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1 Korean J Clin Microbiol Vol. 14, No. 1, March, 2011 DOI: /KJCM Clinical Implications of Multiplex PCR Detection of Fastidious Microorganisms in Vaginitis Patients Nae Yu, Mi-Kyung Lee Department of Laboratory Medicine, Chung-Ang University College of Medicine, Seoul, Korea Background: Bacterial vaginitis (BV) and Trichomonas vaginitis are the most frequently recurring infectious diseases in women. Therefore, accurate tests for post-treatment follow-up are required. A multiplex PCR assay allows for the simultaneous detection of multiple pathogens in a single specimen. In this study, we assessed the clinical implications of multiplex PCR detection of fastidious s causing vaginitis. Methods: A total of 216 vaginitis patients who presented to Chung-Ang University Yongsan Hospital with more than one result on multiplex PCR (Trichomonas vaginalis (TV), Neisseria gonorrhoeae (NG), Chlamydia trachomatis (CT), Ureaplasma urealyticum (UU), Mycoplasma genitalium (MG), Mycoplasma hominis (MH)) were retrospectively enrolled in this study. Each patient s clinical symptoms, initial treatment and follow-up for BV, and other related test results were also retrospectively reviewed. Results: The most commonly reported symptom was abnormal discharge, followed by pruritis (73.1%), lower abdominal pain (38.4%), urination difficulties (13%), and others such as fever. According to the multiplex PCR results, there were 116 cases (35.8%) of MH, 86 cases (26.5%) of UU, 62 cases (19.1%) of CT, and 84 cases (38.9%) were mixed infections. Among those patients with single infections, treatment changed for 63 cases (65.6%) while treatment remained unchanged for 17 (17.7%) after PCR results were reported. Conclusion: The diagnosis of BV using multiplex PCR is clinically effective and the results of which can be incorporated in antibiotic selection for patients with multiple sexually transmitted diseases (STD). Multiplex PCR may be especially helpful in the diagnosis of patients in whom the differentiation of STD pathogens is difficult using traditional methods. (Korean J Clin Microbiol 2011;14:30-35) Key Words: Bacterial vaginitis, Multiplex PCR, Sexually transmitted pathogen 서 세균성질염 (bacterial vaginitis, BV) 은질내정상세균의분포에변화가생겨산도가감소하고특정세균이과다증식하는것을특징으로하는질환으로서, 가임기여성의하부생식기계의가장흔한감염원인으로알려져있다 [1-4]. 