Alexis Carrel and the origins of veterinary vascular surgery
MeSH keywords:dog, cat, historical article, vascular surgical procedures
Human surgeons performed the earliest repair of vascular incisions experimenting in animals 250 years ago. New methods and instruments were devised resulting in the development and improvement of peripheral vascular surgery, vascular grafts and organ transplantation. Alexis Carrel performed the first successful vascular anastomosis and organ transplantation in humans and animals by early 1900. Veterinary surgeons applied these principles in dogs and cats not until the middle of twentieth century performing ligations, aortic embolectomies, renal transplants and portosystemic shunt attenuations.
The very first vascular surgeries in animals were performed not by veterinarians but human surgeons who experimented in dogs and cats and other animal species for many decades; new techniques and instrumentation were devised, and these experiments led to the development and improvement of peripheral vascular surgery, vascular grafts and organ transplantation in humans (Watts 1907, Cusimano et al. 1984, Friedman 2005). Veterinary surgeons started to apply these principles in dogs and cats not until the middle of twentieth century.
Early repair of vascular incisions
Permanent vascular interruption by ligature application was the oldest vascular technique used by human surgeons to control haemorrhage, but with devastating results, as they led to ischemic necrosis of the limbs. Repair of a vascular laceration or incision by placing sutures was the primary goal of surgeons. Haemorrhage and thrombosis were the major issues that surgeons had to overcome for a successful outcome (Watts 1907, Friedman 2005).
In 1772, Assman attempted to close arteriotomies in femoral arteries of dogs but immediate thrombus formation in most of the dogs made him abandon these experiments and regarded these methods as not applicable and dangerous (Watts 1907, Friedman 2005). Assman’s findings were widely accepted by the surgical community and a vascular repair crisis, that lasted for a century, began. In 1833, Gensoul performed for the first time venous closures in horses but failure associated with thrombosis occurred (Friedman 2005). Further attempts were not made until 1881, when Gluck sutured incisions in iliac arteries of dogs and aortas in rabbits by the aid of ivory clamps and succeeded in partial repair of the arterial wounds (Watts 1907). In 1889, Jassinowsky experimented in large dogs, horses and calves and successfully repaired longitudinal and transverse incisions on carotids with preservation of the vessel lumen (Watts 1907). In 1890, Burci repeated Jassinowsky’s experiments by suturing arteries in dogs and horses using a continuous suture pattern and reported favourable results in four out of six experiments (Watts 1907). In 1897, Murphy did numerous experiments for closure of arterial incisions in dogs and sheep with promising results (Watts 1907). Silberberg experimented in arterial sutures in dogs in 1897-1898, emphasizing the importance of strict asepsis for a successful result (Watts 1907). In 1899, Dorfler reported his successful results on arterial suturing and Jakobsthal confirmed histologically arterial wound healing from samples obtained in these experiments (Watts 1907).
Animal experimentation documented a successful outcome in arteriotomy or venotomy closure based on the aseptic technique, tension free closure in clean cut wound edges, careful surgical technique using fine sutures that penetrated the vessel wall full thickness in a continuous suture pattern. In case of haemorrhage through the incision line slight pressure with fingers resulted in control (Watts 1907, Friedman 2005).
