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1 Clinical Article The Korean Journal of Sports Medicine 2012;30(2): 사람의슬관절전방십자인대에서감각신경의조직학적분포 초당대학교간호학과 1, 원광대학교의과대학정형외과학교실 2, 원광의과학연구소 3 김광미 1 ㆍ전철홍 2,3 ㆍ김봉규 2 The Histologic Mapping of Sensory Innervation in the Human Anterior Cruciate Ligament Kwang Mee Kim, PhD 1, Churl Hong Chun, MD 2,3, Bong Gyu Kim, MD 2 1 Department of Nursing School, Chodang University, Muan, 2 Department of Orthopaedic Surgery, Wonkwang University School of Medicine, Iksan, 3 Institute of Wonkwang Medical Science, Iksan, Korea Recently, rising curiosity on remnant preservation technique of anterior cruciate ligament (ACL) reconstruction, there is much interested in being and distribution of the mechanoreceptor of ACL. So, we performed histologic analyzing and mapping of sensory nerve fiber of the human ACL in this study. Total of 20 anterior cruciate ligaments were obtained from total knee replacement. Each ACL samples was divided into seven specimens; tibial insertion site, mid transitional site, femoral insertion site, and in between the sites, and total of 140 tissue samples were stained with hematoxylin-eosin and immunohistochemical, and observed with light microscope. Five hundred thirty-four fine neuroparticle structures, Ruffini corpuscles, and free nerve endings were observed in 20 ACL samples. The mean of fibers observed were 1.88, 1.71, 1.15, 1.08, 1.15, 1.55, and 1.82, respectively from tibial insertional site to femoral insertional site. With immunohistochemical stain, S-100 protein was strong positive at nerve cells, but was weak positive or negative at neurofilament. Mapping of sensory nerve distribution were done based on the results. We identified the mechanoreceptor of the human ACL using optical and immunohistochemical methods and mapped the histologic distribution of that. Key Words: Anterior cruciate ligament, Proprioception, Histological mapping, Mechanoreceptor 서 론 Received: August 14, 2012 Revised: October 10, 2012 Accepted: November 14, 2012 Correspondence: Churl Hong Chun Department of Orthopaedic Surgery, Wonkwang University School of Medicine, 859 Muwang-ro, Iksan , Korea Tel: , Fax: cch@wonkwang.ac.kr CC This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. 슬관절의전방십자인대손상은진행성의슬관절불안정성과무력감을초래하게되는데, 근래진단및수술방법등의발전에힘입어술후만족할만한결과를보이고있다. Chun 등 1) 은동종건을이용한전방십자인대재건술 12개월후광학현미경상정상전방십자인대와조직학적으로유사한소견을보인다고보고하였다. 그러나전방십자인대재건술을통해전방십자인대의기계적안정성을복원하였음에도불구하고, 실제스포츠활동등의기능적결과와는일치하지않는경우들을경험하게된다. Hogervorst와 Brand 2) 는전방십자인대의기 130 대한스포츠의학회지

김광미외. 사람의슬관절전방십자인대에서감각신경의조직학적분포 계적수용기 (mechanoreceptor) 에의한고유수용감각 (proprioception) 기능이슬관절기능과많은관련이있을것이라고하였다. 최근이런고유수용감각의보존을통해술후재활치료의효과를증진시키기위해여러저자들에의해잔류조직보존술식을이용한전방십자인대재건술이많이보고되고있다 3-5).

그리고, 보고된결과를살펴보면, Zimny 등 13) 은경골부착부에감각신경수용체가주로분포되어있다고보고한반면, Schultz 등 11) 은대퇴부착부에감각신경수용체의주된분포를보고하여아직이견이많이있다. 최근잔류보존술을이용한전방십자인대재건술의관심이높아지면서전방십자인대에서기계적수용기의존재및분포에대한관심역시높아지고있다.

