兽研[内容请查看原文]
引言
骶髂关节（SIJ）是一个兼具滑膜和纤维软骨性质的关节，连接骶骨与髂骨，从而将脊柱与骨盆相连（Evans & de Lahunta, 2013）。在功能上，SIJ充当后肢与身体其余部分之间的连接环节，后肢产生推进力，该关节在动物四足步态运动学中发挥重要作用。除作为连接环节和力传递结构外，SIJ还具有减震功能。这对于家猫等习惯性行为包括跳跃、攀爬和奔跑的物种尤为重要（Dalin & Jeffcott, 1986a; Ellenberger & Baum, 1943; Mijsberg, 1920; Nickel et al., 2004; Salomon et al., 2020）。这些特征要求SIJ具有独特的构型和组织结构。在兽医解剖学中，SIJ通常被描述为包括一个耳状或新月形光滑、无韧带的耳状面区域，以及一个粗糙的结节区，伴有紧密的骨间韧带（Evans & de Lahunta, 2013; Salomon et al., 2020）。对马的研究为理解该耳状面的构型提供了见解，识别出三种主要形状类型，这些类型可能随年龄或病理变化而改变（Dalin & Jeffcott, 1986a; Jeffcott et al., 1985）。在老年动物和已记录有SIJ问题的动物中，观察到轮廓的不规则性，特别是关节面规则边缘出现延伸。在猫科动物中，最近一项研究识别出SIJ的六种不同形状类型（Pallandre et al., 2020）。作者将观察到的形状多样性归因于体重、捕猎行为以及由此产生的生物力学需求的差异，因为SIJ在力量传递中发挥核心作用。此外，在女性中，骨盆带和SIJ必须适应与妊娠和分娩相关的动态变化。这种性二态在女性耳状面的大小和形状上表现明显（Anastasiou & Chamberlain, 2013; Nishi et al., 2020）。然而，在马中未观察到性二态（Dalin & Jeffcott, 1986b）。值得注意的是，Dalin和Jeffcott（1986b）已证明髂骨大小与其对应骶骨之间存在正相关（Dalin & Jeffcott, 1986b）。除形态学外，SIJ因其与疼痛的关联而具有临床意义。在马医学中，SIJ功能障碍表现为跛行、椎旁肌肉紧张和触诊疼痛等问题（Barstow & Dyson, 2015; Dyson & Murray, 2003; Jeffcott et al., 1985; Nagy et al., 2020）。在人类临床环境中，SIJ功能障碍被认为是下腰痛的病因之一，疼痛可沿既定的牵涉痛模式放射至臀部、大腿甚至膝部（Fortin, Aprill, et al., 1994; Fortin, Dwyer, et al., 1994; Schwarzer et al., 1995; Slipman et al., 2000）。在此背景下，SIJ的神经支配也受到研究，尽管人类医学中关于支配SIJ结构的起源存在分歧（Cox & Fortin, 2004; Grob et al., 1995; Kampsen, 2019; McGrath & Zhang, 2005; Roberts et al., 2014; Steinke et al., 2022; Vilensky et al., 2002）。在大鼠中，SIJ的神经支配也已得到证实，这些神经已被证明可传递伤害性信号（Murata et al., 2000, 2001, 2007）。同样，在猫中，SIJ区域已发现神经组织存在，被归类为潜在伤害性组织（Sakamoto et al., 2001）。
尽管有上述所有研究，但据我们所知，小动物医学中，尤其是家猫中，关于SIJ详细形态学和神经解剖学特征的信息仍然缺乏。因此，本研究的目的是记录猫SIJ的形态变异并鉴定猫SIJ的神经支配。
[内容请查看原文]
材料与方法
为研究猫骶髂关节（SIJ）的神经支配和解剖结构，对40只成年家猫（17只绝育雌性、3只未绝育雌性和20只绝育雄性）进行了解剖。所检查动物的年龄、可能疾病及生活条件未知。动物平均体重为4.74 kg，平均臀冠长度为40.74 cm（见表S1）。安乐死后，所有标本立即冷冻（−18°C），并在进行解剖检查前解冻。所有猫均因与本无关的原因，按照动物福利法规和适用法律实施安乐死，并经主治兽医确认。标本由莱比锡的兽医诊所捐赠给解剖学、组织学和胚胎学研究所，用于研究和教学目的。解剖和三维扫描在解剖学、组织学和胚胎学研究所解剖大厅内按照现行卫生法规进行。骨盆、后肢或脊柱有明显创伤的动物，以及明显肥胖的动物被排除在本研究之外。本研究经德国莱比锡莱比锡大学兽医学院伦理委员会评估并批准（EK 7/2021）。
[内容请查看原文]
标本解剖
首先对所有猫进行称重，使用软卷尺测量冠臀长度，并记录性别。随后，将动物剃毛并使用手术刀（4号）沿背中线切开。解剖过程中使用放大倍数为3.5×的放大镜以增强精细结构的可视性。
将皮肤向侧方翻开以暴露其下的皮下组织和筋膜。识别并仔细解剖覆盖于骶髂关节上方皮肤区域内的神经，使用精细镊子进行操作。这些神经被沿腹侧追踪，穿过臀中肌和尾部的背侧横突间肌，朝向脊柱方向。暴露19只猫的椎管和脊髓以确定所发现神经的确切起源，并从皮肤处回溯追踪。在未打开椎管的标本中，神经被追踪至椎间孔和背侧骶孔。记录仅限于观察到穿过背侧骶髂韧带的神经的存在。为实现背侧皮支起源的精确定位，将脊柱分为若干节段。分段的依据是棘突的长度及其之间的间隙（图1）。棘突区域命名根据其与相应椎骨的解剖邻近关系确定。棘间区域以其紧邻的两个相邻椎骨命名。在识别神经起源的过程中，从其皮肤附着处向内侧画一条垂线至相应的棘突或棘突之间的区域，然后记录相应的节段。
[图：在神经所在区域，根据棘突长度进行分区的示意图]
[内容请查看原文]
组织学分析
完成脊神经背侧支的解剖后，从十只随机选取的猫中切除位于骶髂关节前缘与第一骶椎棘突之间的左右背侧骶髂韧带，并进行组织学检查处理。20份样本在室温下于4%缓冲福尔马林中固定48–72小时。随后，组织经脱水并包埋于石蜡中。从每个组织块切取四张连续切片（1 μm），依次经二甲苯、异丙醇、递减乙醇梯度（96%至70%）及蒸馏水脱蜡。四张切片中的两张采用苏木精-伊红（H&E）染色（Carl Roth GmbH + Co. KG；Karlsruhe，Germany）。其余两张切片按照Constantin法采用天狼星红染色（Winter et al., 2004）。H&E是评估整体组织形态并确定切片结构方向的标准组织学染色技术。为了更精确地区分各种组织类型，并更准确地将神经纤维束与周围致密结缔组织区分开来，采用了按照Constantin法的天狼星红染色。神经的组织学鉴定依据既定的形态学标准进行。在H&E切片中，这些结构表现为染色浅淡、平行排列的神经纤维束，其之间具有特征性的扁平施万细胞核，并被神经外膜包围。在按照Constantin法的天狼星红染色中，平滑肌组织呈黄色，胶原纤维呈红色，弹性纤维呈亮紫色。相反，细胞核呈棕色。为此程序，脱蜡切片随后用3%乙酸处理，并在1%阿尔新蓝溶液（Dr. K. Hollborn & Söhne GmbH & Co. KG, Leipzig, Germany）中染色30分钟。自来水中冲洗3分钟后，样本短暂浸入70%乙醇，随后在醛品红溶液中染色15分钟（Dr. K. Hollborn & Söhne GmbH & Co. KG, Leipzig, Germany），再浸入70%乙醇。切片在自来水中冲洗3分钟，并用Weigert苏木精染色5分钟。