Open Access
Open Peer Review

This article has Open Peer Review reports available.

How does Open Peer Review work?

The risk factors for tuberculosis in liver or kidney transplant recipients

BMC Infectious Diseases201414:387

DOI: 10.1186/1471-2334-14-387

Received: 4 March 2014

Accepted: 3 July 2014

Published: 11 July 2014

Abstract

Background

Liver or kidney transplant recipients are at a higher risk of developing tuberculosis (TB) than general population. We aimed to clarify the incidence density of and risk factors for TB in liver or kidney transplant recipients in the present study.

Methods

All patients with TB following liver or kidney transplantation were investigated retrospectively at the Third Xiangya Hospital, Central South University, Changsha, China. The incidence density of TB was calculated. We performed a nested case–control study (1:1) to investigate by univariate and multivariate logistic regression analysis the potential risk factors for TB.

Results

From January 2000 to August 2013, 1748 kidney and 166 liver transplant recipients were performed at a university teaching hospital. Among the 1914 recipients, 45 cases (2.4%) of TB were reported. The incidence density was 506 cases per 105 patient-years in kidney or liver transplant recipients, which was 7 times higher than in the general Chinese population (around 70 cases per 105 person-years). The median time to develop TB was 20.0 months (interquartile ratio: 5.0-70.0). The receipt of a graft from a cadaveric donor (odds ratio [OR] = 3.7; 95% confidence interval [CI] = 1.4-10.0; P = 0.010) and the preoperative evidence of latent TB (OR = 6.8; 95% CI = 2.0-22.7; P = 0.002) were identified as two risk factors for developing TB in liver or kidney transplant recipients.

Conclusions

The incidence density of TB among liver or kidney transplant recipients was much higher than in the general Chinese population. Recipients receiving a graft from a cadaveric donor and the preoperative evidence of latent TB were two major risk factors for developing TB in liver or kidney transplant recipients.

Keywords

Tuberculosis Infection Transplantation Risk factor

Background

Tuberculosis (TB) remains a major global health problem. The incidence rate of TB among transplant recipients relies on its incidence rate in the general population. Recipients following organ transplantation are placed at a 20-74 times higher risk for developing TB than the general population [15]. TB in solid organ transplant (SOT) recipients is a challenge because of its atypical and extrapulmonary presentations, metabolic interactions between the immunosuppressive drugs and the drugs used to treat TB, the side effects from long-term treatment of TB, as well as a high mortality rate [1, 69]. Among transplant recipients, the development of TB is mainly caused by reactivation of an old dormant infection [1012]. China is one of the world’s 22 countries with the highest burden of TB and has great liver and kidney transplant activity. We aimed to clarify the incidence density of and risk factors for TB in liver or kidney transplant recipients in China in the present study.

Methods

Ethics statement

The study protocol, which included participants providing written consent prior to the study, was approved by the Third Xiangya Hospital, Central South University, Medical Ethical Committee.

Patient population and definitions

From January 2000 to August 2013, all liver or kidney transplant recipients with TB were identified using the electronic medical record system at the Third Xiangya Hospital, Central South University, Changsha, China; their clinical and demographic characteristics were carefully reviewed. A nested case-control study was then performed to reveal the association between risk factors and TB following liver or kidney transplantation.

A patient was considered to have TB if Mycobacterium tuberculosis was isolated by culture, acid-fast bacilli were present on the smear, polymerase chain reaction was positive for Mycobacterium tuberculosis, or caseating granulomas were found in histopathology [13, 14]. Patients whose TB was diagnosed and treated on the basis of clinical or radiological suspicion were excluded from the study. Old TB lesions on chest x-ray were defined as fibrotic pulmonary lesions in upper lobes or anywhere in the lung. Incidence density was calculated by the number of new cases divided by the population-time (person-years of observation) in which they occur. Controls were randomly chosen at a ratio of 1:1 from recipients who had liver or kidney transplantation not complicated by TB at the same time as the cases. Subjects in the control group were well matched to the cases with regard to gender, transplant organ type, and date of transplantation (±1 year). Clinical records of liver or kidney recipients with TB were analyzed including demographic characteristics, diabetes mellitus, etiology of renal or hepatic insufficiency, chronic hepatitis B or C virus infection, previous transplantation, pure protein derivative (PPD) skin test, transplant organ type, graft origin, immunosuppressive regimen, rejection episode within 6 months prior to TB, cytomegalovirus (CMV) infection and major infections within 3 months prior to TB, TB sites, diagnostic methods, time of TB onset, and body temperature at the onset of TB. CMV infection was defined as biopsy-proven CMV disease or reactivation with positive PCR detection of CMV DNA/positive antigen detection of PP65. Patients who entered the cohort most recently were followed up for at least 3 months after transplantation.

