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4 Chapter 1 A historical review of venous and lymphatic disease
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1.2 Votive tablet offering to Asclepius, the Greek god of medi-
cine, alleged to be commissioned by a man who was suffering
from varicose veins.
Source: (The National Museum of Athens, Greece.)
Galen of Pergamon, a Greek physician, surgeon, and philosopher in the Roman Empire, would be
recognized along with Hippocrates as the most prominent
medical thought leader in antiquity.
4
The theory of the
four humors popularized by Hippocrates was fundamental to Galen’s approach to treatment. His appointment as
the chief physician to the gladiators provided his initial
introduction to human anatomy. Since dissection of human
cadavers was forbidden at that time, he performed anatomic dissections on primates as well as porcine models
to explore various parts of the body and their functions.
In doing so, his experiments and anatomic knowledge
became the basis for his medical ndings and treatment.
Like Hippocrates, he was inuenced by the great philosophers, Aristotle and Plato. Galen’s work advanced the
science of medicine rather than magic and superstition to
a discipline which depended upon observation and empiricism. Galen continued following the dominant humoral
theory—healing of a VLU would lead to bile entrapment
madness and other diseases. He advocated single surgical
ligatures of silk for ligating varicose VVs. Galen’s medical
doctrines would inuence the Eastern and Western world
for the next 1500years.
Surgery for VVs would subsequently be described by
several physicians, including the Greek physician Oribasius
(325–405 ) and the Byzantine physician Aetius of Amida
(502–575 AD).
5
Albucasis (963 ), the greatest of Islamic
surgeons, developed specialized instruments for the surgery
of VVs, where he completely dissected out the varicosity
and ligated the ends with cautery.
1.3 This thirteenth-century fresco from the crypt of the Agnani
Cathedral portrays Hippocrates and his student Claudius Galen,
the two most inuential physicians of several centuries for
treating venous disease. Juxtaposed with this fresco is a pillar that contains the theories of the four elements referencing
the humoral theory of Hippocrates. This theory was to dominate
medical thought for the next 15 centuries.
Roman physicians also addressed the problem of VVs.
Celsus, at the start of the rst century , described the use
of single silk ligatures for bleeding VVs and treated varicosities with avulsion and cauterization of the vein ends.
Plutarch, in his Lives, describes the treatment of Caius
Marius in 75 , who underwent surgery for VVs with
multiple incisions without anesthesia. When approached
about an operation for the second side, he classically said,
“Isee the cure is not worth the pain.”
1.2.3 The Middle Ages (500–1400 AD): Fifth
to sixteenth centuries
Medical thought in the Middle Ages was suspended in animation and relied on the continuation of the Greco-Roman
and Egyptian medical teachings. With the rise of Christianity, the spiritual theme assumed greater importance and
inuence on physicians. Illnesses were considered a punishment from God, so that medical treatment revolved around
the causation of sin and depended on celestial inuences.
The humoral theory espoused by Galen and Hippocrates
persisted as the cause of disease. At the same time, there
was a signicant emphasis on the role of diagnosis by
physicians, which involved palpation of the pulse and,
in particular, examination of the urine. Medicinal plants
and herbs assumed importance for treatment, but their
choice was guided more by their similarity to the body part
treated, rather than by testing their efcacy. The plague was
to course across Europe and ascribed to religious explanations, such as God’s punishment for man’s sins.
Ambrose Pare, the leading surgeon of the Renaissance,
introduced ligature for controlling venous hemorrhage and
described ligation and division with venesection of thigh
7
VVs.
Captured as a prisoner by the Spanish, Pare was
threatened with having his throat slit if he did not heal the
chronic VLU of the governor of Graveline. Pare’s approach
was not unlike today’s—debridement and external compression. The mixture of spiritual and medical care was
reected in his quote, “Idressed the wound, God healed it.”
As a precursor of some of today’s dubious outcome mea-
6
1.2 Chronic venous disease 5
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sures, Pare was able to convince his captors to release him
after 50% of the VLU healed, rather than full healing.
1.2.4 The seventeenth century
Due to a tectonic shift in scientic thought, the seventeenth
century saw emphasis on the laws of mechanics.
Bacon and Rene Descartes emphasized inductive reasoning as an important part of scientic inquiry. Reform in
thought began with anatomy and physiology to provide
physicians with their understanding of human diseases.