经蒸馏水及自来水分别冲洗5分钟后，切片在0.1% van Gieson天狼星红溶液（Dr. K. Hollborn & Söhne GmbH & Co. KG, Leipzig, Germany）中染色30分钟。染色后，所有切片经递增乙醇梯度脱水、二甲苯透明，并使用ROTI® Histokitt（Carl Roth GmbH + Co. KG；Karlsruhe，Germany）封片。如上所述，每个水平制备四张连续切片，每个韧带标本重复该程序四至八次，每个标本共获得16–32张切片。组织学玻片使用配备Axiocam 208 color的Axio lab 5显微镜（Carl Zeiss Microscopy Deutschland GmbH, Oberkochen, Germany）进行检查和拍照。概览图像使用Axio Scan 7（Carl Zeiss Microscopy Deutschland GmbH, Oberkochen, Germany）数字化。随后使用Zen 3.13软件（Carl Zeiss Microscopy Deutschland GmbH, Oberkochen, Germany）对图像进行后续处理。图像使用Adobe Photoshop 2025（version 26.0, Adobe Inc., San José, CA, USA）进行调整，仅用于可视化目的。图形模板和基于矢量的标注使用Adobe Illustrator 2025（version 26.0, Adobe Inc., San José, USA）制作。
[内容请查看原文]
三维扫描、关节测量与形态
完成神经解剖和韧带切除后，使用手术刀小心打开骶髂关节。关节的各组成部分使用Artec Spider三维扫描仪（Artec 3D, Senningerberg; Luxemburg，精度0.05 mm）进行三维扫描。定义了两个区域用于关节测量：总关节面和耳状面。总表面积包括耳状面和形态学上不同的粗隆。耳状面光滑、无韧带附着且略微隆起，而粗隆则覆有韧带。为改善对比度并增强三维扫描仪的边缘检测，关节边缘及关节耳状面边缘用绿色丙烯颜料标记。获取的扫描数据使用Artec Studio软件18和19版（Artec 3D, Senningerberg; Luxemburg）处理。对于每个数据集，在对齐扫描前先去除背景。为生成三维模型，需要配准所有扫描、去除异常值并随后融合扫描。为进行形态计量分析，使用软件的橡皮擦工具沿标记边缘描绘总关节面。所得表面积即可使用软件的测量工具进行量化。为确定耳状面的大小，将该区域单独分割并使用测量工具测量。随后由一名观察者将扫描并分割的耳状面轮廓分类为不同形状类型。对关节的所有部分均独立分析左右侧以及骶骨和髂骨。分类基于Jesse等（2017）和Pallandre等（2020）提出的背侧支和腹侧支的细分（图2）。
[图：家猫左侧髋骨内侧面的3D扫描图，展示耳状面在……的细分]
[内容请查看原文]
统计分析
统计分析使用Origin Pro 2019软件（OriginLab，马萨诸塞州，美国）进行。左右两侧骶骨和髂骨的耳状面大小及总关节大小以及冠臀长采用Shapiro-Wilk检验评估正态性。关节面面积测量值呈正态分布。冠臀长数据未能确定为正态分布。耳状面大小和总关节大小的组间比较采用配对样本t检验。雄性和雌性个体关节各部分的比较采用独立双样本t检验。显著性水平设定为p < 0.05（α = 0.05）。冠臀长与表面积之间的相关性采用Spearman相关分析评估。骶骨表面积与相应髂骨表面积之间的相关性采用Pearson相关分析评估。
为量化左右骶髂关节表面之间的双侧对称性，根据Robinson等（1987）的方法计算对称指数（SI），公式如下：SI=X左侧−X右侧0.5*X左侧+X右侧×100。SI值为0%表示完全对称，而数值越大反映两侧之间不对称程度越高。
使用Python通过桑基图对神经通路进行图形化可视化（Python软件基金会，特拉华州，美国）。
[内容请查看原文]
结果
[内容请查看原文]
骶髂背侧韧带的神经支配
[内容请查看原文]
宏观检查
在所有受检猫中均检测到走行于骶髂关节韧带装置内的神经分支。重点关注第七腰神经（L7）和第一骶神经（S1）的背侧支。L7背侧支从椎间孔穿出后，在疏松结缔组织内沿骶髂关节颅侧缘向背侧走行。到达骶髂背侧韧带后，该神经分支继续在韧带浅层或深层向外侧方向走行。在深层位置，该神经分支到达臀中肌，并由此延伸为颅臀神经，具有可变的尾侧分布（图3和图4）。在1号猫中，右侧L7背侧支被撕裂，因此无法进一步追踪。
[图：第七腰神经和第一骶神经背侧支在……内解剖走行的示意图]
[图：桑基图及相应表格，展示左侧（a）和右侧（b）的神经通路。桑基图]
S1背侧支从第一骶背侧孔穿出，在骶髂关节背侧韧带装置的疏松和致密结缔组织内走行。细小的神经分支延伸进入骶髂背侧韧带。该分支随后在骶髂背侧韧带浅层走行，并经尾侧横突间背侧肌向尾外侧延伸，作为中臀神经继续分布至皮肤（图3）。L7和S1背侧支之间的吻合连接被一致观察到。
在几只猫中注意到骶髂关节神经支配模式的变异。在右侧，共有五只猫仅由S1背侧支支配，而两只猫仅由L7背侧支支配。在20号猫中，右侧骶髂关节区域未能识别到神经分支。在左侧，四只猫仅显示S1背侧支支配，而三只动物显示神经分支起源于L7。在两只动物中，左侧未发现神经分支。部分S1背侧皮支在皮肤区域分为两支。此外，在三例中，L7和S1的背侧支在双侧皮肤分布之前汇合形成共同干（图4和表1）。
TABLE 1. Variations of nerve branch origins of the feline SIJ on the right and left sides.
| Side | R. dors. L7 | Rr. dors. L7 & S1 | R. dors. S1 | None |
|---|---|---|---|---|
| Right | 2 | 32 | 5 | 1 |
| Left | 3 | 31 | 4 | 2 |
[内容请查看原文]
微观检查
韧带组织的组织学检查显示致密结缔组织中散布有疏松、血管化结缔组织束，以及肌肉和脂肪组织区域（图5）。在检查的20个样本中，有16个检测到神经。在三个左侧样本和一个右侧样本中，组织学上未能明确证实神经结构。神经在横切面和纵切面中均被观察到。然而，所有检查的神经纤维均显示有髓鞘。
[图：背侧骶髂韧带组织的组织学切片，包含致密组织、肌肉和脂肪组织以及……]
[内容请查看原文]
关节大小的统计分析
在所有标本中，无论就耳状面面积还是整个关节面而言，髂骨耳状面的平均值在两侧均超过骶骨。Spearman相关分析显示，冠臀长与表面积之间呈弱正相关（r ≤ 0.33）（表2）。相比之下，骶骨与相应髂骨的表面积之间呈强正相关（r ≥ 0.878）（图6a、b和表3）。体重与整个关节面面积或耳状面面积均无相关性。对所有标本左右侧进行比较，平均耳状面面积或整个关节面面积均无统计学显著差异。然而，在个体水平上观察到左右侧差异（图7）。SI在0附近表现出相当大的变异，平均值范围为5.56至10.78（图7和表4）。雄性（n = 20）与雌性（n = 20）猫的平均关节尺寸之间未发现统计学显著差异（表S2）。
TABLE 2. Spearman correlation coefficients ( r ) and corresponding p ‐values for non‐normally distributed parameters and variations.
