The Vascular Injury Legacy

Initial Control of Hemorrhage

Control of hemorrhage following injury has been of prime concern to man since his beginning. Methods for control have included various animal and vegetable tissues, hot irons, boiling pitch, cold instruments, styptics, bandaging, and compression. These methods were described in a historical review by Schwartz in 1958. Celsus was the first to record an accurate account of the use of ligature for hemostasis in CE 25. During the first three centuries, Galen, Heliodorus, Rufus of Ephesus, and Archigenes advocated ligation or compression of a bleeding vessel to control hemorrhage.

Ancient methods of hemostasis used by Egyptians about 1600 BCE are described in the Ebers’ papyrus, discovered by Ebers at Luxor in 1873. Styptics prepared from mineral or vegetable matter were popular, including lead sulfate, antimony, and copper sulfate. Several hundred years later during the Middle Ages in Europe, copper sulfate again became popular and was known as the hemostatic “button.” In ancient India, compression, cold, elevation, and hot oil were used to control hemorrhage, while about 1000 BCE, the Chinese used tight bandaging and styptics.

The writings of Celsus provide most of the knowledge of methods of hemostasis in the first and second centuries CE. When amputation was done for gangrene, the prevailing surgical practice was to amputate at the line of demarcation to prevent hemorrhage. In the first century CE, Archigenes was apparently the first to advocate amputating above the line of demarcation for tumors and gangrene, using ligature of the artery to control hemorrhage.

Rufus of Ephesus (first century CE) noted that an artery would continue to bleed when partially severed, but when completely severed, it would contract and stop bleeding within a short period of time. Galen, the leading physician of Rome in the second century CE, advised placing a finger on the orifice of a bleeding superficial vessel for a period of time to initiate the formation of a thrombus and the cessation of bleeding. He noted, however, that if the vessel were deeper, it was important to determine whether the bleeding was coming from an artery or a vein. If coming from a vein, pressure or a styptic usually sufficed, but ligation with linen was recommended for an arterial injury.

Following the initial contributions of Celsus, Galen, and their contemporaries, the use of ligature was essentially forgotten for almost 1200 years in Western medicine. A tension developed between traditional church teachings and enlightened thought, perhaps holding back any advancement in Western medicine or surgery. Use of the knife on living tissue was considered to be wrong; consequently, amputation was below the line of ischemic demarcation. Abu al-Qasim al-Zahrawi, a prominent Arab physician from Moorish Spain (10th century CE), advocated ligation in his great work Kitab Al-Tasrif almost 600 years before Paré.

Throughout the Middle Ages, cautery was used almost exclusively to control hemorrhage. Jerome of Brunswick (Hieronymus Brunschwig), an Alsatian army surgeon, actually preceded Paré in describing the use of ligatures as the best way to stop hemorrhage. His recommendations were recorded in a textbook published in 1497 and provided a detailed account of the treatment of gunshot wounds. Ambroise Paré, with wide experience in the surgery of trauma, especially on the battlefield, firmly established the use of ligature for control of hemorrhage from open blood vessels. In 1552, he startled the surgical world by amputating a leg above the line of demarcation, repeating the demonstration of Archigenes 1400 years earlier. The vessels were ligated with linen, leaving the ends long. Paré also developed the bec de corbin, ancestor of the modern hemostat, to grasp the vessel before ligating it ( Fig. 1.1 ). Previously, vessels had been grasped with hooks, tenaculums, or the assistant’s fingers. He designed artificial limbs and advanced dressing technique. During the siege of Turin (1536), Paré ran out of oil, which was traditionally used to cauterize. He mixed egg yolk, rose oil, and turpentine and discovered this dressing had better outcomes than oil.

In the 17th century, Harvey’s monumental contribution describing circulation of blood greatly aided the understanding of vascular injuries. Although Rufus of Ephesus apparently discussed arteriovenous communications in the first century CE, it was not until 1757 that William Hunter first described the arteriovenous fistula as a pathological entity. This was despite the fact that, as early as the second century CE, Antyllus had described the physical findings, clinical management (by proximal and distal ligation), and the significance of collateral circulation.

