ORIGILARTICLE DOI : 0.97/ic.009...6 최근임상검체에서의혐기성세균분리현황및 혐기성균혈증의임상적특징 연세대학교의과대학진단검사의학교실, 세균내성연구소, 내과학교실 박용정 이양순 김명숙 최준용 용동은 정석훈 김준명 이경원 정윤섭 RecentTrendsofAnaerobicBacteriaIsolatedfrom ClinicalSpecimensand ClinicalCharacteristicsofAnaerobicBacteremia Yongjung Park, M.D., Yangsoon Lee, M.D., Myungsook Kim, M.S., Jun Yong Choi, M.D., Dongeun Yong, M.D. Seok Hoon Jeong, M.D., June Myung Kim, M.D., Kyungwon Lee, M.D., and Yunsop Chong, Ph.D. Departments of Laboratory Medicine and Research Institute of Bacterial Resistance, Internal Medicine, College of Medicine, Yonsei University, Seoul, Korea Background : Anaerobic bacteria can cause various infections, and their incidence may differ greatly, depending on the country or hospital. We investigated recent trends in anaerobe isolation and clinical characteristics of anaerobic bacteremia in one hospital in Korea to facilitate diagnosis and treatment of anaerobic infections. Materials and Methods : Anaerobic bacteria isolated from blood, body fluids and abscess specimens at a university hospital in Korea during 007 and 00 were analyzed. The medical records of anaerobic bacteremia patients were reviewed. A retrospective cohort study was conducted to determine the risk factors for in-hospital mortality of patients with anaerobic bacteremia. Results : A total of 9 non-duplicated anaerobic isolates were recovered from blood, body fluids and abscess specimens. Bacteroides fragilis (7 isolates,.%) was the most common organism followed by Clostridium perfringens ( isolates, 7.6%), Peptoniphilus asaccharolyticus ( isolates, 7.%) and Anaerococcus prevotii (9 isolates, 6.6%). Eighty-four isolates were recovered from blood specimens, among which B. fragilis ( isolates) and C. perfringens ( isolates) were the most frequently isolated organisms. Among the 96 underlying diseases of anaerobic bacteremia patients, neoplastic, infectious, and gastrointestinal diseases accounted for (7.6%), 6 (.%), and (0.9%) cases, respectively. The alimentary tract was the most common suspected portal of entry. The in-hospital mortality rate of anaerobic bacteremia patients was.%, and neutropenia at the time of blood culture was the only statistically significant factor associated with mortality in this study. Anaerobes were isolated in.