Extra-pulmonary tuberculosis infection in the dialysis patients with end stage renal diseases: case reports and literature review

Extra-pulmonary tuberculosis infection in the dialysis patients with end stage renal diseases: case reports and literature review first-author corresp ‡Corresponding Author ‡Corresponding Author †E-mail:chenjianghua@zju.edu.cn †E-mail:chenjianghua@zju.edu.cn chenjianghua@zju.edu.cn Kidney Disease Center, the First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou 310003, China Kidney Disease Center, the First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou 310003, China The diagnosis of extra-pulmonary tuberculosis (TB) seems relatively difficult due to the absence of specific symptoms and signs in patients on peritoneal dialysis or hemodialysis. We report four cases of extra-pulmonary tuberculosis on dialysis, with two cases on peritoneal dialysis and two cases on hemodialysis. The presentations, therapy, and outcomes of TB infection in these patients were reviewed. Otherwise, the English literature published in the PubMed database associating extra-pulmonary tuberculosis on dialysis over the last three decades is reviewed. A total of 61 studies containing 70 cases were included. The most common primary disease was diabetic nephropathy (22.86%, 16/70). The peritoneum (31.42%, 22/70), bone (21.42%, 15/70), and lymph node (20%, 14/70) were the most frequently infected. Single organ infection was common (90%, 63/70). Fever (58.57%, 41/70), pain (35.71%, 25/70), and enlarged lymph node (20%, 14/70) were the most common symptoms. Biopsy (67.14%, 47/70) and culture (40%, 28/70) provided most reliable methods for clear diagnosis of tuberculosis. The combined treatment of isoniazid, rifampicin, pyrazinamide, and ethambutol (44.29%, 31/70) was the most common therapy. The majority of patients improved (82.86%, 58/70); however, 12 cases got worse (17.14%), with 10 of them dying (14.29%). Physicians should be aware of the non-specific symptoms and location of infection, and consider tuberculosis in their differential diagnoses in dialysis patients presenting with symptoms such as fever, pain, and weight loss. Extra-pulmonary tuberculosis End stage renal disease Dialysis Introduction 1 The incidence of tuberculosis (TB) has been increasing worldwide. One in every three people in the world is infected with the tubercle bacillus bacteria (Hung et al., 2004 2004 ). Many risk factors are associated with TB, such as human immunodeficiency virus (HIV) infections, transplant recipients, substance abuse, renal insufficiency, malignancy, and low socio-economic status (Lee et al., 2009 2009 ; Li et al., 2011 2011 ). Increased TB incidence is also seen in dialysis patients (Pradhan et al., 1974 1974 ; Ates et al., 2010 2010 ). Because of cellular immunity defects, patients with end-stage renal disease (ESRD) are at increased risk of developing TB (El-Shahawy et al., 1994 1994 ; Lui et al., 2001 2001 ; 2007 2007 ; Kuno et al., 2010 2010 ). The incidence of TB in dialysis patients is 6–16 times higher than that in the general population (Kuo et al., 2001 2001 ; Verettas et al., 2006 2006 ; Borrajo et al., 2009 2009 ). However, the clinical manifestations of TB in patients on dialysis are quite non-specific (Oner-Eyuboglu et al., 1999 1999 ; Fukasawa et al., 2001 2001 ; Ko et al., 2004 2004 ), making a timely diagnosis difficult. Moreover, the infected locations are often extra-pulmonary (Tarng et al., 1998 1998 ; Nakamura et al., 2009 2009 ). Here we report four cases of extra-pulmonary TB in ESRD patients on dialysis. Three cases presented with low-grade fever, the other presented with weight loss, finally diagnosed as extra-pulmonary tuberculosis (one bone, one lymph node, and two urinary tract infections). Case Reports 1 Case 1: A 67-year-old female with ESRD due to chronic glomerulonephritis had been on continuous ambulatory peritoneal dialysis (CAPD) since October 2008. She complained of intermittent fever and back pain for more than 4 months. Her body temperature fluctuated between 38.0 and 39.0 °C, with no chills or night sweats. The laboratory tests showed that her hemoglobin (HGB) levels were 86 g/L, erythrocyte sedimentation rate (ESR) was 105 mm/h (normal <20 mm/h), and C-reactive protein (CRP) levels were 0.95 mg/dl (normal <0.8 mg/dl). The tuberculin skin test (TST) was strongly positive. Chest X-ray showed a proliferative lesion in the lower left lung. The computed tomography (CT) scan of the lumbar vertebrae demonstrated the destructive lesion