Dose-dependent effect of daptomycin on the artificial prolongation of prothrombin time in coagulation abnormalities: in vitro verification

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1 Hshimoto et l. BMC Phrmcology nd Toxicology (2017) 18:74 DOI /s RESEARCH ARTICLE Open Access Dose-dependent effect of dptomycin on the rtificil prolongtion of prothrombin time in cogultion bnormlities: in vitro verifiction Hideki Hshimoto 1,2, Mkoto Sito 1, Noki Knd 2, Tkehito Ymmoto 3, Mkiko Mieno 4 nd Shuji Htkeym 2,5* Abstrct Bckground: Severl studies hve reported tht dptomycin induced rtificil prolongtion of prothrombin time (PT) in some test regents, prticulrly in wrfrin users. However, it remins unknown whether the rtificil prolongtion cn be ffected by cogultion bnormlities other thn the use of wrfrin. Thus, we investigted the effect of dptomycin on PT with two types of cogultion bnormlities. Methods: Plsm smples were pooled by four groups: helthy volunteers (Plsm A), wrfrin users with interntionl normlized rtio (INR) of pproximtely 2.0 (Plsm B) or 3.0 (Plsm C), nd ptients with liver cirrhosis with INR of pproximtely 2.0 (Plsm D). Plsm A ws composed of plsm from two helthy individuls (9 ml from ech individul). Plsm B, C, nd D were composed of plsm from 36 ptients (0.5 ml from ech ptient). Dptomycin ws dded to ech smple to crete solutions with severl concentrtions (0 150 μg/ml). The INR for ech solution ws mesured with three PT regents. Liner regression nlyses were used to determine the ssocition between dptomycin concentrtion nd INR. The reltive chnge in INR due to dptomycin concentrtions ws clculted. Results: Strong liner correltions were observed between dptomycin concentrtions nd INR for ll the plsm groups nd regents (R 2 >0.7, P < 0.01). At dptomycin concentrtion of 150 μg/ml, the reltive increse of INR ws 10% in the mjority of the plsm groups with n elevted bseline INR in ll regents tested. Conclusions: Dptomycin induced the rtificil prolongtion of INR in concentrtion-dependent mnner, prticulrly in plsm smples with n elevted bseline INR. PT should be evluted t the trough levels of dptomycin. Keywords: Dptomycin, Prothrombin time, Cogultion bnormlity, Wrfrin, Liver cirrhosis, Flse positive Bckground Dptomycin is cyclic lipopeptide ntibiotic tht is used to tret Grm-positive bcteri, such s methicillinresistnt Stphylococcus ureus (MRSA) [1]. It is inserted into the cytoplsmic membrne of Grmpositive bcteri nd then disrupts the membrne, * Correspondence: shtke-tky@umin.c.jp 2 Division of Generl Internl Medicine, Jichi Medicl University Hospitl, Ykushiji, Shimotsuke-shi, Tochigi , Jpn 5 Division of Infectious Diseses, Jichi Medicl University Hospitl, Ykushiji, Shimotsuke-shi, Tochigi , Jpn Full list of uthor informtion is vilble t the end of the rticle cusing bcteril deth. Dptomycin ws pproved by the United Sttes Food nd Drug Administrtion (FDA) in 2003 for the tretment of complicted skin nd soft tissue infections nd S. ureus bloodstrem infections. Currently, it is lso recommended for mny serious infections cused by Grm-positive bcteri [2]. Some studies hve reported the prolongtion of prothrombin time (PT) in dptomycin users [3 5]. This prolongtion is considered to be rtificil becuse ptients did not hve ctul bleeding tendencies, nd it ws observed when specific recombinnt thromboplstin The Author(s) Open Access This rticle is distributed under the terms of the Cretive Commons Attribution 4.0 Interntionl License ( which permits unrestricted use, distribution, nd reproduction in ny medium, provided you give pproprite credit to the originl uthor(s) nd the source, provide link to the Cretive Commons license, nd indicte if chnges were mde. The Cretive Commons Public Domin Dediction wiver ( pplies to the dt mde vilble in this rticle, unless otherwise stted.