Statistical analysis

Results for continuous variables with a normal distribution were presented as mean ± standard deviation (SD) and compared using Student’s t-test. Chi-square analysis or Fisher’s exact test was used to compare categorical data. Discrete variables were expressed as percentages. Factors associated with TB on a univariate analysis with P < 0.05 were introduced into a multivariate logistic regression analysis. Odds ratio (OR) with 95% confidence interval (CI) was calculated to assess the association of potential risk factors with the development of TB. A two-tailed value of P < 0.05 was established as the threshold of statistical significance. Data analyses were performed with the statistical package SPSS, version 17.0 (SPSS Inc., Chicago, Illinois, USA).

Results

From January 2000 to August 2013, a total of 1914 kidney and liver transplants were performed at the Third Xiangya Hospital (1748 kidney and 166 liver transplants). Patients were followed for a median 6.2 years post-transplant (interquartile range 2.6-11.8), for a total 725 person-years of follow up. During this time 45 patients developed active TB, corresponding to an incidence density of 506 per 105 person-years. Among these 45 cases with TB, there were 34 men and 11 women; 43 received kidney transplants and 2 received liver transplants. The mean age of TB patients at transplantation was 37.9 (37.9 ± 10.0) years. Pulmonary TB was the most common form of the disease and was diagnosed in 28 patients (62.2%). The disease was disseminated in 13 (28.9%) patients. Extrapulmonary TB occurred in four (8.9%) patients (TB lymphadenitis, TB peritonitis, TB spondylitis, and tuberculocele in one patient each). The median interval from the date of transplantation to the development of TB was 20.0 months (interquartile ratio: 5.0-70.0). Of the TB cases, 17 (37.8%) appeared within the first posttransplant year. Of the 45 cases, all underwent preoperative chest x-ray, 36 PPD test, and 4 interferon gamma release assay (IGRA) test. Seventeen patients showed evidence of latent TB. Old TB lesions on chest x-ray existed in 10 patients, the PPD test result was positive for 10 patients, and IGRA test was positive for 1 patient (Table 1). Of the 45 controls, all underwent preoperative chest x-ray, 16 PPD test, and 1 IGRA test. Five showed evidence of latent TB. Screening of latent TB was, but treatment of latent TB was not, the standard of care in our setting. Thus, none of cases and controls with the present of evidence of latent TB received prophylaxis with isoniazid prior to, or in fact after transplantation. Mycobacterium tuberculosis cultures were available in 38 out of 45 cases (84.4%). Of these 38 cases, 23 had a positive culture (60.5%). Of the 45 patients with TB, 4 patients died, and of these deaths, 2 (50.0%) were due to disseminated TB.
Table 1

Main characteristics of 45 kidney or liver transplant patients with TB

Characteristics

No. (%) (n = 45)

Age, mean years ± SD

37.9 ± 10.0

Gender, number of male/number of female

34/11

Temperature of 39°C or greater

15 (33.3)

Primary kidney or liver disease, n (%)

 

 Glomerulonephritis

33 (73.3)

 Diabetes

7 (15.6)

 Adult polycystic disease

1 (2.2)

 Liver cirrhosis

2 (4.4)

 Other

2 (4.4)

Donor type, n (%)

 

 Cadaveric

32 (71.1)

 Living

12 (26.7)

