemodialysis initiation, when malnutrition Intestinal TB is commonly observed in the ileocecal region, and
worsens and cell-mediated immunity greatly decreases.[7] hypertrophic lesions similar to polyps or tumors, segmental
Thereafter, the frequency of TB tends to decrease as the patient’s ulcerations, enterocolitis, and, rarely, diffuse colonic inflamma-
immunity improves with adequate dialysis therapy, although tion occur when M tuberculosis invades the gastrointestinal tract,
active TB itself is considered to be a major risk factor for which can cause the development of abdominal masses, local
increased morbidity and mortality in patients with ESRD.[7] tenderness, and abdominal distention. Chronic abdominal pain is
Because the incidence of extrapulmonary TB is as high as 60% to the most common symptom of intestinal TB, but it can also be
80% in patients with CKD, various non-specific symptoms accompanied by non-specific symptoms, such as unexplained
appear at the time of onset of TB, which may lead to delay in early fever, weight loss, nausea, vomiting, diarrhea, and bloody stools.
diagnosis and appropriate treatment.[2,3] In the analysis of 70 Therefore, it is important to make a differential diagnosis from
cases of extrapulmonary TB in patients with ESRD on other gastrointestinal diseases, such as malignant tumors,
maintenance dialysis, Yang et al reported that the mean age Crohn’s disease, intestinal lymphoma, Yersinia infection, and
was 51.4 ± 17.8 years, and the male-to-female distribution was amoebic enteritis.[11]
0.9:1. They also described that the peritoneum (31.4%) was the Our patient had been undergoing conservative management
major organ that developed extrapulmonary TB, followed by the for advanced CKD for several years and complained of general
bone, lymph nodes, bone marrow, spleen, and liver.[9] In weakness, anorexia, nausea, and vomiting at the time of
addition, fever (58.6%), pain, and lymphadenopathy were the admission. Based on the laboratory findings and the patient’s
most common clinical findings at the presentation of extrap- pre-existing diseases, hemodialysis along with a diagnosis of
ulmonary TB, but non-specific symptoms, such as weight loss, ESRD was recommended. After the initiation of hemodialysis,

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Figure 2. (A and B) 18F-fluorodeoxyglucose (FDG) positron emission tomography/computed tomography at presentation shows wall thickening with increased
18
F-FDG uptake (maximum standardized uptake value 13.55) in ascending colon and enlarged lymph nodes with increased 18F-FDG uptake (7.09) in pericolic,
aortocaval, and porta hepatis areas. FDG = fluorodeoxyglucose.

laboratory abnormalities and systemic symptoms improved, but intestinal TB cannot be excluded even if chest radiography results
fever developed 2 weeks after the start of hemodialysis. We are negative.[3] In our case, abnormal findings suggestive of
conducted empirical antimicrobial therapy for catheter-related pulmonary TB scarring or active TB lesion were not found on the
infections. Thereafter, PMC also developed; accordingly, chest radiography. PCR and TST of the patient’s colonic mucosa
metronidazole was administered orally and intravenous anti- also showed negative results. However, as formation of caseating
biotics were discontinued. However, low-grade pyrexia, night granulomas and positive results on AFB staining were identified
sweats, and abdominal discomfort continued, and ascending on microscopic examination of the colon specimen, he was
colon cancer with distant lymph node metastases was suggested diagnosed with colonic TB (Fig. 4A and B). In this patient, it was
based on the results of abdominal CT and whole-body PET/CT postulated that male sex, diabetes mellitus, chronic anemia,
(Fig. 1A, 2). When colonic disease is suspected, radiologic hypoalbuminemia, and malnutrition were significant risk factors
examinations such as barium colonography, abdominal CT, and of colonic TB. However, the definitive diagnosis of colonic TB
abdominal magnetic resonance imaging are recommended. and treatment initiation were delayed because of non-specific
However, it is not easy to confirm colonic TB with these symptoms, catheter-related bacteremia that occurred after the
studies.[10] Gross identification of intestinal lesions by colonos- initiation of hemodialysis, and PMC.
copy, microscopic analysis, and culture of the colonic tissue are For the primary treatment of intestinal TB in patients with CKD,
the most useful diagnostic procedures for colonic TB.[10] PCR standard chemotherapy, that is, quadruple therapy (HRZE) for the
analysis of intestinal mucosa is another adjunctive diagnostic first 2 months followed by dual therapy (HR) for a further period of
method for confirming TB and has been reported to be more 4 to 7 months thereafter, is recommended.[13] However,
sensitive than tissue culture or AFB staining.[10] TST is widely administration of anti-TB medications is often continued for a
used as an additional diagnostic tool for TB, but its usefulness is period longer than 9 months and, in particular, up to 12 to
limited because of immune abnormalities in patients with ESRD 18 months.[14,15] Patients with CKD are more susceptible to
undergoing dialysis.[12] Because active or past pulmonary TB is treatment failure of TB because of a higher incidence of adverse
accompanied only in 25% of patients with extrapulmonary TB, effects related to anti-TB medications and poor adherence to

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Figure 3. Colonoscopic findings. (A) Initial colonoscopy shows a large fungating circumferential mass with hypertrophic ulcerations in the ascending colon. (B)
Semi-pedunculated polypoid masses of reduced size are noted on the 9-month follow-up colonoscopy.

