题目及作者
Title: The APR triangle: A practical zone in the Glissonean approach to laparoscopic anatomical right hepatectomy
中文题目：APR三角，腹腔镜Glissonean入路右肝解剖性切除的实用结构
通讯作者：陈亚进
摘 要
Abstract
Background: An understanding of vascular anatomy is crucial for the safe performance of laparoscopic anatomical liver excision. We discovered a triangular zone during the laparoscopic right liver surgery and termed this zone the APR triangle. The purpose of this study was to determine the probability of the existence of the APR triangle and elucidate its various forms.
Methods: Analyzed three-dimensional image reconstructions of 66 individuals who underwent liver surgery and calculated the statistics for various types of APR triangles under various grouping settings.
Results: The APR triangle was present in the majority of cases, with right hepatic vein(RHV) trunk type in 68% and right hepatic vein branch type in 21%, respectively. The angle between the right anterior and right posterior hepatic pedicles (AP&PP) was at most between 45 and 90 (74%). There was a 35% chance that at least one of the AP&PP was longer than 2 cm, and a 39% chance that both were. The right posterior pedicle first branch would appear at the bifurcation of AP&PP in 13% only.
Conclusions: The APR triangle is objectively present and may represent a practical zone for performing laparoscopic right hepatic anatomical resection more simply and safely.
Keywords: Laparoscopic anatomical liver resection; Vascular anatomy; ARP triangle
摘要
背景：对血管解剖的充分认知对于安全实施腹腔镜解剖性肝切除术意义重大。在临床实践中笔者团队发现右肝存在一个三角形解剖区域并将之命名为APR三角。本研究旨在阐明APR三角的存在及不同分型。
方法：分析66例在我中心接受肝切除手术患者的肝脏术前三维重建图像，测量各参数以统计不同分型。
结果：APR三角在绝大部分病例中均存在，其中RHV主干型与分支型分别占68%、21%；大部分病例（74%）中右前肝蒂（AP）与右后肝蒂（PP）的夹角在45°与90°之间；35%的病例中AP和PP中有一支长度大于2cm，39%的病例中两支均大于2cm；在13%的病例中观察到在AP与PP分叉处有较粗的右后肝蒂第一分支（PPa）出现。
结论：APR三角客观存在，并且是腹腔镜右肝解剖性切除过程中一个简单、安全的实用解剖结构。
关键词：腹腔镜解剖性肝切除；血管解剖；APR三角
全文解读
1. Introduction
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Knowledge of vascular anatomy is crucial for the safe performance of anatomical liver resection. The structural variation of the right liver is extremely complex, which is one reason why anatomical resection of a right hepatic segment or region is challenging 1-3. The divisions of the right anterior lobe are controversial; some scholars propose segmenting the right anterior sector into ventral and dorsal segments 4,5, while others utilize Couinaud's segmentation6. Similarly, the right posterior lobe is divided into distinct groups 7. These various anatomical divisions remain debatable.
Computer simulation techniques have undergone dramatic advancements, and three-dimensional (3D) visualization of intrahepatic structures from any position is now possible preoperatively 8. This precise visualization of hepatic vessels provides new insights into the surgical anatomy of the liver. 3D liver analysis is widely utilized as a preoperative evaluation before hepatectomy 9.
While performing laparoscopic right liver surgery in our clinical practice, we discovered a triangular region with sparse vascular branches when the hepatic pedicle was dissected via Rouviere's sulcus using the Glissonean approach. The three sides of this triangular area in the common caudate view of laparoscopy are the right anterior hepatic pedicle, the right posterior hepatic pedicle, and the right hepatic vein (RHV) trunk. The first branch of the right posterior pedicle (PPa) occasionally arises from the bifurcation of this area, but it usually does not because few blood vessels pass through this triangular location. We termed this triangular area the “APR triangle” (Fig. 1).
The present study was performed to investigate the probability of the existence of this APR triangle and elucidate the different forms of its appearance in an effort to facilitate safer and more precise anatomical excision of the right liver. Therefore, we analyzed patients’ livers using 3D reconstruction software and examined the different morphologies of certain APR triangles.