Vascular anastomosis era
Alexis Carrel was considered the father of vascular anastomosis and transplantation in both animals and humans (Cusimano et al. 1984, Friedman 2005, Sade 2005, Dutkowski et al. 2008, Rotwell 2011, Merchani & Tan 2013). Carrel was a French surgeon that developed a strong interest in vascular surgery, while living in France, following the assassination of French president Sadi Carnot in 1894 due to portal vein trauma (Cusimano et al. 1984, Rotwell 2011). Carell was taught the skills of anastomosis by Madame Leroidier, an embroider in Lyon (Cusimano et al. 1984, Dutkowski et al. 2008, Rotwell 2011). He learnt sewing techniques by using fine straight needles and monofilament threads and practiced these techniques on paper many times before he performed vascular anastomosis in dogs and cats in the University of Lyon (Cusimano et al. 1984, Dutkowski et al. 2008, Rotwell 2011, Merchani & Tan 2013). Carrel soon realized that in order to achieve a successful anastomosis he had to address haemorrhage of the vessels, vascular stenosis and thrombosis. Working for many hours in the surgical laboratory, he used straight needles instead of curved and fine silk moistened with Ringer’s solution and coated in petroleum jelly to decrease friction and eliminate needle holes created through the vessel wall (Cusimano et al. 1984, Dutkowski et al. 2008, Rotwell 2011, Merchani & Tan 2013). He sutured the vessels in a continuous pattern by everting the vascular edges to make direct contact of tunica intima in the incision line, thus preventing clot formation (Cusimano et al. 1984, Rotwell 2011). He devised the triangulation technique by placing three stay sutures at equal points at the edges of the two vessels to be anastomosed (Carrel 1963, Cusimano et al. 1984, Rotwell 2011). By doing so, he achieved easier and rapid suturing along a straight line in a continuous suture pattern. By keeping the vessel wall under tension, stenosis at the incision line was prevented (Figure 1). Carrel practiced end-to-end, end-to-side or side-to-side anastomoses in dogs and cats (Carrel 1963, Cusimano et al. 1984, Rotwell 2011). He published his first paper on vascular anastomosis in 1902 (Carrel 1963). Soon after, he moved to Chicago where he worked with Charles Guthrie (Cusimano et al. 1984, Dutkowski et al. 2008, Rotwell 2011, Merchani & Tan 2013). In the USA, Carrel improved his vascular anastomosis technique and performed renal transplants in dogs and cats (Cusimano et al. 1984, Sade 2005, Dutkowski et al. 2008, Rotwell 2011, Merchani & Tan 2013). His fruitful collaboration with Guthrie resulted in more than 20 publications. In 1912, Carrel was awarded the Nobel Prize in medicine in recognition of his work in vascular anastomosis and organ transplantation (Cusimano et al. 1984, Dutkowski et al. 2008, Rotwell 2011, Merchani & Tan 2013). In his Nobel Prize speech that was delivered in December 11, 1912, he established the principles for a successful vascular anastomosis, emphasizing on aseptic surgical technique, gentle vascular tissue handling with hands or fine forceps, vascular wall irrigation with Ringer’s solution to prevent desiccation and remove blood clots or debris and minimize thrombosis, and using sutures coated in petroleum jelly to prevent direct contact of wounded tissue and foreign material with blood (Carrel 1912).
Veterinary vascular surgery
The advent of veterinary vascular surgery was traced in the middle of the 20th century. Before that, surgical techniques for vascular reconstruction were not used in veterinary medicine. This is because the size of the vessels was small to allow for vascular repair in case of injury and vascular interruption by ligation was performed instead (Butler 1975). The development of collateral circulation aided in the maintenance of adequate blood supply to most parts of the animal body (Butler 1975). Vascular interruption is the most common form of vascular surgery in veterinary medicine. Vascular ligation is commonly performed in animals during ovariohysterectomy, castration, splenectomy or limb amputations. In 1952, the first ligation of patent ductus arteriosus, a congenital cardiac malformation that connects the aorta to the pulmonary artery, was performed in a dog (Walters & Bramer 1952). Surgical ligation is the treatment of choice for vascular ring anomalies; these are congenital malformations of the aortic arch causing stricture of the oesophagus by the ligamentun arteriosum, trachea and great vessels. The earliest ligation of the right aortic arch with a left ligamentum arteriosum in dogs, the most common vascular ring anomaly, was reported in 1955 (Detweiler & Allam 1955). Temporary arterial occlusion was attempted to decrease blood loss and improve visualization and surgical exploration of nasal cavity in dogs with nasal disease (Hedlund et al. 1983).