medications as well as immune system abnormalities. Therefore, colonic lesions was demonstrated in the follow-up colonoscopy.
adequate dosing intervals and careful follow up are required.[16,17] However, ileocecal resection was additionally performed because
Surgical intervention should be considered in addition to anti-TB residual lesions were noted in the ascending colon even after 9
drug therapy if there is bowel perforation with or without abscess months of anti-TB chemotherapy (Fig. 3B). It has been reported
or fistula, massive gastrointestinal bleeding, complete bowel that colon cancer might develop later because of chronic
obstruction, or intestinal obstruction with no response to anti- inflammation and abnormal immune responses at the site of a
TB medications.[11] There were no medication-related toxicities or previous intestinal TB lesion.[18,19] Therefore, appropriate surgical
specific side effects observed in our patient during the 12-month intervention is needed for residual lesions after completion of anti-
standard anti-TB therapy. In contrast, his systemic symptoms such TB chemotherapy.
as fever and abdominal pain were markedly resolved after the In summary, in our patient with stage 5 CKD secondary to
initiation of anti-TB medications, and gradual improvement in diabetic nephropathy, hemodialysis was initiated for suspected

Figure 4. Microscopic features of colon specimen. (A) Hematoxylin and eosin stain shows confluent granulomatous inflammation with caseous necrosis below
muscularis mucosa. Lymphocyte cuffing around the granulomas is also seen (100). (B) Acid-fast bacillus stain demonstrates mycobacterium as a red rod (arrow)
in the interface of caseous necrosis and viable cells (400).

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exacerbation of uremia. Colon cancer with lymph node [5] Siu YP, Tong MK, Kwok YL, et al. An unusual case of both upper and
lower gastrointestinal bleeding in a kidney transplant recipient. Transpl
metastases was suggested in the radiologic examinations, but
Infect Dis 2008;10:276–9.
colonic TB was documented by colonoscopic biopsy. In addition, [6] Romanowski K, Clark EG, Levin A, et al. Tuberculosis and chronic
our patient was treated with standard anti-TB chemotherapy for kidney disease: an emerging global syndemic. Kidney Int 2016;90:34–40.
12 months and underwent ileocecal resection. Based on the [7] Hussein MM, Mooij JM, Roujouleh H. Tuberculosis and chronic renal
findings of this case, if non-specific uremic symptoms persist in disease. Semin Dial 2003;16:38–44.
[8] Li SY, Chen TJ, Chung KW, et al. Mycobacterium tuberculosis infection
patients with advanced CKD, the possibility of extrapulmonary of end-stage renal disease patients in Taiwan: a nationwide longitudinal
TB must be considered in addition to conducting dialysis therapy. study. Clin Microbiol Infect 2011;17:1646–52.
Also, in patients with radiologic suspicion of colon cancer, [9] Yang WF, Han F, Zhang XH, et al. Extra-pulmonary tuberculosis
endoscopy with biopsy should be performed promptly to exclude infection in the dialysis patients with end stage renal disease: case reports
and literature review. J Zhejiang Univ Sci B 2013;14:76–82.
colonic TB with similar clinical manifestations.
[10] Donoghue HD, Holton J. Intestinal tuberculosis. Curr Opin Infect Dis
2009;22:490–6.
[11] Weledji EP, Pokam BT. Abdominal tuberculosis: Is there a role for
Author contributions
surgery? World J Gastrointest Surg 2017;27:174–81.
Conceptualization: In Hee Lee. [12] Giouleme O, Paschos P, Katsaros M, et al. Intestinal tuberculosis: a
diagnostic challenge—case report and review of the literature. Eur J
Data curation: Joong Goo Kwon, Chun-Seok Yang, Sungmin
Gastroenterol Hepatol 2011;23:1074–7.
Kang. [13] Milburn H, Ashman N, et al. British Thoracic Society Standards of Care
Formal analysis: In Hee Lee. Committee and Joint Tuberculosis CommitteeGuidelines for the
Methodology: In Hee Lee, Seong Gyu Kim. prevention and management of Mycobacterium tuberculosis infection
Validation: Min-Kyung Kim, Dong Jik Ahn. and disease in adult patients with chronic kidney disease. Thorax
2010;65:557–70.
Writing – original draft: In Hee Lee, Seong Gyu Kim. [14] Sharma MP, Bhatia V. Abdominal tuberculosis. Indian J Med Res
Writing – review & editing: In Hee Lee. 2004;120:305–15.
In Hee Lee orcid: 0000-0003-3562-7586. [15] Debi U, Ravisankar V, Prasad KK, et al. Abdominal tuberculosis of
the gastrointestinal tract: revisited. World J Gastroenterol 2014;
20:14831–40.
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[3] Chong VH, Lim KS. Gastrointestinal tuberculosis. Singapore Med J associated with intestinal tuberculosis, and an analysis of 26 cases
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[4] Abdelrahman M, Sinha AK, Karkar A. Tuberculosis in end-stage renal [19] Falagas ME, Kouranos P, Athanassa Z, et al. Tuberculosis and
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