The development of the tourniquet was another advance that played an important role in the control of hemorrhage. Tight bandages had been applied since antiquity, but subsequent development of the tourniquet was slow. Finally, in 1674, a military surgeon named Morel introduced a stick into the bandage and twisted it until arterial flow stopped. The screw tourniquet came into use shortly thereafter. This method of temporary control of hemorrhage encouraged more frequent use of the ligature by providing sufficient time for its application. In 1873, Freidrich von Esmarch, a student of Langenbeck, introduced his elastic tourniquet bandage for first aid use on the battlefield. Previously it was thought that such compression would injure vessels irreversibly. His discovery permitted surgeons to operate electively on extremities in a dry, bloodless field.

Ligation was not without its complications, as British Admiral Horatio Nelson discovered after amputation of his right arm after the attack at Tenerife, “A nerve had been taken up in one of the ligatures at the time of the operation,” causing considerable pain and slowing his recovery. Furthermore, the long ligatures meant delayed wound healing. It was Haire, an assistant surgeon at the Royal Naval Hospital Haslar, who took the risk of cutting sutures short (rather than leaving them long) to allow suppuration, necrosis, and granulation before the suture was pulled away. He observed that “the ligatures sometimes became troublesome and retarded the cure,” and that cutting them short allowed stumps to heal in the course 10 days.

In addition to the control of hemorrhage at the time of injury, the second major area of concern for centuries was the prevention of secondary hemorrhage. Because of its great frequency, styptics, compression, and pressure were used for several centuries after ligation of injured vessels became possible. Undoubtedly, the high rate of secondary hemorrhage after ligation was due to infection of the wound, often promoted by dressing choices or infection spread by well-meaning attendants. Although John Hunter demonstrated the value of proximal ligation for control of a false aneurysm in 1757, failure to control secondary hemorrhage resulted in the use of ligature only for secondary bleeding from the amputation stump. Subsequently, Bell (1801) and Guthrie (1815) performed ligation both proximal and distal to the arterial wound with better results than those previously obtained.

Some of the first clear records of ligation of major arteries were written in the 19th century and are of particular interest. The first successful ligation of the common carotid artery for hemorrhage was performed in 1803 by Fleming, but was not reported until 14 years later by Coley (1817), because Fleming died a short time after the operation was performed. A servant aboard the HMS Tonnant attempted suicide by slashing his throat. When Fleming saw the patient, it appeared that he had exsanguinated. There was no pulse at the wrist and the pupils were dilated. It was possible to ligate two superior thyroid arteries and one internal jugular vein. A laceration of the outer and muscular layers of the carotid artery was noted, as well as a laceration of the trachea between the thyroid and cricoid cartilages. This allowed drainage from the wound to enter the trachea, provoking violent seizures of coughing, although the patient seemed to be improving. Approximately 1 week following the injury, Fleming recorded: “On the evening of the 17th, during a violent paroxysm of coughing, the artery burst, and my poor patient was, in an instant, deluged with blood!”

The dilemma of the surgeon is appreciated by the following statement: “In this dreadful situation I concluded that there was but one step to take, with any prospect of success; mainly, to cut down on, and tie the carotid artery below the wound. I had never heard of such an operation being performed; but conceived that its effects might be less formidable, in this case, than in a person not reduced by hemorrhage.” The wound rapidly healed following ligation of the carotid artery, and the patient recovered.

Ellis (1845) reported the astonishing experience of successful ligation of both carotid arteries in a 21-year-old patient who sustained a gunshot wound of the neck while he was setting a trap in the woods in 1844, near Grand Rapids, Michigan, when he was unfortunately mistaken for a bear by a companion. Approximately 1 week later, Ellis had to ligate the patient’s left carotid artery because of hemorrhage. An appreciation of the surgeon’s problem can be gained by Ellis’ description of the operation: “We placed him on a table, and with the assistance of Dr. Platt and a student, I ligatured the left carotid artery, below the omohyoideus muscle; an operation attended with a good deal of difficulty, owing to the swollen state of the parts, the necessity of keeping up pressure, the bad position of the parts owing to the necessity of keeping the mouth in a certain position to prevent his being strangulated by the blood, and the necessity of operating by candle light.”