1. 引言
对血管解剖的充分认知对于安全实施腹腔镜解剖性肝切除术意义重大。右肝错综复杂的解剖变异是实施右肝手术的主要挑战之一[1-3]。肝右前叶的分段目前尚存争议，许多学者也主张将肝右前叶分为腹侧、背侧段[4,5]，然而经典Couinaud分段仍有诸多拥趸[6]。类似地，肝右后叶也有不同的划分方式[7]。这些解剖划分方式仍未统一结论。
得益于计算机模拟技术的巨大进步，术前肝脏三维重建可视化图像使术者可从不同角度清晰观察肝内管道的分布情况，对肝脏解剖的认识更加清晰[8]，同时也是术前评估的重要内容[9]。
基于腹腔镜右肝切除手术的临床实践，笔者团队发现经Glissonean入路从Rouviere沟解剖肝蒂可获得一个乏血管的三角形区域：经腹腔镜足侧视野可观察到此三角形的三个边分别为右前肝蒂（AP）、右后肝蒂（PP）、肝右静脉(RHV)。右后肝蒂的第一分支(PPa)仅在少部分情况下出现在此区域。我们将此三角形区域命名为APR三角。
本研究旨在阐明APR三角的存在及不同分型，并展示经此解剖区域安全、精细实施腹腔镜右肝解剖性手术的理念。因此，我们通过三维重建图像对APR三角进行形态学的分析。
Fig. 1 (A) APR triangle on the liver surface. Red line, right anterior hepatic pedicle; yellow line, right posterior hepatic pedicle; blue line, right hepatic vein trunk. (B) Three-dimensional reconstructed image of the APR triangle. (C) APR triangle in the liver.(D) Scheme of the APR triangle.
图1：（A）肝脏表面的APR三角。红线：右前肝蒂；黄线：右后肝蒂；蓝线：肝右静脉。（B）APR三角的三维重建图像。（C）肝脏解剖过程中展示的APR三角。（D）APR三角的示意图。
2. Methods
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2.1. Patients and 3D image reconstruction
From January 2019 to June 2021, 66 patients (median age, 42 years; range, 29–66 years; male: female ratio, 40:26) underwent contrast-enhanced computed tomography as part of their preoperative examination for laparoscopic right liver surgery at Sun Yat-sen Memorial Hospital. The inclusion criteria were as follows: the lesion was located in the right liver, the largest diameter was <5 cm, and there was no compression of major blood vessels. All patients underwent 3D reconstruction with liver simulation software as part of the protocol (Hisense Group, Qingdao, China). 3D reconstruction views of the liver parenchyma, intrahepatic vascular systems, and their associated relationships were obtained. Additionally, this technique allowed for measurement of the length of the hepatic pedicles and the angle between the hepatic pedicles.
2.2. Data analysis
Image measurement data were entered into a spreadsheet (Excel for Mac; Microsoft Corporation, Redmond, WA, USA), and all analyses were conducted in accordance with the Sun Yat-sen Memorial Hospital's ethical guidelines for clinical studies.
2. 方法
2.1患者与三维重建图像
2019年1月至2021年6月，66名患者（29-66岁，中位年龄42岁，男女性别比=40:26）接受了高分辨率计算机断层扫描检查(CT)作为腹腔镜解剖性右肝手术的常规术前评估。本研究的纳入标准包括：肿瘤位于右肝且最大直径小于5cm、对肝内主要管道没有直接压迫。电脑软件基于影像学图像重建得到肝脏三维可视化图像，可对肝实质、肝内管道及其毗邻关系有清晰的观察及客观的测量。
2.2 数据分析
三维重建可视化软件：中国青岛海信集团。
测量数据分析软件：Excel for Mac; Microsoft Corporation, Redmond, WA, USA。
所有数据分析遵循孙逸仙纪念医院临床研究伦理指引。
3. Results
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The following results pertain to the caudal view during laparoscopic liver surgery (Table 1). All 66 patients’ clinical data are shown in the supplementary material. The APR triangle group comprised 20 patients, and the non-APR triangle group comprised 46 patients. We compared the characteristics, surgery types, and perioperative outcomes between the two groups. There were no statistically significant differences in the operation time, intraoperative bleeding, or postoperative complications; however, the APR triangle group showed better trends of these indices.
The APR triangle was classified into three groups based on the anatomy of the RHV within it (Fig. 2). Forty-five (68%) patients had the RHV trunk type, 14 (21%) patients had the RHV branch type, and 7(11%) patients had the RHV absence type. The absence of the RHV can also be interpreted as the absence of the traditional APR triangle in these patients; however, the risk of bleeding due to hepatic vein injury is reduced and the procedure is safer when operating in this hypothetical triangular area.
The APR triangle was divided into three groups according to the angle formed by the right anterior and right posterior hepatic pedicles (AP&PP) (Fig. 3). The <45-degree type was present in 8 (12%) patients, the 45- to 90-degree type was present in 49 (74%) patients, and the >90-degree type was present in 9 (14%) patients.