연구재료 2008년 1월 19일부터 2008년 12월 16일까지슬관절퇴행성관절염에대해슬관절전치환술을시행받은환자중육안적으로건강한전방십자인대를가지고있는 20명의환자에서수술중경골및대퇴골부착부의골을포함하여 20개의전방십자인대를채취하였다. 보관중전방십자인대의해부학적방향의착오를없애기위해, 채취하면서대퇴부착부의내측에실을 이용하여매듭을만들었다 (Fig. 1).

2 김광미외. 사람의슬관절전방십자인대에서감각신경의조직학적분포 계적수용기 (mechanoreceptor) 에의한고유수용감각 (proprioception) 기능이슬관절기능과많은관련이있을것이라고하였다. 최근이런고유수용감각의보존을통해술후재활치료의효과를증진시키기위해여러저자들에의해잔류조직보존술식을이용한전방십자인대재건술이많이보고되고있다 3-5). 동물을이용한십자인대의감각신경섬유에대한동물적연구는종종보고되고있으나 6-10), 인체의전방십자인대의감각신경섬유에대한연구는전방십자인대조직의습득이어렵기때문에드물다 11,12). 그리고, 보고된결과를살펴보면, Zimny 등 13) 은경골부착부에감각신경수용체가주로분포되어있다고보고한반면, Schultz 등 11) 은대퇴부착부에감각신경수용체의주된분포를보고하여아직이견이많이있다. 최근잔류보존술을이용한전방십자인대재건술의관심이높아지면서전방십자인대에서기계적수용기의존재및분포에대한관심역시높아지고있다. 이에저자들은전방십자인대에서기계적수용기의존재및분포범위에대한조직학적확인후이를지도화 (histologic mapping) 하기위해연구를시행하였다. 연구방법 1. 연구재료 2008년 1월 19일부터 2008년 12월 16일까지슬관절퇴행성관절염에대해슬관절전치환술을시행받은환자중육안적으로건강한전방십자인대를가지고있는 20명의환자에서수술중경골및대퇴골부착부의골을포함하여 20개의전방십자인대를채취하였다. 보관중전방십자인대의해부학적방향의착오를없애기위해, 채취하면서대퇴부착부의내측에실을 이용하여매듭을만들었다 (Fig. 1). 채취된전방십자인대의평균길이는 40.9 cm ( 범위, cm) 였으며, 평균두께는 18.4 cm ( 범위, cm) 였다. 환자의평균연령은 60.9세 ( 범위, 51 66세 ) 였으며, 남자는 3명이었으며, 여자는 17명이었다 (Table 1). 2. 연구방법신경조직을관찰하기위하여핵과주변단백을각각염색하여관찰하는 hematoxylin & eosin (H&E) 염색법과항원항체결합을이용하여 S-100 단백에대한면역조직화학염색법을통해관찰하였다. 환자로부터채취된조직을 20% formaldehyde가함유된마스크폼 2A (DanaKorea, Seoul, Korea) 에 24시간고정하였고, 이때뼈조직이포함된조직에대하여는탈회를시행하였으며, 각각의조직을경골부착부 (tibial insertion, TI), 중간이행부 (segment, S2-6), 대퇴골부착부 (femoral insertion, FI) 및그사이범위에서각각 2개군으로구분하여 7개씩, 총 140개의조직을얻었다 (Fig. 1). 이후자동침투기를이용하여탈수, 투명, 침투과정을거친다음에파라핀으로포매하여 4 μm 두께의연속절편을제작하고유리슬라이드에부착해서 H&E 염색을, ProbeOn Plus Microscope-slide (Fisher Scientic, Pittsburgh, PA, USA) 에부착하여면역조직화학염색을시행하였다. 1) H&E 염색조직이부착된유리슬라이드를 dry oven (58 o C) 에서 1시간이상가열처리한후에실온에서식힌후탈파라핀및저농도의알코올과정을거쳐함수한다. 이후 hematoxylin 용액 (5분), 분별및청색화과정을거쳐 eosin 염색 (1분) 을한다음탈수, 투명과정을거쳐봉입하였다. Fig. 1. (A) Intraoperative photograph showed gross finding of healthy anterior cruciate ligaments. (B) The anterior cruciate ligament was completely excised with attached bone blocks and was tagged at femoral attachment site. (C) The specimens was respectively cross-sectioned by 7 groups. 제 30 권제 2 호

6.24. Normal 5 63/F Left DO 2008.10.7. Normal 6 61/M Right DO 2008.1.19. Normal 7 63/F Left DO 2008.2.25. Normal 8 51/F Right DO 2008.12.16. Normal 9 66/F Left DO 2007.12.15.

