Received: Fri 07, Mar 2025
Accepted: Fri 11, Apr 2025
Abstract
In Taiwan, surgical treatment of hepatic hydatid cyst and liver abscess were first introduced by Fukusaburo Kuroiwa in 1900. Primary liver cancer was first reported by Kyoshigazu Hayashi and Tensei Mou in 1907. Hepatectomy for hepatocellular carcinoma (HCC) was pioneered by Takashikuni Hayashi in 1943. After World War II, Feng TT reported 23 patients of HCC treated between 1950-1953 at National Defense Medical Hospital (NDMC) in 1954. Milestones in liver surgery continued, liver cancers treated with left hepatectomy reported in 1958, and right hepatectomy by Lin TY at National Taiwan University Hospital (NTUH) in 1959. Around the same time, Chang HL et al. also performed a right hepatectomy successfully from NDMC in 1960. A great step of improvement of hepatectomy had brought to light the possibility of benefits for patients with liver cancers since 1950. Laparoscopic hepatectomy was presented first for treating HCC patients by Ker CG et al. in 1998. Robotic-assisted hepatectomy was initiated by Wu YM et al. in 2012. Hepatectomy as a primary treatment for liver cancer rose significantly from 8.05% in 1995 to 28.66% in 2021 in Taiwan.
The first successful liver transplantation in Taiwan and Asia, was performed by Chen CL at Keelung Chang Gung Memorial Hospital (CGMH) in 1984, treating a woman with Wilson’s disease. Jeng LB performed successfully a liver transplantation for a patient of end-stage cirrhotic liver due to hepatitis B at Taipei CGMH in 1991. Subsequent breakthrough included total laparoscopic living donor right hepatectomy performed by Chen KH et al. at Far Eastern Memorial Hospital in 2012, by Lei HJ et al. from 2014 at Taipei VGH, and by Chen PD et al. from 2013 at NTUH, highlighting continual progress in liver surgery.
In conclusion, the history of hepatic surgery illustrates progressive resolution of challenges. In addition to the efforts from our ancient surgeons, we must remember what enabled to achieve today made by excellent developments in anesthesiology, infection control, radiologic techniques, and surgical instruments.
Keywords
Hepatectomy, liver resection, liver surgery, history of liver surgery, surgery in Taiwan
Introduction
Hepatic surgery developed relatively late compared to other gastrointestinal procedures. Tracing back, Taiwan became a Japanese colony under the Treaty of Shimonoseki in May 8, 1885. Four years later, Japanese doctors established Taiwan Medical Association to promote medical sciences. The first medical journal, Journal of Taiwan Medical Affairs written in Japanese was launched in 1898, and renamed the Journal of Taiwan Medical Association (JTMA) in 1902. After World War II, this journal was transitioned to the Journal of the Formosan Medical Association (JFMA) written in Chinese and English in 1945 [1]. Then, experienced Japanese surgeons returned to Japan and well-trained Chinese surgeons relocated to Taiwan from mainland China. Subsequently, these skillful physicians and surgeons from mainland China founded a medical association resumed from China (the original founded in Shanghai in 1915), and renamed it to the Chinese Medical Association, Republic of China, in 1951, and the official journal named Journal of Chinese Medical Association (JCMA), Taipei, established in 1954 [2]. During this period, liver surgery, particularly hepatectomy, was still recognized as a difficult and challenging procedures in 1950s. This led to the establishment of the Surgical Society of Republic of China by Professor Lin TY in 1967. Its official Journal, Journal of Surgical Society Republic of China was founded in 1968, and later renamed the Formosan Journal of Surgery (FJS) in 2001 [3]. Thereafter, the hepatic surgery and other surgical procedures were gradually matured and advanced in Taiwan.
After World War II, initial surgical interventions on the liver primarily targeted liver abscess and trauma. These procedures, conducted at a few hospitals, faced challenges due to limited anatomical knowledge and technology. During this period, the 1960s and 1970s, Taiwanese surgeons began to adopt techniques from Western countries, further enhancing their capabilities to perform advanced liver surgery. Today, liver surgery in Taiwan has made significant technological breakthroughs, reflecting achievements in various surgical fields. This article chronicles the history of hepatic surgery in Taiwan, highlighting key milestones, and the advancements in surgical technology.