 DCD

1 (2.2)

The type of transplantation, n (%)

 

 Liver

2 (4.4)

 Kidney

43(95.6)

 Two or more transplants

4 (8.9)

Immunosuppressive drugs, n (%)

 

 Methylprednisolone

45 (100)

 Prednisone

45 (100)

 Mycophenolate mofetil

44 (97.8)

 Tacrolimus

34 (75.6)

 Cyclosporine

10 (22.2)

 Sirolimus

1 (2.2)

 Antilymphocytic or antithymocytic agents

7 (15.6)

Time of TB diagnosis posttransplant, no. of cases (%)

 

 < 7 mo

13 (28.9)

 7th to 12th mo

4 (8.9)

 > 12 mo

28 (62.2)

Evidence of latent TB (No. of positive test/No. of patients tested)

17 (37.8)

 Untreated TB lesion in chest plain radiograph

10/40 (25.0)

 Preop PPD test positive

10/36 (27.8)

 Preop IGRA test positive

1/4 (25.0)

 Recent TB contact history

1/45 (2.2)

Type of TB, n (%)

 

 Pulmonary

28 (62.2)

 Extrapulmonary1

4 (8.9)

 Disseminated

13 (28.9)

Diagnostic modalities (No. of positive test/No.of patients tested)

 

 Culture positive

23/38 (60.5)

 Smear positive

15/36 (41.7)

 PCR positive

12/20 (60.0)

 Pathology only

3/3 (100.0)

 IGRA positive

6/30 (20.0)

 PPD positive

5/20 (25.0)

Diabetes mellitus, n (%)

7 (15.6)

Rejection within 6 months prior to TB, n (%)

15 (33.3)

CMV infection within 3 months prior to TB

18 (40)

HCV, HBV

10 (22.2)

Major infection within 3 months prior to TB

13 (28.9)

ESR at the onset of TB > 40 mm/h

18 (40.0)

Creatinine at the onset of TB > 2 mg/dl

10 (22.2)

Crude mortality

4 (8.9)

1Cases with extrapulmonary TB in 4 patients, TB lymphadenitis, TB peritonitis, TB spondylitis, and tuberculocele in 1 patient each.

TB, tuberculosis; SD, standard deviation; DCD, donation after cardiac death; PPD, pure protein derivative; IGRA, interferon gamma release assay; PCR, polymerase chain reaction; CMV, cytomegalovirus; HCV, Hepatitis C Virus; HBV, Hepatitis B Virus; ESR, Erythrocyte Sedimentation Rate.

Eighteen cases (40.0%) had CMV infection within 3 months prior to TB presentation. All 7 cases with a history of diabetes mellitus (15.6%) underwent a kidney transplant. Six cases had hepatitis B and 4 hepatitis C virus infection prior to transplantation. The general characteristics of these 45 kidney or liver transplant patients with TB were described in Table 1.

Table 2 described the clinical characteristics of kidney or liver transplant recipients with TB compared with controls using the univariate and multivariate analysis. The univariate analysis showed that CMV infection within 3 months prior to TB (P = 0.012), the receipt of a graft from a cadaveric donor (P = 0.031) and the preoperative evidence of latent TB (P = 0.003) were more frequent in the case group, but age, gender, immunosuppressive drugs received, diabetes mellitus, history of rejection or use of antilymphocytic or antithymocytic agents prior to TB, hepatitis B or C virus infection, and the occurrence of major infections prior to diagnosis of TB did not differ between cases and controls (Table 2). The potential risk factors that were consistently retained in the multiple logistic regression analysis were the receipt of a graft from a cadaveric donor (OR = 3.7; 95% CI = 1.4-10.0; P = 0.010) and the preoperative evidence of latent TB (OR = 6.8; 95% CI = 2.0-22.7; P = 0.002).
Table 2

Clinical characteristics of kidney or liver transplant recipients with TB compared with controls

Characteristics

Cases (n = 45)

Controls (n = 45)

P

Univariate analysis

   

