H i s t o r y o f He p a t i c

Surgery
Kuno Lehmann, MD, Pierre-Alain Clavien, MD, PhD*

KEYWORDS
 Liver  Transplantation  Hepatic surgery  Resection

THE LIVER IS A FRAGILE BLEEDING MYSTERY

Many years lie between the first historical reports on hepatic anatomy and todays
hepatic surgery. One of the first tales is the legend of Prometheus, written by Hesoid
(750700 BC), recounting ancient times. Prometheus stole fire from Zeus, the godfather
of ancient Greece, and gave it to mankind. For this infringement, Zeus chained him to
a rock and sent an eagle to devour his liver. The liver regenerated and gained its
normal size overnight. Each morning the hungry eagle returned, and Prometheus
was captured in eternal pain. Today, the amazing regenerative capacity of the liver
is no longer an inspiration for mystical tales but is the basis for modern hepatobiliary
surgery.1
An Alexandrian physician Herophilus (330280 BC) was one of the first anatomists to
describe the liver, although his written work is not available. The Greek physician
Galen (AD 130200) cited his work and accurately described the lobar anatomy and
vasculature, interpreting the liver as the source of blood. However, in the following
centuries of the Middle Ages, knowledge on hepatic anatomy moved forward very
little.
More than 350 years ago, anatomists started exploring hepatic anatomy with clever
ideas. In 1654, Glisson2 from Cambridge, England, cooked the organ in hot water,
removed the hepatic parenchyma, and explored the hepatic blood flow with colored
milk. He discussed the intrahepatic anatomy and topography of the vasculature
(Fig. 1). The growing knowledge of hepatic anatomy was one of the substantial
preconditions for the development of hepatic surgery. However, this precondition
was still far from realization, and the liver remained a fragile bleeding mystery.

ANATOMIC INSIGHTS PROVIDED THE FUNDAMENTAL BASIS FOR HEPATIC SURGERY

In the nineteenth century, two fundamental concepts enabling major surgery were
introduced: anesthesia and asepsis. In 1842, Crawford W. Long used ether as

Swiss Hepato-Pancreatico-Biliary & Transplantation Center, Department of Surgery, University

Hospital of Zurich, Ramistrasse 100, Zurich 8091, Switzerland
* Corresponding author.
E-mail address: clavien@access.uzh.ch

Surg Clin N Am 90 (2010) 655664

doi:10.1016/j.suc.2010.04.018 surgical.theclinics.com
0039-6109/10/$ see front matter 2010 Elsevier Inc. All rights reserved.
656 Lehmann & Clavien

Fig. 1. Intrahepatic vasculature. (From Glisson F. Anatomia hepatis. London: Dugard; 1654.)

a surgical anesthetic for the first time in the United States. In 1867, Joseph Lister from
Glasgow, Ireland, introduced antiseptic techniques against bacterial infections after
Louis Pasteur from Paris, France, had discovered the dangers of bacteria.
Before this period, only anecdotal records of hepatic surgery existed. Usually, the
surgeons described the removal of protruding hepatic tissue after trauma. Among
these surgeons were Ambroise Pare  from Paris, France, J.C. Massie from the United
States, and Victor von Bruns from Germany. However, hepatic trauma at that time was
generally managed without operation. It took many years before any courageous
surgeon was successful in the first attempt of a planned hepatic resection.
Carl Langenbuch from Berlin, Germany (Fig. 2), performed the first cholecystec-
tomy. He reported the first elective and successful hepatic resection in 1888.3 In
1891, William W. Keen from Philadelphia performed the first resection in the United
States. He used the finger fracture technique to divide the hepatic parenchyma.
Intraoperative bleeding control remained the most striking challenge then. In 1896,
Michel Kousnetzoff and Jules Pensky4 suggested the use of a continuous mattress
suture above the resection line for controlling bleeding. In 1908, Pringle5 from Scot-
land, described a method of temporary compression of the portal ligament in a small
series of patients. However, the major discoveries were still ahead.
It was again the fine work of anatomists that provided the key insights to overcome
major bleeding. About 120 years ago, in 1888, Hugo Rex from Germany,6 and in 1897,
James Cantlie from Liverpool, England,7 challenged the accepted anatomic division of
the liver by the falciform ligament. Using corrosion studies, they separated the liver by
the branches of the portal vein. Furthermore, they defined an avascular plane through
the gallbladder bed toward the vena cava and through the right axis of the caudate
lobe along the middle hepatic vein. Today, this plane is known as the Rex-Cantlie
line. At the beginning of the twentieth century, Walter Wendell from Magdeburg,
Germany,8 and Hansvon Haberer from Graz, Austria,9 were the first surgeons to
perform resections along this anatomic plane.
Hepatic anatomy was further refined by the description of the intrahepatic biliary
duct system and the vascular tree by Carl-Herman Hjortsjo10 from Lund, Sweden,
and John Healey and colleagues11 from Houston, Texas. In 1954, Claude Couinaud12
 History of Hepatic Surgery 657