in the fifth verbebrae. A presumptive diagnosis of lumbar vertebrae TB was made, and the empirically diagnostic anti-TB therapy of isoniazid (INH) and rifampin (RFP) was initiated. She showed significant improvements with no fever or lumbar pain after one month. The anti-TB treatment was given for 12 months, keeping the condition under control with no recurrence of fever or lumbar pain. The CT scan of lumbar vertebrae also showed no active TB focus. Case 2: A 46-year-old male with ESRD secondary to hypertension commenced hemodialysis (HD) in January 2010. One month later, the patient developed low-grade fever. His temperature ranged from 37.0 to 37.7 °C, at nights, with no chill or night sweats. The laboratory examination showed significant increases of ESR and CRP to 100 mm/h and 1.69 mg/dl, respectively. The serum anti-TB antibody was negative. The acid-fast bacilli were detected in the urine three times. The ultrasound of the kidneys showed no signs of obstruction. Diagnosis of urinary tract TB was made and the combined anti-TB treatment of INH, RFP, pyrazinamide (PZA), and ethambutol (EMB) was given immediately. The fever vanished after two weeks of treatment. The urine was retested one month later and no acid-fast bacilli were detected. The patient received anti-TB therapy for 12 months, keeping the condition under control with no recurrence of fever. Case 3: A 76-year-old male with ESRD due to chronic nephritis began regular HD in July 2010. The patient developed low-grade fever and no other symptoms accompanied. The body temperature fluctuated between 37.2 and 38.5 °C. Upon admission, his laboratory tests showed that HGB 71 g/L and ESR 110 mm/h. Smear of acid-fast bacilli in the urine was positive three times, confirming the diagnosis of urinary tract TB. The ultrasound of the kidneys showed no signs of obstruction. An anti-TB therapy of INH, RFP, and EMB was administered afterwards. The fever was gone after two weeks of treatment. The urine was retested one month later and no acid-fast bacilli were found. The patient remained on anti-TB treatment for 18 months, which kept the condition under control with no recurrence of fever. Case 4: A 48-year-old male with ESRD due to chronic nephritis started CAPD in March 2009. The patient complained of severe headache in May 2010, and reported significant weight loss in the recent months. The laboratory tests showed the levels of ESR and CRP increased to 85 mm/h and 2.8 mg/dl, respectively. The tumor-screening tests for the gastrointestinal tract and the hematological system were negative. Later, an enlarged lymph node was found in his neck and the biopsy showed typical pathologic changes of caseating granulomas. An anti-TB therapy of INH, RFP, and EMB was given. After three months, the patient developed numbness in his lower extremities, and subsequently discontinued treatment. The clinical characteristics of the reported four cases are summarized in Table 1 1 . HD: hemodialysis; PD: peritoneal dialysis; CGN: chronic glomerulonephritis; HTN: hypertension; CN: chronic nephritis; H: isoniazid; R: rifampicin; Z: pyrazinamide; E: ethambutol Patient No. Age (year)/sex Primary disease Dialysis/time (month) Clinical symptom Location of TB Treatment/time (month) Follow-up time (month) Outcome 1 67/F CGN PD/15 Fever, back pain Lumbar vertebrae HR/12 18 Remission 2 46/M HTN HD/1 Fever Urinary tract HRZE/12 18 Remission 3 76/M CN HD/0.5 Fever Urinary tract HRE/18 18 Remission 4 48/M CN PD/2 Weight loss Lymph node HRE/3 18 Discontinuation of therapy for side effects Review of the literature 1 The English literature published from Jan. 1, 1980 to Jan. 1, 2010, was searched in the PubMed database using the key words “dialysis” and “tuberculosis”. The article type was confined to case reports. The diagnosis of extra-pulmonary TB in dialysis population was the inclusion criteria, whether the patients were adult or children. A total of 61 studies containing 70 cases were included. The clinical characteristics of the included studies are summarized in the Tables 2 2 – 4 4 . The clinical characteristics of the different types of dialysis are summarized in the Table 5 5 . Data were analyzed using the chi square and t tests. A P -value of less than 0.05 was considered to be statistically significant. HD: hemodialysis; PD: peritoneal dialysis; DM: diabetes mellitus; CGN: chronic glomerulonephritis; HTN: hypertension; SLE: systemic lupus erythematosis; CIN: chronic interstitial nephritis; PKD: polycystic kidney disease; NS: nephrotic syndrome Values