William Harvey’s (1578–1657) well-detailed discovery of
the circulation of blood resulted in the demise of Galen’s
theories, where blood was felt to be produced in the liver
and distributed to the body in a centrifugal manner.
vey showed that blood circulated unidirectionally, underlined by his famous, but simple, experiment of compressing
the veins of the forearm, which graphically demonstrated
the role of valves in the venous circulation (Figure1.4). It
was Malpighi who subsequently showed how blood transverses from the arteries to the veins through the microcirculation. Harvey exemplied a different approach to the
practice of medicine, where his knowledge of human anat-
8
Francis
9
Har-
omy and pathophysiology formed the basis of “rational”
medicine versus empirical medicine.
Richard Wiseman (1622–1676) developed his skills as
a surgeon to Charles II during the Royalist wars and was
the rst consultantsurgeonin London.
10
Wiseman served
for a period as assistant to Edward Molines ofSt.Thomas’s Hospital and observed the relationship between VVs
and VLUs—a “varicose ulcer.” Wiseman became famous
for his development of the rst compression garment, a
laced leather stocking to treat VLUs. Opposed to surgical
treatment of VVs, he advocated purging. As a last resort,
Wiseman advocated ligation of the vein with a subsequent
venotomy. The author of Severall Chirurgicall Treatises—
an esteemed landmark in British surgery—Wiseman was
the best-known surgeon of the seventeenth century.
1.2.5 The eighteenth century
This century saw the rise of VLUs as a major disease in
the general population. Physicians, however, persisted with
the Galenic concept that VLUs were related to humors.
As a consequence, open VLUs were considered benecial,
because humors could drain from the body. Treatment
of VLUs was by polypharmacy, which John Bell (1763–
1820), a Scottish surgeon and anatomist, was quick to
criticize for the lack of scientic basis.
12
Bell proposed an
alternative treatment strategy of bed rest and leg elevation
to heal venous ulcers. Compression, initially proposed by
Wiseman, was practiced with adhesive bandages.
In his text Practical Observations on the Treatment of
Venous Ulcers in the Leg, Sir Everard Home (1756–1832),
brother-in-law of John Hunter, illustrated that VLUs were
a major societal problem.
13
He believed that ligating VVs
promoted healing of VLUs. Like other surgeons at that
time, however, he abandoned this procedure because of
the high infection rate and pain during the procedure. Two
major advances led to the growth of surgery: anesthesia,
introduced by Morton in 1846,
in 1864 by the Scottish surgeon, Lister, who adopted Pasteur’s germ theory.
15
In a perceptive observation, William
Gay in the 1850s eschewed the single causation doctrine
that VLUs were solely due to VVs.
14
and asepsis, introduced
16
His careful dissections
showed that VLUs and typical skin changes of advanced
chronic venous insufciency were a consequence of
post-thrombotic disease of the deep veins. Presciently, Gay
proposed that VLUs, although healed temporarily after
ligation of VVs, quite often would recur.
11
1
1.4 Drawing of venous valves (1585) in a leg vein by Salo-
mon Alberti, which is putatively the rst visual description of
this important anatomic structure. William Harvey was later to
describe in De Motu Cordis (1628) the valve’s important functions of promoting unidirectional blood ow.
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1.2.6 Nineteenth century
Although Giovanni Rima (1777–1843) introduced
midthigh ligation of the great saphenous vein (GSV), it
was Friederich Trendelenburg (1844–1924) who received
recognition for using this site. Afew years later, his pupil,
George C. Perthes (1869–1927), modied the site of GSV
ligation to the current saphenofemoral junction. Contemporaneously, William Moore (1859–1927), an Australian
surgeon, also recommended ligation at the saphenofemoral junction.
Clinic, dissatised with ligation alone, advocated a long
incision from the groin to the below-knee area to extirpate the GSV. Although the diagnosis of venous disease
17
Charles H. Mayo (1865–1939), at the Mayo
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and reux relied solely on clinical grounds, the institution
of tourniquet tests for supercial and deep venous incompetence by Trendelenburg, Brodie, and Perthes improved
patient selection
1.2.7 Twentieth century
The twentieth century saw a rapid growth in both the diagnosis and treatment of chronic venous disease. This huge
advance in medicine in general is well recognized by historians, like Thomas Soderqvist: “More than ninety percent
of all scientic history has been made during the last half
century (20th). So far, however, only a fraction of historical scholarship has dealt with this period.”
the discussion of medical advances in the twentieth century will be divided into specic areas: surgery for varicose
veins, VLUs, reporting standards, and deep venous reconstruction. Discussion of venous and lymphatic disease in
the twenty-rst century will be a component of the individual chapters of this handbook.