% of all positive blood cultures. Conclusions : B. fragilis and C. perfringens are expected to be commonly isolated from clinical specimens. Despite its low prevalence, anaerobic bacteremia displays a significant in-hospital mortality rate. Ongoing investigations into anaerobic bacteremia are necessary because of ambiguous risk factors for mortality. Key Words : Anaerobe, Bacteremia, Bacteroides fragilis, Clostridium perfringens ) 서 혐기성세균은사람의장관, 구강, 비뇨생식기등의점막 Submitted : April, 009, Accepted : 0 August, 009 Corresponding author : Kyungwon Lee, M.D. Department of Laboratory Medicine and Research Institute of Bacterial Resistance, Yonsei University College of Medicine, Seodaemun-Gu, Seoul 0-7, Korea Tel : +---6, Fax: +---090 E-mail : leekcp@yuhs.ac 론 에존재하는상재균으로, 당뇨병, 혈관질환및호기성세균감염이나악성종양, 장기이식등으로인하여면역억제치료를받은환자에서다양한감염을일으킬수있다 (). 혐기성세균에의한균혈증은전체균혈증의 0.-% 로연구자에따라다양하게보고되어왔다 (-9). 즉, 최근의한연구에서는혈액배양,000건당혐기성세균분리빈도가 997-00 년에.6에서 00-006 년에는 7.0 으로감소하였으나 (0), 반면다른연구자는 99년.6 에서 00년.7 로약 0% 증가하였다고보고하였다 (9). 6 Infection and Chemotherapy : Vol., No., 009
혐기성세균에의한균혈증은치명적인장기부전을일으키기도하며 (), 여러연구에서 -% 의사망률을보였다 (7,, ). 이러한임상적중요성으로인하여, 국외의경우혐기성세균에대한임상연구가지속적으로이루어지고있는데반하여, 국내에는이러한연구가최근거의없는실정이다 (-). 따라서, 본연구에서는국내의한대학병원에서최근 년간임상검체로부터분리된혐기성세균의분리현황과혐기성세균에의한균혈증의임상양상에대하여조사하여, 혐기성세균에의한균혈증의진단, 치료및예후판정에도움을주고자하였다.. 혐기성균혈증환자의예후인자조사를위한연구설계및자료수집병원내사망 (in-hospital mortality) 과관련된인자를조사하기위하여 명의혐기성균혈증환자중생존및사망이확인된 79명을대상으로후향적코호트연구를시행하였다. 의무기록을검토하여연령, 성별, 기저질환, 원발병소, 분리된세균균종을기록하였고, 균혈증발생시점에서의호중구감소증과패혈성쇼크, 양성혈액배양병수, 원내감염, 복합감염, 입원기간중중환자실치료및인공호흡기사용, 입원전 개월로부터퇴원또는사망까지수술및침습적시술이력및적절한항생제치료여부등을조사하였다. 재료및방법. 대상 007년 월부터 00년 월까지서울의한대학병원환자로부터채취한혈액, 체액및농양검체의세균배양에서분리된혐기성세균을대상으로하였다. 혈액배양에서혐기성세균이분리된 명환자의의무기록을후향적으로조사하였다.. 혐기성세균의배양및동정면봉으로채취된검체는 Stuart 수송배지에넣어가능한빨리검사실로운반하였으며, 흡인액은검체가채취된주사기의바늘을막아서운반하였다. 검사실로운반된검체는혐기성상자 (Forma Scientific, Marietta, Ohio, U.S.A.) 안에서환원된 phenylethanol blood agar (phenylethyl alcohol blood agar, PEBA) (Difco, Detroit, MI, U.S.A.) 에접종하여혐기성조건으로 항온기에서 시간배양하였다. 호기성배양은검체에따라통상의배지및방법을사용하였다. 혈액검체의경우약 0 ml를채혈하여호기성배지인 Bact/Alert FA와혐기성배지인 thioglycollate broth (007 년 월부터 00년 월 일까지 ) 또는 Bact/Alert FN (biomerieux, Lyon, France) (00년 월 6일부터 00년 월까지 ) 에각각접종하여 일간배양하였다. 