특히임신중인여성에서임신 2, 3분기의유산, 골반내감염, 조산, 조기양막파수, 융모양막염등의합병증을유발할수있고수술후감염증가, 후천성면역결핍증감염등의원인이된다 [4-7]. 그중편모충질염은가장흔한성전염성질환 (sexual transmitted disease, STD) 으로서미국에서매년 3백만명의여성이감염되고있고, 한국에서는질의불편감을호소하는여성들의 10.4% 에서원인이된다고보고된바있다 [8]. Received 4 May, 2010, Revised 28 June, 2010 Accepted 20 July, 2010 Correspondence: Mi-Kyung Lee, Department of Laboratory Medicine, Chung-Ang University Yongsan Hospital, Hangangno 3-ga, Yongsan-gu, Seoul , Korea. (Tel) , (Fax) , ( ) cpworld@cau.ac.kr 론 현재임상적으로세균성질염의진단을위해사용되고있는 Amsel s criteria, 혹은 Nugent s score를이용한진단방법 [9-11] 으로는증상이있는여성의 30% 에서는진단을내릴수없고 [12], 민감도와특이도가각각 92% 와 77% 로보고되어있다 [13]. 또한이를이용시, 검사과정의인적숙련도가요구되며, 사용되는용어가모호하여진단의정확성에의문이제기되고있다 [1,4]. 이에따라, 최근중합효소연쇄반응 (polymerase chain reaction, PCR) 을이용하여질염의원인미생물을밝혀내는방법의유용성에대한연구가이루어지고있으며, 결과적으로높은특이도 (98 100%) 와민감도 (95 100%) 를보여그유용성이입증되고있다 [1,12,14]. 질염의치료후완치율은 1주후 80 90% 지만 3달내의재발률이 15 30% 로, 장기간의연구결과에서는약 52% 의질염완치환자에서적어도 1회이상재발된것이보고되어, 정확하고치료후에도쉽게추적검사를할수있는검사방법이요구되고있는실정이다. 본연구에서는중앙대학교용산병원산부인과에내원한질염환자를대상으로배양이까다로운미생물검출을시행하고 30

2 Nae Yu and Mi-Kyung Lee : Multiplex PCR of Fastidious Microorganisms in Vaginitis 31 PCR 결과보고후의항생제처방변화를확인하여질염의진단에있어서 PCR 검사의유용성을확인하고자하였다. 1. 대상 대상및방법 2006년 5월에서 2009년 7월까지중앙대학교용산병원산부인과를방문한환자중 PCR에의해 Trichomonas vaginalis (TV), Neisseria gonorrhoeae (NG), Chlamydia trachomatis (CT), Ureaplasma urealyticum (UU), Mycoplasma genitalium (MG), Mycoplasma hominis (MH) 중 1균종이상검출된 216명을대상으로하였다. 본연구는중앙대학교용산병원 Institutional Review Board의심의를통과하였다. 2. 방법 분자유전학적방법에의한미생물검출은환자의질분비물을 Stuart Agar Gel Transport Swabs (COPAN Italia, Brescia, Italy) 으로채취하여수송후, QIAamp DNA Mini Kit (QIAgen Korea, Seoul, Korea) 로 DNA를추출하였고, Seeplex TM STD6 ACE detection kit (Seegene, Biotechnology Inc, Seoul, Korea) 을사용하여제조사의지시에따라 PCR 을시행하였다. PCR 은 GeneAmp PCR system 9700 (Applied biosystems Inc, California, USA) 을사용하였고, PCR 산물은 2% 아가로스젤전기영동을통하여확인하였다. 또한각미생물이검출된환자의임상기록지를후향적으로검토하여진단명, 임상증상 ( 복통, 발열, 질분비물이상, 성교시불편감, 내진소견 ), 사용한치료제및치료후추적검사등에대하여조사하였다. 1. 임상증상 결 216명의임상증상은질분비물증가나악취또는소양증 (158명, 73.1%), 복통 (83명, 38.4%), 발열 (13명, 6%) 등이었다. 성교시불편감을호소하는경우는 15명 (6.9%), 무증상의환자들은 16명 (7.4%) 이었다 (Table 1). 복통은하복부통증을주로호소하였으며발열은체온이 38 C 이상으로측정된경우로간주하였다. 질분비물에서는백색이나황색의질분비물, 악취, Table 1. Clinical symptom and physical examination of patients (including overlapping results, N=216) Clinical symptoms Number (%) Abnormal vaginal discharge, pruritis 158 (73.1) Lower abdominal pain 83 (38.4) Urination difficulties 28 (13) Dyspareunia 15 (6.9) Fever 13 (6.0) No symptom 16 (7.4) 과 맑은분비물등의증상을보였다. 