1.2.7.1 Surgery for VVs
17
Due to the obvious long incision, which was subject to
infection and a cosmetically displeasing result, in 1906,
Mayo reported his less invasive technique with an external stripper for ligation and stripping (L&S) (Figure1.5).
Modications in the technique ensued over the rest of the
18
As a result,
century: 1905, invagination by Keller; 1907, endoluminal
stripping by Babcock; 1947, exible endoluminal stripper
by Myers; and 1960s, the standardization of the procedure
by the Mayo’s Lofgren brothers. Restricting L&S to the
above-knee segment, stripping downwards rather than
upwards, and PIN stripping all were associated with less
morbidity, especially neurological. Percutaneous endovenous thermal ablation by radiofrequency (RF) received
Food and Drug Administration (FDA) approval in 1999.
Laser ablation therapy followed shortly thereafter, with
FDA approval in 2002. Importantly, these techniques were
validated for the rst time by multiple randomized controlled trials, as will be discussed in the chapters on VV
surgery.
1.2.7.2 Venous ulcers
Paul Gerson Unna (1850–1929), the German dermatologist, developed a noncompliant zinc oxide and paste dress-
19
John Homans’s sequential 1916 and 1917 scientic
ing.
papers revolutionized our treatment of VLUs based on
a surgical approach for correcting the pathophysiology
of venous hypertension. “In surface varix complicated
by varicosity of the perforating veins not only must the
great saphenous be eradicated but many of its branches
in the calf must be followed and excised in the search for
incompetent perforating channels.”
thrombus led to vein incompetence with reux and venous
20
Valve destruction by
1.5 This drawing depicts the external stripping method for the great saphenous vein developed by Mayo in 1906. Others, like Bab-
cock and Keller, were to modify this procedure, including an internal stripping device. The Mayo Clinic was to play a major role in
developing the standard technique for ligation and stripping of varicose veins, including the exible endoluminal stripper by Myers
in 1947.
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hypertension. The objective validation of the role of venous
hypertension in the genesis of VLU was derived from two
studies by Henry Beecher. In 1936 Beecher’s measurement
of venous pressure changes in ambulatory normal volunteers showed that during ambulation, venous ow was
from the supercial venous system to the deep, due to the
latter’s lower pressure with activation of the calf muscle
pump. By contrast, in patients with VVs, Beecher’s second study demonstrated a lack of reduction in an elevated
supercial venous pressure during walking.
21
Linton described the benecial reduction of venous
pressure due to the calf muscle pump, which he termed
the “venous heart.” Linton would illustrate these pathophysiologic changes in his magnum opus, where he advocated ligation of the “supercial” femoral vein as a method
for the prevention of deep venous reux.
26
Although the
eponym of the “Linton procedure” has devolved to the
interruption of incompetent perforating veins, its original
description also included removal of dilated supercial
veins and resection of the area around the ulcer, including
20
fascia.
The British surgeon at St. Thomas’s Hospital, Frank
Cockett, who spent a year studying with Linton, would
later rene Linton’s concept into what Cockett termed the
“blowout theory”—VLUs were a consequence of a local
rise in venous pressure in the peri-malleolar area—and as
Homans and Linton espoused, they could be healed by
perforator interruption.
27
The next several decades were
devoted to reducing supercial venous hypertension by
interruption of the perforating veins through a progression of less invasive approaches to “cure” venous ulcers.
There were doubters to this relatively simple concept. In
1971 Bjordal performed direct venous pressure studies
and ow measurements of the GSV and a perforating vein
with sequential occlusions of those veins. Normalization of
ambulatory venous hypertension resulted only when reux
via the GSV was abolished and was not brought back to
normal by occlusion of the incompetent perforating vein
alone. Most importantly, in those limbs with post-thrombotic deep venous systems, the occlusion of neither the
saphenous nor the perforator normalized elevated ambulatory venous pressures.
20
Two studies in the mid-1970s by
the St. Thomas’s Hospital group cast doubt on the simple
approach of ablating incompetent perforating veins for
all patients with VLU, specically for patients with deep
venous involvement: The rst, a retrospective study in
1976, showed that patients with deep venous involvement
by phlebography had a signicant recurrence of VLUs in a
5-year follow-up versus a cohort with normal deep venous
systems; a subsequent prospective study of patients undergoing surgery to reduce venous hypertension either by L&S
alone or combined with perforator interruption revealed
that the surrogate outcome of reduction in venous pressure
failed to occur when there was deep venous involvement.