혐기성세균의동정은 ATB A (biomerieux SA, Mary I Etoile, France), 또는 Vitek ANI (Vitek system, biomerieux Vitek Inc., Hazelwood, MO, USA) 를이용하였으며, 필요에따라서전통적인생화학적방법이나분자유전학적방법을이용하였다 (6).. 정의및분석방법 Propionibacterium 균종은피부의상재균으로임상검체에서분리되는대부분의경우감염과관련이없는것으로알려져있으므로 (7-9), 모든검체에서 Propionibacterium 균종이분리된경우오염균으로간주하였다. 혐기성균혈증은혐기성세균이 회이상분리되고, 발열, 빈맥, 오한, 백혈구증가또는저혈압등의임상증상이동반된경우로정의하였다. 혈액배양에서한종류의세균만분리되었을경우단독감염으로, 두종류이상이분리되었을경우복합감염으로정의하였다. 원내감염은입원 시간이후의뢰된혈액배양에서세균이분리되고입원시감염의증가가없는경우나타병원에서감염이발생한후전원된경우, 또는이전입원기간중감염이발생한후재입원한경우로하였다. 미국질병관리본부의원내감염에대한정의에따라병소를분류하고 (0), 병원체의원발병소를추정하기위하여의무기록을후향적으로조사하였다. 입원시점부터혈액배양에서혐기성세균이분리되기전까지감염의임상적증상이있고, 이와관련된임상검체의세균배양이양성인경우검체를채취한장기또는부위를원발병소로하였으며, 이외에도침습적시술이나수술을받은경우에는해당부위를기록하였다. 호중구감소증은절대호중구수가 00/μL 미만인경우로하였으며, 패혈성쇼크는균혈증과연관하여수축기혈압이 90 mmhg 미만이거나환자의평상시혈압에비하여 0 mmhg 를초과한혈압감소가있는경우, 또는혈압을유지하기위하여혈관수축제를사용해야했던경우로하였다. 적절한항생제치료는혈액배양을의뢰한시점이나혈액배양결과가보고된시점부터일정기간동안, 보고된균종에통상적으로항균력이있는것으로알려진항생제를사용한경우로정의하였다. Clinical Characteristics of Anaerobic Bacteremia Vol., No., 009 7
. 통계학적분석균혈증의병원내사망과관련된인자에대한통계학적인분석을위하여비연속변수에대해서는 Fisher 의정확검정 (Fisher s exact test) 또는카이제곱검정 (Chi-square test) 을, 연속변수에대하여는 t-test를시행하였고, 다변량분석 (multivariate analysis) 에는다중로지스틱회귀분석 (multiple logistic regression) 을시행하였다. 분석결과는 9% 신뢰구간과 odds ratio로나타내었으며, 양측성 (-tailed) 으로검정하여 P 값이 0.0 미만인경우를통계적으로유의한것으로하였다. 통계분석에는 SPSS.0 for Windows 소프트웨어 (SPSS, Chicago, IL, USA) 를사용하였다. 결과. 혐기성세균의분리현황 007년 월부터 00년 월까지혈액, 체액및농양검체의세균배양에서중복분리주를제외하고 9주의혐기성세균이분리되었다 (Table ). 이중검체별로농양검체에서 6주 (0.%), 혈액 주 (9.%), 복막액과늑막액등의체액검체에서 9주 (0.%) 의혐기성세균이분리되었다. 균종별로는 Bacteroides fragilis 가 7주 (.%) 로가장많았고, 다음으로 Clostridium perfringens 주 (7.6%), Peptoniphilus asaccharolyticus 주 (7.%), Anaerococcus prevotii 9주 (6.6%) 순이었다. B. fragilis 는검체의종류에관계없이많이분리되었으나, C. perfringens 는전체 주중 주가혈액검체로부 Table.DistributionofAnaerobicBacterialStrainsIsolatedfrom VariousClinicalSpecimensinaSingleKoreanHospital in007 and00 Organism Abscess Blood Bodyfluids Total Gram-positivecocci Anaerococcusprevoti Finegoldiamagnus Peptoniphilusasaccharolyticus Peptostreptococcusanaerobius Peptostreptococcusmicros Anaerobicgram-positivecocci Subtotal Gram-positivebacili Actinomycesisraeli Actinomycesodontolyticus Actinomycesspp. Bifidobacterium spp. Clostridium dificile Clostridium perfringens Clostridium spp. Subtotal Gram-negativebacili Bacteroidesdistasonis Bacteroidesfragilis Bacteroidesovatus Bacteroidesthetaiotaomicron