자궁경부와질내진소견에서자궁경부미란, 충혈, 출혈등의증상이관찰되었다. 2. 균종분포 다중 PCR에서한가지이상의균종양성이확인된환자에서, 단일균종양성은 132명 (61.1%), 2가지중복균종양성은 62명 (28.7%) 그리고 3가지이상중복균종양성은 22명 (10.2%) 이었다. 중복을허용한균종별양성환자는 MH가 116명 (53.7%) 으로가장많았고, UU는 86명 (39.8%), CT는 62명 (28.7%) 순으로나타났다 (Table 2). 단일균종양성도 MH가 59 명 (27.3%), UU는 32명 (14.8%), CT는 25명 (11.6%) 순으로비슷한양상이었으며, 그외에 TV와 NG도각각 6명 (2.8%) 과 2명 (0.9%) 에서단일양성이었다. 2가지이상균종양성에서도 MH 와 UU의복합감염이가장높게 (22명, 10.2%) 나타났다 (Table 3). Table 2. The numbers of s in results (including overlapping results, N=216) Positive Number (%) Mycoplasma hominis 116 (53.7) Ureaplasma urealyticum 86 (39.8) Chlamydia trachomatis 62 (28.7) Mycoplasma genitalium 24 (11.1) Trichomonas vaginalis 23 (10.6) Neisseria gonorrhoeae 13 (6.0) Table 3. The numbers of single, double and multiple results Single No (%) Double No (%) Multiple No (%) MH 59 (27.3) MH&UU 22 (10.2) TV, MH&UU 5 (2.3) UU 32 (14.8) CT&MH 10 (4.6) CT, MH&UU 5 (2.3) CT 25 (11.6) CT&UU 7 (3.2) CT, MG&UU 2 (0.9) MG 8 (3.7) TV&MH 6 (2.8) CT, NG&MG 1 (0.5) TV 6 (2.8) CT&MG 4 (1.9) CT, NG&MH 1 (0.5) NG 2 (0.9) NG&UU 3 (1.4) CT, NG&UU 1 (0.5) TV&UU 2 (0.9) CT, TV&MH 1 (0.5) MG&MH 2 (0.9) CT, TV&UU 1 (0.5) MG&UU 2 (0.9) CT, MG&MH 1 (0.5) CT&NG 1 (0.5) NG, MH&UU 1 (0.5) NG&TV 1 (0.5) MG, MH&UU 1 (0.5) NG&MG 1 (0.5) CT, TV, MG&UU 1 (0.5) NG&MH 1 (0.5) CT, MG, MH&UU 1 (0.5) Total 132 (61.1) 62 (28.7) 22 (10.2) Abbreviations: TV, Trichomonas vaginalis; NG, Neisseria gonorrhoeae; CT, Chlamydia trachomatis; UU, Ureaplasma urealyticum; MG, Mycoplasma genitalium; MH, Mycoplasma hominis.

3 32 Korean J Clin Microbiol 2011;14(1):30-35 Table 4. Prescribed drugs for 216 patients at first (before PCR results reported, including overlapping results) Prescribed drugs for treatment Patients numbers (%) No treatment prescription 56 (22.6) Cefazodone, Ceftrizine* 45 (18.1) Doxycycline 39 (15.7) Metronidazole 39 (15.7) Levofloxacin 23 (9.3) 3rd generation cephalosporin 16 (6.5) Cefditoren, Ceftriaxone Ciprofloxacin 16 (6.5) Fluconazole 12 (4.8) Amoxicillin 2 (0.8) Total 248 (100) *1st generation cephalosporin; 3rd generation cephalosporin. 3. 항생제치료현황 단일, 중복양성을포함한전체환자에서초진후항생제를처방받지않은경우는 56명 (22.7%) 이었고, 그외세파조돈및세프트리진 (45명, 18.1%), 독시사이클린 (39명, 15.8%) 을, 메트로니다졸 (39명, 15.8%) 등을처방받았다 (Table 4). 