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Review

Prevention and treatment of tuberculosis in solid organ transplant recipients

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Pages 63-73 | Received 29 Sep 2019, Accepted 10 Dec 2019, Published online: 18 Dec 2019

References

  • Munoz P, Rodriguez C, Bouza E. Mycobacterium tuberculosis infection in recipients of solid organ transplants. Clin Infect Dis. 2005;40(4):581–587.
  • Abad CLR, Razonable RR. Mycobacterium tuberculosis after solid-organ transplantation: A review of more than 2000 cases. Clin Transplant. 2018;32:e13259.
  • Abad CLR, Deziel PJ, Razonable RR. Treatment of latent TB infection and the risk of tuberculosis after solid organ transplantation: comprehensive review. Transpl Infect Dis. 2019 Sep 21:e13178.
  • Abad CLR, Razonable RR. Donor derived mycobacterium tuberculosis infection after solid-organ transplantation: A comprehensive review. Transpl Infect Dis. 2018;20(5):e12971.
  • Frieden TR, Sterling TR, Munsiff SS, et al. Tuberculosis. Lancet. 2003;362(9387):887–899.
  • Hill PC, Brookes RH, Fox A, et al. Large-scale evaluation of enzyme-linked immunospot assay and skin test for diagnosis of mycobacterium tuberculosis infection against a gradient of exposure in The Gambia. Clin Infect Dis. 2004;38(7):966–973.
  • Mathema B, Kurepina N, Fallows D, et al. Lessons from molecular epidemiology and comparative genomics. Semin Respir Crit Care Med. 2008;29(5):467–480.
  • Ahmad S. Pathogenesis, immunology, and diagnosis of latent mycobacterium tuberculosis infection. Clin Dev Immunol. 2011;814943:2011.
  • Marks GB, Bai J, Simpson SE, et al. Incidence of tuberculosis among a cohort of tuberculin-positive refugees in Australia: reappraising the estimates of risk. Am J Respir Crit Care Med. 2000;162(5):1851–1854.
  • Trauer JM, Moyo N, Tay EL, et al. Risk of active tuberculosis in the five years following infection … 15%? Chest. 2016;149(2):516–525.
  • Fox G, Barry S, Britton W, et al. Contact investigation for tuberculosis: a systematic review and meta-analysis. Eur Respir J. 2015;46(2):578.
  • Munoz L, Prevention SM. Management of tuberculosis in transplant recipients: from guidelines to clinical practice. Transplantation. 2016;100(9):1840–1852.
  • Subramanian AK, Theodoropoulos NM. Mycobacterium tuberculosis infections in solid organ transplantation: guidelines from the infectious diseases community of practice of the american society of transplantation. Clin Transplant. 2019;e13513.
  • Aguado JM, Torre-Cisneros J, Fortun J, et al. 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.
  • Benito N, Sued O, Moreno A, et al. Diagnosis and treatment of latent tuberculosis infection in liver transplant recipients in an endemic area. Transplantation. 2002;74(10):1381–1386.
  • Aguado JM, Silva JT, Samanta P, et al. Transplantation. Microbiol Spectr. 2016;4:6.
  • Currie AC, Knight SR, Morris PJ. Tuberculosis in renal transplant recipients: the evidence for prophylaxis. Transplantation. 2010;90(7):695–704.
  • Holty JE, Gould MK, Meinke L, et al. Tuberculosis in liver transplant recipients: a systematic review and meta-analysis of individual patient data. Liver Transpl. 2009;15(8):894–906.
  • Agoglia L, Balbi E, Halpern M, et al. Tuberculosis in liver transplant recipients: prophylaxis in an endemic area. Transplant Proc. 2011;43(1):199–202.
  • Al-Mukhaini SM, Al-Eid H, Alduraibi F, et al. Mycobacterium tuberculosis in solid organ transplantation: incidence before and after expanded isoniazid prophylaxis. Ann Saudi Med. 2017;37(2):138–143.
  • Apaydin S, Altiparmak MR, Serdengecti K, et al. Mycobacterium tuberculosis infections after renal transplantation. Scand J Infect Dis. 2000;32(5):501–505.