 Age, mean years ± SD

37.9 ± 10.0

37.8 ± 10.0

0.974

 Gender, number of male/number of female

34/11

34/11

-

 Donor type, Deceased/the others

32/13

22/23

0.031

 The type of transplantation, Liver/Kidney

2/43

2/43

-

 Two or more transplants

4

4

1.000

 Tacrolimus/Cyclosporine

34/10

34/11

0.849

 Use of antilymphocytic agents

7

14

0.081

 Preoperative evidence of latent TB1

17

5

0.003

 Diabetes mellitus

7

7

1.000

 Rejection, n (%)

15

13

0.649

 CMV infection

18

5

0.012

 HCV, HBV

10

10

1.000

 Major infection2

13

16

0.499

Multivariate analysis

OR

(95% CI)

 

 Graft from a cadaveric donor

3.7

(1.4-10.0)

0.010

 Preoperative evidence of latent TB

6.8

(2.0 - 22.7)

0.002

1Including positive PPD or IGRA, untreated TB lesion on plain chest radiograph, recent TB contact history.

2Including pneumonia,bloodstream infections,urinary tract infection or intracranial infection.

TB, tuberculosis; SD, standard deviation; DCD, donation after cardiac death; CMV, cytomegalovirus; HCV, Hepatitis C Virus; HBV, Hepatitis B Virus; ESR, Erythrocyte Sedimentation Rate; OR, odds ratio; CI, confidence interval.

Discussion

TB is one of the most important opportunistic infections encountered posttransplantation [9, 11, 15, 16]. The incidence rate of TB in SOT recipients ranged from 1.2% to 15% [1]. According to the 2013 WHO global TB report, China ranks as the second among the world’s 22 high burden countries with a TB incidence around 1.4 million, and the incidence density of TB in general Chinese population was around 70 cases per 105 person-years in 2012 [17]. The incidence density of TB in our present study was 506 per 105 patient-years, indicating that a liver or kidney transplant recipient had 7-fold higher risk of developing TB than a person from the general Chinese population.

Previous studies [9, 11, 13] had demonstrated that the majority of SOT patients developed TB within 1 year of operation. In the present study, we found that less than half (37.8%) of all TB cases appeared within the first posttransplant year. The possible explanation for this result was that in the current study, the subjects with TB mainly comprised kidney transplant recipients (43 out of 45 TB cases). Kidney transplant recipients were less immunosuppressed and lived longer than other transplant recipients, which could have accounted for the later occurrence of TB in these population [9].

Pre-transplantation parameters that could predict the development of TB would be extremely valuable since the classic presentation of TB was atypical among transplant recipients. Various variables previously described in the literature as risk factors for TB include: age, racial background, blood group, diabetes mellitus, previous exposure to TB, protein-calorie malnutrition, hemodialysis for longer periods, chronic liver disease (in kidney transplant), type of transplantation and immunosuppressive agents, allograft rejection, chronic graft dysfunction, hepatitis C virus or CMV infection, and concomitant opportunistic infections [9, 11, 14, 15, 1827].

There was an understandably high rate of pre-existing positive PPD and chest x-ray changes in our study population (37.8% in cases vs. 11.1% in controls), accordant with Basiri A and colleagues [14] who reported that 64.2% of patients and 0.2% of controls had radiological evidence compatible with tuberculosis. In view of this, we would expect high rates of transmission of TB after renal or liver transplantation. Actually, an incidence 2.2% (1/45) of donor-derived transmission of TB was found in the current study, consistent with other studies [9, 28] which suggested that in American, donor-derived transmission of TB accounted for < 5% of TB cases after SOT. We found in the present study that the preoperative evidence of latent TB was an independent risk factor for posttransplant TB, similar to other studies [14, 18], but having major discrepancy from some reports [25, 29] that did not confirm the association between latent TB and risk of TB. Although some transplant centers have observed a low likelihood of the development of TB in untreated PPD-positive transplant recipients without other risk factors for TB [3, 3032], several existing guidelines made recommendations that all patients awaiting organ transplant should be screened for latent TB infection, and that patients diagnosed with latent TB infection should be ideally treated pretransplant or if time does not permit, therapy should be started or completed posttransplant [19, 3335]. Our finding highlighted the importance of treatment of latent TB infection, which was recommended by other studies [11, 29, 36, 37].