다중 PCR 결과가보고된단일양성환자의 2번째방문에서는 63 (65.6%) 명이처음처방받았던항생제와다른항생제를처방받거나다른항생제를추가로처방받았다 (Table 5). 16명 (16.7%) 은추가로방문하지않았으며초진과같은항생제를유지한환자는 17명 (17.7%) 이었다. 검출된미생물종류에따른치료를분석한결과, MH는단독양성 59명중 45명 (76.3%) 에서초진시항생제를처방받았고, 그중에 25명 (55.6%) 이 PCR 결과가보고된후초진때와다른항생제를처방받았다. UU의경우단독양성인 32명중 20명 (62.5%) 이초진시항생제처방을받았으나그중 19명 (95%) 이 PCR 결과확인후다른항생제를처방받았다. CT는단독양성인 25명중 19명 (76%) 이항생제치료를받았고, PCR 결과확인후 12명 (63.2%) 이변경된항생제를처방받았다. MG는단독양성환자 8명중에서 5명 (62.5%) 이초진시항생제처방을받았고, PCR 결과후 3명 (60%) 이항생제처방이바뀌었다. TV의경우는단독양성이었던 6명에서초진시 5명 (83.3%) 이항생제치료를받았고, 그중 2명 (40%) 이 PCR 결과확인후바뀐항생제를처방받았다. NG는단독양성은 2명이었고, 모두 (100%) PCR 결과확인후바뀐항생제를처방받았다 (Table 3, 5). 따라서단일균종양성일경우, PCR 결과확인후초진시처방받은항생제가변경된비율은평균적으로 65.6% 로세균성질증, 트리코모나스질염, 임질을진단받은환자중절반이상이 PCR 결과로치료받는항생제의변화를보였다. Table 5. The treatment change of each single patients (after PCR results reported) Single No. No. (%*) of treatment prescribed at first No. (% ) of treatment change after PCR results MH (76.3) 25 (55.6) UU (62.5) 19 (95) CT (76.0) 12 (63.2) MG 8 5 (62.5) 3 (60.0) TV 6 5 (83.3) 2 (40.0) NG 2 2 (100) 2 (100) Total *Percent ratio of single results and treatment prescribed at first; Percent ratio of treatment prescribed at first and treatment change after PCR results. Abbreviations: TV, Trichomonas vaginalis; NG, Neisseria gonorrhoeae; CT, Chlamydia trachomatis; UU, Ureaplasma urealyticum; MG, Mycoplasma genitalium; MH, Mycoplasma hominis. 고 세균성질염은칸디다성질염, 트리코모나스질염, 세균성질염으로구분되는질염중의가장흔한원인으로가임기여성의 20 30% 까지유병률이보고된바있다 [13]. 국내에서증상이있는폐경전여성을대상으로한연구에서는 MH는 44.4%, UU는 18.9% 등의유병률이보고되었고 [15], 아프리카계미국여성에서의유병률은 51% 까지보고되어인종간, 사회적환경간의유병률의차이를보인다 [16]. 미국에서는매년천만명의환자가질의불편함으로산부인과를방문하며그중 40 50% 가세균성질염으로진단받고, 그원인을진단하기위하여전통적인방법인문진, 이학적검사소견인내진, 질분비물을현미경으로확인하는방법등을사용하고있다 [4]. 하지만전통적인진단방법은비용이저렴하다는경제적인면의장점이있으나 [17], 증상이있는환자도진단받지못하는경우가있으며방법상의번거로움이있고, 또한정확한진단에어려움이있음이보고되고있다 [1,4]. 특히편모충질염은상부비뇨생식기감염, 분만, 수술, 낙태시술후의감염, 골반내감염, 조기분만, 불임, 자궁경부의이형성증, 저체중출생아, 조기분만진통, 자궁내태아발육지연, 저체중출생아등과밀접한관련이있음이잘알려져있어원인미생물검출이중요하다 [5,18-20]. 추가적으로 UU, MG, MH는건강한성인남녀비뇨생식기의정상균으로도존재하지만기회감염균으로작용하여앞서언급한합병증들은유발할수있기때문에최근임상적중요성이강조되어국내외에서검출률과검출방법에대한연구가계속되어왔다. 보고된연구에따르면과거 UU, MG, MH를검출하기위해주로사용한방법은배양법이나, 각세균의영양요구성이까다롭고저배율광학현미경에서집락을관찰해야하는등의어려 찰