| Variable 1 | Variable 2 | Correlation ( r ) | p ‐value |
|---|---|---|---|
| CRL | I AS | 0.27 | 0.016 |
| CRL | S AS | 0.33 | 0.003 |
| CRL | I TJ | 0.23 | 0.036 |
| CRL | S TJ | 0.2 | 0.077 |
[图：散点图，展示髂骨与骶骨耳状面面积之间的相关性。(a) 相关性]
TABLE 3. Pearson correlation coefficients ( r ) and corresponding p ‐values for non‐normally distributed parameters and variations.
| Variable 1 | Variable 2 | Correlation ( r ) | p ‐value |
|---|---|---|---|
| I AS | S AS | 0.88 | <0.001 |
| I TJ | S TJ | 0.96 | <0.001 |
[图：Bland–Altman图和箱线图，展示耳状面及总关节面面积的双侧差异。Bland–Altm]
TABLE 4. Descriptive statistics of the Symmetry Index (SI) for the sacroiliac joint surface area.
| SI | Mean | SD | Median | Minimum | Maximum |
|---|---|---|---|---|---|
| % | % | % | % | % | |
| I R AS—I L AS | 10.37 | 8.05 | 9.32 | 0.07 | 31.98 |
| I R TJ—I L TJ | 5.70 | 4.89 | 4.60 | 0.01 | 23.80 |
| S R AS—S L AS | 10.78 | 10.41 | 8.17 | 0.37 | 57.21 |
| S R TJ—S L TJ | 5.56 | 5.94 | 4.59 | 0.05 | 34.28 |
[内容请查看原文]
关节形状
参与形成骶髂关节的骶骨和髂骨耳状面，在左右两侧均分为背侧支和腹侧支（图2）。因此，在家猫中可识别出五种不同的形状类型（图8）。1型（“耳状”）的特征是背侧支明显比腹侧支更宽、更突出。该类型见于58.13%（93例）的受检动物。2型（“新月状”）表现为腹侧支和背侧支宽度大致相同，呈C形。该类型见于28.13%（45例）的猫。3型（“铲状”）的特征是无分支、轮廓不规则，见于一只猫的右侧骶骨（0.63%）。4型（“双叶状”）的特征是表面完全分为两部分。该类型见于8.13%（13例）的受检关节面。5型（“直状”）无弯曲或凹陷，因此无分支。5%（8例）的受检关节面可归入该类型。在大多数标本中，髂骨耳状面的形态与骶骨表面密切对应，左右两侧之间无差异。
[图：不同耳状面轮廓形状的代表性示例。耳状面以g高亮显示]
[内容请查看原文]
讨论
骶髂关节是人类医学当前和既往许多研究的关键焦点。骶髂关节在人类中已被广泛研究，尤其涉及下背痛和骶髂关节牵涉痛模式。然而，在兽医领域，关于骶髂关节的解剖学、神经支配和致痛潜力仍存在知识空白。因此，本研究旨在更详细地检查家猫骶髂关节的宏观解剖学和神经支配。
[内容请查看原文]
背侧骶髂韧带的神经支配
宏观和微观发现表明，背侧骶髂韧带主要受第七腰神经和第一骶神经的背侧支支配。腰神经和骶神经背侧支之间发现的吻合支被认为是常见的解剖学发现，正如兽医和人类文献中所述（Cox & Fortin, 2004; Evans & de Lahunta, 2013; McGrath & Zhang, 2005）。与人类医学和其他动物物种研究的比较揭示了相似性和差异性。一些研究描述人类骶髂关节的背侧神经支配仅来源于数量不等的骶段（Grob et al., 1995; McGrath & Zhang, 2005），而其他研究报道额外的神经支配主要来自腰神经背侧支（Cox & Fortin, 2004; Kampsen, 2019; Roberts et al., 2014）。相比之下，Steinke et al.（2022）已证明神经并不到达骶髂关节，而是L5至S1的分支穿过内侧骶髂韧带，S1至S4的分支穿过外侧骶髂韧带。
在大鼠中，据报道骶髂关节的神经支配来源于L4或L5至S2，显示出与人类解剖学的相似性（Murata et al., 2000, 2001）。Sakamoto et al.（2001）此前利用猫的电生理技术证明，骶髂关节及其周围韧带和肌肉含有来源于第四至第六腰神经的机械敏感性传入单位。导致观察到的支配神经数量及其来源变异的潜在因素是多方面的，且尚未完全阐明。差异的一种可能解释是物种间的解剖学变异，特别是关于腰椎和骶椎的数量。另一种可能的解释可能在于方法学差异，特别是解剖区域和所采用的检查方法。例如，在Sakamoto et al.（2001）的研究中，仅检查了L4–L6的背侧根丝。在本研究中，切开骶髂关节背尾侧区域的皮肤，然后向腹侧解剖。这种方法能够有针对性地研究骶髂关节上方特定区域的皮支。在任一研究中扩大研究区域都可能潜在地揭示腰部和骶部区域额外的神经分支。此外，本研究中神经组织的评估通过宏观和微观观察进行，而Sakamoto et al.（2001）使用了电生理方法。尽管两项研究通常都适用于验证骶髂关节的神经支配，但它们的方法学差异可能导致差异，特别是关于功能纤维类型和区域分布模式。尽管存在这些差异，骶髂关节通过腰神经和骶神经背侧支支配的基本原理在物种间保持一致。
有髓神经纤维的特征是轴突被髓鞘包围，髓鞘由施万细胞形成。在单个施万细胞之间，髓鞘中存在小间隙，称为朗飞结（Liebich, 2010; Welsch, 2006）。已知有髓神经纤维将多种刺激传递至脊髓，包括机械、热和伤害性信号（Breves et al., 2022）。本研究中韧带样本的组织学检查证明朗飞结的存在，因此20个样本中有16个存在有髓神经纤维小束（图5）。四个样本中骶髂关节神经支配证据的缺失可归因于方法学因素。组织学分析仅限于组织的特定区域。因此，神经纤维可能存在于样本未切片的部位。此外，神经纤维的尺寸可能低于标准光学显微镜的分辨率极限。在这种情况下，其检测将需要实施专门的免疫组织化学染色方法。Sakamoto et al.（2001）将骶髂关节及邻近组织中的神经分类为高阈值III类，提示伤害性功能。这可能表明本研究中描绘的某些神经结构构成伤害性传入纤维。然而，此处缺乏对伤害性神经纤维的确定性验证，但可以通过在未来的研究中使用更特异的功能性或免疫组织化学标记物来实现。
正如人类医学中大量研究已证实骶髂关节（SIJ）可作为下背痛或牵涉痛的来源一样，马医学中SIJ功能障碍也通过多种临床表现形式体现（Barstow & Dyson, 2015; Dyson & Murray, 2003; Fortin, Aprill, et al., 1994; Fortin, Dwyer, et al., 1994; Jeffcott et al., 1985; Nagy et al., 2020; Schwarzer et al., 1995; Slipman et al., 2000）。SIJ所致疼痛的这些多变临床表现可以用牵涉痛的概念来解释，牵涉痛通常发生在具有相同节段神经支配的区域（Bogduk, 2009）。鉴于SIJ神经支配的节段多样性，牵涉痛区域可能广泛且异质（Grob et al., 1995; Slipman et al., 2000）。SIJ背侧区域神经分支的解剖学鉴定为未来显微学、功能学和临床研究提供了结构基础，以评估猫的SIJ是否可引起疼痛、运动改变或临床症状。
[内容请查看原文]
关节形状
除SIJ的神经支配外，人类医学还关注耳状面的宏观形状，目前已描述三种主要形状（Jesse et al., 2017）。在兽医教科书中，耳状面在各物种中通常被描述为耳状（Dyce et al., 2010; Ellenberger & Baum, 1943; Salomon et al., 2020）或新月形（Evans & de Lahunta, 2013）。相比之下，对健康和临床正常马的研究也显示了三种主要类型（Dalin & Jeffcott, 1986a）。与对人类和马的研究以及兽医教科书中的观点不同，本研究不仅能够证明家猫中存在类似的形态多样性，还能证明其形态学特征，如Pallandre et al.（2020）所述。耳状面形态的总体相似性当然可归因于猫科物种间的解剖学相似性。研究间观察到的差异以及形状上相当大的变异可能有多种解释。Pallandre et al.（2020）将耳状面的形状归因于捕食行为的差异以及由此产生的力和运动。然而，家猫耳状面形状的多样性可能不仅由捕食行为解释，还可能受到不同运动模式的影响。家猫既作为户外宠物也作为室内宠物饲养，运动自由度各不相同。运动行为的差异，包括狩猎、跳跃和攀爬，可能影响SIJ耳状面形状的机械负荷和形态发育。此外，形状的多样性，特别是不规则轮廓或曲度，可能与年龄相关或病理性变化有关。例如，Dalin和Jeffcott（1986b）报道了马SIJ耳状面形状的年龄相关改变。老年马更频繁地表现出不规则轮廓和非典型关节形状。此外，与临床健康个体相比，表现不佳和轻度后肢跛行的马已显示出异常的关节轮廓（Jeffcott et al., 1985）。同样，Jesse et al.（2017）提出了耳状面形状与下背痛或SIJ病理之间可能存在的关联。然而，由于本研究中检查动物的生活条件、年龄和病史未知，任何关于年龄或疾病对家猫SIJ形态潜在影响的评估都应保留态度。
[内容请查看原文]
关节大小
本研究中检测到冠臀长与SIJ大小之间存在弱相关性。在其他物种中也有类似观察的报道。例如，在马中，SIJ的关节表面积从10 kg小马驹的约1.0 cm²增加到体重500–600 kg成年马的约18 cm²（Dalin & Jeffcott, 1986b）。在人类中，关节表面积从新生儿的约1.5 cm²增加到成人的约17.5 cm²（Brooke, 1924）。这些比较表明SIJ表面不一定与体型相关。此外，我们的发现显示所检查猫的关节大小无性别二态性。这与人类中的发现形成对比，人类中已描述女性和男性之间耳状面在大小和形态上的差异（Anastasiou & Chamberlain, 2013; Brooke, 1924; Nishi et al., 2020）。这种差异的一个可能解释是SIJ的性别二态性在青春期发育（Brooke, 1924）。由于大多数家猫在青春期前或青春期开始时（四至六个月龄）已绝育，可能促进性别二态性发育的激素影响可能被减弱或缺失。这初步提示SIJ形态的性别相关差异可能并非在所有个体中均匀发展至相同程度。