Materials and Methods
Ancient medical records in Taiwan were primarily sourced only from three domestical medical journals; JFMA (from 1899), JCMA (from 1954), and FJS (from 1968). Evidence and information of hepatic surgery will be reported from these three journals especially before and after the World-War II. All early articles published before 1978 were not enrolled in the data bank published by global databases publisher, making historical documentation challenging. For searching the recent surgery, Web of Science Core Collection Database (WOS) and PubMed databases were used for searching the innovative hepatic surgery from 1978 to November of 2024. Keywords relevant to specific fields of hepatic surgery were used to identify publications from Taiwan and worldwide, allowing for bibliometric analysis of recent developments.
History of Hepatic Surgery
Hepatic Hydatid Cyst
Hepatic hydatid cyst disease is primarily caused by infection with Echinococcus. In Taiwan, the first case about the Echinococcus was reported by Singoro Aizawa in 1900 [4], and surgical treatment for hepatic hydatid cyst was first performed by Fukusaburo Kuroiwa in 1900 [5]. Subsequently, only sporadic cases were reported only as it was remained an uncommon disease in Taiwan. Post-World War II, a case of hydatid cyst of liver in a 60 year-old female immigrant from mainland China was successfully treated by surgical approach reported by Chang WS and Hong CR at National Taiwan University Hospital (NTUH) in 1960 [6]. Contrasting this rarity, cases of hepatic echinococcosis were more prevalent in regions like Saudi Arabia. A team including Chou YH, Yu SC and Lin FY performed 19 operations for hepatic echinococcosis at Jeddah General Hospital, Saudi Arabia between 1980 and 1982, publishing their findings in 1983 [7]. Globally, Echinococcus granulosus, the larval stage of an animal tapeworm, remains the most common cause of human hydatid disease, but it is rare in Taiwan.
Liver Abscess
The first documented liver abscess in Taiwan was reported by Kawasoe Seido in 1900 [8] with successful surgical treatment performed by Kuroiwa Fukusaburo in 1900 [5]. At the ancient period, Japanese physician in Taiwan initially referred to this condition as “tropical liver abscess” reflecting their limited familiarity with etiology of this diseases in 1900 [8]. Consequently, Yamakuchi Hiroshio provided more detailed reports on livers abscess in 1901 [9] and Ukai Zirou documented four cases to identify co-infection of ameba and Staphylococcus based autopsy findings from Taipei Hospital in 1902 [10]. Hence, further studies explored and noticed association of diarrhea and amebic infection in liver abscess patients. Thereafter, Japanese physician started to discuss the epidemiology and etiology of tropical liver abscess with Western physicians and surgeons in Taiwan [10]. In 1905, Zawata Sougoro emphasized that diarrhea was not always a concomitant symptom, spurring deeper investigations into the etiology and classification of liver abscesses [11]. By 1907, Kubo Nobueki categorized liver abscesses into "tropical" and "dysenteric" [12, 13]. Therefore, we can imagine that physicians and surgeons studied extensively the etiology and give a different term of diagnosis for liver abscess in 1900s in Taiwan. Until 1913, clinical application of X-ray imaging for early liver abscess diagnosis was first reported by Kado Gifu [14].
Advances in confirmation of ameba existed in the liver abscess was found by tissue staining method by Koikai Yakukura in 1918 [15]. A rare complication of dysenteric amebic liver abscess ruptured into pleural cavity was reported by Nokugi Tachiuki in 1916 [16]. Around this stage, it was difficult to make differential diagnosis between liver abscess or tumor only based on the clinical symptoms and physical examination [17]. A report of 45 patients (amebic in 35 and pyogenic in 9 patients) of liver abscess was extensively studied by Yoshitakei Seiko and revealed the mortality was 80-90% in pyogenic liver abscess in 1929 [18]. The treatment by needle aspiration drainage method was introduced by Hatakeyama Kasuo in 1933 [19]. Owing to more matured concept about the diagnosis and treatment of liver abscess, Sho BK provided a comprehensively reports in 1943 [20]. Besides, Wang YL and Chen WT reported 80 cases of liver abscess from Kung Tien Hospital in 1958 with mortality by 4.5% for non-jaundiced and 28.6%-60% for jaundiced patients [21]. Hence, they strongly suggested that early diagnosis and surgical drainage within a week in addition to emetine and antibiotics therapy would reduce mortality.