20
1.2.7.3 Venous reconstruction
Approximately 40%–60% of patients with VLU present
with underlying deep venous disease, which can be caused
by outow obstruction or reux. The latter is not amenable
to reduction of venous hypertension by treatment of supercial venous incompetence alone.
1.2.7.3.1 Outflow obstruction
Palma transposed the GSV distal to an iliac vein occlusion
to the contralateral femoral vein to bypass the obstruc-
22
Andrew Dale and others expanded the work of
tion.
Palma for venous-venous bypass, but unfortunately, longterm patency in most series was disappointing. In the twenty-rst century angioplasty and stent replacement would
become the procedures of choice for venous obstruction.
1.2.7.3.2 Reflux
Direct deep venous surgical procedures were developed
for patients with deep venous involvement not responsive
to reduction of supercial venous ablation. Along with
his other major contributions to venous disease, it was
Robert Kistner who initiated the direct repair of the deep
venous valve in 1979. Appropriately, he has been called the
“father” of deep venous surgery. Kistner’s results provided
symptomatic relief for approximately 60% in 10-year
follow-up, particularly in patients with primary valvular
incompetence.
23
In contrast, patients with post-thrombotic
valve involvement did less well. Several indirect alternatives
to direct valve repair were developed, such as transposition
of a proximal GSV segment containing a competent valve
(usually this segment has been removed in prior treatment)
and transplantation of a venous segment from elsewhere
containing a competent valve like the brachial or axillary
veins. Articial valves have been explored experimentally.
1.2.7.4 Reporting standards for chronic venous
disease
Like those for arterial disease, John Porter, under the auspices of the AVF, recommended a classication for chronic
venous disease like the tumor, node, metastases (TNM)
classication for cancer. The worldwide recognized CEAP
classication system was developed by expanding the original classication system (1994) of three clinical severity
stages for CVD to six and adding three other elements:
Etiologic, Anatomical, and Pathophysiology.
24
While the
CEAP classication permitted comparison of like groups, it
was not appropriate as an outcome measure. Acombined
task force of the AVF and an international group formulated the physician-reported outcome assessments: Venous
Clinical Severity Score, Venous Disability Score, and
Venous Segmental Disease Score. Patient-reported venous
disease–specic outcomes were subsequently developed.
1.2.8 Acute venous disease
In contrast to chronic venous disease, the historical timeline for acute venous disease, usually presenting as deep
venous thrombosis (DVT), is much shorter. The rst case
was reported and memorialized pictorially in the Middle Ages (1271) by Guillaume de Saint Pathus, when he
described a 20-year-old cobbler with right calf pain and
swelling, who ultimately developed a leg ulcer.
the Renaissance, the most common cause of DVT was
attributed to retention of unconsumed breast milk during
pregnancy, retained in the legs—the so-called “milk leg.”
Consequently, breastfeeding was encouraged as a method
for preventing DVT, again relying on the humoral theory of
25
During
1
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Hippocrates and Galen. Bloodletting also was prescribed
to discharge these evil humors. In the late 1600s Richard
Wiseman, developer of the leather compression stocking,
opined that DVT was a result of changes in the blood. It
would be Hunter who described an occlusion of the vein
by “blood clots” and observed the relationship between
DVT and fatal pulmonary embolus (PE).
25
This nding
prompted Hunter to ligate proximally in the vein to prevent extension of the clot. The fear of migration of the
thrombus dominated medical thought, so that strict bed
rest became the fundamental treatment for DVT and to the
extreme that legs were immobilized in splints. The underlying pathophysiologic process was ascribed to infection
with inammation of the vein wall, as DVT was observed
frequently postpartum or with postsurgical sepsis. Thus,
the fundamental treatment up until the early twentieth
century was bed rest, elevation, and application of warm
compresses. Additionally, anti-inammatory medication,
like salicylates, as well as the prevention and treatment
of infectionwere prescribed. In 1856, Rudolf Virchow, a
revered Berlin scientist and physician, described his famous
triad which pointed to the major mechanism of venous
thrombosis: vessel wall damage, stasis of ow, and the
presenceof a hypercoagulable state.