此外，本队列中右侧或左侧关节面相对较大的动物在统计上相互平衡，导致在群体水平上整体表现无明显差异，这可能是平均耳状面大小或总关节面大小未出现显著差异的一个可能解释。然而，个体水平的检查揭示了关节大小的不对称性，研究人群的SI值显示出较宽的范围。由于猫的SIJ尚无比较阈值，因此在本病例中无法进行明确的解释或与其他研究进行比较。然而，低SI值通常表明高度双侧对称，可能反映平衡的解剖发育和均匀的负荷分布。相比之下，较高的SI值意味着不对称性增加，从形态学角度可能提示代偿机制或单侧关节退变。普遍认为生物体并非完美的镜像；器官和骨骼结构自然表现出一定程度的不对称。原因之一是身体对“优势”侧的适应，该侧经历更频繁或更强烈的机械负荷（Auerbach & Ruff, 2006; Bass et al., 2002; Kontulainen et al., 2002; Nishi et al., 2020; Stirland, 1993; Zhang et al., 2022）。鉴于SIJ是将力从后肢传递至中轴骨骼的主要结构，这些差异可能源于高冲击活动（如跳跃或快速加速）期间的不对称负荷模式。因此，SI升高并不一定表明病理状态，而可能代表对机械需求的正常功能适应，或是既往损伤的结果。
此外，骶髂关节的骨性组成部分包括骨盆和骶骨。后者悬吊于髂翼之间，具有更大的活动度（Kiapour et al., 2020）。由于骶骨的独特位置，髂骨的关节面略大于骶骨的关节面从而有效地将其“包绕”是合理的。腹侧和背侧骶髂韧带广泛附着于髂骨，这可能进一步解释了髂骨组成部分相对较大的表面积。
[内容请查看原文]
研究局限性
在解释结果时，必须考虑研究设计固有的局限性。所检查猫的确切年龄、生活方式和病史未知，且队列主要由绝育动物组成。这限制了就功能性磨损、激素影响或特定功能障碍得出更明确结论的能力。此外，手工制备可能导致细小神经分支的漏检。缺乏关于神经模式的电生理或免疫组化确认，妨碍了关于确切神经解剖亚型的明确结论。此外，神经分支皮肤终止点的确切位置可能存在轻微偏差，因为组织未经固定而是解冻的，因此柔软且灵活。而且，形态学分类本质上具有主观性，且由于缺乏观察者误差评估而无法进行统计控制。最后，组织学评估基于代表性样本而非完整连续切片。因此，不能确定地排除可能存在微小神经支配或极细小纤维——特别是在显微镜下未检测到神经的四份样本中。
[内容请查看原文]
结论
总之，本研究对家猫SIJ的结构理解提供了两项主要贡献。研究表明背侧骶髂韧带受第七腰神经和第一骶神经支配。此外，研究记录了耳状面宏观形状的相当大的变异。雄性和雌性猫之间在耳状面大小或总关节大小方面未观察到显著差异。
然而，必须承认形态学发现并不提供临床疾病、关节功能或疼痛的直接证据。相反，它们旨在作为谨慎的描述性解剖学基础，以指导和启发未来关于SIJ功能障碍在小动物兽医医学中影响的免疫组化、功能和临床研究。
作者贡献
概念/设计：AK，NR。数据获取：AK。数据分析/解释：AK，MK，TG，SF，CM，NR。手稿起草：AK。手稿批判性修订和文章批准：AK，MK，TG，SF，CM，NR。
资助信息
本研究由Dr. Heidi und Karl‐Heinz Kübler Stiftung资助。
利益冲突声明
所有作者均无利益冲突需要披露。
支持信息
[内容请查看原文]
查看英文原文▾
[内容请查看原文]
INTRODUCTION
The sacroiliac joint (SIJ) is a combined synovial and fibrocartilaginous joint connecting the sacrum and the ilium, thereby linking the spine and the pelvis (Evans & de Lahunta, 2013). Functionally, the SIJ acts as a connecting link between the hindlimbs, which generate thrust, and the rest of the body, playing an important role in the animal's quadrupedal gait kinematics. In addition to its role as a connecting link and force transmitter, the SIJ exhibits a shock‐absorbing function. This is particularly relevant for species such as the domestic cat, whose habitual behaviors include jumping, climbing, and running (Dalin & Jeffcott, 1986a; Ellenberger & Baum, 1943; Mijsberg, 1920; Nickel et al., 2004; Salomon et al., 2020). These characteristics necessitate a distinct configuration and organization of the SIJ. In veterinary anatomy, the SIJ is commonly described as comprising an ear‐shaped or crescent‐shaped smooth, ligament‐free auricular surface area, and a rough tuberosity with tight interosseous ligaments (Evans & de Lahunta, 2013; Salomon et al., 2020). Research in equines has provided insight into the configuration of this auricular surface, identifying three principal shape types that may change with age or pathology (Dalin & Jeffcott, 1986a; Jeffcott et al., 1985). Irregularities in the outlines, particularly the presence of extensions of the regular margins of the articular surface, have been observed in older animals and in those with documented SIJ problems. Within the Felidae family, a recent study identified six distinct shape types of the SIJ (Pallandre et al., 2020). The authors attribute the observed diversity of shapes to differences in body mass, hunting behavior, and the resulting biomechanical demands, given that the SIJ plays a central role in power transmission. Additionally, in women, the pelvic girdle and SIJ must accommodate dynamic changes associated with pregnancy and parturition. This sexual dimorphism is evident in the size and shape of the auricular surface of women (Anastasiou & Chamberlain, 2013; Nishi et al., 2020). However, in horses, no sexual dimorphism has been observed (Dalin & Jeffcott, 1986b). Notably, Dalin and Jeffcott (1986b) have demonstrated a positive correlation between the size of the ilium and its corresponding sacrum (Dalin & Jeffcott, 1986b). Beyond morphology, the SIJ is of clinical interest due to its association with pain. In equine medicine, SIJ dysfunction manifests among other problems as lameness, paraspinal muscle tension, and pain upon palpation (Barstow & Dyson, 2015; Dyson & Murray, 2003; Jeffcott et al., 1985; Nagy et al., 2020). In the human clinical setting, SIJ dysfunction is recognized as a cause of lower back pain, which may radiate to the buttocks, thighs, and even the knee along established referred pain patterns (Fortin, Aprill, et al., 1994; Fortin, Dwyer, et al., 1994; Schwarzer et al., 1995; Slipman et al., 2000). In this context, the innervation of the SIJ was also investigated, though there was disagreement in human medicine about the origin of the structures innervating the SIJ (Cox & Fortin, 2004; Grob et al., 1995; Kampsen, 2019; McGrath & Zhang, 2005; Roberts et al., 2014; Steinke et al., 2022; Vilensky et al., 2002). In rats, the innervation of the SIJ has also been demonstrated and these nerves have been shown to transmit nociceptive signals (Murata et al., 2000, 2001, 2007). Similarly, in cats, the presence of nerve tissue has been revealed in the SIJ area, which was classified as potentially nociceptive (Sakamoto et al., 2001).