Liver Trauma
Surgical treatment for liver trauma was first documented by Kobayashi Tomoshitodo in a 21 year-old male injured by bicycle in 1931 [22]. According to his report, a laceration wound at the right inferior segment of liver with bleeding by using gauze packing to control bleeding first, and removed gauze seven days later and discharged uneventfully after operation. In general, liver trauma carried a high mortality rate before the 1930s [22]. In 1936, Katzuota Hideo reported 23 cases of liver trauma in southern Taiwan [23]. Subsequent advances included three cases of liver penetration injury by gunshot through chest, and treated successfully by surgical approach reported by Tsai KM in 1947 [24]. Then, a series of 64 cases of liver trauma; penetrating injury in 29 and blunt injury in 35 cases by Chen WF et al. from NTUH in 1968, which demonstrated a mortality of 14.1% (9/64) [25]. In 1982, Jan YY et al. also reported 60 cases; penetrating injury in 6, blunt injury in 54 cases with operative mortality was 13% (7/54) in Chang-Gung Memorial Hospital (CGMH) [26]. This marked an improvement in survival outcomes for liver trauma patients in 1980s.
4. Non-Parasitic Liver Cyst
Non-parasitic liver cystic diseases were managed with total excision or fenestration of the cyst wall depending on the cyst location and type. Operative success was first reported by Lin TY from NTUH with 3 cases in 1967, and 5 cases in 1968 [27, 28]. Later, in 1978, Chen MF also reported surgical treatment for non-parasitic liver cyst from Chang Gung Memorial Hospital (CGMH) [29] and Lee WC et al. in 1992 [30]. Until 1991, Ker CG et al. first documented to performed laparoscopic fenestration successfully at Kaohsiung Medical University Hospital(KMUH) reported in 1994 and 1997 [31, 32].
5. Liver Resection for Liver Cancer
The first documented case of primary liver cancer in Taiwan was reported by Hayashi Kyoshigazu and Mou Tensei in 1907 [33], and two cases reported by Chin SS in 1911 [34]. Interest on pathology grew when Chokei Uchita identified a rare mixed cell type of hepatocellular and cholangiocellular carcinoma in a primary liver cancer patient in 1926 [35]. A case of HCC was successfully treated by left hepatectomy with a specimen weighting 752 grams in a 62 year-old male by Takashikuni Hayashi at Surgical Department of Zawata of NTUH in 1943 [36]. Several years after World War II, Feng TT reported 23 patients of HCC collected from 1950-1953 and medium survival time was 3.5 months without liver resection in all patients from National Defense Medical Hospital (NDMH) in 1954 [37] In this stage, the diagnosis of liver tumor was not easy due to lack of diagnostic instrument but symptoms and signs. Therefore, Liao YL and Hsu KY reported that 44.3% of HCC were misdiagnosed as others among 61 cases [38].
Until 1953, Hsu FC and Chen-Huang YP performed successfully a partial liver resection on a 33 year-old female with a huge tumor size raised from the edge of right liver and pathology revealed hepatocellular carcinoma (HCC) and survived for 5 years after hepatectomy reported at Taipei Hsu’s Surgical Hospital in 1958 [39]. Lin TY, Hsu KY, Hsieh CM, and Chen CS performed left hepatectomy on three HCC patients since 1954 reported in 1958 [40]. After that, a new surgical technique named “finger ruptured method” was raised by Lin TY and proposed for hemi-hepatectomy by means of a finger fracture dissection of liver parenchymal tissue with individual ligation of the intrahepatic ductal structures. Therefore, more difficult operation, right hepatectomy, was performed successfully by Lin TY, Chen KM, Liu TK in 1959 in a 36 year-old man and a 6 month-old female infant from NTUH reported in 1960 [41]. At the same year, Chang HL, Wen CC, and Yang ST also performed a right hepatectomy to resect a large tumor successfully in August 1959 at National Defense Medical Center(NDMC) reported in 1960 [42]. A mild step of improvement in surgical technique of hepatectomy had brought to light the possibility of benefits for patients with primary liver cancers in 1960s.
Lin PW and Wei TC reported a 10-year (1976-1985) experiences of hepatectomy on 46 patients with primary HCC underwent major hepatic resections at NTUH [43]. Among these 46 patients with tumor size were ranged from 5 to 25 cm, 23 received major or extended lobectomy with operative one-month mortality was 6.5% (3/46). Resection of large HCC located in the central portion of the liver remains a surgical challenge. Wu CC et al. reported 19 HCC patients whose main tumor (mean diameter 11.3 cm, range 6-19 cm) located in the central part of the liver, defined as Couinaud's segments IV, V, VIII, accepted liver resections from July 1989 successfully without mortality in Taichung VGH [44]. For managing the hemorrhage at dissection liver plane, a comparative study was reported by Lee PH by using of microwave tissue coagulator and Lin's hepatic clamp for HCC, and disclosed no statistical difference between the operation time, and intraoperative blood transfusion from NTUH in 1994 [45]. In a large series of 370 hepatic resections for HCC during a period from 1981 to 1994, age less than 60 year-old and total bilirubin > 1.5 mg/dl had crucial effects on long-term survival reported by Chiu ST, Chiu JH, Lui WY, Chau GY, Loong CC and Wu CW from Taipei VGH in 1997 [46]. The overall five-year survival rate for liver cancer (n=2,558) in Taiwan was 15% for the year of 1987 reported by Lee CL, Ko YC, Choong CS [47]. But nowadays, the five-year survival rate was 66.4% for negative micro-vascular invasion (MVI) and 53.4% for positive MVI for HCC patients after hepatectomy reported by author in 2024 [48].