The APR triangle was also divided into three groups based on whether the length of the AP&PP from the root to the first branch was >2 cm (Fig. 4). Both pedicles were >2 cm in 26 (39%) patients, one was >2 cm in 23 (35%) patients, and both were <2 cm in 17 (26%) patients.
Finally, the APR triangle was divided into two groups based on the existence of the PPa at the bifurcation of the AP&PP (Fig. 5). The PPa was present at the bifurcation in 11 (13%) patients and not present at the bifurcation in 55 (87%) patients.
3. Results 结果
由腹腔镜足侧视野对患者APR三角进行观察测量。66例患者的临床基线数据展示在补充材料中。经APR三角手术组的患者20人，非APR三角手术组的患者46人。两组间的基线情况、围术期数据如手术时间、术中出血量、术后并发症发生率无统计学差异，但APR三角组在上述参数中体现出更好的趋势。
基于RHV形态位置可将APR三角划分为三种类型（图2）：45例（68%）患者为RHV主干型，14例（21%）患者为RHV分支型，7例（11%）患者为RHV远离型。在RHV远离型的患者中无法观察到严格意义上的APR三角，在经此入路为此类型患者实施手术时损伤重要分支血管导致出血的风险较低，可在乏血管区中更为安全地操作。
基于AP的PP的夹角可将APR三角划分为三种类型（图3）：8例（12%）患者中此夹角＜45°，49例（74%）患者中此夹角介于45°与90°之间，角度＞90°见于9例（14%）患者中。
基于AP与PP从根部到第一分支的主干长度是否＞2cm可将APR三角划分为三种类型（图4）：AP&PP均＞2cm见于26例（39%）患者中，单支＞2cm见于23例（35%）患者中，两支均＜2cm见于17例（26%）患者中。
最后，基于PPa是否出现在AP的PP分叉处可将APR三角划分为两种类型（图5）：11例（13%）患者可观察到PPa，55例（87%）患者在此分叉处未观察到PPa。
Fig. 2 Division of the APR triangle into three groups based on the morphology of the right hepatic vein (RHV) within the APR triangle. The top images are three dimensional reconstructed images, and the bottom images are schemas of the anatomy of the APR triangle.
(A) RHV trunk type. (B) RHV branch type. (C) RHV absence type. RHV, right hepatic vein.
图2 基于RHV形态位置的APR三角分型
上方图片为三维重建图像，下方图片为APR三角解剖模式图。
(A) RHV主干型；(B) RHV分支型.；(C) RHV 远离型。RHV, 肝右静脉。
Fig. 3 Division of the APR triangle into three groups based on the angle formed by the AP&PP. The top images are three-dimensional reconstructed images, and the bottom images are schemas of the anatomy of the right AP&PP.
(A) < 45-degree type. (B) 45- to 90-degree type. (C) > 90-degree type. AP&PP, right anterior pedicle and posterior pedicle.
图3 基于AP&PP夹角的APR三角分型
上方图片为三维重建图像，下方图片为AP&PP夹角模式图。
(A) < 45°型；(B) 45°-90°型；(C)＞90°型。AP&PP, 右前肝蒂与右后肝蒂。
Fig. 4 Division of the APR triangle into three groups based on the length of the AP&PP.
(A) Both pedicles are >2 cm. (B) One pedicle is > 2 cm. (C) Both pedicles are<2 cm. AP&PP, right anterior pedicle and posterior pedicle.
图4 基于AP&PP长度的APR三角分型
(A) 两支均＞2cm；(B)单支＞2cm；(C)两支均＜2cm。AP&PP, 右前肝蒂与右后肝蒂。
Fig. 5 Division of the APR triangle into two groups based on the presence of the PPa at the bifurcation of the AP&PP. The top images are three-dimensional reconstructed images, and the bottom images are schemas of the anatomy of the APR triangle.
(A) PPa absence type. (B) PPa presence type.
AP&PP, right anterior pedicle and posterior pedicle; PPa, first branch of the right posterior pedicle.
图5 基于PPa位置的APR三角分型
上方图片为三维重建图像，下方图片为APR三角解剖模式图。
(A) PPa不位于AP&PP分支区域内；(B) PPa位于AP&PP分支区域内。
AP&PP, 右前肝蒂与右后肝蒂；PPa, 右后肝蒂第一分支。
4. Discussion
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With the advancements in the theory and technology of laparoscopic liver surgery, the surgical scope of laparoscopic liver resection has gradually expanded [10] from left lateral lobectomy and left and right hemihepatectomy to right anterior and right posterior lobectomy11,12; additionally, more precise segment hepatectomy can now be performed13,14. Subsegmental anatomical resection and a variety of complex surgical procedures in traditional open hepatectomy can be performed successfully under laparoscopy15,16. When Makuuchi18 first developed the notion of anatomical liver resection, the target liver segment had to be dyed with methylene blue to denote the border and fully disclose the indicated hepatic vein17,18. Indocyanine green fluorescence imaging has been increasingly introduced during laparoscopic anatomical liver resection over the last few years19. After staining the target liver parenchyma through the portal vein, a distinct demarcation can be produced both on the liver surface and in the deep parenchyma20. Regardless of whether the target hepatic pedicle is stained positively or negatively, careful injection or dissection of the target hepatic pedicle is essential prior to severing the liver parenchyma. A better understanding of the right hepatic pedicle branches is critical for successful laparoscopic anatomical hepatectomy.
