The SLCO1B1*15 haplotype associated with lower clinical outcome in Indonesian tuberculosis patients

https://doi.org/10.19106/JMedSci005001201806

Sunarto Ang(1*), Akhmad Kharis Nugroho(2), Ahmad Hamim Sadewa(3), Lukman Hakim(4), . Mustofa(5)

(1) Department of Internal Medicine, Abdul Wahab Sjahranie General Hospital, Samarinda, East Kalimantan
(2) Department of Pharmaceutics, Faculty of Pharmacy, Universitas Gadjah Mada, Yogyakarta, Indonesia
(3) Department of Biochemistry, Faculty of Medicine, Universitas Gadjah Mada, Yogyakarta, Indonesia
(4) Department of Pharmacology and Clinical Pharmacy, Faculty of Pharmacy, Universitas Gadjah Mada, Yogyakarta, Indonesia
(5) Department of Pharmacology and Therapeutic, Faculty of Medicine, Universitas Gadjah Mada, Yogyakarta, Indonesia
(*) Corresponding Author

Abstract


Rifampin is one of first-line drugs for the treatment of tuberculosis. In Indonesia nearly all
tuberculosis patients show lower rifampin plasma concentrations possibly due to genetics.
Rifampin is a substrate of the organic anion-transporting polypeptide 1B1 (OATP 1B1)
encoded by the solute carrier organic anion transporter family member 1B1 (SLCO1B1).
This study aimed to identify haplotype polymorphisms of tuberculosis drug transporters
with an impact on clinical outcome in tuberculosis patients. Thirty-six patients from Abdul
Wahab Sjahranie General Hospital, Samarinda, East Kalimantan were involved in the
study. Buffy coat from patient blood samples were tested for SLCO1B1 and SLCO1B3
polymorphisms by RFLP and ARMS PCR, whereas the clinical outcome was examined
based on the sputum conversion. The frequency of patients with SLCO1B1*15 haplotype
was 63.9%. The SLCO1B1*15 haplotype was associated with susceptibility to failure
of clinical outcome (p=0.005; RR=4.52; 95% CI: 1.22-16.64). The OATP1B1*15
haplotype revealed that the failure of clinical outcome was markedly increased compared
to the three other haplotypes. These results suggest that the SLCO1B1*15 haplotype
is an important predisposing factor for lower clinical outcome. Our data indicate that
individualized treatment should be considered for Indonesian tuberculosis patients based
on genetics characteristics of patients.