Another finding of ours was that the receipt of a graft from a cadaveric donor was independently associated with an increased risk for developing TB following liver or kidney transplantation. The reasons for this result were not clear. One possible explanation was that the remainder of the donors mainly comprised living relative donors (12 out of 13 non-cadaveric donors). Protective immunity against TB infection was a cell-mediated process [38, 39]. The ability of T-cell to inhibit the growth of mycobacteria was impaired more in patients receiving a graft from a cadaveric donor than in patients receiving a graft from a living relative donor, because more immunosuppressive agents must be administrated against acute cellular rejection. There were many other factors contributing to predisposing SOT recipients to TB, such as higher rates of cadaveric donor active or latent TB infection leading to a certain incidence rate of donor-derived transmission of TB [9, 28]. Thus, patients receiving a graft from a cadaveric donor might be at a higher risk of TB. Our study contributed to the literature by demonstrating, for the first time, that the receipt of a graft from a cadaveric donor could be a risk factor for increased TB among liver or kidney recipients. The results of this study might be useful in avoiding TB in liver or kidney transplant recipients.

In short, we found the incidence density of TB to be 7-fold higher among liver or kidney transplant recipients than among the general Chinese population. The receipt of a graft from a cadaveric donor rather than other sources of donors, and the preoperative evidence of latent TB were significant risk factors for developing TB in liver or kidney transplant recipients. Nevertheless, the small sample size and the retrospective nature of the study design were two major limitations in the present study. Clinicians should pay more attention to these risk factors and properly administer preventive therapy to improve the outcome of liver or kidney transplant recipients.

Conclusions

The incidence density of TB among liver or kidney transplant recipients was much higher than in the general Chinese population. Recipients receiving a graft from a cadaveric donor and the preoperative evidence of latent TB were two major risk factors for developing TB in liver or kidney transplant recipients.

Declarations

Acknowledgements

We would like to thank Mister Tianmu Chen for his help in performing the statistical analysis.

Authors’ Affiliations

(1)
Nursing School of Central South University
(2)
Department of Transplant Surgery, The Third Xiangya Hospital, Central South University
(3)
Nursing Department, the Third Xiangya Hospital, Central South University
(4)
Department of Internal Medicine, Thoracic Hospital of Hunan Province