  • Bravo C, Roldan J, Roman A, et al. Tuberculosis in lung transplant recipients. Transplantation. 2005;79(1):59–64.
  • Chaparro SV, Montoya JG, Keeffe EB, Rhee JT, Small PM. Risk of tuberculosis in tuberculin skin test-positive liver transplant patients. Clin Infect Dis. 1999;29(1):207–208.
  • Costa JM, Meyers AM, Botha JR, et al. Mycobacterial infections in recipients of kidney allografts. A seventeen-year experience. Acta Med Port. 1988;1(1):51–57.
  • de Lemos AS, Vieira MA, Halpern M, et al. Results of implementation of preventive recommendations for tuberculosis after renal transplantation in an endemic area. Am J Transplant. 2013;13(12):3230–3235.
  • Edathodu J, Varghese B, Alrajhi AA, et al. Diagnostic potential of interferon-gamma release assay to detect latent tuberculosis infection in kidney transplant recipients. Transpl Infect Dis. 2017;19:2.
  • Fabrega E, Sampedro B, Cabezas J, et al. Chemoprophylaxis with isoniazid in liver transplant recipients. Liver Transpl. 2012;18(9):1110–1117.
  • Ghafari A, Makhdoomi K, Ahmadpoor P, et al. Tuberculosis in Iranian kidney transplant recipients: a single-center experience. Transplant Proc. 2007;39(4):1008–1011.
  • Gras J, De Castro N, Montlahuc C, et al. Clinical characteristics, risk factors, and outcome of tuberculosis in kidney transplant recipients: A multicentric case-control study in a low-endemic area. Transpl Infect Dis. 2018;20(5):e12943.
  • Guida JP, Bignotto Rosane D, Urbini-Santos C, et al. Tuberculosis in renal transplant recipients: a Brazilian center registry. Transplant Proc. 2009;41(3):883–884.
  • Higgins RM, Cahn AP, Porter D, et al. Mycobacterial infections after renal transplantation. Q J Med. 1991;78(286):145–153.
  • Higgins RSD, Kusne S, Reyes J, et al. Mycobacterium tuberculosis after liver transplantation management and guidelines for prevention. Clin Transplant. 1992;6:81–90.
  • Higuita LM, Nieto-Rios JF, Daguer-Gonzalez S, et al. Tuberculosis in renal transplant patients: the experience of a single center in Medellin-Colombia, 2005-2013. J Bras Nefrol. 2014;36(4):512–518.
  • Jafri SM, Singal AG, Kaul D, et al. Detection and management of latent tuberculosis in liver transplant patients. Liver Transpl. 2011;17(3):306–314.
  • Jahng AW, Tran T, Bui L, et al. Safety of treatment of latent tuberculosis infection in compensated cirrhotic patients during transplant candidacy period. Transplantation. 2007;83(12):1557–1562.
  • Jeong JC, Koo TY, Jeon HJ, et al. Utility of QuantiFERON-TB assay for prediction of tuberculosis development in kidney transplant patients in an intermediate-tuberculosis-burden country: lack of evidence for enhanced prediction for short-term tuberculosis development. Transplant Proc. 2014;46(2):583–587.
  • Kim JS, Cho JH, Park GY, et al. Comparison of QuantiFERON-TB gold with tuberculin skin test for detection of latent tuberculosis infection before kidney transplantation. Transplant Proc. 2013;45(8):2899–2902.
  • Kim SH, Lee SO, Park JB, et al. A prospective longitudinal study evaluating the usefulness of a T-cell-based assay for latent tuberculosis infection in kidney transplant recipients. Am J Transplant. 2011;11(9):1927–1935.
  • Liu J, Yan J, Wan Q, et al. The risk factors for tuberculosis in liver or kidney transplant recipients. BMC Infect Dis. 2014;14:387.
  • Matuck TA, Brasil P, Alvarenga Mde F, et al. Tuberculosis in renal transplants in Rio de Janeiro. Transplant Proc. 2004;36(4):905–906.
  • Meinerz G, da Silva CK, Goldani JC, et al. Epidemiology of tuberculosis after kidney transplantation in a developing country. Transpl Infect Dis. 2016;18(2):176–182.