Keywords


SLCO1B1*15 haplotype; rifampin; tuberculosis; clinical outcome

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References

  1. Diacon AH, Patientia RF, Venter A, van Helden PD, Smith PJ, McIlleron H, et al. Early bactericidal activity of high-dose rifampin in patients with pulmonary tuberculosis evidenced by positive sputum smears. Antimicrob Agents Chemother 2007; 51(8):2994-96. http://dx.doi.org/10.1128/AAC.01474-06
  2. Weiner M, Benator D, Burman W, Peloquin CA, Khan A, Vernon A, et al. Association between acquired rifamycin resistance and the pharmacokinetics of rifabutin and isoniazid among patients with HIV and tuberculosis. Clin Infect Dis 2005; 40(10):1481-91. http://dx.doi.org/10.1086/429321
  3. Gumbo T, Louie A, Deziel MR, Liu W, Parsons LM, Salfinger M, et al. Concentration-dependent mycobacterium tuberculosis killing and prevention of resistance by rifampin. Antimicrob Agents Chemother 2007; 51(11):3781-8. http://dx.doi.org/10.1128/AAC.01533-06
  4. Weiner M, Peloquin C, Burman W, Luo CC, Engle M, Prihoda TJ, et al. Effects of tuberculosis, race, and human gene SLCO1B1 polymorphisms on rifampin concentrations. Antimicrob Agents Chemother 2010; 54(10):4192-200. http://dx.doi.org/10.1128/AAC.00353-10
  5. Pasipanodya JG, Srivastava S, Gumbo T. Meta-analysis of clinical studies supports the pharmacokinetic variability hypothesis for acquired drug resistance and failure of antituberculosis therapy. Clin Infect Dis 2012; 55(2):169-77. http://dx.doi.org/10.1093/cid/cis353
  6. Srivastava S, Pasipanodya JG, Meek C, Leff R, Gumbo T. Multidrug-resistant tuberculosis not due to noncompliance but to between-patient pharmacokinetic variability. J Infect Dis 2011; 204(12):1951-9. http://dx.doi.org/10.1093/infdis/jir658
  7. Ruslami R, Nijland HM, Alisjahbana B, Parwati I, van Crevel R, Aarnoutse RE. Pharmacokinetics and tolerability of a higher rifampin dose versus the standard dose in pulmonary tuberculosis patients. Antimicrob Agents Chemother 2007; 51(7):2546-51. http://dx.doi.org/10.1128/AAC.01550-06
  8. Chigutsa E, Visser ME, Swart EC, Denti P, Pushpakom S, Egan D, et al. The SLCO1B1 rs4149032 polymorphism is highly prevalent in South Africans and is associated with reduced rifampin concentrations: dosing implications. Antimicrob Agents Chemother 2011; 55(9):4122-7. http://dx.doi.org/10.1128/AAC.01833-10
  9. Vavricka SR, Van Montfoort J, Ha HR, Meier PJ, Fattinger K. Interactions of rifamycin SV and rifampicin with organic anion uptake systems of human liver. Hepatology 2002; 36(1):164-72. http://dx.doi.org/10.1053/jhep.2002.34133
  10. Tamai I, Nozawa T, Koshida M, Nezu J, Sai Y, Tsuji A. Functional characterization of human organic anion transporting polypeptide B (OATP-B) in comparison with liver-specific OATP-C. Pharm Res 2001; 18(9):1262-9. http://dx.doi.org/10.1023/A:1013077609227
  11. Ramesh K, Hemanth Kumar AK, Kannan T, Vijayalakshmi R, Sudha V, Manohar Nesakumar S, et al. SLCO1B1 gene polymorphisms do not influence plasma rifampicin concentrations in a South Indian population. Int J Tuberc Lung Dis 2016; 20(9):1231-5. http://dx.doi.org/10.5588/ijtld.15.1007
  12. Seng KY, Hee KH, Soon GH, Chew N, Khoo SH, Lee LS. Population pharmacokinetics of rifampicin and 25-deacetyl-rifampicin in healthy Asian adults. J Antimicrob Chemother 2015; 70(12):3298-306. http://dx.doi.org/10.1093/jac/dkv268
  13. Ministry of Health RoI. Indonesian Tuberculosis Treatment Guidelines [Internet]. 2014 [cited 2017 Jan 3]. Available from: http://www.tbindonesia.or.id/2015/02/11/buku-bpnptb-2014
  14. Giannakopoulou E, Ragia G, Kolovou V, Tavridou A, Tselepis AD, Elisaf M, et al. No impact of SLCO1B1 521T>C, 388A>G and 411G>A polymorphisms on response to statin therapy in the Greek population. Mol Biol Rep 2014; 41(7):4631-8. http://dx.doi.org/10.1007/s11033-014-3334-z
  15. Xu LY, He YJ, Zhang W, Deng S, Li Q, Zhang WX, et al. Organic anion transporting polypeptide-1B1 haplotypes in Chinese patients. Acta Pharmacol Sin 2007; 28(10):1693-7. http://dx.doi.org/10.1111/j.1745-7254.2007.00643.x
  16. Tsujimoto M, Hirata S, Dan Y, Ohtani H, Sawada Y. Polymorphisms and linkage disequilibrium of the OATP8 (OATP1B3) gene in Japanese subjects. Drug Metab Pharmacokinet 2006; 21(2):165-9. http://dx.doi.org/10.2133/dmpk.21.165
  17. Tirona RG, Leake BF, Merino G, Kim RB. Polymorphisms in OATP-C: identification of multiple allelic variants associated with altered transport activity among European- and African-Americans. J Biol Chem 2001; 276(38):35669-75. http://dx.doi.org/10.1074/jbc.M103792200
  18. Nozawa T, Nakajima M, Tamai I, Noda K, Nezu J, Sai Y, et al. Genetic polymorphisms of human organic anion transporters OATP-C (SLC21A6) and OATP-B (SLC21A9): allele frequencies in the Japanese population and functional analysis. J Pharmacol Exp Ther 2002; 302(2):804-13. http://dx.doi.org/10.2133/dmpk.21.165
  19. Niemi M, Schaeffeler E, Lang T, Fromm MF, Neuvonen M, Kyrklund C, et al. High plasma pravastatin concentrations are associated with single nucleotide polymorphisms and haplotypes of organic anion transporting polypeptide-C (OATP-C, SLCO1B1). Pharmacogenetics 2004; 14(7):429-40. http://dx.doi.org/10.2133/dmpk.21.165
  20. van Crevel R, Alisjahbana B, de Lange WC, Borst F, Danusantoso H, van der Meer JW, et al. Low plasma concentrations of rifampicin in tuberculosis patients in Indonesia. Int J Tuberc Lung Dis 2002; 6(6):497-502. https://doi.org/10.5588/09640569513002
  21. Kameyama Y, Yamashita K, Kobayashi K, Hosokawa M, Chiba K. Functional characterization of SLCO1B1 (OATP-C) variants, SLCO1B1*5, SLCO1B1*15 and SLCO1B1*15+C1007G, by using transient expression systems of HeLa and HEK293 cells. Pharmacogenet Genomics 2005; 15(7):513-22. https://doi.org/10.1097/01.fpc.0000170913.73780.5f
  22. Nozawa T, Minami H, Sugiura S, Tsuji A, Tamai I. Role of organic anion transporter OATP1B1 (OATP-C) in hepatic uptake of irinotecan and its active metabolite, 7-ethyl-10-hydroxycamptothecin: in vitro evidence and effect of single nucleotide polymorphisms. Drug Metab Dispos 2005; 33(3):434-9. http://dx.doi.org/10.1124/dmd.104.001909
  23. Iwai M, Suzuki H, Ieiri I, Otsubo K, Sugiyama Y. Functional analysis of single nucleotide polymorphisms of hepatic organic anion transporter OATP1B1 (OATP-C). Pharmacogenetics 2004; 14(11):749-57. https://doi.org/10.1097/00008571-200411000-00006
  24. Tirona RG, Leake BF, Wolkoff AW, Kim RB. Human organic anion transporting polypeptide-C (SLC21A6) is a major determinant of rifampin-mediated pregnane X receptor activation. J Pharmacol Exp Ther 2003; 304(1):223-8. http://dx.doi.org/10.1124/jpet.102.043026
  25. Pasipanodya JG, McIlleron H, Burger A, Wash PA, Smith P, Gumbo T. Serum drug concentrations predictive of pulmonary tuberculosis outcomes. J Infect Dis 2013; 208(9):1464-73. http://dx.doi.org/10.1093/infdis/jit352
  26. Jayaram R, Gaonkar S, Kaur P, Suresh BL, Mahesh BN, Jayashree R, et al. Pharmacokinetics-pharmacodynamics of rifampin in an aerosol infection model of tuberculosis. Antimicrob Agents Chemother 2003; 47(7):2118-24. https://doi.org/10.1128/AAC.47.7.2118-2124.2003



DOI: https://doi.org/10.19106/JMedSci005001201806

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