3 KM Kim, et al. The Histologic Mapping of Sensory Innervation in the Human Anterior Cruciate Ligament Table 1. Patient analysis data Pt Age/sex Side Diagnosis Operation date ACL gross finding 1 63/F Left DO Normal 2 61/M Right DO Normal 3 62/F Left DO Normal 4 59/M Right DO Normal 5 63/F Left DO Normal 6 61/M Right DO Normal 7 63/F Left DO Normal 8 51/F Right DO Normal 9 66/F Left DO Normal 10 63/F Right DO Normal 11 61/F Left DO Normal 12 62/F Left DO Normal 13 59/F Right DO Normal 14 63/F Left DO Normal 15 61/F Left DO Normal 16 63/F Left DO Normal 17 51/F Right DO Normal 18 66/F Left DO Normal 19 65/F Left DO Normal 20 55/F Right DO Normal Pt: patient, ACL: anterior cruciate ligament, DO: degenerative osteoarthritis. Fig. 2. (A) Ruffini s corpuscles and bundle with perineurium are observed (H&E, 100). (B) Nerve bundles with perineurim are seen in the loose and dense connective tissues (H&E, 400) (black arrow). 2) 면역조직화학염색조직이부착된 ProbeOn Plus Microscope slide를 dry oven (58 o C) 에서 1시간이상가열처리한후에실온에서식힌후탈파라핀및수세과정을거친후내인성과산화효소억제방법으로 Hydrogen Peroxide Block (Lab Vision, Fremont, CA, USA) 용액을사용하여 45 o C에서 5분간반응시킨후 Tris 완충액으로 4회세정하였다. 비특이적반응을줄이기위하여 Ultra V Block (Lab Vision) 용액으로 45 o C에서 3분간반응시킨후 Tris 완충액에 4회세정하였다. 일차항체인 S-100 단백 (Lab Vison, USA; 1:200) 을 45 o C에서 30분반응시키고 Tris 완충액에 4회세정한후일차항체의역가를증가시켜주고 Polymer-HRP (Lab Vision) 가일차항체에잘침투할수있도록 Primary Antibody Enhancer (Lab Vision) 용액을 45 o C에서 10분간반응시킨후 Tris 완충액에 4회세정하였다. 이차항체반응으로 F(AB) 2 fragment에 horseradish peroxidase가표지되어있는 mouse immunoglobulin G (IgG) 와 rabbit IgG 항체를검출할수는 Polymer-HRP (Lab Vision) 용액을이용하여 45 o C에서 132 대한스포츠의학회지

김광미외. 사람의슬관절전방십자인대에서감각신경의조직학적분포 Fig. 3. (A) S-100 protein positive nerve cells are presented by immunohistochemical staining for S-100 protein ( 100).

Morphological classification of mechanoreceptors according to Freeman and Wyke 8) Type Eponyms Average size (μm) Morphology I Ruffini 100 40 Globular or ovoid corpuscle with thin capsule II Pacini