In case of the liver tumor ruptured, acute abdominal type was termed for the clinical classification of HCC, and 4 cases reported by Lio YL, Hsu FC and Koo SC from NTUH in 1956 [49]. Besides, another 3 cases were reported from NDMC by Yu SC in 1959 [50]. During 1960’s, explorative abdominal laparotomies were usually performed for stopping the bleeder only for all the patients presented acute abdomen and hemoperitoneum due to ruptured liver tumor with a emergent lethal condition. Until 1962, a right hepatectomy was performed emergently for a 35 year-old male patient due to ruptured liver cancer reported by Kuo TP, Lin YT, and Yang ZT from KMUH [51]. But this patient was lost due to hepatic failure week after hepatectomy. Therefore, emergent hepatectomy for treatment of ruptured liver tumor with bleeding was not recommended by Lin TY and Kuo TP, unless there was no better way to stop bleeding for life saving [51]. In 1970, Kuo TP et al. reported twelve cases of rupture of liver tumors, and incidence was 12.9% (12/93) among 1962-1969 [52]. Chen TX et al. reported eighty-four patients with ruptured HCC were treated by supportive in 50 patients, operation in 21 and transcatheter arterial embolization (TAE) in 13, and their median survivals were 13, 30 and 202 days respectively from Taipei VGH in 1996 [53]. The imaging study for demonstrating the bleeding ruptured side was limited, and author would like to show the tumor ruptured side proved by ultrasound and another by trans-arterial angiography in our two patients as shown in the (Figures 1 & 2).
6. Laparoscopic and Robotic Hepatectomy
Laparoscopic hepatectomy in Taiwan began in 1998, performed by Ker CG and Chen HY to treat nine patients with HCC at Yuan’s General Hospital, Kaohsiung [54, 55]. To overcome grasping the liver during laparoscopic parenchymal dissection, Hsieh CS et al. have begun using transparenchymal suture traction at Changhua Christian Hospital in 2000 [56]. Huang MT et al. reported seven patients with hepatic tumors involving the posterior portion of the right lobe of liver underwent hand-assisted laparoscopic hepatectomy with hand-port system at En-Chu-Kong Hospital in 2003 [57]. Around the year of 2000s, HCC patient treated with laparoscopic hepatectomy was deserved in selected patients with single, smaller and peripherally-located tumor [58]. A significant milestone was reached in 2009, when Chang TC et al. developed gasless laparoscopic hepatectomy, using a self-designed abdominal wall-lifting systems at NTUH, eliminating the complications associated with the pneumoperitoneum [59]. Hsu KF et al. began to use 3-port laparoscopic liver resection with the marionette technique that could help surgeons ease liver resection and achieve better results performed in 2009 at NDMC [60]. Laparoscopic caudate hepatectomy is feasible procedure for caudate hepatic tumors in selected patients since 2006 reported by Chen KH performed at Far Eastern Memorial Hospital(FEMH) [61].
Regarding robotic-assisted hepatectomy was introduced in 2012 by Wu YM et al. at NTUH reported in 2014 [62, 63], and in 2013 by surgical team of Ko KK, Wang SN and Lee KT at KMUH [64]. These patients surgical outcomes were comparable to open surgery and significantly shorter length of hospital stay. Moreover, Chen KH et al. reported robotic major hepatectomy with hepaticoenterostomy in a patient with a previous history of choledochocyst resection at FEMH in 2014 [65]. Therefore, we have to adopt, to adapt and to adept the pure laparoscopic or robotic hepatectomy for our patients in Taiwan.