Bacteroidesvulgatus Bacteroidesspp. Fusobacterium necrophorum Fusobacterium nucleatum Porphyromonasendodontalis Prevotelaintermedia Prevotelaspp. Subtotal 7 9 7 7 9 * *, 0 6 9 9 6 7 7 9 67 Total 6 9 9 * OneClostridium innocuum andoneb.fragilisisolateswererecoveredfrom thesamepatient OneF.nucleatum andoneb.fragilisisolateswererecoveredfrom thesamepatient Infection and Chemotherapy : Vol., No., 009
터분리되었다.. 혐기성균혈증환자의연령및성별에따른분포혈액배양에서혐기성세균이분리된 명환자의평균연령은 6.±. 세였으며, 6-70 세와 7세이상환자중각각 9명 (.%) 과 명 (.%), -60 세환자중 7명 (0.%) 에서혐기성균혈증이발생하여대부분의환자 (.%) 가 0세이상이었다. 또한남자가 명 (60.7%) 으로여자에비해많았다.. 혐기성균혈증의선행질환및원발병소혐기성균혈증환자 명의선행질환은총 96개가있었고, 이중악성종양 ( 소화관의악성신생물, 백혈병및림프종등의혈액암등 ) 예 (7.6%), 감염성질환 ( 폐렴, 요로감염, 결핵, 복강내또는피부및결체조직의농양등 ) 6예 (.%) 및소화기질환 ( 위장관염, 급성충수염및출혈을동반한위궤양등 ) 이 예 (0.9%) 였으며, 간담도질환 ( 간경화, 만성췌장염및담낭염등 ) 예 (.%), 심혈관질환 ( 급성심근경색, 만성심부전및복부대동맥류등 ) 예 (7.7%) 등도주요한선행질환으로나타났다. 원발병소를추정할수있는경우는 예였고, 이중 예 (.%) 가소화관으로부터기인했을것으로추정되었다. 이외에도 예 (.%) 는간담도, 각각 0예 (.9%) 는호흡기및비뇨기가균혈증의원발병소였을것으로추정되었다 (Table ).. 혐기성세균과동시에분리된호기성세균혐기성균혈증환자 명중 명 (%) 에서 주의호기성세균이혐기성세균과함께분리되었다. 이중 Escherichia coli가 주로가장많았고, 다음으로는 Staphylococcus epidermidis 가 주로많았다 (Table ). Table.SiteofinfectionandtheGenusofAnaerobicBacteriaIsolatedfrom theblood Siteofinfection No.ofisolates Bacteroidesspp. OtherGNR * GPC GPR Total Alimentarytract Hepatobiliarytract Respiratorytract Urinarytract Skinandsofttissue Genitaltract Bone Endocarditis Primarybacteremia 6 7 0 0 Total Abbreviations:GNR,gram-negativerod;GPC,gram-positivecocci;GPR,gram-positiverod * IncludesPrevotelaandFusobacterium species IncludesClostridium andactinomycesspecies Table.AerobicBacteriaConcomitantlyIsolatedwithAnaerobesfrom theblood Organism isolatedconcurently Genusofanaerobicisolates Bacteroidesspp. OtherGNR * GPC Clostridium spp. Total Escherichiacoli Staphylococcusepidermidis Othercoagulasenegative-staphylococci Enterococcusfaecium Klebsielapneumoniae Candidaparapsilosis Enterococcusfaecalis Pseudomonasaeruginosa Streptococcusspp. Total 6 Abbreviations:GNR,gram-negativerod;GPC,gram-positivecocci;GPR,gram-positiverod * IncludesPrevotelaandFusobacterium species Clinical Characteristics of Anaerobic Bacteremia Vol., No., 009 9
