Chinese Journal of Tissue Engineering Research ›› 2023, Vol. 27 ›› Issue (29): 4745-4750.doi: 10.12307/2023.675
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Zhou Guangzhi1, Tai Dongxu2
Received:
2022-08-22
Accepted:
2022-10-12
Online:
2023-10-18
Published:
2022-12-02
Contact:
Tai Dongxu, Doctoral candidate, Professor, Chief physician, Second Department of Orthopedics and Trauma, Affiliated Hospital of Liaoning University of Traditional Chinese Medicine, Shenyang 110032, Liaoning Province, China
About author:
Zhou Guangzhi, Master candidate, Physician, Liaoning University of Traditional Chinese Medicine, Shenyang 110032, Liaoning Province, China
CLC Number:
Zhou Guangzhi, Tai Dongxu. Research advances in animal models of ankle osteoarthritis[J]. Chinese Journal of Tissue Engineering Research, 2023, 27(29): 4745-4750.
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2.1 踝关节骨关节炎病因 2.1.1 创伤性关节炎 创伤性骨关节炎是踝关节骨关节炎最常见的形式[7]。危险因素包括:Weber C型骨折、内外踝骨折、关节脱位、体质量指数、年龄、术后时间,在具有3个或以上危险因素的患者,在术后12-22年中发生创伤性骨关节炎的概率为60%-70%[8]。创伤性骨关节炎的发生是多种因素作用的结果。首先严重的关节内骨折往往影响关节软骨的再生,踝关节中任何部位的软骨损伤都是踝关节创伤性骨关节炎发展的独立危险因素[9];其次创伤后生物力学的改变可能会改变踝关节力学负荷分布,导致关节软骨损伤[10]。慢性踝关节不稳如何导致创伤性骨关节炎的明确机制尚不清楚,机械因素可能在疾病过程中起一定作用[11],在严重的踝关节扭伤时,内侧距骨及穹隆软骨常常受累较大,损伤较外侧病变更深(图3),这种损伤机制可以距骨软骨的解剖学分布解释。但约95%的严重踝关节扭伤导致距骨软骨损伤中,仅半数的患者会出现骨关节炎[12],因此仅靠关节不稳并不能完全解释创伤性骨关节炎的发生率。"
2.1.2 原发性骨关节炎 生理状态下的软骨组织由单一类型的软骨细胞及细胞外基质组成,踝关节局部软骨组织结构特殊,踝关节单位厚度的软骨细胞密度[(41±34)×103/mg]比膝关节软骨[(28±26)×103/mg]高48%[4]。虽然临床中踝关节骨关节炎绝大多数属于创伤性骨关节炎,但与膝关节相比,踝关节不容易罹患软骨退行性疾病(即原发性骨关节炎)[7]。而原发性骨关节发病机制的经典观点是与年龄相关的关节退行性变,严重的关节软骨表面磨损以及软骨下骨的硬化乃至关节力学的改变是其病理学变化的主要的特征[13]。在JALEEL等[14]关于踝关节骨关节炎的流行病学调查中,仅有7%的患者患有原发性踝关节骨关节炎。由于踝关节软骨组织独特的组织学结构,如软骨厚度相对较薄、软骨刚性较高,因此在组织学上稳定性更高[4]。同时踝关节软骨的细胞外基质特性也使得原发性骨关节炎的发生较少[13],见表1。"