4 김광미외. 사람의슬관절전방십자인대에서감각신경의조직학적분포 Fig. 3. (A) S-100 protein positive nerve cells are presented by immunohistochemical staining for S-100 protein ( 100). (B) S-100 protein positive nerve cells are presented by immunohistochemical staining for S-100 protein ( 400) (black arrow). Table 2. Morphological classification of mechanoreceptors according to Freeman and Wyke 8) Type Eponyms Average size (μm) Morphology I Ruffini Globular or ovoid corpuscle with thin capsule II Pacini Cylindrical or corpuscle with thick, lamellate capsule III Golgi Fusiform corpuscle with thin capsule IV Free nerve endings Unmyelinated free nerve endings 15분반응시킨후 Tris 완충액으로 4회세정한다음 diamminobenzidine (Lab Vision) 용액으로실온에서 10분정도발색시킨후 Tris 완충액으로 4회세정하고 Gill s hematoxylin 으로 1분간대조염색하여봉입후광학현미경하에서관찰하였고, 갈색으로발현된신경조직섬유를관찰하였다. 3) 염색결과판독결과판독은단일신경병리학자가관찰하여각슬라이드마다 neurofilament 항체에염색되어과립상으로적갈색염색이되는경우를신경섬유나기계적수용기에대한양성으로판정하였으며, 이렇게염색된신경섬유와자유신경종말의형태를보고조직학적으로분류하였다. 먼저 H&E 슬라이드에서광학현미경저배율 ( 100) 과고배율 ( 400) 로신경조직관찰및형태를확인하였다 (Fig. 2). 또한, S-100 단백면역조직화학염색을통하여저배율 ( 100) 에서갈색으로발현된신경조직의수를측정하였고, 고배율 ( 400) 에서신경조직의형태를관찰하였다 (Fig. 3). 관찰된신경조직의형태적평가는 Freeman과 Wyke 8) 의분류를인용하여, 1형 Ruffini 소체, 2형 Pacini 소체그리고 3형골지의신경인대말단 (neurotendinous endings of Golgi) 의피막이있는 3가지기계적수용체와피막이없는 무수초의자유신경종말로분류하여관찰하였다 (Table 2). 4) 통계처리경골및대퇴골부착부골과함께절제된전방십자인대를 7개의조각으로나누어경골부착부, 대퇴골부착부및 5개의중간이행부로분류하여총 7개의그룹에서 140개의조직을관찰하였으며, 각각의그룹에서관찰된총신경수를비교하였으며, 통계학적의의는 Unpaired Student t-test를통해검정하였다. 결과 1. 광학현미경적관찰소견 20개의전방십자인대를 140개의조직으로나누어광학현미경으로관찰하였을때, 지방변성등의퇴행성변화를보이는조직은없었으며, 총 534개의기계적수용기가관찰되었다. 이들을조직학적형태에따라분류하면, 원형또는타원형의얇은피막에싸인 Ruffini 소체와무수초 (unmyelinated) 의자유신경종말은형태학적으로어떠한신경소체로분류하기힘든 제 30 권제 2 호