There was recurrent hemorrhage on the 11th day after the accident, and right carotid artery pressure helped control the blood loss. It was, therefore, necessary also to ligate the right carotid artery 4½ days after the left carotid artery had been ligated. Ellis remarked: “For convenience, we had him in the sitting posture during the operation; when we tightened the ligature, no disagreeable effects followed; no fainting; no bad feeling about the head; and all the perceptible change was a slight paleness, a cessation of pulsation in both temporal arteries, and of the hemorrhage.” The patient recovered rapidly with good wound healing and returned to normal daily activity. There was no perceptible pulsation in either superficial temporal artery.

The importance of collateral circulation in preserving viability of the limb after ligation was well understood for centuries, as identified by Antyllus nearly 2000 years ago. The fact that time was necessary for establishment of this collateral circulation was recognized. Halsted (1912) reported cure of an iliofemoral aneurysm by application of an aluminum band to the proximal artery without seriously affecting the circulation or function of the lower extremity. Asepsis had been recognized, and the frequency of secondary hemorrhage and gangrene following ligation promptly decreased as an understanding of transmission of infectious disease and its management was developed through Pasteur and Lister. Subsequently, Halsted (1912) demonstrated the role of collateral circulation by gradually, completely occluding the aorta and other large arteries in dogs by means of silver or aluminum bands that were gradually tightened over a period of time.

Early Vascular Surgery

About two centuries after Paré established the use of the ligature, the first direct repair of an injured artery was accomplished. This event more than 250 years ago is credited as the first documented vascular repair. Hallowell, acting on a suggestion by Lambert in 1759, repaired a wound of the brachial artery by placing a pin through the arterial walls and holding the edges in apposition by applying a suture in a figure-of-eight fashion about the pin ( Fig. 1.2 ). This technique (known as the farrier’s stitch) had been utilized by veterinarians but had fallen into disrepute following unsuccessful experiments. Table 1.1 outlines early vascular techniques.

Unfortunately, others could not duplicate Hallowell’s successful experience, almost surely because of the multiple problems of infection and lack of anesthesia. There was one report by Broca (1762) of a successful suture of a longitudinal incision in an artery. However, according to Shumacker (1969), an additional 127 years passed following the Hallowell-Lambert arterial repair before a second instance of arterial repair of an artery by lateral suture in man was reported by Postemski in 1886.

With the combined developments of anesthesia and asepsis, several reports of attempts to repair arteries appeared in the latter part of the 19th century. The work of Jassinowsky, who is credited in 1889 for experimentally proving that arterial wounds could be sutured with preservation of the lumen, was later judged by Murphy in 1897 as the best experimental work published at that time. In 1865, Henry Lee of London attempted repair of arterial lacerations without suture. Glück, in 1883, reported 19 experiments with arterial suture, but all experiments failed because of bleeding from the holes made by the suture needles. He also devised aluminum and ivory clamps to unite longitudinal incisions in a vessel, and it was recorded that the ivory clamps succeeded in one experiment on the femoral artery of a large dog. Von Horoch of Vienna reported six experiments, including one end-to-end union, all of which thrombosed. In 1889, Bruci sutured six longitudinal arteriotomies in dogs; the procedure was successful in four. In 1890, Muscatello successfully sutured a partial transection of the abdominal aorta in a dog. In 1894, Heidenhain closed by catgut suture a 1-cm opening in the axillary artery made accidentally while removing adherent carcinomatous glands. The patient recovered without any circulatory disturbance. In 1883, Israel, in a discussion of a paper by Glück, described closing a laceration in the common iliac artery created during an operation for perityphlitic abscess. The closure was accomplished by five silk sutures. However, from his personal observations, Murphy (1897) did not believe it could be possible to have success in this type of arterial repair. In 1896, Sabanyeff successfully closed small openings in the femoral artery with sutures.