3D visualization software can depict the liver, vessels, tumors, and other anatomical structures in three dimensions and can demonstrate the spatial relationship of tumors and significant vascular structures21. The analysis function of the software program may determine the blood supply range of the portal vein or the blood return range of the hepatic venous system as well as the volume of the liver segment or subsegment22. This can assist in developing an individualized plan for laparoscopic anatomical liver resection. Such an individualized plan is critical in right liver surgery because there are numerous anatomical variances in the portal vein and hepatic vein branches of the right liver23. For this reason, our institution commonly uses preoperative 3D visualization software to mimic anatomical hepatectomy in right liver surgery.
The laparoscope's caudal angle and magnified field of view are extremely beneficial for performing anatomical right liver resections, such as the laparoscopic caudate lobe approach for right posterior lobectomy11,24 and our team's laparoscopic in situ segment 7 resection technique25. When the assistant lifts the right liver during laparoscopic right hepatectomy, Rouviere's sulcus is one of the most evident anatomical landmarks. The hepatic pedicle of segment 6 or the right posterior hepatic pedicle can be readily separated, and the right hepatic pedicle can then be located proximally. Beginning with this bifurcation, the surgeon may easily locate the branches of the right hepatic pedicle in all directions. Preoperative 3D reconstructed images, the Glissonean approach, and fluorescent staining technology facilitate the performance of not only right anterior or right posterior hepatectomy and segmentectomy but also combined anatomical subsegmentectomy. The APR triangle is an important anatomical area of the Glissonean approach in right liver surgery. In this area, analyzing the relationship among RHV and the AP&PP can guide the location and direction of the RHV more rapidly and accurately and can help to determine the plane of the liver parenchyma.
The APR triangle is present in most patients. However, when a thick inferior RHV or middle RHV is present, the RHV does not develop between the right anterior and posterior hepatic pedicles26. Our data indicate that dissecting 2 cm from the root of the right hepatic pedicle branch is a rather safe area of hypovascular branching, but that dissecting more than 2 cm from this root requires extreme vigilance for bleeding from the main RHV or its branches. This margin of dissection denotes a somewhat safe from a relatively dangerous work area during the Glissonean approach for anatomic excision of the right liver (S6 or S5 resection). Through the caudate view in the present study, the right posterior hepatic pedicle was dissected through the superficial liver surface landmark (Rouviere's sulcus), and the APR triangle was immediately found. Its importance in executing right anterior or right posterior lobectomy is unquestionable. Additionally, while performing anatomical hepatectomy on the combined segment or subsegment of the right liver, the APR triangle can serve as a reference coordinate for identifying the branches of each hepatic pedicle in the right liver.