4 Nae Yu and Mi-Kyung Lee : Multiplex PCR of Fastidious Microorganisms in Vaginitis 33 운점이있다. 편모충질염의진단을위한배양법도비교적낮은민감도 (85 90%) 와특이도 (75%) 를보이고, 파파니콜로도말검사 (papanicolaou smear, pap smear) 를이용한방법은위음성이 50% 에달하는등더높은정확성을위하여다른방법의필요성이제기되어, 빠르고편리한방법인액체미세배양법이나, PCR을이용한방법과장점들이소개되고있다 [5,13,21,22]. 따라서최근 PCR을이용하여질염의원인미생물을밝히는것의유용성을검증하는연구 [15,21-23] 가계속되고있으며이러한연구에따르면다중 PCR를이용한 STD의진단은높은특이도 (98 100%) 와민감도 (95 100%) 를보여주고있어 [1,12, 14,22,23] 국내에서도많은검사기관에서사용하고있다. 민감도가검체의총 DNA양에영향을받는단점이있지만, 특히 STD의원인미생물을진단하는데있어서정확하고빠른장점이있고, 비병원성임균등의다른균과교차반응을나타내지않는다 [23]. 또한, 재발된환자의균종을신속히파악할수있어치료후에도도움이될수있다 [16]. 본연구에서조사된이학적소견은복통 (83명, 38.4%), 발열 (13명, 6%), 빈뇨등의요로증상 (28명, 13%), 질분비물증가, 악취또는소양증 (158명, 73.1%) 등으로과거에시행되었던연구들에서다양하게보고되어비교하기어려웠다 [1,4,21]. 조사된증상은매우비특이적인증상으로그증상의정확성에있어서치즈양상의질분비물이칸디다성질염에서자주관찰되고, 불쾌한냄새가관찰되었을경우, 가려움증이보일경우칸디다성질염일가능성이떨어진다는등의보고가있지만 [4] 앞서보고된연구와같이 [19] 세균성질염이나칸디다성질염, 편모충질염등을구분하는데특이적이지않아증상이나, 문진, 내진결과만으로정확한진단이어려움을보여주고있었다. CT와 MH, UU의양성률은각각 19.1%, 35.8%, 26.5% 로과거의국내보고 ( %, %, and %)[5,8, 15,18,19] 과다른양성률을나타내었다. 이는기존보고들이증상이있는폐경전여성, 임산부나만성자궁내막염, 자궁외임신의검체, 정상검체를대상으로시행하였고이번연구는다중 PCR에서양성으로나온환자들을대상으로시행하여대상의차이가있으며, 검사방법도기존연구에서는 pap smear, MYCOFAST Evolution 2 TM (International Microbio Co., France) 등다양하게이용하고있어대상과검사방법등의차이로인하여산부인과를방문한환자를대상으로다중 PCR을시행한본연구와다른결과를보인것으로생각된다. 본연구에서, 추적관찰되지않은환자를제외한환자의약 85% 에서 PCR 결과보고후항생제처방이바뀐것으로조사되어, 다중 PCR을사용한미생물검출이임상적으로질염의증상을보이는환자의항생제선택에영향을줄수있을것으로생각되었다. 또한질염의원인미생물검출은앞서언급한합병증들을유발할수있기때문에그임상적인중요성을고려하여, 특히임신 3분기이후의산모들이나수술후의비특이적인 하복부증상, 발열, 비정상적인질분비물을보이는환자들에서더욱유용하게쓰일수있을것으로생각된다. 국내에서는세균성질염과편모충질염의치료로메트로니다졸, 클린다마이신을권장하고있으나 [23] 실제로는그외에퀴놀론계, 세팔로스포린계항생제도다수처방되고있음을확인할수있었다. 외국의보고들 [3,9,13,19,24,25] 에서는클린다마이신, 메트로니다졸, 티니다졸등을권장하고있었는데실제로이와도다른처방을나타내었다. 또한세균성질염의원인균인 MH와 UU는서로의치료제에내성을보인다고보고되어있고, NG도치료가달라이 3가지균를각각치료제를다르게써야하나, 증상만으로는 3가지균에대한항생제를처방하기어려우므로여러가지원인미생물을구분할수있는다중 PCR 검사의필요성이더욱강조되어야할것으로생각되었다. 본연구에서는세균성질염, 편모충질염이의심되는환자에서초진시다중 PCR검사를시행하여 TV, NG, CT 등 3가지원인미생물이확인된경우, 대부분항생제가변경된것으로나타났으며문진, 임상양상, 진찰등으로는원인미생물감별이어려워항생제처방이힘든경우다중 PCR을통한미생물검출이임상적으로유용할것으로생각된다. 참고문헌 1. Lowe NK, Neal JL, Ryan-Wenger NA. Accuracy of the clinical diagnosis of vaginitis compared with a DNA probe laboratory standard. Obstet Gynecol 2009;113: Eckert LO. Clinical practice. Acute vulvovaginitis. N Engl J Med 2006;355: Owen MK and Clenney TL. Management of vaginitis. Am Fam Physician 2004;70: Anderson MR, Klink K, Cohrssen A. Evaluation of vaginal complaints. JAMA 2004;291: Bae HG, Heo WB, Lee NY, Lee WK, Koo TB. Detection of Ureaplasma urealyticum and Mycoplasma hominis in pregnant Women Using MYCOFAST(R) Evolution 