2.2 踝关节骨关节炎动物模型 2.2.1 创伤性骨关节炎动物模型 (1)小鼠踝关节不稳致骨关节炎模型:小鼠踝关节骨关节炎的3种不稳定模型包括离断内踝韧带的内侧不稳模型、离断外踝韧带的外踝不稳模型及内外踝韧带皆离断的不稳模型。因内踝韧带对于维持胫距关节稳定的重要性,在内侧不稳模型中,损伤主要累及胫距关节,而距下关节受累较少;相反,在外侧不稳模型中,距下关节主要受累较为明显,而胫距关节受到的损伤较少[15]。 在踝关节外侧韧带中,目前缺乏小鼠距腓前韧带(ATFL)与人类的距腓前韧带功能(限制距骨前移及内翻,踝关节主要稳定装置)是否一致的研究[16]。跟腓韧带(CFL)是距下关节的主要稳定器,并且是小鼠踝关节外侧唯一坚固的韧带,在外踝不稳模型中,一般切除外侧韧带(包括距腓前韧带,跟腓韧带)就可导致距下关节的严重不稳定,是踝关节骨关节炎模型最常用,较简便的动物造模方式。 在内侧不稳模型中,末端转移酶(terminal deoxyribonucleotidyl transferase,TdT)介导的脱氧尿嘧啶核苷三磷酸(dUTP)和Adamts5(ADAM Metallopeptidase With Thrombospondin Type 1 Motif 5)表达在骨关节炎早期和中期均得到增强,基质金属蛋白酶13(MMP13)的表达在骨关节炎发展过程中也呈逐渐升高的态势[17]。在人类中,距腓前韧带或跟腓韧带断裂是踝关节骨关节炎的常见原因;然而,单侧不稳与胫距关节或距下关节骨关节炎之间的关系还未完全阐明。需要对人类和动物模型的进一步的研究[18]。 (2)猪踝关节内骨折模型:该模型用于研究关节内骨折诱导的创伤性骨关节炎以及因关节表面损伤而引起的慢性踝关节力学改变的影响[19]。GOETZ等[20]将尤卡坦迷你猪的胫骨远端采用开放骨折手术,并使用骨板内固定进行修复,术后进行关节液分析、影像学及力学分析,12周时处死动物。检测了相关炎性细胞因子的表达,进行骨软骨组织学分析。到术后12周,所有骨折均愈合,肢体负荷恢复正常;滑液中的炎性细胞因子浓度,包括肿瘤坏死因子α、白细胞介素1β、白细胞介素6和白细胞介素8在骨折后2周内短暂升高;与解剖学重建的关节相比,关节不协调关节的组织学评分更差。该模型复制了人类关节内骨折的关键特征,包括手术稳定、炎症反应和进展为骨关节炎软骨变性,从而为将有希望的治疗方案转化为临床实践提供了一个潜在的有用模型。 2.2.2 非创伤性动物模型 (1)大鼠踝关节内药物注射诱导骨关节炎模型:此方法主要将致炎或有毒化合物注射至关节腔内,通过腐蚀软骨组织的细胞外基质从而诱导骨关节炎发生。与膝关节常用的木瓜蛋白酶不同,踝关节并未有使用该药物诱导踝骨关节炎发生的报道,可能与踝关节与膝关节软骨组织结构不同有关。SCOTT等[21]将白细胞介素1β注射到大鼠的踝关节诱导急性骨关节炎模型,注射后24 h检测关节灌洗液以及整个关节组织的基因表达和组织病理学。100 ng的白细胞介素1β即可引起关节促炎和分解代谢介质的基因表达上调,包括白细胞介素6、前列腺素内过氧化物合成酶2(PTGS2)、诱导型一氧化氮合酶(NOS2)、肿瘤坏死因子α、核因子κB、ADAMTS5和白细胞介素1β;关节灌洗液的生化分析显示氨基聚糖(glycosaminoglycan,GAG)、白细胞介素6蛋白和NO的积累;造模24 h,组织病理学已显示确切的滑膜炎改变,但因造模时间尚短,没有软骨破坏的组织学证据,但氨基多糖释放到关节灌洗液中可能表明早期细胞外基质降解。该模型的优势包括在4 h内诱导可重复的关节炎症和氨基多糖释放,有助于白细胞介素1通路拮抗剂的初始评估,但其效用受到研究持续时间短和疾病启动的非生理学方法的限制。 (2)大鼠踝关节软骨萎缩骨关节炎模型:此方法是通过关节制动,限制关节活动使关节周围软组织挛缩,从而改变关节周围应力,导致软骨萎缩、软骨下骨异常骨改建而诱导骨关节炎的方法。