Despite all these studies mentioned above, there is, to our knowledge, a lack of information regarding the detailed morphological and neuroanatomical features of the SIJ in small animal medicine, particularly in domestic cats. The objective of this study is therefore to document the morphological variation of the feline SIJ and to identify the innervation of the SIJ in cats.
[内容请查看原文]
MATERIALS AND METHODS
To investigate the innervation and anatomy of the sacroiliac joint (SIJ) in cats, 40 (17 spayed female, 3 intact female, and 20 neutered male) adult domestic cats were dissected. The age, possible diseases, and the living conditions of the animals examined were unknown. The animals had an average weight of 4.74 kg and an average crown‐rump‐length of 40.74 cm (see Table S1). Post‐euthanasia, all specimens were immediately frozen (−18°C) and thawed before the anatomical examinations were conducted. All cats were euthanized for reasons unrelated to this study in accordance with animal welfare regulations and applicable legislation, as confirmed by the attending veterinarian. The specimens were donated by veterinary practices in Leipzig to the Institute of Anatomy, Histology, and Embryology for research and teaching purposes. Dissections and three‐dimensional scanning were performed in compliance with prevailing hygiene regulations in the dissecting hall of the Institute of Anatomy, Histology, and Embryology. Animals exhibiting evident trauma to the pelvis, hindlimbs, or spine, as well as those with marked obesity, were excluded from this study. The study was evaluated and approved by the Ethics Committee of the Faculty of Veterinary Medicine, Leipzig University, Leipzig, Germany (EK 7/2021).
[内容请查看原文]
Specimen dissection
Initially all cats were weighed, the crown‐rump‐length was measured using a flexible measuring tape, and sex was recorded. Subsequently, the animals were shorn and dissected along the dorsal midline using a scalpel (size No. 4). Magnifying glasses with a magnification of 3.5× were used during dissection to enhance visualization of fine structures.
The skin was reflected laterally to expose the underlying, subcutaneous tissue and fascia. Nerves within the cutaneous area overlying the SIJ were identified and carefully dissected using fine forceps. These nerves were traced ventrally through the middle gluteal muscle and the dorsal intertransversarius muscle of the tail, towards the spine. The spinal canal and the spinal cord of 19 cats were exposed to determine the exact origin of the nerves found and traced back from the skin. In specimens in which the vertebral canal was not opened, the nerves were traced to the intervertebral and dorsal sacral foramen. The documentation exclusively pertained to the presence of nerves that were observed to be passing through the dorsal sacroiliac ligament. To achieve precise localization of the origins of the dorsal cutaneous branches, the spine was divided into segments. The basis of this division was the length of the spinous processes and the spaces between them (Figure 1). The nomenclature of the regions of the spinous processes was determined by their anatomical proximity to the corresponding vertebrae. Interspinal areas are named after the two adjacent vertebrae in their immediate vicinity. In the process of identifying the origin of a nerve, a perpendicular line was drawn medially from its skin attachment to the corresponding spinous process or the area between those, and the corresponding segment was then documented.
[图：Schematic illustration of the division according to the length of the spinous processes in the regions where the nerves ]
[内容请查看原文]
Histological analysis
After completion of the dissection of the dorsal branches of the spinal nerves, the right and left dorsal sacroiliac ligaments located between the cranial margins of the SIJ and the first sacral spinous process were excised from ten randomly chosen cats and processed for histological examination. The 20 samples were fixed in 4% buffered formalin for 48–72 h at room temperature. Subsequently, tissues were dehydrated and embedded in paraffin. From each tissue block, four serial sections (1 μm) were cut and deparaffinized in xylene followed by isopropanol, a descending ethanol series (96% to 70%) and distilled water. Two of these four cuts were stained with hematoxylin and eosin (H&E) (Carl Roth GmbH + Co. KG; Karlsruhe, Germany). The remaining two sections were stained using picrosirius red according to Constantin (Winter et al., 2004). H&E is a standard histological staining technique to evaluate the overall tissue morphology and to establish structural orientation across the sections. To facilitate more precise differentiation between the various tissue types, and to enable more accurate differentiation of bundles of nerve fibers from the surrounding dense connective tissue picrosirius red according to Constantin was utilized. Histological identification of nerves was conducted using established morphological criteria. In H&E sections, these structures were defined by bundles of faintly stained, parallel nerve fibers with characteristic flattened Schwann cell nuclei situated between them and surrounded by epineuria. In picrosirius red according to Constantin staining, smooth muscle tissue is observed to appear yellow, while collagen fibers are seen to appear red and elastic fibers appear bright violet. Conversely, the nuclei manifest as brown. For this procedure deparaffinized sections were then treated with 3% acetic acid and stained for 30 min in 1% Alcian blue solution (Dr. K. Hollborn & Söhne GmbH & Co. KG, Leipzig, Germany). After rinsing in tap water for 3 min, the samples were briefly immersed in 70% ethanol and subsequently stained in aldehyde fuchsin solution for 15 min (Dr. K. Hollborn & Söhne GmbH & Co. KG, Leipzig, Germany) followed by another immersion in 70% ethanol. The sections were rinsed in tap water for 3 min and stained with Weigert's hematoxylin for 5 min. After washing in distilled water followed tap water for 5 min, the sections were stained for 30 min in 0.1% picrosirius red solution according to van Gieson (Dr. K. Hollborn & Söhne GmbH & Co. KG, Leipzig, Germany). Following staining, all sections were dehydrated through an ascending alcohol series, cleared in Xylene, and mounted using ROTI® Histokitt (Carl Roth GmbH + Co. KG; Karlsruhe, Germany). As described above, four serial sections were prepared per level, and this procedure was repeated four to eight times for each ligament specimen, resulting in 16–32 sections per specimen. Histological slides were examined and photographed using an Axio lab 5 microscope equipped with an Axiocam 208 color (Carl Zeiss Microscopy Deutschland GmbH, Oberkochen, Germany). Overview images were digitized using an Axio Scan 7 (Carl Zeiss Microscopy Deutschland GmbH, Oberkochen, Germany). Subsequent image processing of the images was performed using Zen 3.13 software (Carl Zeiss Microscopy Deutschland GmbH, Oberkochen, Germany). Images were adjusted using Adobe Photoshop 2025 (version 26.0, Adobe Inc., San José, CA, USA) for visualization purposes only. The graphical templates and vector‐based labeling were developed using Adobe Illustrator 2025 (version 26.0, Adobe Inc., San José, USA).