2 and PCR. Korean J Clin Microbiol 2003;6: Atashili J, Poole C, Ndumbe PM, Adimora AA, Smith JS. Bacterial vaginosis and HIV acquisition: a meta-analysis of published studies. AIDS 2008;22: Mitchell C, Moreira C, Fredricks D, Paul K, Caliendo AM, Kurpewski J, et al. Detection of fastidious vaginal bacteria in women with HIV infection and bacterial vaginosis. Infect Dis Obstet Gynecol 2010; in press. 8. Ryu JS and Min DY. Trichomonas vaginalis and trichomoniasis in the Republic of Korea. Korean J Parasitol 2006;44: Dickey LJ, Nailor MD, Sobel JD. Guidelines for the treatment of bacterial vaginosis: focus on tinidazole. Ther Clin Risk Manag 2009;5: Thomason JL, Gelbart SM, Anderson RJ, Walt AK, Osypowski PJ, Broekhuizen FF. Statistical evaluation of diagnostic criteria for bacterial vaginosis. Am J Obstet Gynecol 1990;162: Nugent RP, Krohn MA, Hillier SL. Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain interpretation. J Clin Microbiol 1991;29:

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6 Nae Yu and Mi-Kyung Lee : Multiplex PCR of Fastidious Microorganisms in Vaginitis 35 = 국문초록 = 질염환자에서다중 PCR 을이용한배양이까다로운미생물검출의임상적유용성 중앙대학교의과대학진단검사의학교실유내, 이미경 배경 : 여성에서세균성질염과편모충질염은매우흔하고치료후재발도많은것으로알려져있어, 정확하고치료후추적검사가가능한검사방법이요구되고있다. 이에본연구에서는질염환자에서중합효소연쇄반응 (polymerase chain reaction, PCR) 을이용한배양이까다로운미생물검출의임상적유용성을평가하고자하였다. 방법 : 중앙대학교용산병원을방문하여다중 PCR에의해 Trichomonas vaginalis (TV), Neisseria gonorrhoeae (NG), Chlamydia trachomatis (CT), Ureaplasma urealyticum (UU), Mycoplasma genitalium (MG), Mycoplasma hominis (MH) 중 1균종이상검출된 216명의환자를대상으로하였다. PCR 검사의임상적중요성을평가하기위해서후향적병록지검토를통하여각환자의증상, 검사결과, 질염치료후결과를조사하였다. 결과 : 질염환자의 73.1% 에서비정상적인질분비물, 가려움증을나타냈고, 38.4% 에서는하복부통증, 13% 에서는요로계불편감을, 그외에발열등을호소하였다. 다중 PCR 검사결과, MH (116명, 53.8%), UU (86명, 39.8%), CT (62명, 28.7%) 등의순으로검출되었다. 86명 (38.9%) 은중복감염을나타내었다. 단일양성결과에서, PCR 검사결과가보고된후에치료제처방이바뀐경우, 치료제처방이바뀌지않은경우는각각전체의 65.6%, 17.7% 를차지하였다. 결론 : 질염환자에서다중 PCR을이용한질염의진단은적절한항생제선택에도움을줄수있으며, 특히원인미생물감별이어려운환자에게임상적으로유용할것으로생각되었다. [ 대한임상미생물학회지 2011;14:30-35] 교신저자 : 이미경, , 서울시용산구한강로 3 가 중앙대학교용산병원진단검사의학과 Tel: , Fax: cpworld@cau.ac.kr

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( )Kju225.hwp 비임균성비뇨생식기감염에서 의진단적효용성 Usefulness of the Mycofast Test (MYCOFAST Evolution 2) for the Diagnosis of Nongonococcal Genitourinary Infections Hang Ro Park, Yang Hyun Kim, Ho Jae Lee, Jea Sang Oh, Hyoung Jin