VASILCEAC等[22]采用Wistar大鼠踝关节固定化的方法,分析了大鼠踝关节胶原纤维的总密度、粗胶原纤维的密度和细胶原纤维的密度,比较了不同组的左右后肢,结果显示,固定化促进了细纤维和总胶原蛋白密度的降低;固定后的关节胶原纤维丢失,固定后的肌肉锻炼方案只能恢复细的胶原纤维。该模型可能有助于研究预防踝关节固定后软骨萎缩,并且与慢性踝关节不稳模型相结合,可以深入了解关节固定在慢性踝关节不稳的退行性和愈合过程中的重要性。 (3)大鼠踝关节衰老骨关节炎模型:增龄大鼠模型中可研究自发性骨关节炎的疾病过程。通过使用增龄动物,创造骨关节炎衰老模型。MORIYAMA等[23]描述了26个月大的CD/BR Sprague Dawley大鼠的自发性踝关节骨关节炎,病变范围主要集中在软骨组织及软骨下骨,滑膜病变出现较少,包括局灶性软骨细胞坏死、蛋白多糖丢失、软骨丢失以及软骨层钙化的全层病变,组织学切片表明局部增加的接触压力可能是引起踝骨关节炎的诱因;另外,雄性大鼠发病率高于雌性,这可能与雄性较高的体质量和内分泌因素引起的机械因素有关。这项研究表明,与该模型中的髋关节和膝关节相比,踝关节的骨关节炎变化的发生率和严重程度最高。但在人类中,膝关节与退行性软骨改变始终比同一个体的踝关节更严重。 (4) STR/ORT小鼠自发性踝骨关节炎模型:STR/ORT小鼠是自发性膝关节骨关节炎的成熟模型[24],雄性易受累,关节周围软组织结构的早期钙化是该模型的突出特征[25]。STR/ORT小鼠膝关节和踝关节骨关节炎的进展不同;在雄性小鼠中,膝关节骨关节炎与年龄的增长相关,而踝关节骨关节炎在五六月龄的小鼠中发病率显著增加,后趋于平稳,组织学显示,踝关节周围异常增生骨质形成,距骨骨间韧带从3月龄左右开始矿化;膝关节和踝关节骨关节炎的发展在单个小鼠内是独立的。STR/ORT小鼠骨关节炎的病因尚不完全清楚,但目前基于转录谱的Meta分析显示,软骨内骨化相关的基因表达被上调,基质金属蛋白酶13和X型胶原表达增加,组织矿化调节因子的差异表达,表明与软骨内生长相关的固有软骨细胞存在缺陷[26]。在该模型中,在软骨变性前的软组织钙化过多,病理生理学不能反映人类踝关节骨关节炎。 (5) BCBC/Y 小鼠踝关节发育不良骨关节炎模型:BCBC/Y小鼠是从一种肉桂色毛发、骨关节病易感的B6C3F1小鼠中诞生,这种小鼠的特征是脚尖走路,骨关节炎改变,如骨组织的侵蚀或融合,在其踝关节中尤为明显。在BCBC/Y小鼠低龄期阶段,组织病理学上即观察到软骨退行性改变,进而可观察到关节软骨松动、裂缝和侵蚀,其特征在于与异常骨赘的关节融合;从9月龄左右开始出现进行性踝关节肿胀;到10-20个月时,这些小鼠表现出异常的姿势和步态。在组织学检查中,BCBC/Y小鼠早期软骨病变包括软骨细胞坏死、软骨纤维化和变薄,进而发展至包括全层软骨缺损以及软骨肥大化,严重的骨赘进展为关节强直,最后导致踝关节的关节融合[27]。这种非典型关节病理变化存在的疾病机制和潜在的遗传因素,对踝关节的偏好尚不能确定。 (6)豚鼠自发性踝骨关节炎模型:Dunkin-Hartley豚鼠作为骨关节炎常用动物模型,自发性骨关节炎相对容易成模,不需通过人为干预,仅令其自由活动,即可成模。此模型与人类原发性骨关节炎发病较相近,可通过此模型研究人类原发性骨关节炎的病理生理过程及环境[28]。通过组织学染色,可反映骨关节炎的特异性表征,在3月龄时,Dunkin-Hartley豚鼠踝关节出现滑膜炎表征,一部分豚鼠踝关节出现局限性软骨面磨损及轻度软骨退行性改变;6月龄时,踝关节均有中度局限性软骨退行性变、软骨细胞外基质丢失、软骨细胞凋亡,并不同程度的出现了边缘性骨赘增生和软骨下骨改变;并且随着年龄的增长Caspase3表达显著增加,软骨裂缝加深,范围变大,软骨细胞肥大化相关蛋白的表达增加,如X型胶原及基质金属蛋白酶13。 各类踝关节骨关节炎动物模型特点总结,见表2。"
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