7. Liver transplantation: Traditional or Laparoscopic Approach
Liver transplantation in Taiwan began with a groundbreaking procedure by Chen CL at Keelung CGMH to treat Wilson’s disease, the first successful liver transplant on March 22, 1984 in Taiwan even first in Asia [66]. On the 1st July 1991, Jeng LB performed successful liver transplantation for end-stage cirrhotic liver due to hepatitis B virus infection in Taiwan in Taipei CGMH [67]. The team of Chen CL performed successfully the first living donor liver transplantation in 1994 [68], the first split liver transplantation in Asia in 1997 [69], and the first dual graft LDLT in 2002 in Kaohsiung CGMH [70]. Subsequently, medical center hospitals stated to perform liver transplantations successfully in Taipei VGH [71], NTUH [72] and Tri-Army Service Hospital [73]. Nowadays, more than 25 registered liver transplantation teams of Taiwan major hospitals have the facilities to perform liver transplantation currently. But, the top-5 largest volume of liver transplantation patients recorded from 2009-2022 were Kaohsiung CGMH, China Medical University Hospital, Linkou CGMH, Changhua Christian Hospital, and Taipei VGH reported from Ministry of Health and Welfare of Taiwan in 2024 [74]. The 5-year and 10-year overall survival rates of liver transplantations were 76% and 63% for male, and 78% and 69% for female respectively reported by Taiwan Ministry of Health and Welfare in 2024 [74].
With the ongoing accumulation of laparoscopic hepatectomy experiences and increased technical innovations, laparoscopic or robotic approach for donor hepatectomy for LDLT has become a feasible task for liver transplantation nowadays. Totally laparoscopic living donor right hepatectomy by Chen KH from FEMH in 2012 (personal communication) [75]. Lei HJ et al. also to initiate total laparoscopic donor right hepatectomy as a safe strategy for liver transplantation started from 2014 at Taipei VGH [76]. Pure robotic liver donor right hepatectomy for LDLT was performed since 2013 by Chen PD et al. at NTUH [77]. While laparoscopic donor hepatectomy continues to evolve, it remains reserved for the experienced and advanced laparoscopic hepatobiliary expertise.
3. Discussion
Pertaining to the liver segmentation, Claude Couinaud’s revolutionary studies on liver anatomy in 1952 [78] and 1954 [79] had clearly introduced the concept of “functional independence” of liver sectors, with segments separated by fissures, each supplied by its own intrahepatic portal pedicles and draining into distinct hepatic venous branch. It took Couinaud four years and 140 corrosion-casting of “fresh” livers to establish his view of hepatic anatomy, which divided the liver into two hemi-livers, four sectors, and eight segments. However, the Vietnamese surgeon Ton That Tung [80, 81] had already endeavor to investigate the liver segmentation through meticulous dissection of autopsy specimens from 1939 antedated the works of Claude Couinaud in 1952 [78], and Healey in 1954 [82]. However, the works of Couinaud and Healey were widely known among liver enthusiasts and also clearly familiar with Tung’s work. Not to be overshadowed, Tung graciously acknowledged that “Couinaud had the merit of defining the distribution and intrahepatic segmental elements in our descriptions in his first text, published in 1939” [80]. Undeterred by limited recognition, Tung emphasized that liver surgery is a delicate and dangerous endeavor requiring precise knowledge of intrahepatic vessel anatomy and preoperative hemostasis measures. Tung’s insights, developed alongside his mentor Meyer-May, underline the importance of meticulous, anatomically informed liver resections in 1940s, a legacy that remains relevant today. For example, while dissecting the left lobe should be care a finger’s breadth to the left of the suspensory ligament to avoid opening the porto-umbilical sinus for preventing massive bleeding. Meticulous liver resection should be firmly rooted in anatomic segmentation as established by our pioneers in liver anatomists or surgeons shown in the (Table 1). As we know that the Brisbane 2000 Terminology of Liver Anatomy and Resections, has been unanimously adopted, providing a standardized framework for describing liver anatomy [83]. However, while Couinaud's classification remains a cornerstone in diagnostic and surgical practices, it does not always align with real-world anatomical variations. Thus, no single standardized strategy exists for performing precise anatomic liver resections in every case [84].
TABLE 1: The anatomy issues of
right and left liver lobes from the literatures.
|
Author, year. country |
Brief note |
Remark, reference |
|
Hugo
Rex, 1888. Czech
|
1.
Contrary to topographical landmarks of the falciform ligament and umbilical
fissure 2.
The true right and left hemi-livers were first defined by regional vessels,
particularly the portal vein, whose tributaries seemed to trace a segmental
anatomy |
anatomist
(1861-1936) [85] |
|
James
Cantlie, 1897 UK |
1.
Anatomic right and left lobes divided by gallbladder to vena cava inferior as
“Cantlie line”. 2.
The left half including the minor lobes, the lobulus. quadratus, the lobulus
spigehi, and the lobulus caudatus. |
surgeon
and anatomist (1851
–1926) [86] |
|
Ton
That Tung, 1939 Vietnam,
Hannoi |
1.