4. 讨论
随着理论与技术的进步，腹腔镜肝脏手术已从左外叶切除、左右半肝切除逐渐推广至右前叶、右后叶切除[10-12]，精确到肝段的手术切除也在临床中不断地施行[13-14]。开腹手术能完成的亚肝段切除及其他复杂手术如今也都可以在腹腔镜手术中实施[15]。Makuuchi教授首次提出解剖性肝切除理念之时，通过结扎目标肝静脉并注入亚甲蓝染色来获取目标肝段的边界[16,17]。近几年吲哚菁绿染色技术被广泛应用于腹腔镜解剖性肝切除术中[18]。ICG通过门静脉在荧光下将目标肝段着色之后肝实质表面与内部均可获得清晰的分界线[19]。不管是通过正染法还是反染法获取荧光边界，精确的穿刺或者目标肝蒂的解剖结扎都是肝实质离断前决定成败的关键操作。因此对右肝蒂分支清晰的术前认知对于腹腔镜解剖性肝切除术至关重要。
三维可视化软件可准确描绘肝实质、管道与肿瘤并展示彼此之间的空间毗邻关系[20]。软件的分析功能可以模拟肝内的血流供应及流域并计算肝段、亚段的体积[21]。在软件的辅助下术者可提前掌握每例患者右肝中存在的门静脉、肝静脉解剖变异，为之制定个体化的手术方式[22]。因此，笔者所在中心在为患者实施腹腔镜解剖性右肝手术前常规通过三维可视化软件进行模拟手术。
腹腔镜独特的足侧视角及视野放大功能对于腹腔镜解剖性右肝手术具备天然优势，例如通过尾状叶入路实施右前叶切除术[11,23]以及我们团队先前报道的腹腔镜原位S7切除术[24]。在助手将右肝提起后，Rouviere沟是最明显的解剖标志之一。对此位置的解剖可获取S6肝蒂或者右后肝蒂，从而实现对右肝蒂主干及其分支的定位。术前三维可视化图像、Glissonean入路与荧光染色技术的结合不仅使右前叶、右后叶、右肝段切除术可以广泛开展，也使联合亚肝段切除术理论与技术可行。APR三角是经Glissonean入路实施右肝手术的重要解剖区域。通过对肝右静脉、右前肝蒂、右后肝蒂空间关系的分析可以更加快速地定位肝右静脉的位置、协助手术医生确定肝实质离断平面。
在大部分患者中可观察到APR三角的存在。然而当出现粗大的肝右后下静脉等解剖变异时，RHV不走行于AP与PP分支的区域之内[25]。本研究的数据提示右肝蒂根部向远侧2cm是相对乏血管区域，于此区域内可以相对安全地进行实质解剖，当解剖超过2cm的位置需要更加谨慎以避免RHV主干或分支造成难以控制的出血。此研究中在足侧入路的视野下在肝脏表面找到Rouviere沟等解剖标志便可迅速定位APR三角，其重要性在实施右前叶或右后叶切除中不言而喻。此外，在实施联合肝段或亚肝段切除的解剖性右肝手术中，APR三角也可作为定位肝段或亚段肝蒂的重要参考。
5. Conclusions 结论
In conclusion, we have herein proposed the concept of the APR triangle. This practical zone is conducive to dissection of the right anterior and posterior hepatic pedicles or their branches, and it is beneficial to localization and protection of the RHV. It has an important role in laparoscopic right hepatic anatomical resection such as right anterior lobectomy, right posterior lobectomy, and segment 7 liver resection.
APR三角对于右前肝蒂、右后肝蒂主干及分支的解剖、肝右静脉的定位与保护有重要的临床应用价值，是进行腹腔镜Glissonean入路解剖性右前叶、右后叶与S7切除手术过程中重要的解剖结构。
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原文链接
https://www.sciencedirect.com/science/article/pii/S2772947822000433
引用格式
Chen J, Zhang Z, Zhou R, et al. The APR triangle: A practical zone in the Glissonean approach to laparoscopic anatomical right hepatectomy. iLIVER, 2022, 1(3): 176-180. https://doi.org/10.1016/j.iliver.2022.08.004
通讯作者
陈亚进 教授
中山大学孙逸仙纪念医院肝胆外科主任、普外科主任
国际肝胆胰协会中国分会肝胆胰ERAS专业委员会主任委员
中国医师协会外科分会常委
广东省医师协会肝胆外科医师分会主任委员
中华医学会外科分会胆道外科学组委员
中国医师协会外科医师分会胆道外科医师专业委员会常务委员
国家卫健委能力建设和继续教育外科学专业委员会胆道专业委员会副主任委员
英国皇家外科学院Fellow（FRCS），国际腹腔镜肝脏外科协会（ILLS）常委
亚太腹腔镜肝脏手术推广委员会委员兼中国分会副主任委员
中国研究型医院学会消化道肿瘤专业委员会副主任委员
广东省医学会肝癌分会副主任委员
广东省医学会肝胆胰外科学分会副主任委员
国家癌症中心肝癌质控专家委员会委员
《中华消化外科杂志》副总编辑
《岭南现代外科临床杂志》主编
腹腔镜肝切除技术获得广东省科技进步二等奖，中华医学科技三等奖
2020获评“国之名医-卓越建树”，2019广东医师奖获得者
2019年和2020年连续两年获得广东省医师协会优秀肝胆外科医师分会。
期刊简介
iLIVER 是由中华人民共和国教育部和清华大学主办，清华大学出版社出版，爱思唯尔全球发行的肝病领域开放式英文期刊。本刊旨在传播肝病领域的创新和实践成果，并为从事肝胆系统研究的多学科专家和学者提供核心学术资源。本刊可发表肝胆系统领域中临床医学、转化医学、基础医学和公共卫生的原创研究、荟萃分析、综述、共识和实践指南等研究。主题涵盖范围包括：
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