Arteriotomies for the removal of emboli were performed in cats with aortic thromboembolism in the early sixties (Bardens & Walker 1962, Buckanan et al. 1966, Lucke & Sumner-Smith 1966, Palumbo & Hubbard 1966). Fogarty embolectomy catheter was also used for the management of these emboli; the catheter was placed through an aortic incision to remove emboli from the aorta and femoral artery in a cat (Figure 2) (Baker & Birk 1974, Crowe 1983). However, these embolectomy techniques were soon abandoned as they met with disappointing results and were replaced with thrombolytic therapy. Fogarty embolectomy manoeuvre has also been used in a dog with aortic thrombosis, but this method needs to be further investigated both for the technique and for the postoperative management of such cases in small animals (Schwede 2018).
Portosystemic vascular anomalies diverting venous blood from the liver to systemic circulation and located extrahepatically or intrahepatically was another challenge for the veterinary surgeon. Strombeck et al. (1977) and Breznock (1979) performed the first attenuation by partial ligation or complete ligation of portosystemic shunts in dogs. Intravascular repair of intrahepatic shunts, a more demanding and technically more difficult procedure, was originally performed by Breznock et al. (1983). Intravascular repair required a venotomy incision through the caudal vena cava and placement of several mattress sutures to attenuate or occlude the shunting vessel was also described. Intrahepatic and extrahepatic shunts can also be attenuated with endovascular procedures (percutaneous coil embolization) (Culp et al. 2018, Weisse et al. 2014).
Surgical removal of canine heartworms by pulmonary arteriotomy was first performed by Roenigk (1956) and evaluated by Horne (1962). Heartworm caval syndrome in dogs was originally addressed by Jackson et al. (1977). This syndrome is associated with massive presence of Dirofilaria immitis worms within the cranial vena cava and right atrium. The authors removed the worms through a right jugular venotomy using long alligator forceps (Jackson et al. 1977). Transvenous cardiac pacing was initially employed in a dog through jugular vein penetration (Darke et al. 1985).
In 1952, the first synthetic aortic prosthesis was experimentally attempted in a dog (Voorhees et al. 1952). Synthetic prostheses were placed successfully in cats and a dog for bypassing part of an occluded subclavian artery (Frye 1967, MacCoy & Trotter 1977). However, indications for vascular prostheses are limited in clinical veterinary surgery; autologous grafts replaced synthetic grafts, using the jugular vein in oncologic and congenital cardiac disease (Holsworth et al. 2004, Pelosi et al. 2006).
Alexis Carrel reported the first successful renal transplantation in dogs in the USA in 1905 (Sade 2005, Merchani & Tan 2013). Carrel developed end-to-end and end-to-side vascular anastomoses currently used in renal transplantation in cats (Carrel 1963, Sade 2005). The first successful renal transplant was performed in a cat in the University of California, Davis in 1984 (Gregory et al. 1990, Gregory 1993). In cats, end-to-side anastomosis of the renal vein to the iliac vein was performed to accommodate the smaller size of the renal vein to the larger iliac vein. Renal artery was anastomosed end-to-end with iliac artery as both vessels are of similar diameter (Gregory et al. 1992, Gregory 1993). Carrel also created the patch technique, first used in humans, for renal transplantation; a patch of aorta along with the renal artery were harvested from the donor and transplanted to avoid the risk of thrombosis (Figure 3) (Sade 2005). Carrel’s patch technique was recently described in feline renal transplantation (Budgeon et al. 2017). Renal transplants in cats are currently considered an acceptable treatment for end-stage kidney disease (Mathews & Gregory 1997).
Veterinary vascular surgery owes its development to experimental vascular surgery performed by pioneers in human surgery. These experimental procedures allowed veterinary surgery to flourish and advances in this particular field led to the development of the era of endovascular surgery in dogs and cats.
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