Fig. 2. Carl Langenbuch (18461881). (Reprinted from The Royal College of Surgeons of
England; with permission.)

from Paris, France, published his seminal work on the segmental architecture of the
liver (Fig. 3).13 Based on the branches of the portal vein, he separated the liver into
8 well-described segments. The systematic descriptions of Carl-Herman Hjortsjo,
John Healey, and Claude Couinaud had a major effect on surgical technique and
related mortality.
In 1950, Ichio Honjo ki14 from Kyoto, Japan, reported the first anatomic resection. The
first resections in Europe and the United States were reported by Jean-Louis and
Lortat-Jacob15 from Paris, France in 1952, followed by Julian. K. Quattlebaum,16
from Georgia in 1953. In the following years, many surgeons reported their
experience, including Alexander Brunschwig17 and George T. Pack and colleagues18
in New York and later, William P. Longmire and Samuel A. Marable19 in Los Angeles,
California.
Over the years, serious concern was growing over hepatic nomenclature.
Throughout the world, liver surgeons used different, sometimes confusing, terms.20
Only a few years ago, in 2000, a group of international liver surgeons proposed a stan-
dardized nomenclature. This terminology was introduced at the biannual meeting of
the International Hepato-Pancreato-Biliary Association in Brisbane, Australia. Subse-
quently, the terminology was called the Brisbane nomenclature.21

LIVER TRANSPLANTATION: A HARD SUCCESS

The transplantation era was an important period and driving force for the development
of hepatobiliary surgery. In 1955, Cristopher S. Welch22 from Albany, New York,
658 Lehmann & Clavien

Fig. 3. Claude Couinaud working with his collection of liver casts at the School of Medicine
in Paris, France, in 1988. (From Sutherland F, Harris J. Claude Couinaud: a passion for the
liver. Arch Surg 2002;137(11):130510. Copyright (2002) American Medical Association. All
rights reserved; with permission.)

published the first report of heterotopic liver transplantation in a dog. J. A. Cannon,

Thomas E. Starzl, and Francis D. Moore and colleagues23 continued with orthotopic
liver transplantations (OLTs) in dogs and established the basis for transplantation in
humans. In 1963, Starzl and colleagues24 (Fig. 4) made the first attempt to transplant
a human liver in Denver, Colorado. However, the young patient died during the oper-
ation due to uncontrollable bleeding. Another attempt by Moore25 in Boston, Massa-
chusetts, also did not succeed. It was again Starzl and colleagues26 who reported the
first series of successful OLT in 1968. Shortly after, Sir Roy Calne and colleagues27
performed the first OLT in Europe in Cambridge, England. At that time, most patients
did not survive OLT longer than a few weeks or months, although many patients
initially tolerated the surgery well.
The solution to this problem was the discovery of cyclosporine A (CyA) by Hartmann
F. Stahelin and Jean-Francois Borel from Basel, Switzerland, in 1972. Seven years
later, Calne and colleagues28 reported the first use of CyA in patients undergoing
OLT. The result was a dramatic improvement in long-term survival. Before the intro-
duction of CyA, the 5-year survival rate after OLT was less than 20%. But the survival
rate improved to 60% or more with the introduction of CyA.29 In the late 1980s, Tom E.
Starzl introduced FK-506 (tacrolimus) as a new and promising immunosuppressant at
the University of Pittsburgh. In the following years, immunosuppression was refined,
 History of Hepatic Surgery 659

Fig. 4. Tom E. Starzl performed the first successful OLT in 1968. (Reprinted from the
PittChronicle, University of Pittsburgh, October 15, 2007; with permission.)

and the introduction of effective drugs such as polyclonal antilymphocyte antibodies,

anti-CD3 antibodies in the 1980s, mycophenolate mofetil in the early 1990s, and rapa-
mycin in the late 1990s offered further alternatives in the management of patients after
OLT.
Surgeons already recognized the critical role of adequate preservation in the early
stage of solid-organ transplantation. Cold preservation technique was described in
1912 by the French surgeon Alexis Carrel, who preserved and transplanted vessels,
skin, and connective tissues in dogs.30 Together, Carrel and Charles A. Lindberg,31
the famous aviator and engineer, constructed a perfusion pump and successfully
preserved thyroid glands. The relevance of cooling the donor organ was recovered
years later during animal experiments by Moore and colleagues.23 For many years,
storage in cold Collins solution was the standard for organ procurement.32 A landmark
advance was the development of the University of Wisconsin (UW) solution by Folkert
O. Belzer and James H. Southard33 in 1988. The UW solution represents an important
gain of knowledge in the pathophysiology of ischemia and reperfusion injury. The UW
solution contains colloids to prevent cell swelling, oxygen scavengers like allopurinol
and glutathione for cell protection, and adenosine to facilitate adenosine triphosphate
production.34
Nearly 30 years ago, in 1983, the National Institutes of Health Consensus Confer-
ence accepted liver transplantation as a therapy for patients with end-stage liver
disease. Consequently, the number of patients on waiting lists increased massively
in the following years, resulting in a dramatic shortage of available donor organs for
transplantation. The mortality of patients waiting for an organ stimulated the develop-
ment of new concepts.
This shortage was more accentuated in pediatric patients. Because children require
size-matched organs, there was a high death rate in the pediatric waiting list for
cadaveric organs. This high death rate stimulated the development of technical inno-
vations based on the segmental anatomy of the liver. In 1984, Henri Bismuth,35 from
Paris, France, performed the first OLT using only the left hemiliver. In 1988, Rudolf
Pichlmayr and colleagues,36 from Hannover, Germany applied the concept of partial
liver graft transplantation. They reported the use of a split graft, in which the right
660 Lehmann & Clavien