2 Hshimoto et l. BMC Phrmcology nd Toxicology (2017) 18:74 Pge 2 of 5 regents were used to exmine PT [3]. PT prolongtion ws concentrtion dependent, nd therefore, the FDA suggests tht PT should be evluted t the trough levels of dptomycin [6]. Since this prolongtion ws not previously evluted cliniclly, we did prospective in vivo study to determine the effect of the dptomycin-induced PT prolongtion in clinicl settings using nine PT regents tht re vilble in Jpn. Using severl specific regents, we confirmed tht PT ws significntly prolonged when dptomycin concentrtions were high, prticulrly in wrfrin users [7]. However, in vitro studies in more controlled condition should be conducted to verify the results of our in vivo study. In ddition, it remins unknown whether this prolongtion is similrly observed in ptients with other cogultion disorders, such s liver cirrhosis. Therefore, we conducted n in vitro study to determine whether dptomycin ffects the PTinterntionl normlized rtio (INR) in ptients with cogultion bnormlities in ddition to wrfrin users. Methods Study popultion nd setting This study ws bsed on pooled plsm smples from four groups: helthy volunteers (Plsm A), ptients who took wrfrin nd whose INR vlues were pproximtely 2.0 (Plsm B) or 3.0 (Plsm C), nd ptients who hd liver cirrhosis nd whose INR vlues were pproximtely 2.0 (Plsm D). Ptients who hd liver cirrhosis nd took wrfrin were excluded in ddition to ptients with ntiphospholipid syndrome. Plsm from two helthy individuls plsm ws used for Plsm A. Plsm B, C, nd D consisted of 36 ptients plsm ech. All ptients were outptients who visited the Jichi Medicl University Hospitl between June 2016 nd August Smple preprtion Plsm smples were collected from 108 ptients (0.5 ml ech) nd two helthy individuls (9 ml ech) nd stored t 80 C. After ll the smples were collected, frozen plsm smples were thwed nd pooled by group. Dptomycin ws dded to ech group of plsm smples to obtin 0, 5, 15, 50, 100, nd 150 μg/ ml solutions. Dptomycin ws purchsed from Merck Shrp & Dohme (Tokyo, Jpn). We exmined the INR of these solutions using three regents. Regent 1 (HemosIL RecombiPlsTin 2G: recombinnt humn thromboplstin) ws purchsed from Werfen Jpn (Tokyo, Jpn). Regent 2 (Neoplstin plus: rbbit brin thromboplstin) nd Regent 3 (STA Neoplstin R: recombinnt humn thromboplstin) were purchsed from Roche Dignostics K. K. (Tokyo, Jpn). The interntionl sensitivity index for ech regent ws 0.97, 1.29, nd 0.94, respectively. Dt collection nd sttisticl nlyses The INR of ll plsm smples were mesured three times. The men nd stndrd devition (SD) were clculted. Liner regression nlyses for ech plsm group nd regent were used to ssess the ssocitions between dptomycin concentrtions nd INR. P- vlues less thn 0.05 were considered sttisticlly significnt. Sttisticl nlyses were performed using JMP Pro 12 (SAS Institute, Cry, North Crolin, USA). In ddition, we clculted the reltive chnge in INR between high dptomycin concentrtions (50, 100, nd 150 μg/ml) versus the control (0 μg/ml) in ech plsm group. We regrded 10% of the reltive chnge in INR s cliniclly significnt, s described in previous studies [3, 7]. Results We found strong nd significnt liner correltions between dptomycin concentrtions nd INR for ll the plsm groups nd regents (R 2 > 0.7, P < 0.01 for ll the groups nd regents) (Tble 1 nd Fig. 1). When the dptomycin concentrtion ws 100 μg/ml, the INR ws prolonged by more thn 10% in Plsm C using Regent 1 nd Plsm B, C, nd D, respectively, using Regent 3 (Tble. At dptomycin concentrtion of 150 μg/ml, lmost ll the reltive chnges in INR in Plsm B, C, nd D were more thn 10% for ll regents. The mximum INR prolongtion ws 22% when the dptomycin concentrtion ws 150 μg/ml in Plsm D using Regent 3 (Tble. Tble 1 Results of the liner regression nlysis of dptomycin concentrtions nd INR Regent Plsm group R 2 β SE (β) P-vlue 1: HemosIL RecombiPlsTin 2G A (INR 1) < < C (wrfrin, INR < D (LC, INR < : Neoplstin Plus A (INR 1) < < C (wrfrin, INR < D (LC, INR < : STA Neoplstin R A (INR 1) < < C (wrfrin, INR < D (LC, INR < INR interntionl normlized rtio, SE stndrd error, LC liver cirrhosis