The classic studies of J.B. Murphy of Chicago (1897) contributed greatly to the development of arterial repair and culminated in the first successful end-to-end anastomosis of an artery in 1896. Previously, Murphy had carefully reviewed earlier clinical and experimental studies of arterial repair and had evaluated different techniques extensively in laboratory studies. Murphy attempted to determine experimentally how much artery could be removed and still allow an anastomosis. He found that 1 inch of a calf’s carotid artery could be removed and the ends still approximated by invagination suture technique because of the elasticity of the artery. He concluded that arterial repair could be done with safety when no more than 3/4 inch of an artery had been removed, except in certain locations, such as the popliteal fossa or the axillary space, where the limb could be moved to relieve tension on the repair. He also concluded that when more than half of the artery was destroyed, it was better to perform an end-to-end anastomosis by invagination rather than to attempt repair of the laceration. This repair was done by introducing sutures into the proximal artery, including only the two outer coats, and using three sutures to invaginate the proximal artery into the distal one, reinforcing the closure with an interrupted suture ( Fig. 1.3 ).

In 1896, Murphy was unable to find a similar recorded case involving the suture of an artery after complete division, and he consequently reported his experience (1897) and carried out a number of experiments to determine the feasibility of his procedure. Murphy’s patient was a 29-year-old male shot twice with one bullet entering the femoral triangle. The patient was admitted to Cook County Hospital in Chicago on September 19, 1896, approximately 2 hours after wounding. There was no hemorrhage or increased pulsation noted at the time. Murphy first saw the patient 15 days later, October 4, 1896, and found a large bruit surrounding the site of injury. Distal pulses were barely perceptible. When demonstrating this patient to students 2 days later, a thrill was also detected. An operative repair was decided on. Because of the historical significance, the operation report is quoted:

Operation, October 7, 1896. An incision five inches long was made from Poupart’s ligament along the course of the femoral artery. The artery was readily exposed about one inch above Poupart’s ligament; it was separated from its sheath and a provisional ligature thrown about it but not tied. A careful dissection was then made down along the wall of the vessel to the pulsating clot. The artery was exposed to one inch below the point and a ligature thrown around it but not tied: a careful dissection was made upward to the point of the clot. The artery was then closed above and below with gentle compression clamps and was elevated, at which time there was a profuse hemorrhage from an opening in the vein. A cavity, about the size of a filbert, was found posterior to the artery communicating with its caliber, the aneurysmal pocket. A small aneurysmal sac about the same size was found on the anterior surface of the artery over the point of perforation. The hemorrhage from the vein was very profuse and was controlled by digital compression. It was found that one-eighth of an inch of the arterial wall on the outer side of the opening remained, and on the inner side of the perforation only a band of one-sixteenth of an inch of adventitia was intact. The bullet had passed through the center of the artery, carried away all of its wall except the strands described above, and passed downward and backward making a large hole in the vein in its posterior and external side just above the junction of the vena profunda. Great difficulty was experienced in controlling the hemorrhage from the vein. After dissecting the vein above and below the point of laceration and placing a temporary ligature on the vena profunda, the hemorrhage was controlled so that the vein could be sutured. At the point of suture the vein was greatly diminished in size, but when the clamps were removed it dilated about one-third the normal diameter or one-third the diameter of the vein above and below. There was no bleeding from the vein when the clamps were removed. Our attention was then turned to the artery. Two inches of it had been exposed and freed from all surroundings. The opening in the artery was three-eighths of an inch in length; one-half inch was resected and the proximal was invaginated into the distal for one-third of an inch with four double needle threads which penetrated all of the walls of the artery. The adventitia was peeled off the invaginated portion for a distance of one-third of an inch: a row of sutures was placed around the edge of the overlapping distal end, the sutures penetrating only the media of the proximal portion; the adventitia was then brought over the end of the union and sutured. The clamps were removed. Not a drop of blood escaped at the line of suture. Pulsation was immediately restored in the artery below the line of approximation and it could be felt feebly in the posterior tibial and dorsalis pedis pulses. The sheath and connective tissue around the artery were then approximated at the position of the suture with catgut, so as to support the wall of the artery. The whole cavity was washed out with a five percent solution of carbolic acid and the edges of the wound were accurately approximated with silk worm-gut sutures. No drainage. The time of the operation was approximately two and one-half hours, most of the time being consumed in suturing the vein. The artery was easily secured and sutured, and the hemorrhage from it readily controlled. The patient was placed in bed with the leg elevated and wrapped in cotton.