1.2.9 Twentieth century
1.2.9.1 Treatment
The rst anticoagulant was discovered by McLean in 1916
as a medical student. Charles and Scott produced pure crystalline heparin for use in humans in 1935, while 2years
later Murray described in animals the ability of heparin to
prevent developing blood clots. The initial focus for the use
of heparin was to prevent DVT in postoperative patients,
as shown by Crafoord in 1939. The effectiveness of heparin was felt immediately to be unquestionable, so that no
rigorous prospective studies were carried out. As an example, the comparative historical series of patients, described
by Bauer in two time periods—1929–1938 (pre-heparin)
versus 1940–1949 (heparin)—showed a drop in mortality
due to symptomatic DVT from 18% to 0.4%. There was
a dramatic shift in the treatment of DVT from prolonged
bed rest due to the necessity of administering continuous
intravenous infusions of heparin to earlier ambulation with
the development of injectable low-molecular-weight heparin (LMWH), not requiring monitoring. Hugo Partsch
challenged bed rest as standard of care, when in a modest
RCT he showed early ambulation with compression stockings improved pain and counteracted swelling, but without
increasing the risk of PE.
1.2.9.2 Diagnosis
Diagnostic tests for either acute venous disease or chronic
venous insufciency are based on morphologic (imaging)
or hemodynamic (functional) changes. True contrast imaging of the veins was rst introduced by dos Santos in 1938
and 2years later by Bauer with injections through a surgically exposed vein. Welch and colleagues made the test
less invasive by injecting contrast directly into a supercial
vein of the foot with tourniquet occlusion of the supercial veins. The early focus of venous imaging studies was
26
27
35
chiey on acute DVT.
Thirty years later Rabinov and Paulin standardized the technique of ascending phlebography
for the diagnosis of DVT. Since ascending phlebography
was invasive and difcult to repeat, however, a series of
less invasive diagnostic tests were developed sequentially
over the next several years. An important consequence of
assessing the validity of these tests was improvements in
determining their value by comparing these tests to the
gold standard of phlebography. Outcome measures of a
diagnostic test were changed to sensitivity and specicity rather than accuracy, as that outcome metric will vary
with disease prevalence. The sensitivity and specicity,
however, for I-125–labeled brinogen, strain gauge plethysmography, impedance plethysmography, and continuous
wave Doppler showed signicant disadvantages for these
modalities. Since they were based on detecting hemodynamic changes, nonocclusive thrombi went unrecognized,
particularly in the calf region. The Tufts group introduced
to vascular noninvasive testing the tool of receiver operator
characteristic curve analysis, which describes the dynamic
relationship between sensitivity and specicity dependent
on the threshold value for the disease selected. Duplex
ultrasound imaging would eventually become the test of
choice to replace phlebography.
1.2.9.3 Prevention of DVT and PE
Prophylaxis against PE is accomplished by compartmentalization,
DeBakey and Ochsner advocated inferior vena cava ligation to prevent Pes in 1932. This procedure, however, was
associated with a signicant mortality due to the profound
hemodynamic changes as well as the morbidity of lower
extremity edema. To avoid the high operative mortality,
2years later Homans modied the compartmentalization
approach to ligation of the femoral vein as a true preventive procedure. In 1958 DeWeese employed the cross-caval
suture technique, which prevented emboli from migrating to the lungs while not altering venous hemodynamics.
Apartially occluding plastic clip placed externally, which
divided the IVC into multiple channels, was developed by
Miles in 1964 and Adams and DeWeese in 1965. Aless
invasive approach with an umbrella-shaped intraluminal
device, which could be placed under local anesthesia, and
a cut-down was invented by Mobin Uddin. Unfortunately,
this was complicated by thrombotic occlusion below the
device as well as device migration. In 1981, Greeneld
developed the rst truly percutaneous lter with excellent
efcacy and safety.
28
pharmacologic,25 or mechanical means.29
1.2.9.4 Pharmacologic
Sevitt and Gallagher’s autopsy study indicated that patients
treated with Coumadin had no fatal emboli versus the 10%
incidence in untreated patients. Given the disadvantages of
oral anticoagulants—time to achieve therapeutic efcacy,
risk of bleeding, and close monitoring—heparin was forwarded as a better drug. Sharnoff reported a signicant
reduction in the incidence of fatal PE, but unfortunately
this study had no control cohort or objective evaluation
of underlying DVT. The validation of low-dose heparin to
prevent DVT/PE was ushered in by a series of randomized
controlled trials. While this regimen reduced calf DVT, it
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was less effective in orthopedic patients and for proximal
DVT, particularly when initiated after trauma. The most
signicant step for anticoagulant prophylaxis was simplied by the development of LMWH, introduced in Europe
at the beginning of the 1980s, which usually did not require
monitoring. Numerous RCTs have validated its efcacy.