3 Hshimoto et l. BMC Phrmcology nd Toxicology (2017) 18:74 Pge 3 of 5 Fig. 1 Liner regression nlysis of dptomycin concentrtion nd INR for ech regent nd plsm group. Dt re presented s the men nd stndrd devition. PT: prothrombin time, INR: interntionl normlized rtio, LC: liver cirrhosis For Regents 1 nd 3, the reltive increse in INR ppered to be greter in the plsm groups with high bseline INR (Plsm B, C, nd D) thn in Plsm A with norml bseline INR (Tble. On the other hnd, there were no pprent differences in the reltive chnges in INR between Plsm B nd D, which hd comprble INR levels t bseline. For Regent 2, there were no obvious differences between the plsm groups with high bseline INR (Plsm B, C, nd D) nd tht with norml bseline INR (Plsm A): ll groups responded to the similr extent. Discussion We found strong nd significnt liner ssocition between dptomycin concentrtions nd the INR prolongtion in ll the plsm groups nd regents. When the dptomycin concentrtion ws higher thn 100 μg/ ml, INR ws prolonged by pproximtely 10 20%, prticulrly in those with elevted bseline INR. These results re consistent with the findings in our previous in vivo study [7]. In our previous study, the liner ssocition ws observed only in Regents 2 nd 3. However, this result might be due to other clinicl fctors tht cn ffect the vitl cogultion system. Moreover, plsm smples with high concentrtion (e.g., > 100 μg/ml) were limited in our previous study. Not ll regents used in this study hve been tested in previous in vitro studies. In the present study, we confirmed the dptomycin concentrtion-dependent prolongtion of INR under controlled conditions. In our previous study, pek dptomycin concentrtions rnged from 30 to 90 μg/ml fter the dministrtion of

4 Hshimoto et l. BMC Phrmcology nd Toxicology (2017) 18:74 Pge 4 of 5 Tble 2 Bseline INR vlues nd rtios of INR to the bseline INR t designted dptomycin concentrtions Regent Plsm group Bseline INR (men ± SD) 1: HemosIL RecombiPlsTin 2G 2: Neoplstin Plus 3: STA Neoplstin R INR 50 /INR 0 INR 100 / INR 0 INR 150 / INR 0 A (INR 1) 0.96 ± ± C (wrfrin, INR 2.57 ± D (LC, INR 1.63 ± A (INR 1) 0.97 ± ± C (wrfrin, INR 2.75 ± D (LC, INR 1.83 ± A (INR 1) 0.99 ± ± C (wrfrin, INR 2.86 ± D (LC, INR 1.54 ± PT prothrombin time, INR interntionl normlized rtio, SD stndrd devition, LC liver cirrhosis INR 0 represents the bseline INR. INR 50, INR 100, nd INR 150 represent the INR t dptomycin concentrtions of 50, 100, nd 150 μg/ml, respectively. The reltive chnge in INR ws clculted using the men vlues of INR mesured in triplicte t ech dptomycin concentrtion 6 mg/kg of dptomycin [7]. Another study showed tht dptomycin doses of more thn 6 mg/kg led to higher pek dptomycin concentrtions of more thn 100 μg/ml [8]. Currently, the high doses of dptomycin re sometimes recommended for the tretment of serious infections. For exmple, 10 mg/kg of dptomycin is recommended for the tretment of persistent MRSA bcteremi [2]. We must tke into considertion tht severe infections cused by Grm-positive pthogens frequently occur in wrfrin users becuse some of them hve intr-crdic devices, such s ventriculr ssist