hemiliver was transplanted to an adult and the left to a child. Christoph E. Broelsch and
colleagues37 published the first patient series on split liver transplantation in Chicago,
Illinois. Living donor liver transplantation was first reported in Brazil, in 1989, by Silvano
Raia and colleagues.38 A year later, Russel W. Strong and colleagues,39 from Bris-
bane, Australia, published the next case of a mother donating the left hemiliver to
her son. In 1994, Yoshio Yamaoka and colleagues,40 from Kyoto, Japan, used the right
hemiliver for transplantation and enabled living donor liver transplantation in adults.
The report on first series of patients was published by Broelsch and colleagues41 in
Chicago, Illinois and later by Chung-Mau Lo and colleagues42 in Hong Kong.
A potential approach to solve the shortage of donor organs was shown with a favor-
able outcome by the use of steatotic donor organs.43 Donor risk scores and appro-
priate matching to selected recipients may further improve the outcome of these
organs.44 Today, liver transplantation is a great success and has become a standard
procedure with excellent outcomes.45

HEPATIC SURGERY BECOMES SAFE AND EFFECTIVE

In the sixties, perioperative mortality rates up to 50% were common after right hemi-
hepatectomy. Parallel to the progress in liver transplantation, hepatic surgery, mostly
for oncologic diseases, became more sophisticated. In 1983, William P. Longmire and
colleagues46 from Los Angeles, California, published the results of 138 patients after
major resections with a 30-day mortality of 10%. A few years later, in the 1990s,
Jacques Belghiti and colleagues47 from Paris, France, in a large series of 747 patients,
reported a mortality of 1% in patients with normal liver parenchyma. Leslie H. Blum-
gart48 from New York and Sheung Tat Fan and colleagues49 from Hong Kong pub-
lished similar results. However, the presence of cirrhosis,50 portal hypertension,51
and liver steatosis52 were identified as important risk factors for perioperative
morbidity and mortality. Because of the complexity of the diseases, and the perioper-
ative care, these patients required specialized teams. An important step for the
improved outcomes was the promotion of specialized, interdisciplinary centers.53 A
higher caseload in such hepato-pancreatico-biliary (HPB) centers translates into
more experience, which is an important factor for favorable outcomes.54,55
Many technical tools further refined hepatic surgery. Masatoshi Makuuchi and
colleagues56 from Tokyo, Japan, introduced the concept of routine intraoperative
ultrasonography for liver surgery. These investigators were also among the first to
use portal vein embolization to increase the future liver remnant before major resec-
tion.57 However, the concept of selective portal occlusion and subsequent contralat-
eral hypertrophy was known since 1920.58 Radiofrequency was introduced as
a treatment for unresectable tumors.5961 For further details and an in-depth coverage
of hepatic surgery in the twentieth century, the authors recommend the comprehen-
sive overviews by Joseph G. Fortner and Lesilie H. Blumgart62 and James H. Foster.63
The complex treatment strategies for metastatic liver disease are illustrative exam-
ples for the progress and success of HPB surgery.1 In 1940, Richard B. Cattell,64 in
Boston, Massachusetts, performed the first resection of a metastatic tumor. However,
still in the early eighties, resection of colorectal liver metastases remained controver-
sial because of the high operative mortality.65 Today, resection for liver metastasis
provides favorable outcomes compared with the natural history.66 In a series of
1001 consecutive patients, the 5-year survival rate was 37%.67 Multistage procedures
are currently recognized as effective strategies for patients with otherwise unresect-
able tumors.1
 History of Hepatic Surgery 661

SUMMARY

Surgical experience and outcomes after major surgery have improved as a result of
progress in many fields. Consequently, hepatic surgery has enjoyed a dramatic devel-
opment during the last 3 decades. Today, liver surgery has lost the threat of the early
years. In experienced hands, hepatic surgery has become reliable and effective and
has consequently saved the life of many patients.

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