Right and left livers divided by the distribution of postal veins and their
branches termed with classic anatomic names. 2.
The basic concepts of liver segmentation were near the same we used
currently, and agree the nomenclature of segment of Couinaud. |
surgeon
and anatomist (1912-1982) [81]
|
|
Hjortsjo
CH 1951 Sweden |
1.
The division of the liver into 6 segments. 2.
The left lobe was divided into a medial and lateral segment by the line of
the falciform ligament. |
anatomist [87] |
|
Couinaud
C 1952 France,
Paris |
Right
and left livers divided by the distribution of postal veins and their
branches into 8 segments termed as “Couinaud classification.” |
surgeon
and anatomist 1922-2008.
[78] |
|
Rapp
E 1953 France,
Montpellier |
1.
The principal branches of the trunk of the portal vein makes a formal
symmetry exists between left and right portal systems. 2.
Coerning the original livers segmentation, Rapp and Couinaud are exposed in
the conservatory of the faculty of medicine (Montpellier). |
surgeon
and anatomist. [88]
|
|
Healey and Schroy 1953 USA |
1.Four
segments were divided into a superior and an inferior area for each segment. 2.
The prevailing pattern of drainage of these segments is presented the major
variants, and so-called accessory hepatic ducts are actually not accessory
but aberrant segmental or area ducts. |
surgeon
and anatomist. [89]
|
|
Mikami
J 1956 Japan |
1.
Hepatic segmentation with 12 divisions. 2.
Systematic hepatic resection based on the distribution of intrahepatic
vessels. |
surgeon, [90] |
|
Goldsmith
NA 1957, USA |
1.
Left portal vein divided into median and lateral branches and right portal
vein divided into anterior and posterior branches. 2.
Each segment has been further divided so that a total 8 sub-segments. 3.
Segment IV subdivided by its portal blood supply into segments IVa and IVb. |
surgeon
and anatomist. [91] |
1991 Reich et al. reported on the excision.
The key aspects of hepatectomy are to minimize bleeding and preserve the remnant liver. As Dr. Brunchwig once said “Liver surgeons have often been fearful of operating upon the liver resection because of the general impression that severe hemorrhage was an inevitable complication” [92]. On January 15, 1886, Lius excised a 15.5 × 13 × 11 cm solid tumor of the left lobe of the liver from a woman and died six hours later due to severe hemorrhage from the surgical stump in Italy [93] cited by Foster JH [94]. Until in 1888, Carl von Langenbuch successfully performed the first planned hepatectomy, removing 370 grams of parenchyma from a pedicle-shape tumor hanging from left liver lobe in a 30-year-old woman suffering from abdominal discomfort [95]. Despite a difficult postoperative course, the patient eventually recovered. Keen reported a successful hepatic resection for an adenoma of the bile duct in 1892 [96], and the first left lateral segmentectomy (bi-segmentectomy II-III) in USA in 1899 [97]. During the 1890’s, the techniques for controlling hemorrhage at resecting liver were largely based on transfixing suture and electric cauterization with a high mortality rate about 30-50% [94]. In 1911, Wendel has been credited with the first case of true right lobectomy using hilar ligation, based on the anatomical landmark "Cantlie’s line" illustrated by Cantlie in 1897 [86, 98].
Intraoperative bleeding remained a major challenge, often leading to lethal complications. Therefore, early surgeons try to design new surgical methods to mitigate massive hemorrhage and minimize the liver failure. In 1885, Postemski recommended suturing the liver stump to control bleeding, a practice later adopted by Italian surgeons [99]. In 1896, Kousnetzoff and Pensky introduced a technique using a blunt-ended needle with a double thread, passed through the whole liver in a continuous manner along the resection line. As sutures pulled into the soft liver tissue as series of guards to compress the intended resection plate to prevent bleeding along the resection line [100]. In Taiwan, Chang’s liver needle, introduced in 2006 by National Cheng Kung University Hospital, was also based on a similar principle [101].