devices or prosthetic hert vlves. Ptients with intr-crdic devices hve higher INR levels (up to 3.5) [9, 10]. If serious infection cused by Grm-positive bcteri occurs in such ptients, high doses of dptomycin will be dministered, leding to pek dptomycin concentrtion of more thn 100 μg/ml. Consequently, INR my be rtificilly prolonged by more thn 10%, consequentilly leding to n inpproprite reduction of the wrfrin dose. We should ensure tht PT is checked t the trough time of dptomycin concentrtions. For Regents 1 nd 3, the reltive increse in INR ws higher in the plsm groups with high bseline INR (Plsm B, C, nd D) thn in the plsm group with norml bseline INR (Plsm A). The etiology of the cogultion bnormlity lso did not ffect the reltive chnge in INR in ll three regents. These results cn be explined by the fct tht dptomycin interferes with phospholipids contined in the regents rther thn the cogultion fctors in the plsm, which re decresed in both wrfrin users nd ptients with liver cirrhosis. Although Webster et l. reported tht prolonged bseline PT itself did not ffect the reltive chnge in PT, they lcked dt on the reltive chnge in PT in nticogulted plsm smples with more thn 100 μg/ml of dptomycin [3]. Our findings suggest tht with high bseline INR, it becomes more likely to observe cliniclly importnt reltive chnge of >10% in INR in t lest some regents. Previous studies hve shown tht two fctors in PT regents my be responsible for the flse PT prolongtion: the thromboplstin source nd the phospholipid type of regents [3, 4]. It is conceivble tht dptomycin tht is inserted into the phospholipid component of PT regents cn interfere with tissue fctor-induced cogultion, resulting in flse PT prolongtion [3]. Regents mde from recombinnt humn or rbbit tissue fctors were highly susceptible to dptomycin when phosphtidylglycerol is dded [4]. In this study, Regents 1 nd 3 were mde from recombinnt humn tissue fctors, lthough Regent 2 ws mde from the rbbit brin. Therefore, the differences in the thromboplstin source might ffect the susceptibility to dptomycin. Our study hd severl limittions. First, we did not conduct sttisticl comprisons of the reltive chnges in INR between the plsm groups due to the smll smple sizes. In ddition, biochemicl studies re required to ssess the mechnism by which dptomycininduced rtificil prolongtion ws lrger in the plsm with elevted bseline INR levels thn in the norml plsm, regrdless of the cuse. Conclusions In summry, we found tht dptomycin induced the dose-dependent rtificil prolongtion of INR in individuls with or without cogultion bnormlities. For some regents, the extent of the reltive chnge in INR ws higher in the plsm groups with higher bseline INR due to either wrfrin or liver cirrhosis thn in the plsm group with lower INR. The etiology of cogultion bnormlities did not pprently ffect the reltive chnge. The evlution of INR t the trough time of dptomycin must be considered, prticulrly in ptients with higher bseline INR. Abbrevitions FDA: Food nd drug dministrtion; INR: Interntionl normlized rtio; LC: Liver cirrhosis; MRSA: Methicillin-resistnt Stphylococcus ureus; PT: Prothrombin time; SD: Stndrd devitions; SE: Stndrd error Acknowledgements We would like to cknowledge ll of the ptients involved in this study. We would lso like to thnk Tkko Muto from the Center for Community Medicine of Jichi Medicl University for collecting nd preserving the serum smples. We express our grtitude to the following compnies for the technicl support during PT mesurements: Werfen Jpn (Tokyo, Jpn) nd Roche Dignostics K. K. (Tokyo, Jpn). Funding The uthors hve no funding to declre.