Table.DemographicsandFactorsAssociatedwithIn-hospitalMortalityin79 PatientswithAnaerobicBacteremia Characteristics/factors Overal(n=79) Alive(n=) Dead(n=7) Oddsratio(9% CI) P-value Age,mean±SD Male/female(male%) Underlyingdisease,n(%) Neoplastic Infectious Gastrointestinal Hepatobiliary Cardiovascular Siteofinfection,n(%) Digestive Hepatobiliary Urinary Respiratory Isolatedorganism,n(%) Bacteroidesspp. Clostridium spp. Polymicrobialinfection,n(%) Nosocomialinfection,n(%) No.ofpositiveculturebotle,mean±SD Cancerhistory,n(%) Neutropenia,n(%) Presentationwithshock,n(%) Recentsurgeryorinvasiveprocedure,n(%) Mechanicalventilation,n(%) ICU admission,n(%) Adequateantibiotictherapy,n(%) 6.±. /(60.) (6.) (.) 0(0.6) (9.) (9.0) (.) (.9) 9(.) 7(.9) 7(6.) (.) 7(.) 9(6.0).±0.9 (67.) (6.) (0.) (.) (.9) 9(.) 6(70.9) 6.9±.6 /0(6.) (6.) 9(.) (.) (.) 9(7.) (.) 6(.) 7(.) (7.7) 7(.9) (0.) 0(9.) 9(.).7±0.9 (6.) (.9) (.6) (.) 7(.) 0(9.) 7(7.) 6.6±. 6/(9.) 0(7.) (.) (.6) (9.6) 6(.) (.6) (.) (7.) (.) 0(7.0) (.9) 7(.9) 0(7.).9±0.9 0(7.) (.) (.9) (9.6) (.) 9(.) 9(70.).00(0.6-.).76(0.60-.9) 0.76(0.90-.7).0(0.-.).76(0.6-.0).7(0.79-6.6) 0.(0.0-.).90(0.6-.0).70(0.-.9).66(0.7-6.).6(0.-.60).70(0.99-.0).0(0.79-.) 0.(0.69-.).(0.97-.6).00(0.70-6.09) 0.96(0.7-.67) 0.60 0. 0.6 0.0 0. 0.9 0.9 0.09 0.0 0.9 0. 0.6 0. 0.06 0.9 0. 0.69 0.6 0.9 Abbreviations:CI,confidenceinterval;,notapplicable. 혐기성균혈증의예후인자생존이나사망여부를확인할수있었던 79명의환자중 7명이입원중사망하여.% 의사망률을보였으며, 대상환자의특성및예후인자는 Table 에정리하였다. 혈액배양시점의호중구감소가병원내사망과통계적으로유의한관련이있었으나, 다변량분석에서는유의하지않았다. 또한, 악성종양의기왕력, 중환자실치료, 균혈증발생시점에서의패혈성쇼크, 복합감염및원내감염등의비율이사망환자군에서더높았으나통계적으로유의하지않았다. 고찰혐기성세균은흔히여러감염증을일으킬수있다. 혐기성세균감염중에는다른혐기성혹은호기성세균과의혼합감염이흔하고 (), 혐기성세균배양에상당한시간, 비용및기술이요구되므로감염증의진단과치료에어려움이있을수있다. 본연구에서는임상검체에서분리된혐기성세균에대한해석의어려움을피하기위하여농양, 혈액및체액검체에 서분리된세균만을분석하였다. 그결과 B. fragilis 가 7 주 (.%) 로가장많이분리되었고, 다음으로 C. perfringens가 주 (7.6%) 였다. Bacteroides 균종은임상검체에서분리되는혐기성세균중가장흔하며높은사망률과관련되어있는것으로알려져있다 (). 또한, B. fragilis 는사람의장에서분리되는상재균의 0.% 에불과하나임상검체에서혐기성세균들중가장흔하게분리되는만큼, 병원성이상대적으로강하고다른혐기성세균에비하여항균제내성률이높다고알려져있다 (). 본연구에서 종의대상검체모두에서그람음성간균 (67/9,.%) 이가장많이분리되었으나, 농양검체의경우에는그람양성구균의비율 (7/6, 9.0%) 이다른검체에비하여높았다. 이는각종인체부위에서채취한농양검체를분석한이전의연구에서그람음성간균과그람양성구균이각각 6.% 와 6.% 를차지한다고보고하였던결과와유사하여 (), 검체의종류에따라흔히분리되는세균의종류에차이가있음을알수있었다. 혈액을제외한임상검체의혐기성배양에사용한 PEBA 는 Enterobacteriaceae 의증식과 Proteus 균종의유주 (swarming) 는억제하는반면혐기성그람양성및음성세균은증식하여 0 Infection and Chemotherapy : Vol., No., 009