  • Moon HH, Park SY, Kim JM, et al. Isoniazid prophylaxis for latent tuberculosis infections in liver transplant recipients in a tuberculosis-endemic area. Ann Transplant. 2017;22:338–345.
  • Olithselvan A, Rajagopala S, Vij M, et al. Tuberculosis in liver transplant recipients: experience of a South Indian liver transplant center. Liver Transpl. 2014;20(8):960–966.
  • de Castilla DL, Rakita RM, Spitters CE, et al. Short-course isoniazid plus rifapentine directly observed therapy for latent tuberculosis in solid-organ transplant candidates. Transplantation. 2014;97(2):206–211.
  • Guirao-Arrabal E, Santos F, Redel J, et al. Efficacy and safety of short-term treatment with isoniazid and rifampicin for latent tuberculosis infection in lung transplant candidates. Clin Transplant. 2017;31:3.
  • Knoll BM, Nog R, Wu Y, et al. Three months of weekly rifapentine plus isoniazid for latent tuberculosis treatment in solid organ transplant candidates. Infection. 2017;45(3):335–339.
  • Rafiei N, Williams J, Mulley WR, et al. Mycobacterium tuberculosis: active disease and latent infection in a renal transplant cohort. Nephrology (Carlton). 2019;24(5):569–574.
  • Roman A, Bravo C, Levy G, et al. Isoniazid prophylaxis in lung transplantation. J Heart Lung Transplant. 2000;19(9):903–906.
  • Sayiner A, Ece T, Duman S, et al. Tuberculosis in renal transplant recipients. Transplantation. 1999;68(9):1268–1271.
  • Sgarabotto D, Fasolato S, Vianello F, et al. Antibiotic prophylaxis for preventing postorthotopic liver transplant tuberculosis: is there a safe alternative to isoniazid? Transpl Int. 2017;30(7):734–736.
  • Sherkat R, Yaran M, Shoaie P, et al. Concordance of the tuberculin skin test and T-SPOT((R)).TB test results in kidney transplant candidates. J Res Med Sci. 2014;19(Suppl1):S26–29.
  • Sidhu A, Verma G, Humar A, et al. Outcome of latent tuberculosis infection in solid organ transplant recipients over a 10-year period. Transplantation. 2014;98(6):671–675.
  • Simkins J, Abbo LM, Camargo JF, et al. Twelve-week rifapentine plus isoniazid versus 9-month isoniazid for the treatment of latent tuberculosis in renal transplant candidates. Transplantation. 2017;101(6):1468–1472.
  • Spence RK, Dafoe DC, Rabin G, et al. Mycobacterial infections in renal allograft recipients. Arch Surg. 1983;118(3):356–359.
  • Stucchi RS, Boin IF, Angerami RN, et al. Is isoniazid safe for liver transplant candidates with latent tuberculosis? Transplant Proc. 2012;44(8):2406–2410.
  • Theodoropoulos N, Lanternier F, Rassiwala J, et al. Use of the QuantiFERON-TB gold interferon-gamma release assay for screening transplant candidates: a single-center retrospective study. Transpl Infect Dis. 2012;14(1):1–8.
  • Yildiz A, Sever MS, Turkmen A, et al. Tuberculosis after renal transplantation: experience of one Turkish centre. Nephrol Dial Transplant. 1998;13(7):1872–1875.
  • Tien V, Robilotti E, Callister D, et al. Tolerability of fluoroquinolones in management of latent tuberculosis in liver transplant candidates. Clin Infect Dis. 2015;61(10):1631–1632.
  • Agarwal SK, Gupta S, Dash SC, et al. Prospective randomised trial of isoniazid prophylaxis in renal transplant recipient. Int Urol Nephrol. 2004;36(3):425–431.
  • John GT, Thomas PP, Thomas M, et al. A double-blind randomized controlled trial of primary isoniazid prophylaxis in dialysis and transplant patients. Transplantation. 1994;57(11):1683–1684.
  • Kim SH, Lee SO, Park IA, et al. Isoniazid treatment to prevent TB in kidney and pancreas transplant recipients based on an interferon-gamma-releasing assay: an exploratory randomized controlled trial. J Antimicrob Chemother. 2015;70(5):1567–1572.