are expressed as mean±SD or n (%) n M : n F =number (male):number (female) Variation Value Age (year) 51.37±17.78 * * n M : n F 34:36 # # Time on dialysis (month) 35.78±38.12 Dialysis  HD 43 (61.43%) * *  PD 27 (38.57%) Primary disease  DM 16 (22.86%)  CGN 5 (7.14%)  HTN 3 (4.29%)  SLE 3 (4.29%)  CIN 3 (4.29%)  PKD 2 (2.86%)  NS 2 (2.86%)  Others 12 (17.14%)  Not reported 24 (34.29%) HPS: hemophagocytic syndrome; TB: tuberculosis; PCR: polymerase chain reaction; PPD: purified protein derivative Variation Case number Percentage (%) Clinical symptoms  Fever 41 58.57  Pain 25 35.71  Enlarged lymph node 14 20.00  Hypercalcemia 7 10.00  HPS 4 5.71  Painless mass 5 7.14  Increased CA125 2 2.86 Location of TB  Peritoneum 22 31.42  Bone 15 21.42  Lymph node 14 20.00  Bone marrow 4 5.71  Lung 3 4.29  Spleen 3 4.29  Liver 2 2.86  Esophagus 2 2.86  Parathyroid gland 2 2.86  Brain 2 2.86  Latent 2 2.86  Others 6 8.57 Method of diagnosis  Biopsy 47 67.14  Culture 28 40.00  Smear 21 30.00  PCR 16 22.86  PPD 17 24.29 H, INH: isoniazid; R, RFP: rifampicin; Z: pyrazinamide; E, EMB: ethambutol Variation Case number Percentage (%) Treatment  HRZE 31 44.29  HRE 12 17.14  HRZ 9 12.85  Others 5 7.14  Unknown 13 18.57 Side effect  INH 2 2.86  RFP 1 1.43  EMB 1 1.43 Outcome  Better 58 82.86  Deteriorate 12 17.14 TB: tuberculosis; HD: hemodialysis; CAPD: continuous ambulatory peritoneal dialysis; DM: diabetes mellitus; SLE: systemic lupus erythematosis; CGN: chronic glomerulonephritis; CIN: chronic interstitial nephritis Values are expressed as mean±SD n M : n F =number (male):number (female) 2 Variation 2 Case number 2 P -value HD ( n =43) CAPD ( n =27) Age (year) 54.37±17.26 * * 46.59±17.52 * * 0.038 n M : n F 23:20 # # 11:16 # # 0.299 Primary disease 0.403  DM 10 6  SLE 0 3  CGN 3 2  CIN 3 1  Others 12 6  Unknown 15 10 Location of TB 0.354  Peritoneum 4 18  Bone 11 2  Lymph node 10 4 Two cases had a history of TB. One was diagnosed with lymph-node TB based on a biopsy and had been on anti-TB therapy for nine months and five years before starting dialysis (Hung et al., 2003 2003 ). The other patient, diagnosed with pulmonary TB by chest X-ray, had been initiated on anti-TB treatment before renal transplant, but later turned to dialysis due to graft rejection (Prakash, 1999 1999 ). Although TB was found in most organs of the body, it was most frequently reported in the peritoneum, bone, and lymph node. Some relatively uncommon cases were also reported, including intestinal TB, renal TB, breast TB, and tuberculous orchitis (Peces et al., 1996 1996 ; Alper et al., 2004 2004 ; Siu et al., 2008 2008 ; Yazici et al., 2011 2011 ). Tuberculous peritonitis (TBP) ( n =22) took up the largest part of extra-pulmonary TB. Abdominal pain or discomfort was the most common clinical presentation ( n =15), followed by fever ( n =14) and cloudy dialysate ( n =8). The white blood cell (WBC) count of peritoneal dialysate ranged from 120 to 3 000/L. A predominance of neutrophils was more common in peritoneal dialysate ( n =13). Four cases reported development of hypercalcemia (Lee et al., 2002 2002 ; Wang et al., 2005 2005 ; Borrajo et al., 2009 2009 ; Kuno et al., 2010 2010 ), with three cases on HD, one case on peritoneal dialysis (PD). The condition improved with normalization of hypercalcemia after the anti-TB treatment. It was concluded that hypercalcemia can be an early sign of TBP in the absence of obvious symptoms (Lee et al., 2002 2002 ), but hypercalcemia related to dialysis should be excluded. Single organ infections were common, occurring in 90% of the patients ( n =63). The remaining seven patients were infected as follows: peritoneum with lung involvement ( n =3), lymph node with breast involvement ( n =1), lymph node with liver involvement ( n =1), lymph node with parathyroid gland involvement ( n =1), and liver with joint involvement ( n =1). Fever, pain, and enlarged lymph nodes were the most common symptoms in the different focus of extra-pulmonary TB. The non-specific symptoms such as body weight loss, anorexia, and vomit were common. Anemia was common in the patients. HBG was reported in 35 cases (50%), with a mean value of 87.91 g/L (range from 50 to 124 g/L). The inflammation indexes, CRP and ESR, significantly increased. CRP was available in 26 cases (37.14%), with a mean value of 42.86 mg/dl (range from 0.5 to 202.6 mg/dl). While for ESR, 22 cases (31.43%) were reported, with a mean value 94.82 mm/h (range from 22 to 169 mm/h). Diagnosis of TB was mainly based on the findings of positive