혐기성세균배양에유용하다 (). 그러나, 일부혐기성세균은억제되어균종별분포및분리율에영향을줄수있다 (). Chung 등은혐기성세균배양에 PEBA 를사용하는경우 Fusobacterium nucleatum 이다른배지에비하여잘증식되지않았다고보고하였다 (). 본연구에서도 Fusobacterium 균종의분리가적어, 정확한혐기성세균균종별분포및분리율을알기위하여 가지이상의혐기성세균배양용배지를사용하는것이바람직할것으로생각된다. 본연구에서는 Propionibacterium acnes가분리된경우오염균으로간주하여연구대상에포함하지않았다. 007 년에시행한흡인액, 혈액및복막액배양에서분리된혐기성세균은중복분리주를제외하고총 주였으며, 이중 P. acnes 는각각 주, 주및 주로총 주 (.7%) 였다. 특히혈액배양에서는 주의혐기성세균중 P. acnes 가 주 (.9%) 로가장많았다. 그러나, 그중 환자에서만혈액배양 병에서 P. acnes 가분리되었고그외의모든경우 병에서만분리되었으며, 이에대하여본연구에서는더이상임상적의의를조사하지않았다. 과거의혐기성세균분리율증가는혐기성세균분리기술의발전에의한것으로생각되어왔으나, Fenner 등은최근 0년간혐기성세균의분리빈도가감소하였다고보고하였다 (0). 그러나, 다른연구자들은혐기성균혈증의빈도가최근다시증가하고있다고하여연구기관이나시기에따라차이를보였으며 (9, 6), 이는연구기관의규모, 환자군, 혈액배양건수및양성률등의차이로인한것으로생각된다. 지난 0년간본대학병원에서시행된혈액배양에서의혐기성세균분리빈도를살펴보면, 우선연구대상기간동안처방된혈액배양건수는연평균 9, 건으로 97-9년의 7,7건, 9-99 년 0,7 건, 99-00년,69건과비교하여현저히증가하였다. 양성혈액배양중혐기성세균이차지하는백분율은 97-9 년.% 에서 (7) 9-99 년.% (), 99-00년.9% 로증가였다가 (9), 본연구대상기간에는.% 로다시감소하였다. 혈액배양양성환자중혐기성세균이분리된환자의백분율도해당대상기간별로각각.9%,.7%,.6%,.96% 로변화하여양성혈액배양중혐기성세균의백분율변화와유사하였다. 한편, 혐기성균혈증의원인균종중 B. fragilis 가.6 % 로가장많았고다음으로 C. perfringens 가 % 를차지하였다. 다른연구들에서도혐기성균혈증의원인균으로 B. fragilis 군세균이약 6-6%, Clostridium 균종이약 -6% 를차지하여가장흔한원인균이라하였다 (9,, 0). 또한, Claros 등은 B. fragilis 가성인환자에서균혈증 의원인중약 0% 를차지하며혈액에서분리된 B. fragilis 중 9% 에서장독소를생성하여병독성이높은균종이라하였다 (). 본연구에서혐기성균혈증은주로 0세이상과악성종양을가지고있는환자에서호발하는것으로나타났고, 소화기및간담도의악성종양이나감염이주요한선행질환이었으며, 이는국내에서시행된이전의연구결과와유사하였다 (). 암환자를대상으로시행된한연구에서는혈액종양 (9%) 및소화기종양 (7%) 이가장흔한선행질환으로나타났고, 적절한항균제치료를받지않은환자의경우사망률이 6% 로높았다 (0). 혐기성균혈증의원발병소로는소화기를통한감염이가장흔하였으며, 다른여러연구에서도비슷한결과를보였다 (,, ). 또한, 혐기성세균과함께분리되는호기성세균으로 E. coli 주 (.%) 를비롯하여, E. faecium 주 (.%), K. pneumoniae 주 (9.%) 등의장내세균이.% 를차지하여, 다른연구결과와유사하였고 (, ), 이는균혈증의원발병소로소화관이가장흔하기때문으로생각된다. 따라서, 소화기수술을받거나소화기의악성종양이있는환자의경우, 예방적항혐기성항생제치료가필요할것이다 (). 본연구에서는혐기성균혈증환자의병원내사망과관련된위험인자를찾기위하여환자의의무기록을후향적으로검토하였다. 그결과, 혈액배양시의호중구감소가병원내사망과통계적으로유의한관련이있었으나, 다변량분석에서는통계적유의하지않았다. 악성종양의기왕력, 패혈성쇼크, 중환자실입원, 복합감염및원내감염등의인자가환자의불량한예후와관련된것으로추정되었으나, 연구대상환자수가제한적이어서통계적유의성을증명할수없었다. 이번연구에서본대학병원의임상검체에서흔히분리되는혐기성세균은 B. fragilis 와 C. perfringens 이었으며, 혐기성균혈증은주로고령및악성종양이있는환자에서소화관의감염을통하여발생하였고 % 의사망률을보였다. 그러나병원내사망과관련된명확한위험인자를발견할수없어이에대한지속적인연구가필요할것으로생각된다. 감사의글본연구는 00 년보건의료기술연구개발사업 (A000) 연구비로수행되었습니다. Clinical Characteristics of Anaerobic Bacteremia Vol., No., 009
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