  • Naqvi R, Naqvi A, Akhtar S, et al. Use of isoniazid chemoprophylaxis in renal transplant recipients. Nephrol Dial Transplant. 2010;25(2):634–637.
  • Torre-Cisneros J, San-Juan R, Rosso-Fernandez CM, et al. Tuberculosis prophylaxis with levofloxacin in liver transplant patients is associated with a high incidence of tenosynovitis: safety analysis of a multicenter randomized trial. Clin Infect Dis. 2015;60(11):1642–1649.
  • Vikrant S, Agarwal SK, Gupta S, et al. Prospective randomized control trial of isoniazid chemoprophylaxis during renal replacement therapy. Transpl Infect Dis. 2005;7(3–4):99–108.
  • Bumbacea D, Arend SM, Eyuboglu F, et al. The risk of tuberculosis in transplant candidates and recipients: a TBNET consensus statement. Eur Respir J. 2012;40(4):990–1013.
  • Isoniazid. Tuberculosis (Edinb). 2008;88(2):112–116.
  • Zhang Y. Isoniazid. In: Rom W, Garay S, editors. Tuberculosis. Philadelphia, PA: Lippincott Williams & Wilkins; 2003; 739–58.
  • Cohen-Gonsaud M, Ducasse S, Hoh F, et al. Crystal structure of MabA from mycobacterium tuberculosis, a reductase involved in long-chain fatty acid biosynthesis. J Mol Biol. 2002;320(2):249–261.
  • Abal AT, Ahmad S, Mokaddas E. Variations in the occurrence of the S315T mutation within the katG gene in isoniazid-resistant clinical mycobacterium tuberculosis isolates from Kuwait. Microb Drug Resist. 2002;8(2):99–105.
  • Hazbon MH, Brimacombe M, Bobadilla Del Valle M, et al. Population genetics study of isoniazid resistance mutations and evolution of multidrug-resistant mycobacterium tuberculosis. Antimicrob Agents Chemother. 2006;50(8):2640–2649.
  • Mokrousov I, Narvskaya O, Otten T, et al. High prevalence of KatG Ser315Thr substitution among isoniazid-resistant mycobacterium tuberculosis clinical isolates from northwestern Russia, 1996 to 2001. Antimicrob Agents Chemother. 2002;46(5):1417–1424.
  • Ramaswamy SV, Reich R, Dou SJ, et al. Single nucleotide polymorphisms in genes associated with isoniazid resistance in mycobacterium tuberculosis. Antimicrob Agents Chemother. 2003;47(4):1241–1250.
  • Silva MS, Senna SG, Ribeiro MO, et al. Mutations in katG, inhA, and ahpC genes of Brazilian isoniazid-resistant isolates of mycobacterium tuberculosis. J Clin Microbiol. 2003;41(9):4471–4474.
  • Wehrli W, Knusel F, Schmid K, et al. Interaction of rifamycin with bacterial RNA polymerase. Proc Natl Acad Sci U S A. 1968;61(2):667–673.
  • Huitric E, Werngren J, Jureen P, et al. Resistance levels and rpoB gene mutations among in vitro-selected rifampin-resistant mycobacterium tuberculosis mutants. Antimicrob Agents Chemother. 2006;50(8):2860–2862.
  • Mitchison DA. Role of individual drugs in the chemotherapy of tuberculosis. Int J Tuberc Lung Dis. 2000;4(9):796–806.
  • Rifabutin. Tuberculosis (Edinb). 2008;88(2):145–147.
  • Burman WJ, Gallicano K, Peloquin C. Comparative pharmacokinetics and pharmacodynamics of the rifamycin antibacterials. Clin Pharmacokinet. 2001;40(5):327–341.
  • Schechter M, Zajdenverg R, Falco G, et al. Weekly rifapentine/isoniazid or daily rifampin/pyrazinamide for latent tuberculosis in household contacts. Am J Respir Crit Care Med. 2006;173(8):922–926.
  • Bemer-Melchior P, Bryskier A, Drugeon HB. Comparison of the in vitro activities of rifapentine and rifampicin against mycobacterium tuberculosis complex. J Antimicrob Chemother. 2000;46(4):571–576.
  • Kunin CM. Antimicrobial activity of rifabutin. Clin Infect Dis. 1996;22(Suppl 1):S3-13; discussion S13-14.