[内容请查看原文]
3D‐scan, joint measurements and form
After completion of nerve dissection and ligament removal, the SIJs were carefully opened using a scalpel. The individual components of the joint were scanned in three dimensions using an Artec Spider 3D‐scanner (Artec 3D, Senningerberg; Luxemburg, accuracy 0.05 mm). Two areas were defined for the measurement of the joint: the total joint surface and the auricular surface. The total surface area comprises the auricular surface and the morphologically different tuberosity. The auricular surface is smooth, ligament‐free, and slightly elevated, whereas the tuberosity is covered with ligaments. To improve contrast and enhance edge detection for the 3D‐scanner, the edges of the joint and auricular surface of the joint were marked with green acrylic paint. The acquired scans were processed using Artec Studio software versions 18 and 19 (Artec 3D, Senningerberg; Luxemburg). For each dataset, the background was removed prior to alignment of the scans. To generate a 3D model, it was necessary to register all scans, remove any outliers, and subsequently fuse the scans. For morphometric analysis, the total joint surface was delineated along the marked margins using the eraser tool of the software. The resulting surface area could then be quantified using the software's measuring tool. To determine the size of the auricular surface, this area was separately segmented and measured using the measuring tool. The outlines of the scanned and segmented auricular surfaces were subsequently classified into different shape types by one observer. The right and left sides, as well as the sacrum and ilium, were analyzed independently for all parts of the joint. The classification was based on the subdivision into dorsal and ventral limbs introduced by Jesse et al. (2017) and Pallandre et al. (2020) (Figure 2).
[图：3D scan of the medial view of the left hip bone of a domestic cat presenting the subdivision of the auricular surface in]
[内容请查看原文]
Statistical analysis
Statistical analyses were performed using the software Origin Pro 2019 (OriginLab, Massachusetts, USA). The normality of the auricular surface size and total joint size for both sacrum and ilium of left and right side as well as of the crown‐rump‐length was assessed by the Shapiro–Wilk test. Joint surface area measurements were normally distributed. The data collected on crown‐rump‐length could not be identified as normally distributed. Intergroup comparisons of the auricular surface size and total joint size were conducted using a paired‐samples t‐test. Comparison of the individual joint parts of male and female was done with an independent two‐sample t‐test. The level of significance was set at p < 0.05 (α = 0.05). To assess the correlation between the crown‐rump‐length and surface area Spearman correlations was used. To assess the correlation between the surface area of the sacrum and the corresponding ilium Pearson correlations was used.
To quantify bilateral symmetry between the left and right SIJ surfaces, the Symmetry Index (SI) according to Robinson et al. (1987) was calculated using the following formula: SI=Xleft−Xright0.5*Xleft+Xright×100 An SI value of 0% represents perfect symmetry, whereas increasing values reflect greater asymmetry between the sides.
Python was used for the graphical visualization of the nerve pathway using sanky diagrams (Python Software Foundation, Delaware, USA).
[内容请查看原文]
RESULTS
[内容请查看原文]
Innervation of the dorsal sacroiliac ligaments
[内容请查看原文]
Macroscopic examination
Nerve branches coursing within the ligamentous apparatus of the SIJ were detected in all examined cats. The focus was on the dorsal branches of the seventh lumbar (L7) and first sacral (S1) spinal nerves. After emerging from the intervertebral foramen, the dorsal branch of L7 runs dorsally along the cranial edge of the SIJ within loose connective tissue. Upon reaching the dorsal sacroiliac ligament, the nerve branch continued either superficially or deep within the ligament in a lateral direction. In this latter location, the nerve branch reached the middle gluteal muscle, and from there, it extends as the cranial clunial nerves, with variable caudal distribution (Figures 3 and 4). In cat number one, the right dorsal branch of L7 was torn and could therefore not be traced further.
[图：Schematic illustration of the anatomical course of the seventh lumbar and first sacral dorsal nerve branches within the ]
[图：Sankey plots with corresponding tables illustrating nerve pathways on the left (a) and right (b) sides. The Sankey plot ]
The dorsal branch of S1 emerged from the first dorsal sacral foramen and proceeded within the loose and tight connective tissue of the dorsal ligamentous apparatus of the SIJ. Fine nerve branches extended into the dorsal sacroiliac ligaments. This branch then coursed superficially over the dorsal sacroiliac ligaments and extended caudolaterally through the dorsal intertransversarius muscle of the tail, continuing to the skin as the middle clunial nerve (Figure 3). Anastomotic connections between the dorsal branches of L7 and S1 were consistently observed.
Variations in the pattern of SIJ innervation were noted in several cats. On the right side, a total of five cats exhibited innervation exclusively from the dorsal branch of S1, whereas two cats exhibited innervation exclusively from the dorsal branch of L7. In cat number 20, no nerve branches could be identified in the SIJ region on the right side. On the left side, four cats demonstrated innervation from the dorsal branch of S1 exclusively, while three animals exhibited nerve branches originating from L7. In two animals, no nerve branches were found on the left side. Some of the dorsal cutaneous branches of S1 split into two in the skin area. Moreover, in three cases, the dorsal branch of L7 and S1 converged to form a common trunk prior to their cutaneous distribution bilaterally (Figure 4 and Table 1).
TABLE 1. Variations of nerve branch origins of the feline SIJ on the right and left sides.
| Side | R. dors. L7 | Rr. dors. L7 & S1 | R. dors. S1 | None |
|---|---|---|---|---|
| Right | 2 | 32 | 5 | 1 |
| Left | 3 | 31 | 4 | 2 |
[内容请查看原文]
Microscopic examination
Histological examination of the ligamentous tissue revealed dense connective tissue interspersed with strands of loose, vascularized connective tissue, as well as areas of muscle and adipose tissue (Figure 5). Nerves were detected in 16 of the 20 samples examined. In three left side samples and one right side sample, nervous structures could not be clearly verified histologically. The nerves were observed in both transverse and longitudinal sections. However, all nerve fibers examined showed myelination.
[图：Histological sections of the dorsal sacroiliac ligamentous tissue containing dense, muscle and adipose tissue as well as]
[内容请查看原文]
Statistical analysis of joint size
Across all specimens, the mean auricular surface of the ilium, both with respect to the auricular surface area and the total joint surface, exceeded that of the sacrum on both sides. Spearman correlation analyses demonstrated a weak positive correlation (r ≤ 0.33) between crown‐rump‐length and surface area (Table 2). By contrast, a strong positive correlation was observed between the surface area of the sacrum and the corresponding ilium (r ≥ 0.878) (Figure 6a,b and Table 3). Body weight demonstrated no correlation with either total joint surface area or auricular surface area. Comparison of the right and left sides across all specimens revealed no statistically significant differences in mean auricular surface or total joint surface area. However, side‐to‐side differences were observed at the individual level (Figure 7). The SI showed a considerable variation around 0, with mean values ranging from 5.56 to 10.78 (Figure 7 and Table 4). No statistically significant disparities were identified in mean joint dimensions between male (n = 20) and female (n = 20) cats (Table S2).