5 KM Kim, et al. The Histologic Mapping of Sensory Innervation in the Human Anterior Cruciate Ligament Fig. 4. Typical mapping of an anterior cruciate ligament specimen representing the frequency and distribution of neural structures. TI: tibial insertion, FI: femoral insertion, S: segment. 구조물로간주하여관찰하였다. 원뿔형의두꺼운피막에싸인 Pacini 소체는관찰되지않았다. 이렇게관찰되어진소견을토대로각각의기계적수용기의위치를지도화 (mapping) 하였다 (Fig. 4). 2. 면역세포화학검사소견 면역세포화학검사상 S-100 protein에대해서는강한양성발현을보였으나, neurofilament에대해서는약한양성발현이나음성을보여준경우가많았다. 골부착부와활액막으로이행하는부위에서양성인신경조직이많이분포하고있었고, 주로경골과대퇴골부착부인대를둘러싸는활막하층 (subsynovial) 과섬유속사이 (interfascicular) 기질내에산재하였고특히혈관주위에많았다. 전방십자인대에서각부위별로관찰된평균신경수는경골부착부에서대퇴골부착부순으로 1.88개, 1,71개, 1.15개, 1.08 개, 1.15개, 1.55개, 1.82개였다 (Fig. 5). 각부위에서관찰된신경수를토대로경골 (TI) 또는대퇴골부착부 (FI) 와중간이행부의중앙조직 (S4) 의평균신경수의차이에대한분석에서중간이행부보다통계학적의의가있는증가를보였으나 (p=0.038), 대퇴골부착부에서는중간이행부보다다소는증가하였으나통계학적의의는없었다 (p=0.057). 고 찰 저자들은사람의전방십자인대를채취한후이들의기계적수용기를조직학적으로확인하였으며이를바탕으로전체 Fig. 5. Site dependent difference of nerve cell numbers. 전방십자인대에서의기계적수용기를지도화하여표시하였다. 기계적수용기는체내의모든관절주위조직및인대내에서발견되며, 그기능은생리적자극을중추신경계로전달하여관절의운동범위와관절낭의긴장도를조절하며, 관절의퇴행성변화및불안정성을방지하는근육반사에중요한역할을한다 14). Zimny 등 13) 은전방십자인대의기계적수용기로자유신경종말외에 Ruffini 소체와 Pacini 소체를관찰하였고, 이중크기가큰 Ruffini 소체는 Golgi 소체와유사하다고하였으며이를 Ruffini 소체의변형으로간주하였다. Chun과 Lee 15) 는동종건의이식후에대한조직학적연구에서, 수술후 12개월째다량의 Golgi 소체및내형질세망이관찰되었다고보고하였다. 여러연구에서전방십자인대의기계적수용기는주로 Ruffini 소체와자유신경종말이며, Ruffini 소체가가장흔한것으로기술되고있다 2,13,16). 본연구에서는기계적수용기의신경종말인자유신경종말, Ruffini 소체와 Pacini 소체가운데 Ruffini 소체와자유신경종말이관찰되었고, Pacini 소체는주로관절낭에존재하므로관절강내의인대내에서는관찰되지않았던것으로생각된다. 또한 Golgi tendon organ-like 구조의신경인대말단은주로근육과인접한부위에서관찰되므로역시관절강내인대에서는관찰되지않았던것으로생각된다. 또한여러임상연구에서고령및관절염의진행에따라고유수용감각의저하가나타난다고하였다 17-19). 본연구에사용되어진전방십자인대가고령의것이기때문에관찰되지않는기계적수용기의숫자및형태학적분류가있을수있다고생각되어진다. 각기계적수용기의기능중자유신경종말은염증과통증자극에반응하는통각수용체 (nociceptor) 이며, Pacini 소체는압박 (compression) 자극에주로활성화되는반면, Ruffini 소체는 134 대한스포츠의학회지