  • Schaberg T, Rebhan K, Lode H. Risk factors for side-effects of isoniazid, rifampin and pyrazinamide in patients hospitalized for pulmonary tuberculosis. Eur Respir J. 1996;9(10):2026–2030.
  • Vernon A. Rifamycin antibiotics, with a focus on newer agents. In: Rom W, Garay S, editors. Tuberculosis. Philadelphia, PA Lippincott Williams & Wilkins; 2003;759–71
  • Zhang Y, Wade MM, Scorpio A, et al. Mode of action of pyrazinamide: disruption of mycobacterium tuberculosis membrane transport and energetics by pyrazinoic acid. J Antimicrob Chemother. 2003;52(5):790–795.
  • Pyrazinamide. Tuberculosis (Edinb). 2008;88(2):141–144.
  • Chan E. Pyrazinamide, ethambutol, ethionamide and aminoglycosides. In: Rom W, Garay S, editors. Tuberculosis. Philadelphia, PA: Lippincott Williams & Wilkins; 2003; 773–89
  • Peloquin CA, Bulpitt AE, Jaresko GS, et al. Pharmacokinetics of ethambutol under fasting conditions, with food, and with antacids. Antimicrob Agents Chemother. 1999;43(3):568–572.
  • Lewinsohn DM, Leonard MK, LoBue PA, et al. Official American thoracic society/infectious diseases society of America/centers for disease control and prevention clinical practice guidelines: diagnosis of tuberculosis in adults and children. Clin Infect Dis. 2017;64(2):111–115.
  • Levofloxacin. Tuberculosis (Edinb). 2008;88(2):119–121.
  • Streptomycin. Tuberculosis (Edinb). 2008;88(2):162–163.
  • Para-aminosalicylic acid. Tuberculosis (Edinb). 2008;88(2):137–138.
  • Linezolid. Tuberculosis (Edinb). 2008;88(2):122–125.
  • Ethionamide. Tuberculosis (Edinb). 2008;88(2):106–108.
  • Cycloserine. Tuberculosis (Edinb). 2008;88(2):100–101.
  • Zumla A, Nahid P, Cole ST. Advances in the development of new tuberculosis drugs and treatment regimens. Nat Rev Drug Discov. 2013;12(5):388–404.
  • Koul A, Vranckx L, Dendouga N, et al. Diarylquinolines are bactericidal for dormant mycobacteria as a result of disturbed ATP homeostasis. J Biol Chem. 2008;283(37):25273–25280.
  • Rao SP, Alonso S, Rand L, et al. The protonmotive force is required for maintaining ATP homeostasis and viability of hypoxic, nonreplicating mycobacterium tuberculosis. Proc Natl Acad Sci U S A. 2008;105(33):11945–11950.
  • Diacon AH, Pym A, Grobusch M, et al. The diarylquinoline TMC207 for multidrug-resistant tuberculosis. N Engl J Med. 2009;360(23):2397–2405.
  • Veziris N, Ibrahim M, Lounis N, et al. A once-weekly R207910-containing regimen exceeds activity of the standard daily regimen in murine tuberculosis. Am J Respir Crit Care Med. 2009;179(1):75–79.
  • Lounis N, Gevers T, Van Den Berg J, et al. Prevention of drug carryover effects in studies assessing antimycobacterial efficacy of TMC207. J Clin Microbiol. 2008;46(7):2212–2215.
  • Cohen J. Infectious disease. Approval of novel TB drug celebrated–with restraint. Science. 2013;339(6116):130.
  • Matsumoto M, Hashizume H, Tomishige T, et al. OPC-67683, a nitro-dihydro-imidazooxazole derivative with promising action against tuberculosis in vitro and in mice. PLoS Med. 2006;3(11):e466.
  • Gler MT, Skripconoka V, Sanchez-Garavito E, et al. Delamanid for multidrug-resistant pulmonary tuberculosis. N Engl J Med. 2012;366(23):2151–2160.
  • Makarov V, Manina G, Mikusova K, et al. Benzothiazinones kill mycobacterium tuberculosis by blocking arabinan synthesis. Science. 2009;324(5928):801–804.