TABLE 2. Spearman correlation coefficients ( r ) and corresponding p ‐values for non‐normally distributed parameters and variations.
| Variable 1 | Variable 2 | Correlation ( r ) | p ‐value |
|---|---|---|---|
| CRL | I AS | 0.27 | 0.016 |
| CRL | S AS | 0.33 | 0.003 |
| CRL | I TJ | 0.23 | 0.036 |
| CRL | S TJ | 0.2 | 0.077 |
[图：Scatter plots illustrating the correlation between the auricular surface areas of the ilium and sacrum. (a) Correlation ]
TABLE 3. Pearson correlation coefficients ( r ) and corresponding p ‐values for non‐normally distributed parameters and variations.
| Variable 1 | Variable 2 | Correlation ( r ) | p ‐value |
|---|---|---|---|
| I AS | S AS | 0.88 | <0.001 |
| I TJ | S TJ | 0.96 | <0.001 |
[图：Bland–Altman plots and boxplot illustrating bilateral differences in auricular and total joint surface areas. Bland–Altm]
TABLE 4. Descriptive statistics of the Symmetry Index (SI) for the sacroiliac joint surface area.
| SI | Mean | SD | Median | Minimum | Maximum |
|---|---|---|---|---|---|
| % | % | % | % | % | |
| I R AS—I L AS | 10.37 | 8.05 | 9.32 | 0.07 | 31.98 |
| I R TJ—I L TJ | 5.70 | 4.89 | 4.60 | 0.01 | 23.80 |
| S R AS—S L AS | 10.78 | 10.41 | 8.17 | 0.37 | 57.21 |
| S R TJ—S L TJ | 5.56 | 5.94 | 4.59 | 0.05 | 34.28 |
[内容请查看原文]
Joint shape
The auricular surfaces of the sacrum and ilium involved in the formation of the SIJ, on both the right and left sides, were divided into a dorsal and a ventral limb (Figure 2). Consequently, five different shape types could be identified in domestic cats (Figure 8). Type 1 (“auricular‐shaped”) was characterized by a distinctly wider and more prominent dorsal limb compared with the ventral limb. This type was found in 58.13% (93 cases) of the examined animals. Type 2 (“crescent‐shaped”) showed a ventral and dorsal limb with approximately the same width and resembled a C‐shape. This Type was identified in 28.13% (45 cases) of cats. Type 3 (“spatula‐shaped”) was characterized by no limbs, an irregular outline and was found on the right sacrum of one cat (0.63%). Type 4 (“bifoliate‐shaped”) was characterized by a complete division of the surface into two parts. This Type was identified in 8.13% (13 cases) of the joint surfaces examined. Type 5 (“straight‐shaped”) showed no curvature or indentation and therefore no limbs. 5% (8 cases) of the joint surfaces examined could be assigned to this type. In most specimens, the morphology of the iliac auricular surface corresponded closely to that of the sacral surface with no difference between the right and left sides.
[图：Representative examples of the different auricular surface outline shapes. The auricular surfaces are highlighted with g]
[内容请查看原文]
DISCUSSION
The SIJ is a key focus of many current and previous studies in human medicine. The SIJ has been extensively studied in humans, particularly in relation to lower back pain and SIJ referred pain patterns. However, in veterinary medicine, there are still gaps in knowledge regarding the SIJ's anatomy, innervation, and pain‐inducing potential. Therefore, the aim of this study was to examine the macroscopic anatomy and innervation of the SIJ in domestic cats in more detail.
[内容请查看原文]
Innervation of the dorsal sacroiliac ligaments
The macroscopic and microscopic findings indicate that the dorsal sacroiliac ligaments are primarily innervated by the dorsal branches of the seventh lumbar and first sacral spinal nerves. The anastomoses found between dorsal branches of the lumbar and sacral spinal nerves are regarded as common anatomical findings, as described in both veterinary and human literature (Cox & Fortin, 2004; Evans & de Lahunta, 2013; McGrath & Zhang, 2005). Comparison with studies in human medicine and other animal species reveals both similarities and differences. Some studies describe dorsal innervation of the human SIJ originating exclusively from varying numbers of sacral segments (Grob et al., 1995; McGrath & Zhang, 2005), whereas others report additional innervation mostly from the dorsal branch of the lumbar spinal nerves (Cox & Fortin, 2004; Kampsen, 2019; Roberts et al., 2014). By contrast, Steinke et al. (2022) have demonstrated that nerves do not reach the SIJ but rather that branches of L5 to S1 pass through the inner sacroiliac ligaments and that branches of S1 to S4 pass through the outer sacroiliac ligaments.
In rats, the SIJ innervation has been reported to arise from L4 or L5 to S2, demonstrating similarities to human anatomy (Murata et al., 2000, 2001). Sakamoto et al. (2001) have previously utilized electrophysiological techniques in cats to demonstrate that the SIJ and the surrounding ligaments and muscles contain mechanosensitive afferent units originating from the fourth to sixth lumbar spinal nerves. The underlying factors contributing to the observed variations in the number of innervating nerves and their origin are multifaceted and not fully elucidated. One possible explanation for the discrepancies is the anatomical variation between species, particularly regarding the number of lumbar and sacral vertebrae. Another potential explanation may lie in methodological differences, particularly in the dissection areas and the examination methods employed. For instance, in the study by Sakamoto et al. (2001), only the dorsal rootlets of L4–L6 were examined. In the present study, the skin in the dorsocaudal area of the SIJ was incised and then dissected ventrally. This approach enabled the targeted investigation of cutaneous branches in a specific area above the SIJ. Expanding the investigated areas in either study could potentially reveal additional nerve branches in the lumbar and sacral regions. Furthermore, the evaluation of nerve tissue in the current study was performed by macroscopic and microscopic observations, whereas Sakamoto et al. (2001) used an electrophysiological approach. Although both investigations are generally suited for the verification of the innervation of the SIJ, their methodological differences may result in discrepancies, particularly with regards to functional fiber types and regional distribution patterns. Despite these differences, the fundamental principle of SIJ innervation via dorsal branches of the lumbar and sacral spinal nerves remains consistent across species.
Myelinated nerve fibers are characterized by axons, which are surrounded by a myelin sheath, formed by Schwann cells. Among the individual Schwann cells, there are small gaps in the sheath, called Ranvier nodes (Liebich, 2010; Welsch, 2006). Myelinated nerve fibers are known to transmit a variety of stimuli to the spinal cord, including mechanical, thermal, and nociceptive signals (Breves et al., 2022). The histological examination of the ligament samples in this study demonstrated the presence of Ranvier nodes and, consequently, the presence of small bundles of myelinated nerve fibers in 16 of 20 samples (Figure 5). The missing evidence of SIJ innervation in the four samples can be attributed to methodological factors. The histological analysis was confined to a specific area of the tissue. Hence, it is possible that nerve fibers were present in unsectioned parts of the samples. Additionally, the dimensions of the nerve fibers might have been below the resolution limit of standard light microscopy. In such cases, their detection would have necessitated the implementation of specialized immunohistochemical staining methods. Sakamoto et al. (2001) classified the nerves in the SIJ and adjacent tissues as high threshold Group III, suggesting a nociceptive function. This might suggest that some of the nervous structures delineated in this study constitute nociceptive afferents. However, a definitive validation of nociceptive nerve fibers is lacking here, but could be achieved, for instance by using more specific functional or immunohistochemical markers in future studies.
Just as numerous studies in human medicine have demonstrated that the SIJ can be a source of lower back pain or referred pain, SIJ dysfunction in equine medicine manifests through diverse clinical signs (Barstow & Dyson, 2015; Dyson & Murray, 2003; Fortin, Aprill, et al., 1994; Fortin, Dwyer, et al., 1994; Jeffcott et al., 1985; Nagy et al., 2020; Schwarzer et al., 1995; Slipman et al., 2000). These variable clinical manifestations of pain caused by the SIJ can be explained by the concept of referred pain, which typically occurs within regions sharing the same segmental innervation (Bogduk, 2009). Given the segmental diversity of SIJ innervation, referred pain zones may be extensive and heterogeneous (Grob et al., 1995; Slipman et al., 2000). The anatomical identification of nerve branches in the dorsal SIJ region provides a structural basis for future microscopical, functional, and clinical studies assessing whether the feline SIJ can contribute to pain, altered locomotion, or clinical signs.