The “finger-fracture” technique for liver dissection was first mentioned by Keen in 1899 [97], and later emphasized first by Anschutz in 1905 [102]. In 1956, Fineberg et al. refined this approach using the surgeon’s finger or the back of the scalpel for rapid parenchymal dissection [103]. In 1958, Lin TY introduced the finger-fracture technique in Taiwan, involving the insertion of the thumb and index finger into the liver to crush the tissue, with vessels and ducts tied and divided as encountered [40, 104]. In 1963, Tung TT modified this technique in Vietnam by occluding the portal pedicle, which resembled the pringle maneuver, to improve hemorrhage control [105]. However, intra-operative vascular control method, Pringle maneuver, has been started to use since 1908 [106], and was adopted widely in many institutions worldwide nowadays. In Taiwan, in 1996, Wu CC et al. reported a study involving 83 patients undergoing hepatectomy with repeated clamping for 15 minutes and decamping for 5 minutes at Taichung VGH. The longest total ischemia time recorded was 204 minutes through the upper time limit for hepatic ischemia is still undetermined [107]. In 2001, Belghiti et al. introduced the liver “hanging maneuver” that avoid mobilization of live and reduces intraoperative blood loss during right hepatectomy [108]. In 2008, Chen et al. in China performed right hepatectomy on 65 patients underwent right hepatectomy using “double-hanging maneuver” achieving successful outcome without major bleeding [109]. Modern advancements have introduced numerous surgical tools for safe and effective liver resections, including microwave tissue coagulators, radiofrequency dissecting sealers, cavitron ultrasonic surgical aspirators, and ultrasonic energy scalpels [110, 111]. These innovations have significantly improved the safety and outcomes of hepatectomies in contemporary practice.
The concept of “anatomic hepatectomy” was first reported by Lortat-Jacob and Kobert in France in 1952 [112]. Actually, Honjo and Araki have performed an anatomic right lobectomy for metastatic carcinoma as early as 1949 in Japan and later, cases reported in 1955 [113]. In USA, the Quattlebaum and his son successfully resected the right lobe of a 65-year-old woman with primary liver carcinoma reported in 1953 using hilar ligation, and died 19 months later due to recurrent disease [114]. During the 1950s, other groundbreaking major liver resections were reported, including Brunschwig [92], and Pack et al. [115] in New York, Longmire [116] in Los Angeles, and McDermott et al. [117] in Boston. Meanwhile, in Asia where primary liver neoplasms were more prevalent, Honjo and Araki in Japan [113], Tang et al. in Shanghai [118], Ong and Leong in Hong Kong [119], Balasegaram in Malaysia [120] Tung in Hanoi [105, 121] and Lin in Taiwan [40] pushed the boundaries of hepatectomy, overcoming the high incidence of cirrhosis among their patients. The efforts of these pioneers greatly improved surgical techniques and patient outcomes, resulting in significantly lower operative mortality rates compared to earlier eras.
In Taiwan, progress in liver surgery has been driven by advancements in surgical instruments and a growing understanding of liver anatomy. The use of liver resection as the primary treatment for liver cancer has increased significantly, rising from 8.05% (370/4,596 cases) in 1995 to 28.66% (3,088/107,524 cases) in 2021 respectively as reported by the Ministry of Health and Warfare, Taiwan [122] shown in the (Figure 3). Regarding liver cancer research, academic contributions from Taiwan have also grown. A total of 5,543 liver cancer articles (2.6% of the global total of 214,021 articles) were published from Taiwan’s researchers, ranking Taiwan 12th in the world, according to the Web of Science database (accessed November 21, 2024). The top-3 contributors globally were the United States (70,983 articles, 33.2%), China (50,881 articles, 23.8%), and Japan (22,131 articles, 10.3%).
In 1991, Reich et al. reported on the excision of a tumor originated from the liver edge in a 37-year-old female found incidentally during laparoscopic gynecologic surgery; and pathology revealed a liver focal nodular hyperplasia. At the initial stage, selected liver superficial neoplasm can be managed expediently by laparoscopic approach [123]. Concerning the laparoscopic hepatectomy for HCC, Kaneko H et al. since 1993 [124] and Hashizume M in 1995 [125] had performed these challenges successfully in Japan. A laparoscopic left lateral sectonectomy on a woman with hepatic adenoma was successfully performed by Azagra in 1996 [126]. In Taiwan, laparoscopic hepatectomy was first started to use for treatment of HCC presented by author since 1998 [127]. Nowadays, laparoscopic hepatectomy was extensively and routinely used in Taiwan even in the world. The academic search through WOS, there were 5,964 articles totally concerning laparoscopic hepatectomy, and 119 published from Taiwan, ranked 14th in the world. The top-3 contributors globally were the China (n=1,323), USA(n=1,044), and then Japan (n=851) access on Nov. 22. 2024.