References

  1. Chen CH, Lian JD, Cheng CH, Wu MJ, Lee WC, Shu KH: Mycobacterium tuberculosis infection following renal transplantation in Taiwan. Transpl Infect Dis. 2006, 8: 148-156. 10.1111/j.1399-3062.2006.00147.x.View ArticlePubMedGoogle Scholar
  2. Meyers BR, Halpern M, Sheiner P, Mendelson MH, Neibart E, Miller C: Tuberculosis in liver transplant patients. Transplantation. 1994, 58: 301-306. 10.1097/00007890-199408000-00008.View ArticlePubMedGoogle Scholar
  3. SakhujaV JV, Varma PP, Joshi K, Chugh KS: The high incidence of tuberculosis among renal transplant recipients in India. Transplantation. 1996, 61: 211-215. 10.1097/00007890-199601270-00008.View ArticleGoogle Scholar
  4. Schulman LL, Scully B, McGregor CC, Austin JH: Pulmonary tuberculosis after lung transplantation. Chest. 1997, 111: 1459-1462. 10.1378/chest.111.5.1459.View ArticlePubMedGoogle Scholar
  5. Graham JC, Kearns AM, Magee JG, El-Sheikh MF, Hudson M, Manas D, Gould FK, Orr KE, Freeman R: Tuberculosis transmitted through transplantation. J Infect. 2001, 43: 251-254. 10.1053/jinf.2000.0879.View ArticlePubMedGoogle Scholar
  6. Queipo JA, Broseta E, Santos M, Sánchez-Plumed J, Budía A, Jiménez-Cruz F: Mycobacterial infection in a series of 1261 renal transplant recipients. Clin Microbiol Infect. 2003, 9: 518-525. 10.1046/j.1469-0691.2003.00532.x.View ArticlePubMedGoogle Scholar
  7. Ergun I, Ekmekci Y, Sengul S, Kutlay S, Dede F, Canbakan B, Erbay B: Mycobacterium tuberculosis infection in renal transplant recipients. Transplant Proc. 2006, 38: 1344-1345. 10.1016/j.transproceed.2006.03.029.View ArticlePubMedGoogle Scholar
  8. Higgins RSD, Kusne S, Reyes J: Mycobacterium tuberculosis after liver transplantation: management and guidelines for prevention. Clin Transplant. 1992, 6: 81-90.Google Scholar
  9. Singh N, Paterson DL: Mycobacterium tuberculosis infection in solid-organ transplant recipients: impact and implications for management. Clin Infect Dis. 1998, 27: 1266-1277. 10.1086/514993.View ArticlePubMedGoogle Scholar
  10. Ram R, Swarnalatha G, Prasad N, Dakshinamurty KV: Tuberculosis in renal transplant recipients. Transpl Infect Dis. 2006, 9: 97-101.View ArticleGoogle Scholar
  11. Munoz P, Rodriguez C, Bouza E: Mycobacterium tuberculosis infection in recipients of solid organ transplants. Clin Infect Dis. 2005, 40: 581-587. 10.1086/427692.View ArticlePubMedGoogle Scholar
  12. Chan AC, Lo CM, Ng KK, Chan SC, Fan ST: Implications for management of Mycobacterium tuberculosis infection in adult-to-adult live donor liver transplantation. Liver Int. 2007, 27: 81-85.View ArticlePubMedGoogle Scholar
  13. Ha YE, Joo EJ, Park SY, Wi YM, Kang CI, Chung DR, Joh JW, Lee SK, Song JH, Peck KR: Tacrolimus as a risk factor for tuberculosis and outcome of treatment with rifampicin in solid organ transplant recipients. Transpl Infect Dis. 2012, 14: 626-634. 10.1111/j.1399-3062.2012.00721.x.View ArticlePubMedGoogle Scholar
  14. Basiri A, Moghaddam SM, Simforoosh N, Einollahi B, Hosseini M, Foirouzan A, Pourrezagholi F, Nafar M, Zargar MA, Pourmand G, Tara A, Mombeni H, Moradi MR, Taghizadeh A, Gholamrezaee HR, Bohlouli A, Nezhadgashti H, Amirzadehpasha A, Ahmad E, Salehipour M, Yazdani M, Nasrollahi A, Falaknazi K, Mahdavi MR, Shamsa A, Feizzadeh B, Mojahedi MJ, Oghbaee N, Azad RE, Mohammadi Z: Preliminary report of a nationwide case-control study for identifying risk factors of tuberculosis following renal transplantation. Transplant Proc. 2005, 37: 3041-3044. 10.1016/j.transproceed.2005.07.041.View ArticlePubMedGoogle Scholar