The anatomic location of the injuries, the gross pathology involved, and the detailed repair contributed to Murphy’s historically successful arterial anastomosis. Murphy mentioned that a pulsation could be felt in the dorsalis pedis artery 4 days following the operation. The patient had no edema and no disturbance of his circulation during the reported 3 months of observation.

Subsequently, Murphy (1897) reviewed the results of ligature of large arteries before the turn of the century. He found that the abdominal aorta had been ligated 10 times, with only 1 patient surviving for 10 days. Lidell reported only 16 recoveries after ligation of the common iliac artery 68 times, a mortality of 77%. Balance and Edmunds reported a 40% mortality following ligation of a femoral artery aneurysm in 31 patients. Billroth reported secondary hemorrhage from 50% of large arteries ligated in continuity. Wyeth collected 106 cases of carotid artery aneurysms treated by proximal ligation, with a mortality rate of 35%.

In 1897, Murphy summarized techniques he considered necessary for arterial suture. They bore a close resemblance to principles generally followed today:

• 1.

  Complete asepsis

• 2.

  Exposure of the vessel with as little injury as possible

• 3.

  Temporary suppression of the blood current

• 4.

  Control of the vessel while applying the suture

• 5.

  Accurate approximation of the walls

• 6.

  Perfect hemostasis by pressure after the clamps are taken off

• 7.

  Toilet of the wound

Murphy also reported that Billroth, Schede, Braun, Schmidt, and others had successfully sutured wounds in veins. He personally had used five silk sutures to close an opening 3/8-inch long in the common jugular vein.

Several significant accomplishments occurred in vascular surgery within the next few years. In 1903, Matas described his endoaneurysmorrhaphy technique, which remained the standard technique for aneurysms for over 40 years. In 1906, Carrel and Guthrie performed classic experimental studies over a period of time with many significant results. These included direct suture repair of arteries, vein transplantation, and transplantation of blood vessels as well as organs and limbs. In 1912, Guthrie independently published his continuing work on vascular surgery. Following Murphy’s successful case in 1896, the next successful repair of an arterial defect came 10 years later when Goyanes used a vein graft to bridge an arterial defect in 1906. Working in Madrid, Goyanes excised a popliteal artery aneurysm and used the accompanying popliteal vein to restore continuity ( Fig. 1.4 ). He used the suture technique developed by Carrel and Guthrie of triangulating the arterial orifice with three sutures, followed by continuous suture between each of the three areas. A year later in 1907, Lexer in Germany first used the saphenous vein as an arterial substitute to restore continuity after excision of an aneurysm of the axillary artery. In his 1969 review, Shumacker commented that within the first few years of the 20th century, the triangulation stitch of Carrel (1902), the quadrangulation method of Frouin (1908), and the Mourin modification (1914) had been developed.