[内容请查看原文]
Joint shape
In addition to the innervation of the SIJ, human medicine pays attention to the macroscopic shape of the auricular surface, for which three main shapes have been described (Jesse et al., 2017). In veterinary textbooks, the auricular surface is generally described across species as either auricular‐shaped (Dyce et al., 2010; Ellenberger & Baum, 1943; Salomon et al., 2020) or crescent‐shaped (Evans & de Lahunta, 2013). Comparably, research on healthy and clinically normal horses also showed three main types (Dalin & Jeffcott, 1986a). In contrast to the studies on humans and horses, and the views expressed in veterinary textbooks, this study was able to demonstrate not only similar diversity of forms but also morphological characteristics in domestic cats, as described by Pallandre et al. (2020). The overall similarity in auricular surface morphology can certainly be attributed to the anatomical similarities among feline species. The differences observed between studies as well as the considerable large variation in shape may have multiple explanations. Pallandre et al. (2020) attributed the shape of the auricular surface to differences in predatory behavior and the resulting forces and movements involved. However, the diversity in auricular surface shape in domestic cats might not be explained by predatory behavior alone but could potentially be influenced by different locomotion patterns. Domestic cats are kept as both outdoor and indoor pets, with varying degrees of freedom of movement. Differences in locomotion behavior, including hunting, jumping, and climbing, could influence the mechanical loading and morphological development of the auricular surface shape of the SIJ. Additionally, the diversity of shape, particularly irregular outlines, or curvature might potentially be linked to age‐related or pathological changes. For example, Dalin and Jeffcott (1986b) reported age‐related alterations to the shapes of the auricular surface of the SIJ in horses. Elderly horses exhibited irregular outlines and atypical joint shapes more frequently. Furthermore, horses with poor performance and low‐grade hindlimb lameness have been shown to display abnormal joint outlines compared to clinically healthy individuals (Jeffcott et al., 1985). Similarly, Jesse et al. (2017) proposed a possible association between auricular surface shape and lower back pain or SIJ pathology. However, since living conditions, age, and medical background of the animals examined in the current study were unknown, any assessments regarding a potential impact of age‐ or disease on SIJ morphology in domestic cats should be regarded with reservation.
[内容请查看原文]
Joint size
In this study, a weak correlation between crown‐rump‐length and SIJ size was detected. Similar observations have been reported in other species. In horses, for example, the joint surface area of the SIJ increases from approximately 1.0 cm2 in a 10 kg pony foal to around 18 cm2 in adult horses weighing 500–600 kg (Dalin & Jeffcott, 1986b). In humans, the joint surface area increases from approximately 1.5 cm2 in newborns to about 17.5 cm2 in adults (Brooke, 1924). These comparisons suggest that SIJ surface does not necessarily correlate with body size. Additionally, our findings show no sexual dimorphism in joint size in the examined cats. This stands in contrast with findings in humans, where differences in both size and morphology of the auricular surface between females and males have been described (Anastasiou & Chamberlain, 2013; Brooke, 1924; Nishi et al., 2020). One potential explanation for this discrepancy is that sexual dimorphism of the SIJ develops during puberty (Brooke, 1924). As most domestic cats are neutered before or at the onset of puberty, at four to six months of age, the hormonal influences that may contribute to the development of sexual dimorphism could possibly be reduced or absent. This tentatively suggests that the sex‐related differences in SIJ morphology may not be uniformly developed to the same extent across all individuals.
Furthermore, one possible explanation for the absence of significant differences in the mean size of the auricular surface or the total joint surface might be that in the present cohort, animals with relatively larger right or left joint surfaces statistically balance each other, resulting in an overall appearance at the group level. However, examinations at the individual level revealed asymmetries in joint size and the SI of the study population showed a wide range of values. As no comparative threshold exists for the feline SIJ, no clear interpretation or comparison with other studies is not possible in this case. However, low SI values generally indicate a high degree of bilateral symmetry, potentially reflecting balanced anatomical development and uniform load distribution. By contrast, higher SI values signify increasing asymmetry, which may suggest compensatory mechanisms or unilateral joint degeneration from a morphological perspective. It is widely accepted that the biological body is not a perfect mirror image; both organs and skeletal structures naturally exhibit a certain degree of asymmetry. One reason is the body's adaptation to a “dominant” side, that experiences more frequent or intense mechanical loading (Auerbach & Ruff, 2006; Bass et al., 2002; Kontulainen et al., 2002; Nishi et al., 2020; Stirland, 1993; Zhang et al., 2022). Given that the SIJ is the primary transmitter of force from the hindlimbs to the axial skeleton, these discrepancies potentially result from asymmetric loading patterns during high‐impact activities, such as jumping or rapid acceleration. Consequently, an elevated SI does not necessarily indicate a pathological condition but could represent a normal functional adaption to mechanical demands, or be the consequence of a past injury.
In addition, the osseous components of the sacroiliac joint comprise the pelvis and the sacrum. The latter is suspended between the iliac wings and exhibits greater mobility (Kiapour et al., 2020). Due to the sacrum's unique position, it is reasonable that the joint surface of the ilium is slightly larger than that of the sacrum, thus effectively “enclosing” it. The broad attachment of the ventral and dorsal sacroiliac ligaments to the ilium may further explain the relatively larger surface area of the iliac component.
[内容请查看原文]
Limitations of the study
When interpreting the results, it is essential to consider the limitations inherent in the study design. The exact age, lifestyle, and medical history of the cats examined were unknown, and the cohort consisted predominantly of neutered animals. This restricts more definitive conclusions that can be drawn regarding functional wear and tear, hormonal influence, or specific functional disorders. Additionally, the manual preparation may have led to the under‐detection of fine nerve branches. The absence of electrophysiological or immunohistochemical confirmation regarding the nerve modality precludes definitive conclusions regarding the exact neuroanatomical subtypes. Furthermore, there may have been slight deviations in the exact position of the cutaneous termination points of the nerve branches, as the tissue was not fixed but thawed, and therefore soft and flexible. Moreover, the classification of morphological forms is by its very nature subjective and could not be statistically controlled due to the lack of assessment of observer error. Finally, the histological evaluation was based on representative samples rather than complete serial sections. Therefore, the possible presence of micro innervation or very small fibers—particularly in the four samples in which no nerve were detected microscopically—cannot be ruled out with certainty.
[内容请查看原文]
CONCLUSIONS
In conclusion, the present study provides two primary contributions to the structural understanding of the SIJ in domestic cats. It indicates that the dorsal sacroiliac ligaments are innervated by the seventh lumbar and first sacral spinal nerves. Additionally, it documents considerable variation in the macroscopic shape of the auricular surface. There were no significant differences observed in the size of the auricular surface or the total joint size between male and female cats.
However, it is imperative to acknowledge that the morphological findings do not provide direct evidence of clinical disease, joint function, or pain. Instead, they are intended to serve as a cautious, descriptive anatomical basis to guide and inform future immunohistochemical, functional, and clinical research regarding the impact of SIJ dysfunction in small animal veterinary medicine.
AUTHOR CONTRIBUTIONS
Concept/design: AK, NR. Acquisition of data: AK. Data analysis/interpretation: AK, MK, TG, SF, CM, NR. Drafting of the manuscript: AK. Critical revision of the manuscript and approval of the article: AK, MK, TG, SF, CM, NR.
FUNDING INFORMATION
The research was supported by the Dr. Heidi und Karl‐Heinz Kübler Stiftung.
CONFLICT OF INTEREST STATEMENT
None of the authors have a conflict of interest to disclose.
Supporting information
[内容请查看原文]