  15. Aguado JM, Herrero JA, Gavalda J, Torre-Cisneros J, Blanes M, Rufí G, Moreno A, Gurguí M, Hayek M, Lumbreras C, Cantarell C: Clinical presentation and outcome of tuberculosis in kidney, liver, and heart transplant recipients in Spain. Transplantation. 1997, 63: 1278-1286. 10.1097/00007890-199705150-00015.View ArticlePubMedGoogle Scholar
  16. Blackwell Munksgaard: Guidelines for the prevention and management of infectious complications of solid organ transplantation. Am J Transplant. 2004, 4 (Suppl 10): 37-41.Google Scholar
  17. WHO: World Health Organization: Global tuberculosis control. WHO report. 2013, Available at: http://www.who.int/tb/publications/global_report/2013/pdf/fullreport.pdf. Accessed 27 December 2013Google Scholar
  18. Benito N, Sued O, Moreno A, Horcajada JP, González J, Navasa M, Rimola A: Diagnosis and treatment of latent tuberculosis infection in liver transplant recipients in an endemic area. Transplantation. 2002, 74: 1381-1386. 10.1097/00007890-200211270-00006.View ArticlePubMedGoogle Scholar
  19. Aguado JM, Torre-Cisneros J, Fortun J, Benito N, Meije Y, Doblas A, Muñoz P: Tuberculosis in solid-organ transplant recipients: consensus statement of the group for the study of infection in transplant recipients (GESITRA) of the Spanish Society of Infectious Diseases and Clinical Microbiology. Clin Infect Dis. 2009, 48 (9): 1276-1284. 10.1086/597590.View ArticlePubMedGoogle Scholar
  20. Rubin RH: Infection In Organ Transplant Recipients. Clinical Approach to Infection in the Compromised Host. Edited by: Rubin RH, Young LS. 1994, NewYork: Plenum Medical, 573-680. 3View ArticleGoogle Scholar
  21. John GT, Shankar V, Abraham AM, Mukundan U, Thomas PP, Jacob CK: Risk factors for post-transplant tuberculosis. Kidney Int. 2001, 60: 1148-1153. 10.1046/j.1523-1755.2001.0600031148.x.View ArticlePubMedGoogle Scholar
  22. Basiri A, Hosseini-Moghaddam SM, Simforoosh N, Einollahi B, Hosseini M, Foirouzan A, Pourrezagholi F, Nafar M, Zargar MA, Pourmand G, Tara A, Mombeni H, Moradi MR, Afshar AT, Gholamrezaee HR, Bohlouli A, Nezhadgashti H, Akbarzadehpasha A, Ahmad E, Salehipour M, Yazdani M, Nasrollahi A, Oghbaee N, Azad RE, Mohammadi Z, Razzaghi Z: The risk factors and laboratory diagnostics for post renal transplant tuberculosis: a case-control, country-wide study on definitive cases. Transpl Infect Dis. 2008, 10: 231-235. 10.1111/j.1399-3062.2007.00271.x.View ArticlePubMedGoogle Scholar
  23. Lopez de Castilla D, Schluger NW: Tuberculosis following solid organ transplantation. Transpl Infect Dis. 2010, 12: 106-112. 10.1111/j.1399-3062.2009.00475.x.View ArticlePubMedGoogle Scholar
  24. Tharayil John G, Shankar V, Talaulikar G, Mathews MS, Abraham Abraham M, Punnakuzhathil Thomas P, Korula Jacob C: Epidemiology of systemic mycoses among renal-transplant recipients in India. Transplantation. 2003, 75: 1544-1551. 10.1097/01.TP.0000061610.34110.04.View ArticlePubMedGoogle Scholar
  25. Torre-Cisneros J, Doblas A, Aguado JM, San Juan R, Blanes M, Montejo M, Cervera C, Len O, Carratala J, Cisneros JM, Bou G, Muñoz P, Ramos A, Gurgui M, Borrell N, Fortún J, Moreno A, Gavalda J, Spanish Network for Research in Infectious Diseases: Tuberculosis after solid-organ transplant: incidence, risk factors, and clinical characteristics in the RESITRA (Spanish Network of Infection in Transplantation) cohort. Clin Infect Dis. 2009, 48: 1657-1665. 10.1086/599035.View ArticlePubMedGoogle Scholar
  26. Rungruanghiranya S, Ekpanyaskul C, Jirasiritum S, Nilthong C, Pipatpanawong K, Mavichak V: Tuberculosis in Thai renal transplant recipients: a 15-year experience. Transplant Proc. 2008, 40: 2376-2379. 10.1016/j.transproceed.2008.07.034.View ArticlePubMedGoogle Scholar