The surgical robotic system is superior to traditional laparoscopy in regards to 3-dimensional images and better instrumentations. Robotic surgery for hepatic resection has not yet been included or expected in the robotic abdominal surgery reported around 2004 [128]. From March 2002 to March 2009 in USA and Italy, Giulianotti et al. performed seventy robotic liver resections successfully, 42 (60%) patients of malignant and 28 (40%) patients of benign liver tumor [129]. In Asia, Choi SB et al. performed three robot-assisted left lateral sectonectomies for one with HCC and for two with colon cancers with liver metastasis in Korea in 2007 [130]. Nowadays, robotic liver resection were widely used in Taiwan even in the world. More advance, a day-case robotic liver resection clinical pathway was formulated and implemented when patients were planned for discharge within 24 hours of admission after non-anatomical wedge resections [131]. Regarding publication articles about robotic liver surgery were 483 totally through WOS accessed on Nov.25. 2024. There were 23 articles published from Taiwan, ranked 12th in the world. The top-3 contributors globally were the USA (n=169), Italy (n=94), and China (n=76).
Liver transplantation was first performed in 1963 and first successfully performed in 1968 in the USA, both by Dr. Starzl (1926-2017). This is the major advance in liver surgery in the 20th century as the treatment of end-stage liver disease. Nowadays, the liver transplantation is an acceptance world widely and can be operated on, massively or selectively resected and handled safely. These procedures used are achieved on a long history of innovation by surgeons based on hemorrhage control, mechanism of regeneration and understanding liver anatomy. On the day of Starzl’s 90th birthday party in 1982, a life achievement of liver transplantation from American Liver Transplantation Society for Dr. Starzl, he said: “The history of medicine is that what was inconceivable yesterday, and barely achievable today often becomes routine tomorrow.” In Taiwan, Chen CL as a student of Professor Starzl, has deserved the honor to say “Medicine is about saving lives, and has no place for egoism.” In Taiwan, Chen CL has performed the largest volume of liver transplantation, and he published articles, personally ranked the 6th globally through the searching from WOS. Globally, there were 98,154 articles totally published and 1,771 from Taiwan ranked 17th among the world. The top-3 globally were USA (n=31,493), then China (n=10,038) and Japan (n=9122) accessed on Oct.15, 2024. Laparoscopic approach for donor hepatectomy was an evolution and challenging technique. Soubrane et al. reported the first pure laparoscopic right donor hepatectomy in 2013 [132]. This procedure should be reserved for highly specialized team with well experience of advanced laparoscopic hepatobiliary surgery as well as living donor liver transplantation. In 2018, the expert panel stated that laparoscopic donor hepatectomy is increasing its role in both pediatric and adult LDLT. However, for laparoscopic donor hepatectomy, more evidences are required for an international registry for future standardization in future [133].
Around 2007, “navigation surgery” guided by indocyanine green (ICG) fluorescence imaging was first introduced as a new imaging technology by Ishizawa et al. [134]. The ICG fluorescence imaging enables the creation of a new surgical concept known as fluorescence navigation surgery. ICG is selectively retained in well or moderately differentiated hepatocellular carcinoma (HCC) tissues due to preserved portal uptake and can highlight poorly differentiated HCC or colon cancer metastases as rim-fluorescing lesions against noncancerous liver tissue. Alongside intra-operative ultrasound, ICG-fluorescent imaging allows the highly sensitive detection of small and otherwise invisible liver tumors in real- time, significantly improving the precision of liver resections and the more accuracy of operative staging in our future.
4. Conclusion
Hepatic surgery has evolved from high-risk, rudimentary interventions to a specialized field incorporating cutting-edge technology. The turning point came in the 1970s, when pioneers, Stig Bengmark in Lund, Leslie Blumgart in Glasgow (and then London), and Henri Bismuth in Paris, the so-called “B-team.” Bach, Beethoven and Brahms, established HepatoBilio-Pancreatic Surgery for the young surgeons to learn in the world [135]. As Dupre and De Crignis aptly stated, “Knowledge of liver anatomy is the key to performing precision surgery for liver tumors. Liver anatomy is king, three-dimensional reconstruction is queen, and liver resections are the princes and princesses.” Indeed, modern hepatic surgeons must integrate anatomical expertise, advanced imaging, and innovative tools to deliver optimal care [136].
Great step of hepatic surgery was launched while the knowledge of liver anatomy and pathophysiology have been served as the lighthouse guiding surgeons in their difficult procedures [137]. Today’s achievements of hepatic surgery were made, and we should never forget the bloods of patients, tears of their families, and sweats of ancient surgeons. Besides, hepatic surgeons were enabled to achieve also by extraordinary developments in anesthesiology, infection control, radiologic investing, and surgical instruments. Moving forward, hepatic surgery continues to be driven by the pursuit of excellence, with the right technique tailored to the right patient at the right time.
Disclaimers
None.
Sources of Support
None.
Confliction of Interest
None.
Funding
None.
Formation
EndNote X9, NLM.
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