1.2.9.5 Mechanical
The simplest approach is the graduated elastic compression
stocking invented by the German engineer, Conrad Jobst,
in 1950. Blood ow is increased in the bedded patient to
prevent stasis on the valve cusps and was validated clinically by multiple RCTs in the 1970s to reduce calf vein
DVT. Due to the low event rate of proximal DVT and PE,
however, the result was less precise for these outcome measures. Progressing in complexity, intermittent pneumatic
compression (IPC) treatment is particularly useful for prophylaxis in patients with contraindications to anticoagulation. In 1970 Calnan and colleagues described the benets
of a prototype pneumatic intermittent compression device
which stimulated activation of the calf muscle pump. Subsequently, multiple RCTs with commercially available IPC
devices showed that this approach was effective.
1.2.9.6 Thrombus removal
Besides the acute threat of sudden death from PE and the
long-term sequalae from thrombus in large veins, like the
iliac, direct surgical removal of a thrombus was pursued.
While this technique and its risks were improved with technical modications, such as Fogarty balloon extraction and
arterial venous stula to maintain patency, results were
disappointing, and this approach was abandoned. Lytic
agents appeared a better, less invasive method to dissolve
a thrombus. The initial approach with systemic streptokinase was plagued by long infusion times, bleeding, and
lower efcacy, however, in the large outow vessels. Catheter-directed local infusion of thrombolytic agents had the
advantages of minimizing bleeding and promoting more
rapid clot dissolution. The National Venous Thrombolysis Registry, with 287 patients treated with urokinase followed up for 1year—the largest published experience with
catheter-based therapy—demonstrated total lysis of clot in
nearly a third of cases and partial lysis in greater than half.
Patency was higher in proximal venous segments and those
with complete lysis. The twenty-rst century would see
advances in both thrombus lysis and its catheter-directed
mechanical removal.
30
in the bloodstream.31 Unfortunately, during the Middle
(Dark) Ages these discoveries were lost, only to be reobserved in the late Renaissance.
The brilliant William Harvey (1578–1657), however,
disputed the existence or the function of the lymphatics. In
1652 Thomas Bartholin described the known segments of
the lymphatic system and was the rst investigator to use
the term “lymphatic” (Figure1.6). Bartholin’s discovery
was not without controversy. Ayear earlier Olaus Rudbeck had presented similar conclusions during an animal
dissection before the queen of Sweden. Both Bartholin and
Rudbeck accused each other of plagiarism. The important
valves of the lymphatic were described by Frederik Ruysch
(1638–1731), although it is highly likely that both Bartlett
and Rudbeck had noticed these structures. Visualization of
the lymphatic system was necessary to better describe these
structures. The anatomic innovation of Anton Nuck (1692)
used mercury to dene the entire lymphatic system.
31
1.2.10.1 Physiology
To William Hunter goes credit in 1784 for describing that
the principal function of the lymphatic vessels throughout
the body was their ability to absorb material and, in conjunction with the thoracic duct, transport chyle to the vas-
1
1.2.10 Lymphedema
Traditional histories of the lymphatics begin with the “discovery of lymphatic vessels” in 1622 by Gaspare Aselli,
the Italian anatomist. The early Greeks, however, probably
had stumbled upon the lymphatics. Hippocrates described
“white blood,” and Aristotle observed structures containing “colorless uid.” In Aselli’s dissection of a postprandial
dog to study diaphragmatic motion, when he incised the
small white vessels in the mesentery, which he presumed
to be nerves, chyle exuded. Aselli named this structure the
vasa lacteal, whose function was to absorb chyle from the
intestines and transport the uid to the liver to be mixed
1.6 Thomas Bartholin, a Danish anatomist, is credited with
being the rst to describe the entire human lymphatic system
in 1652 and was the rst to name these structures lymphatics
(vasa lymphatica in homine nuper inventa).
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cular system. The older concept of direct communication
through thin tubes of the lymphatics with blood vessels was
disproven by Virchow in 1858 and ascribed to an unwanted
consequence of the histologic techniques used by the previous investigators. von Recklinghausen advocated for direct
communication through very small lymphatics to blood vessels, while several theories were posited as to how lymph was
formed. Ludwig’s contention that lymph was a simple ltration of uid due to intravascular pressure was conrmed
in 1894 by Starling. He proposed a theory that dominated
lymphatic physiology for over 100years. Arterial pressure
in the capillary lters uid into the interstitial space. Due
to a reduction in hydrostatic pressure on the venous side of
the capillaries, plasma oncotic pressure becomes the major
force for reabsorption of crystalloids and uid. Finally, the
semi-permeable capillary membrane prevents absorption of
proteins back into the vascular system. Levick and Michel
were to disprove this mechanism and show that the lymphatics were responsible for 80%–90% of interstitial uid.