  • Pasca MR, Degiacomi G, Ribeiro AL, et al. Clinical isolates of mycobacterium tuberculosis in four European hospitals are uniformly susceptible to benzothiazinones. Antimicrob Agents Chemother. 2010;54(4):1616–1618.
  • Lechartier B, Hartkoorn RC, Cole ST. In vitro combination studies of benzothiazinone lead compound BTZ043 against mycobacterium tuberculosis. Antimicrob Agents Chemother. 2012;56(11):5790–5793.
  • Ahmad S. New approaches in the diagnosis and treatment of latent tuberculosis infection. Respir Res. 2010;11:169.
  • Getahun H, Matteelli A, Abubakar I, et al. Management of latent mycobacterium tuberculosis infection: WHO guidelines for low tuberculosis burden countries. Eur Respir J. 2015;46(6):1563–1576.
  • Torre-Cisneros J, Doblas A, Aguado JM, et al. 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(12):1657–1665.
  • Meyers BR, Halpern M, Sheiner P, et al. Acute hepatic failure in seven patients after prophylaxis and therapy with antituberculous agents. Successful treatment with orthotopic liver transplantation. Transplantation. 1994;58(3):372–377.
  • Meyers BR, Papanicolaou GA, Sheiner P, et al. Tuberculosis in orthotopic liver transplant patients: increased toxicity of recommended agents; cure of disseminated infection with nonconventional regimens. Transplantation. 2000;69(1):64–69.
  • Singh N, Paterson DL. Mycobacterium tuberculosis infection in solid-organ transplant recipients: impact and implications for management. Clin Infect Dis. 1998;27(5):1266–1277.
  • Menzies D, Adjobimey M, Ruslami R, et al. Four months of rifampin or nine months of isoniazid for latent tuberculosis in adults. N Engl J Med. 2018;379(5):440–453.
  • Page KR, Sifakis F, Montes de Oca R, et al. Improved adherence and less toxicity with rifampin vs isoniazid for treatment of latent tuberculosis: a retrospective study. Arch Intern Med. 2006;166(17):1863–1870.
  • Grim SA, Layden JE, Roth P, et al. Latent tuberculosis in kidney and liver transplant patients: a review of treatment practices and outcomes. Transpl Infect Dis. 2015;17(5):768–777.
  • Geijo MP, Herranz CR, Vano D, et al. Short-course isoniazid and rifampin compared with isoniazid for latent tuberculosis infection: a randomized clinical trial. Enferm Infecc Microbiol Clin. 2007;25(5):300–304.
  • Martinez Alfaro E, Solera J, Serna E, et al. Compliance, tolerance and effectiveness of a short chemoprophylaxis regimen for the treatment of tuberculosis. Med Clin (Barc). 1998;111(11):401–404.
  • Martinson NA, Barnes GL, Moulton LH, et al. New regimens to prevent tuberculosis in adults with HIV infection. N Engl J Med. 2011;365(1):11–20.
  • Rivero A, Lopez-Cortes L, Castillo R, et al. Randomized clinical trial investigating three chemoprophylaxis regimens for latent tuberculosis infection in HIV-infected patients. Enferm Infecc Microbiol Clin. 2007;25(5):305–310.
  • Chang KC, Leung CC, Yew WW, et al. Dosing schedules of 6-month regimens and relapse for pulmonary tuberculosis. Am J Respir Crit Care Med. 2006;174(10):1153–1158.
  • Lange C, Abubakar I, Alffenaar JW, et al. Management of patients with multidrug-resistant/extensively drug-resistant tuberculosis in Europe: a TBNET consensus statement. Eur Respir J. 2014;44(1):23–63.
  • WHO consolidated guidelines on drug-resistant tuberculosis treatment. Geneva: World Health Organization; 2019. Licence: CC BY-NC-SA 3.0 IGO. (Ed.^(Eds).
  • Huaman MA, Brawley R, Ashkin D. Multidrug-resistant tuberculosis in transplant recipients: case report and review of the literature. Transpl Infect Dis. 2017;19:2.
  • Meije Y, Piersimoni C, Torre-Cisneros J, et al. Mycobacterial infections in solid organ transplant recipients. Clin Microbiol Infect. 2014;20(Suppl 7):89–101.

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