6 김광미외. 사람의슬관절전방십자인대에서감각신경의조직학적분포 신연 (stretch) 자극에반응하는것으로알려져있다 20-22). Clark와 Burgess 23) 는기계적수용기를반응속도에따라 Pacini 소체처럼빠른순응을보이는것은관절운동의감각을매개하고, Ruffini 소체와 Golgi tendon organ-like 구조는느린순응을보이는것들로관절의위치감각을매개한다고보고하였다. 전방십자인대에 Ruffini 소체가많이발견되는것은슬관절에서전방십자인대가신연자극과위치감각에있어주된기능을하는것과관련이있을것으로생각된다. 전방십자인대는슬관절의고유수용감각에중요한구조물이다. Schultz 등 11) 은사람의전방십자인대에서기계적수용기의존재및슬관절의고유수용감각역할에있어전방십자인대의역할대해서보고하였고, Ochi 등 24) 도전방십자인대의고유수용감각기능과기계적기능에대해기술하였으며, Schutte 등 25) 도역시사람의전방십자인대는자유신경말단과같은기계적수용기에의해신경지배를받고있다고하였다. 저자들역시, 사람의전방십자인대를 H&E 염색과 S-100 protein에대한면역조직화학법을통해전방십자인대에서기계적수용기의존재및분포를확인하였으며, 이런기계적수용기가슬관절에서고유수용감각기능에있어서중요한기능을수행할것이라생각한다. Zimny 등 13) 은고유수용감각기능을가진기계적수용기가전방십자인대의경골부착부위에주로존재한다는것을조직학적으로증명하였다. 저자들은전방십자인대에서, 특히양끝의골부착부와활액막으로이행하는부위에서 S-100 protein 면역화학적염색에양성인신경조직이많이분포하고있는점과경골부착부에서대퇴골부착부까지 1.88개, 1,71개, 1.15 개, 1.08개, 1.15개, 1.55개, 1.82개의신경수가관찰되었고, 경골부착부에서통계학적의의가있는결과를가짐을통해경골부착부에고유수용감각을가진기계적수용기들이주로분포함을도출하였다. 더욱이, 본연구에서는신경조직의존재에대한관찰에서그치지않고, 그분포를토대로사람의전방십자인대의신경조직을조직학적으로지도화하여횡단면에서의신경조직의분포도출하여전방십자인대잔류보존술을이용한전방십자인대재건술에이를실제적으로적용할수있게하였다. 관절경적십자인대재건술을시행할때파열된인대의잔류조직을완전히제거하면, 수술중시야를넓히는데도움이되어인대재건작업을손쉽게할수있게할뿐아니라동시에충돌증후군의발생위험도를낮출수있다. 이에반해전방십자인대파열후잔재를보존하는방법은수술시야를좋지않게하여재건술시정확한삽입점을찾기어렵게만들뿐만 아니라 Cyclops lesion 에의한신전장애등을유발할수있다. 그러나, 잔류보존술시잔류조직에남아있는기계적수용기에때문에고유수용감각기능을유지하여좋은결과를얻을수있다고하였다. 이에대해 Lee 등 5) 은전방십자인대재건술시경골부착부에서많은잔류조직을남길수록, 고유감각기능의향상을가져올수있다고하였다. 그리고, Adachi 등 26) 역시전방십자인대재건술을시행할때파열건의잔류조직을보존하는군이파열건을제거하고십자인대재건술을시행한군에비하여전후방안정성과인대말미의강직성등에서좋은결과를보고이며, 관절위치감각의정확도에서도좋은결과를보고하였다. 본연구에서는전체전방십자인대내에서의기계적수용기들의분포를조직학적지도화하였고, 이를통해경골부착부에고유수용감각을가진기계적수용기들이주로분포함을관찰하였다. 이는전방십자인대재건술시에파열된전방십자인대의잔류조직을완전히제거하지않고보존하는것, 특히경골부착부의잔류조직을최대한보존함으로써, 전방십자인대재건후고유수용감각의유지에도움이될것으로생각된다. 본연구의제한점으로는, 사용된전방십자인대가평균연령이 60.9세로비교적고령의것이다. 이는잔류조직보존술을이용한십자인대재건술이흔히시행되는젊은환자의것과는기계적수용기의숫자와발견된수용체의분류에서차이가있을것이라생각된다. 그러나, 젊은환자의전방십자인대전체를얻는것은어려운일이고또한전방십자인대의기계적수용기에대한조직학적지도화의관련된보고가없어, 본연구는앞으로의전방십자인대의기계적수용기에대한연구의초석이될뿐아니라잔류조직보존술을이용한전방십자인대재건술의이론적바탕이될수있을것이라생각된다. 참고문헌 1. Chun CH, Han HJ, Lee BC, Kim DC, Yang JH. Histologic findings of anterior cruciate ligament reconstruction with Achilles allograft. Clin Orthop Relat Res 2004;(421): Hogervorst T, Brand RA. Mechanoreceptors in joint function. J Bone Joint Surg Am 1998;80: Ahn JH, Lee YS, Ha HC. Anterior cruciate ligament reconstruction with preservation of remnant bundle using hamstring autograft: technical note. Arch Orthop Trauma Surg 2009;129: Kim SJ, Jo SB, Kim TW, Chang JH, Choi HS, Oh KS. A modified arthroscopic anterior cruciate ligament double-bundle reconstruction technique with autogenous quadriceps tendon 제 30 권제 2 호

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( )Jkoa123.hwp J Korean Orthop Assoc 2006; 41: 811-817 파열된전방십자인대잔류조직내기계적수용기 이병일 민경대 윤은수 김준범 최형석 이동화 * Mechanoreceptors in the Remnants of Ruptured Anterior Cruciate Ligaments in Human Knees Purpose: This study was performed