The seminal breakthrough in imaging the lymphatics
arose from the work of John B. Kinmonth in 1952. He
directly cannulated the lymphatics under optical magnication and injected contrast material for lymphography.
This imaging tool was to revolutionize our understanding
of lymphatics.
1.2.10.2 Clinical
32
In 1946 Edgar V. Allen of the Mayo Clinic proposed the
basic classication of lymphedema into two types: primary,
related to in utero developmental defects, and secondary,
due to cancer treatment, infection, or advanced venous disease. In 1957 Kinmonth suggested a further clinical classication of primary lymphedema by age of onset: congenital,
present at birth; praecox, present before age 35; and tarda,
occurring after age 35. In 1969 based on his professorial
unit at St. Thomas’s experience with lymphangiography,
Kinmonth developed an anatomic classication of primary
lymphedema: aplasia, where no discernible lymphatic vessels are present; hypoplasia, a reduced number of lymphatic
vessels; and hyperplasia, an increased number of lymphatic
vessels. Linking the anatomy and Kinmonth’s extensive
clinical experience, this classication system had important
prognostic value for these patients, as hyperplasia may be
associated with a lesser clinical degree of lymphedema and
may be more frequently bilateral.
1.2.10.3 Treatment
The nonsurgical management of lymphedema with compression and skin care became the predominant approach
and a formalization of this regimen—complete decongestive therapy or complex decongestivetherapy (CDT), was
implemented in the 1980s. CDT consisted of the following
elements: manual lymph drainage (MLD), compression
therapy, decongestive and breathing exercises, and skin and
nail care. The essential element of MLD was developed in
1932 by Emil and Estrid Vodder, who were massage therapists and naturopaths in France. Their approach relied on a
series of light, rhythmic strokes to stimulate lymph ow and
uid movement rather than heavy external pressure. Subsequent systematic reviews and meta-analyses showed efcacy.
The concept of applying an external pressure to reduce
an edematous limb date back to the use of Wiseman’s
leather compression stocking. The process of applying
high compressive pressures was based on squeezing the
uid through both the interstitial space and any patent
lymphatic vessels. Asingle-cell nonadjustable intermittent
pneumatic compression device commonly used for prevention of DVT was initially employed for compression treatment of lymphedema. Aprospective acute trial of patients
with upper and lower extremity lymphedema showed that
a multicompartmental compression device rather than a
single-cell device led to a signicant limb girth reduction.
Along-term follow-up study of approximately 50 patients
treated by a program entailing (1) multicompartmental
pneumatic compression, (2) elastic compression stockings
to maintain the post-SEP girth, and (3) daily skin care
showed that in long-term follow-up, 50% maintained a
full response (reduction in limb girth at >3 levels) and 20%
had a partial response (reduction in limb girth ≤3 levels).
1.2.10.4 Surgical approaches
34
33
Surgery for lymphedema in the past has been restricted to
a small proportion of patients with lymphedema, while this
type of surgery traditionally has been divided into physi-
ologic procedures and excisional procedures. The British
surgeon Charles in 1912 developed an excisional procedure for tropical elephantiasis which involved removal of
the skin and subcutaneous tissues down to the deep fascia with split-thickness skin grafts applied to the fascia.
Homans modied this approach in 1936, with staged excisions of the subcutaneous tissue and coverage by well-vascularized aps. The use of liposuction for lymphedema, a
less invasive excisional procedure, termed lipoaspiration,
was rst popularized by Brorson and Svensson in 1998.
They showed in a prospective matched trial that the use of
compression therapy plus liposuction had superior results
to compression alone.
Like excisional procedures, physiologic procedures
for lymphedema have a long history. In 1912 Kondoleon
excised a wedge of deep fascia to encourage supercial-to-deep lymphatic anastomoses. This concept of spontaneous lymphatic-to-lymphatic anastomoses was the basis
for several procedures: the popular Thompson procedure
in 1962, which combined excision of subcutaneous tissue
with xation of the buried posterior dermal ap to the
deep fascia; omental transposition by Goldsmith in 1974;
and Kinmonth and Hurst’s enteromesenteric bridge. Aconceptual breakthrough was achieved when Nielubowicz and
Olszewski performed a direct lymphatic vessel(s)-to-venous anastomosis in four patients with secondary lower
extremity lymphedema and showed persistent limb circumference reduction over a 1- to 9-month follow-up period.
In 1977 O’Brien’s clinical report described their experience, which established the clinical effectiveness of microvascular anastomosis of lymphatic vessels with a diameter
of 0.5–1.0mm to veins with a diameter of 2.0–3.0mm in
human patients.