5 Hshimoto et l. BMC Phrmcology nd Toxicology (2017) 18:74 Pge 5 of 5 Avilbility of dt nd mterils All dt generted or nlyzed during this study re included in the published rticle. Authors contributions SH designed nd supervised the study. HH, NK, nd TY obtined the dt. HH, MS, MM, nd SH nlyzed nd interpreted the dt. HH wrote the mnuscript. MS nd SH revised the mnuscript. All uthors reviewed nd pproved the finl version of the mnuscript. Ethics pprovl nd consent to prticipte This study ws pproved by the Ethics Committee of the Jichi Medicl University Hospitl (A16-048). All procedures performed in the studies involving humn prticipnts were in ccordnce with the 1964 Helsinki declrtion nd its lter mendments or similr ethicl stndrds. The written informed consent from the ptients enrolled ws wived by the Ethics Committee becuse the plsm smples were obtined fter routine lbortory tests. 8. Benvenuto M, Benziger DP, Ynkelev S, Viglini G. Phrmcokinetics nd tolerbility of dptomycin t doses up to 12 milligrms per kilogrm of body weight once dily in helthy volunteers. Antimicrob Agents Chemother. 2006;50: Bumnn Kreuziger LM, Kim B, Wieselthler GM. Antithrombotic therpy for left ventriculr ssist devices in dults: systemtic review. J Thromb Hemost. 2015;13: Whitlock RP, Sun JC, Fremes SE, Rubens FD, Teoh KH. Antithrombotic nd thrombolytic therpy for vlvulr disese: ntithrombotic therpy nd prevention of thrombosis, 9th ed: Americn College of Chest Physicins Evidence-Bsed Clinicl Prctice Guidelines. Chest. 2012;141:e576S 600S. Consent for publiction Not pplicble in this study. Competing interests The uthors declre tht they hve no competing interests. Publisher s Note Springer Nture remins neutrl with regrd to jurisdictionl clims in published mps nd institutionl ffilitions. Author detils 1 Deprtment of Infectious Diseses, The University of Tokyo Hospitl, Hongo, Bunkyo-ku, Tokyo , Jpn. 2 Division of Generl Internl Medicine, Jichi Medicl University Hospitl, Ykushiji, Shimotsuke-shi, Tochigi , Jpn. 3 Deprtment of Phrmcy, The University of Tokyo Hospitl (Current ffilition: The Eduction Center for Clinicl Phrmcy, Grdute School of Phrmceuticl Sciences, The University of Tokyo), Hongo, Bunkyo-ku, Tokyo , Jpn. 4 Deprtment of Medicl Informtics, Center for Informtion, Jichi Medicl University, Ykushiji, Shimotsuke-shi, Tochigi , Jpn. 5 Division of Infectious Diseses, Jichi Medicl University Hospitl, Ykushiji, Shimotsuke-shi, Tochigi , Jpn. Received: 29 August 2017 Accepted: 14 November 2017 References 1. Steenbergen JN, Alder J, Thorne GM, Tlly FP. Dptomycin: lipopeptide ntibiotic for the tretment of serious grm-positive infections. J Antimicrob Chemother. 2005;55: Liu C, Byer A, Cosgrove SE, Dum RS, Fridkin SK, Gorwitz RJ, et l. Clinicl prctice guidelines by the Infectious Diseses Society of Americ for the tretment of methicillin-resistnt Stphylococcus Aureus infections in dults nd children. Clin Infect Dis. 2011;52:e Webster PS, Oleson FB Jr, Pterson DL, Arkin CF, Mngili A, Crven DE, et l. Interction of dptomycin with two recombinnt thromboplstin regents leds to flsely prolonged ptient prothrombin time/interntionl normlized rtio results. Blood Cogul Fibrinolysis. 2008;19: vn den Besselr AMHP, Breukink E, Koorengevel MC. Phosphtidylglycerol nd dptomycin synergisticlly inhibit tissue fctor-induced cogultion in the prothrombin time test. J Thromb Hemost. 2010;8: Ymd T, Kto R, Od K, Tnk H, Suzuki K, Ijiri Y, et l. Flse prolongtion of prothrombin time in the presence of high blood concentrtion of dptomycin. Bsic Clin Phrmcol Toxicol. 2016;119: Merck & Co., Inc. (2017) Drug informtion: CUBICIN (dptomycin for injection). cubicin_pi.pdf. Accessed 19 My Sito M, Htkeym S, Hshimoto H, Suzuki T, Jubishi D, Kneko M, et l. Dose-dependent rtificil prolongtion of prothrombin time by interction between dptomycin nd test regents in ptients receiving wrfrin: prospective in vivo clinicl study. Ann Clin Microbiol Antimicrob. 2017;16:27. Submit your next mnuscript to BioMed Centrl nd we will help you t every step: We ccept pre-submission inquiries Our selector tool helps you to find the most relevnt journl We provide round the clock customer support Convenient online submission Thorough peer review Inclusion in PubMed nd ll mjor indexing services Mximum visibility for your reserch Submit your mnuscript t

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