By 1910, Stich had reported more than 100 cases of arterial reconstruction by lateral suture. His review included 46 repairs, either by end-to-end anastomosis or by insertion of a vein graft. With this promising start, it is curious that over 30 years elapsed before vascular surgery was widely employed. A high failure rate, usually by thrombosis, attended early attempts at repair, and few surgeons were convinced that repair of an artery was worthwhile. In 1913, Matas stated that vascular injuries, particularly arteriovenous aneurysms, had become conspicuous features of modern military surgery, and he felt that this class of injury must command the closest attention of the modern military surgeon: “A most timely and valuable contribution to the surgery of blood vessels resulted from wounds in war. Unusual opportunities for the observation of vascular wounds inflicted with modern military weapons … based on material fresh from the field of action, and fully confirmed the belief that this last war, waged in close proximity to well-equipped surgical centers, would also offer an unusual opportunity for the study of the most advanced methods of treating injuries of blood vessels.”

Matas described Soubbotitch’s experience of Serbian military surgery during the Serbo-Turkish and Serbo-Bulgarian Wars at the 1913 London International Congress. He reported that 77 false aneurysms and arteriovenous fistulas were treated. There were 45 ligations, but 32 vessels were repaired, including 19 arteriorrhaphies, 13 venorrhaphies, and 15 end-to-end anastomoses (11 arteries and 4 veins). It is impressive that infection and secondary hemorrhage were avoided. In 1915, Matas, in discussing Soubbotitch’s report, emphasized that a notable feature was the suture (circular and lateral repair) of blood vessels, and the fact that it had been utilized more frequently in the Balkan conflict than in previous wars. He also noted that, judging by Soubbotitch’s statistics, the success obtained by surgeons in the Serbian Army Hospital in Belgrade far surpassed those obtained by other military surgeons in previous wars, with the exception perhaps of the remarkably favorable results in the Japanese Reserve Hospitals reported by Kikuzi.

World War I Experience

During the early part of WWI, with the new techniques of vascular surgery well established, the German surgeons attempted repair of acutely injured arteries and were successful in more than 100 cases. During the first 9 months of WWI, low-velocity missiles caused arterial trauma of a limited extent. In 1915, however, the widespread use of high explosives and high-velocity bullets, combined with mass casualties and slow evacuation of the wounded, made arterial repair impractical.

In 1920, Bernheim went to France with the specific intent of repairing arterial injuries. Despite extensive prior experience and equipment, however, he concluded that attempts at vascular repair were unwise. He wrote: “Opportunities for carrying out the more modern procedures for repair or reconstruction of damaged blood vessels were conspicuous by their absence during the recent military activities. Not that blood vessels were immune from injury; not that gaping arteries and veins and vicariously united vessels did not cry out for relief by fine suture or anastomosis. They did, most eloquently, and in great numbers, but he would have been a foolhardy man who would have essayed sutures of arterial or venous trunks in the presence of such infections as were the rule in practically all of the battle wounded.”

The great frequency of infection with secondary hemorrhage virtually precluded arterial repair. In addition, there were inadequate statistics about the frequency of gangrene following ligation, and initial reports subsequently proved to be unduly optimistic. In 1927, Poole, in the United States Army Medical Department History of WWI, remarked that if gangrene were a danger following arterial ligation, primary suture should be performed, and the patient should be watched very carefully.

Despite the discouragement of managing acute arterial injuries in WWI, fairly frequent repairs of false aneurysms and arteriovenous fistulas were carried out by many surgeons. These cases were treated after the acute period of injury, when collateral circulation had developed with the passage of time and assured viability of extremities. In 1921, Matas recorded that the majority of these repairs consisted of arteriorrhaphy by lateral or circular suture, with excision of the sac or endoaneurysmorrhaphy.

In 1919, Makins, who served in WWI as a British surgeon, recommended ligating the concomitant vein when it was necessary to ligate a major artery. He thought that this reduced the frequency of gangrene by retaining within the limb for a longer period the small amount of blood supplied by the collateral circulation. This hypothesis was debated for more than 20 years before it was finally abandoned.

Payr in 1900, Carrel, and the French surgeon Tuffier described temporary arterial anastomoses with silver and glass tubes that were inserted with some success by Makins and other WWI military surgeons, but patency was limited to 4 days, merely allowing some collateral development.