TST, smear, culture, biopsy and polymerase chain reaction (PCR). Biopsy provided the most reliable method of diagnosis. Surgery played an important role in the process of getting a pathological examination, including laparotomy, omentectomy, parathyroidectomy, craniectomy, laminectomy, splenectomy and debridement. Positive TST, or purified protein derivative (PPD), were strong positives in four cases (Alper et al., 2004 2004 ; Ferrara et al., 2004 2004 ; Ram et al., 2007 2007 ; Yazici et al., 2011 2011 ), with a diameter of induration of 18 mm ( n =2), 21 mm ( n =1), and ulcerative ( n =1). Ascite revealed the highest positive rate in the specimen of smear (33.33%, 7/21), and culture (32.14%, 9/28). The anti-TB therapy in some cases was not clearly stated. The combined treatment of isoniazid, rifampicin, pyrazinamide, and ethambutol (HRZE) was the most common therapy for the extra-pulmonary TB. Less common treatments included HZE combined levofloxacin ( n =2), HRZ combined levofloxacin ( n =1), HRE combined streptomycin ( n =1), and RE combined streptomycin and moxifloxacin ( n =1). Four cases developed obvious side effects, including hepatitis induced by PZA ( n =1), encephalopathy caused by INH ( n =1), peripheral neuropathy induced INH ( n =1), behavioral abnormalities caused by INH ( n =1). The duration of the anti-TB medication was reported for only 12 patients with a mean of 11.25 months (range from 6 to 12 months). The majority of patients responded favorably to treatment. Twelve patients got worse, with 10 of those dying. Of the deaths, four were directly related to TB infection with three dying from TB-associated hemophagocytic syndrom (HPS) (Chien et al., 2004 2004 ; Ko et al., 2004 2004 ; Su et al., 2009 2009 ) and one dying from pulmonary and peritoneal TB (Gupta and Prakash, 2001 2001 ). The remaining six deaths were not directly related to TB infection, including acute hypoxemic respiratory failure of sepsis ( n =1), septicemia and multiorgan failure ( n =1), complications related to a sacral decubitus ulcer( n =1), bowel infarction ( n =1), and unknown unrelated illness ( n =3). Discussion 1 ESRD is a well-known aggravating factor for TB infection (Yalcinkaya et al., 1995 1995 ; Peces et al., 1996 1996 ; Chou et al., 2001 2001 ; Summers et al., 2005 2005 ). Diabetes mellitus (DM), old age, male sex, malnutrition, iron overload, and dialysis inadequacy are major risk factors for TB in dialysis patients (Ahmed et al., 2003 2003 ; Christopoulos et al., 2009 2009 ; Li et al., 2011 2011 ). According to a report by Stevenson et al. ( 2007 2007 ), patients with DM are 1.5–8.0 times more at risk to develop TB than those without DM. The opinion was divided on the issue of catheter removal in TBP cases (Ha et al., 1995 1995 ; Prakash, 1999 1999 ; Dervisoglu et al., 2006 2006 ; Borrajo Prol et al., 2009 2009 ). Some studies suggested the catheter be removed. Most of the cases ( n =13) in our study had the removal of Tenckhoff catheter when TBP occurred, while some cases showed successful treatment continuing on PD ( n =5). There is no consensus on the optimal treatment regimen for extra-pulmonary TB in patients on dialysis (Lui et al., 2001 2001 ). In patients with renal failure, adjustment of doses of anti-TB drugs is required (Fang et al., 1996 1996 ; Fang and Huang, 1997 1997 ; Lund et al., 2000 2000 ). In our study, the most common therapy was the quadruple treatment of HRZE, but the dose and duration in most cases were not recorded. The majority (82.86%, 58/70) made great improvements, while 10 cases died, with mortality of 14.29%. According to previously published studies, the only statistically significant variable predisposing to a poor prognosis of TB is treatment delay (Talwani and Horvath, 2000 2000 ; Ferrara et al., 2004 2004 ; Vadivel et al., 2006 2006 ). Physicians should keep diagnosis of TB in mind, especially when the clinical symptoms are non-specific and microbiological confirmation is difficult. In conclusion, we reported four cases of extra-pulmonary TB on dialysis, and reviewed the English literature associating TB on dialysis over the last three decades. Physicians should be aware of the non-specific symptoms and location of infection, and consider TB in their differential diagnoses in dialysis patients presenting with symptoms such as fever, pain, and weight loss. References W Ahmed , PB Rylance , MA Jackson , JC Nicholas , J Odum . A diabetic haemodialysis patient with dysphagia and weight loss . 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