  27. Torres J, Aguado JM, San Juan R, Andrés A, Sierra P, López-Medrano F, Morales JM: Hepatitis C virus, an important risk factor for tuberculosis in immunocompromised: experience with kidney transplantation. Transpl Int. 2008, 21: 873-878. 10.1111/j.1432-2277.2008.00694.x.View ArticlePubMedGoogle Scholar
  28. Ison MG, Nalesnik MA: An update on donor-derived disease transmission in organ transplantation. Am J Transplant. 2011, 11: 1123-1130. 10.1111/j.1600-6143.2011.03493.x.View ArticlePubMedGoogle Scholar
  29. Subramanian A, Dorman S: Mycobacterium tuberculosis in solid organ transplant recipients. Am J Transplant. 2009, 9 (Suppl 4): S57-S62.View ArticlePubMedGoogle Scholar
  30. Qunibi WJ, Al-Sibai MB, Tasher S, Harder EJ, de Vol E, al-Furayh O, Ginn HE: Mycobacterial infection after renal transplantation: report of 14 cases and review of the literature. Q J Med. 1990, 77: 1039-1060.View ArticlePubMedGoogle Scholar
  31. Lloveras J, Peterson PK, Simmons RL, Najarian JS: Mycobacterial infections in seven cases and a review of the literature. Arch Intern Med. 1982, 142: 888-892. 10.1001/archinte.1982.00340180046010.View ArticlePubMedGoogle Scholar
  32. Lichtenstein IH, MacGregor RR: Mycobacterial infections in renal transplant recipients: report of five cases and review of literature. Rev Infect Dis. 1983, 5: 216-226. 10.1093/clinids/5.2.216.View ArticlePubMedGoogle Scholar
  33. Sidhu A, Verma G, Humar A, Kumar D: Outcome of Latent Tuberculosis Infection in Solid Organ Transplant Recipients Over a 10-Year Period. Transplantation. 2014, [Epub ahead of print]Google Scholar
  34. Blumberg HM, Burman WJ, Chaisson RE, Daley CL, Etkind SC, Friedman LN, Fujiwara P, Grzemska M, Hopewell PC, Iseman MD, Jasmer RM, Koppaka V, Menzies RI, O’Brien RJ, Reves RR, Reichman LB, Simone PM, Starke JR, Vernon AA, American Thoracic Society, Centers for Disease Control and Prevention and the Infectious Diseases Society: American Thoracic Society/Centers for Disease Control and Prevention/Infectious Diseases Society of America: treatment of tuberculosis. Am J Respir Crit Care Med. 2003, 167: 603-662.View ArticlePubMedGoogle Scholar
  35. American Thoracic Society/Centers for Disease Control and Prevention/Infectious Diseases Society of America: Controlling tuberculosis in the United States. Am J Respir Crit Care Med. 2005, 172: 1169-View ArticleGoogle Scholar
  36. Antony SJ, Ynares C, Dummer JS: Isoniazid hepatotoxicity in renal transplant recipients. Clin Transplant. 1997, 11: 34-37.PubMedGoogle Scholar
  37. John GT, Thomas PP, Thomas M, Jeyaseelan L, Jacob CK, Shastry JC: A double-blind randomized controlled trial of primary isoniazid prophylaxis in dialysis and transplant patients. Transplantation. 1994, 57: 1683-1684. 10.1097/00007890-199457110-00030.View ArticlePubMedGoogle Scholar
  38. Seitzer U, Kayser K, Höhn H, Entzian P, Wacker HH, Ploetz S, Flad HD, Gerdes J, Maeurer MJ: Reduced T-cell receptor CD3 zeta chain protein and sustained CD3epsilon expression at the site of mycobacterial infection. Immunology. 2001, 104: 269-277. 10.1046/j.1365-2567.2001.01323.x.View ArticlePubMedPubMed CentralGoogle Scholar
  39. Cohen G, Haag-Weber M, Hörl WH: Immune dysfunction in uremia. Kidney Int. 1997, 62 (Suppl 1): S79-S82.Google Scholar
  40. Pre-publication history

    1. The pre-publication history for this paper can be accessed here:http://www.biomedcentral.com/1471-2334/14/387/prepub

Copyright

© Liu et al.; licensee BioMed Central Ltd. 2014

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.