1.2.10.5 Epilogue
The twenty-rst century would be marked by a shift to
less invasive approaches for interventions on venous and
lymphatic disease with reliance on high-quality evidence
through randomized control prospective trials to prove
their efcacy and safety.
Consensus Statement 1.0 of the American Venous Forum on the historical review of venous and lymphatic disease
https://t.me/med1917
No. Consensus Statement
1.1 “Those who cannot remember the past are condemned to repeat it.”
George Santayana, 1905
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https://t.me/med1917
CHAPTER
2
https://t.me/med1917
Development and anatomy
of the venous system
Peter Gloviczki
Progress in modern imaging studies, such as duplex scanning, computed tomography, and magnetic resonance
imaging, has provided improved insight into our understanding of the development and anatomy of the venous
system.
venography with three-dimensional reconstruction
computer-assisted surgical anatomy mapping (CASAM)
5
anatomic details and enable safer surgical and interventional approaches. Increasing use of minimally invasive
catheter-based therapies has furthermore required a more
thorough knowledge of the venous anatomy to optimize
outcome and minimize thromboembolic complications.
Since the current Terminologia Anatomica
that are frequently different from those used in clinical
practice, a new international anatomic terminology has
been developed to avoid confusion for those clinicians who
treat patients with acute deep vein thrombosis and chronic
venous disease.
consensus documents on the duplex anatomy of the venous
system of the lower limbs.
venous system, followed by a description of the anatomy
of the veins of the lower limb and pelvis. We also discuss
relevant venous anatomy of the trunk and the upper limbs.
The goal is to entice venous specialists around the world
to adopt the new terminology of leg veins to improve the
safety and outcomes of treatments for venous disease and
to permit international collaboration and communication
among scientists who are interested in venous research.
1–3
New techniques like computed tomography
have been helpful to understand and visualize minor
6
suggests terms
7–9
International efforts have also resulted in
10,11
This chapter includes a review of the development of the
4
and
2.1 DEVELOPMENT OF THE VENOUS
SYSTEM
The cardiovascular system is the rst organ system that
develops in the human embryo, and the heart begins to beat
by the end of the third week of embryonic development.
formation of the vascular system is a complex and well-orchestrated process that is essential to the normal growth and
differentiation of all tissues in the human body. Blood vessels are formed through vasculogenesis and angiogenesis.
Vasculogenesis, a process that occurs during embryogenesis,
includes differentiation of primitive mesodermal cells into
2
The
6
endothelial cells. It is driven largely by the signaling protein
vascular endothelial growth factor (VEGF). Angiogenesis is
a process that can occur later in life as well; it includes formation of a capillary network as endothelial cells proliferate,
bud, and migrate to colonize tissues. VEGF is a key regulator of both vasculogenesis and angiogenesis. Recent studies
also shed light on the anatomic and structural similarities
between blood vessels and nerves and identied several
molecules like semaphorins, slits, and netrins that modulate
growth and guide development of both nerves and blood
vessels and play an important role in vascular morphogen-
12
esis.
Primitive vascular channels in the limb rst appear in
the third week of gestation. During development, the vascular system undergoes differentiation through multiple stages,
rst described by Woolard.
stage, with only a capillary network being present. Stage 2
is the retiform stage when large plexiform structures can be
seen. Stage 3, the maturation stage, includes the development of large channels, arteries, and veins.
13
Stage 1 is the undifferentiated
2.1.1 Veins of the trunk
The venous system rst appears in the trunk as bilaterally
symmetrical vessels, with the left vessels regressing and
the right vessels dominating as the superior and inferior
vena cavae. These patterns of development lend themselves
to the anatomic variants found among individuals. In the
4-week-old embryo, three symmetric paired veins develop
and drain into the heart: the umbilical veins, the vitelline
veins, and the cardinal veins. The cardinal veins drain the
body of the embryo. Blood is initially returned to the heart
tube via the paired sinus venosus.
2.1.1.1 Superior vena cava and tributaries
The portion of the body that is cranial to the developing
heart drains through the bilateral anterior cardinal veins,
and the caudal portion of the body drains forward through
the bilateral posterior cardinal veins (Figure2.1). The anterior and posterior cardinal veins join to form the common
cardinal veins, with the right and left common cardinal
veins draining centrally into the sinus venosus. The common cardinal veins also receive the vitelline and umbilical
veins; the vitelline veins later form into the hepatic portal
system.
2
DOI: 10.1201/9781003328971-3
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