European Journal of Orthopaedic & Traumatology (2019) 29:247–254 https://doi.org/10.1007/s00590-019-02378-7

GENERAL REVIEW • GENERAL ORTHOPAEDICS -

The history of microsurgery

Andreas F. Mavrogenis1 · Konstantinos Markatos2 · Theodosis Saranteas3 · Ioannis Ignatiadis4 · Sarantis Spyridonos4 · Marko Bumbasirevic5 · Alexandru Valentin Georgescu6 · Alexandros Beris7 · Panayotis N. Soucacos1

Received: 2 January 2019 / Accepted: 4 January 2019 / Published online: 10 January 2019 © Springer-Verlag France SAS, part of Springer Nature 2019

Abstract Microsurgery is a term used to describe the surgical techniques that require an operating microscope and the necessary spe- cialized instrumentation, the three “Ms” of Microsurgery (microscope, microinstruments and microsutures). Over the years, the crucial factor that transformed the notion of microsurgery itself was the anastomosis of successively smaller blood vessels and nerves that have allowed transfer of tissue from one part of the body to another and re-attachment of severed parts. Cur- rently, with obtained experience, microsurgical techniques are used by several surgical specialties such as , , orthopaedics, gynecology, otolaryngology, , oral and maxillofacial surgery, and more. This article highlights the most important innovations and milestones in the history of microsurgery through the ages that allowed the inauguration and establishment of microsurgical techniques in the feld of surgery.

Keywords Microsurgery · Orthopaedics · Plastics

Introduction Over the years, the crucial factor that transformed the notion of microsurgery itself was the anastomosis of successively Microsurgery is a term used to describe the surgical tech- smaller blood vessels and nerves (typically 1 mm in diam- niques that require an operating microscope and the neces- eter) that have allowed transfer of tissue from one part of sary specialized instrumentation (the three “Ms” of Micro- the body to another and re-attachment of severed parts. Cur- surgery: microscope, microinstruments and microsutures). rently, with obtained experience, microsurgical techniques are used by several surgical specialties such as general sur- * Andreas F. Mavrogenis gery, ophthalmology, orthopaedics, gynecology, otolaryn- [email protected] gology, neurosurgery, oral and maxillofacial surgery, plastic surgery and more [1, 2]. 1 First Department of Orthopaedics, National This article aims to highlight the most important innova- and Kapodistrian University of Athens, School of , 41 Ventouri Street, 15562 Holargos, Athens, Greece tions and milestones in the history of microsurgery through the ages that allowed the inauguration and establishment of 2 Biomedical Research Foundation of the Academy of Athens, Athens, Greece microsurgical techniques in the feld of surgery. 3 Second Department of Anesthesiology, First Department of Orthopaedics, National and Kapodistrian University of Athens, School of Medicine, Athens, Greece Organs transplantation and revascularization 4 Department of Upper Extremity Surgery, and Microsurgery, KAT Hospital, Athens, Greece 5 Orthopaedic and Traumatology University Clinic, The idea of organs transplantation and vascular (arterial) Clinical Center of Serbia, School of Medicine, University repair originates in the mythology and early writings of of Belgrade, Belgrade, Serbia Antiquity [3, 4]. In Greek mythology, there are numerous 6 Clinical Hospital of Rehabilitation, University of Medicine examples of chimeric gods, heroes and beasts with organs Iuliu Hatieganu, Cluj Napoca, Cluj, Romania of diferent species. The word “chimeric” refers to chimera 7 Department of Orthopaedics, University of Ioannina, School (Fig. 1), a mythological creature usually depicted as a lion of Medicine, Ioannina, Greece

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description of a suture and the suture materials used is attributed to the Indian in 500 BC [3]. The initial technique for the treatment of arterial injuries or diseases was described by and his successors in Greek antiquity [5–7]. According to them, a destroyed small was condemned during surgery; therefore, these physi- cians developed techniques and sutures for ligation of vessels to stop . Such primitive sutures were described in the ffth century BC by Hippocrates and later in the Roman era by . In the second century AD, described the use of gut absorbable suture; his techniques were followed by others including Oribasius and Paul of Aegina in the early Middle Ages. Subsequently, in the Arabic world, Abulcasis developed the catgut suture with a surgical needle Fig. 1 Statue depicting the mythological Chimera of Arezzo (Etrus- for wound repair and vessels ligation. In the fourteenth–ff- can, ffth century BC; Archeological Museum of Florence, Italy) teenth century, the barber surgeons of the era neglected liga- ture and started using cautery to prevent bleeding during with the head of a goat arising from its back and a snake traumatic in wars. In that era, the Italian barber instead of a tail. Chimera was thought to live in Lycia, surgeon Gasparo Tagliacozzi performed successful skin auto- nowadays Turkey, and its sight was an omen of disaster. It graft transplantations, but his techniques failed when he used was fnally killed by Bellerophon with the help of Pegasus, allografts because of tissue rejection and necrosis [3]. another chimeric creature with the body of a horse and During the in the sixteenth century, the work wings of an eagle. Satyrs, sirens and others are examples of Ambroise Paré (1510–1590) was remarkable [5–7]. He is of mythological creatures, which were human-like but had often considered the father of modern surgery due to his suc- body parts from other species [4]. cess in treating war injuries, developing surgical techniques In the New Testament, Jesus restored the of a servant and avoiding cauterization and amputations in favor of the that had been cut by the sword of Saint Peter. Additionally, use of ligatures to stop massive bleeding. He was the frst to according to the Christian tradition, Saint Peter reimplanted describe a technique for the anastomosis of an injured artery the breasts of Saint Agatha that were pulled of during tor- through the use of ligature and he even described his own ture, and Saint Marc reimplanted a soldier’s hand that was version of a tourniquet to reduce bleeding of a limb during amputated in a battle [3]. an operation. Nevertheless, the outcomes of his techniques Historic accounts of transplantation are legendary without were not optimal because the tourniquet had to be held in the necessary technical and scientifc background to support place by an assistant, usually hard to be found in a battle- them. In ancient China, Pien Chi’ao reportedly exchanged feld, the lack of prolonged required for the repair hearts between a man of strong spirit but physically weak of an artery and the primitive antisepsis techniques of his and another man with weak spirit but physically strong in an era. He often fnally rejected the eforts to save a damaged attempt to achieve balance in each man [3]. Roman Catholic artery in an injured limb, and he ended developing amputa- accounts report the third century Saints– Damian tion techniques with the use of extended ligature sutures to and Cosmas as replacing the gangrenous leg of the Roman control bleeding and save the lives of injured soldiers with deacon Justinian with the leg of a recently deceased Ethio- major limb trauma [5–7]. pian. Similarly, in the second century BC the Indian surgeon Early notable microsurgical attempts are documented in Sushruta used skin autografts for reconstruction of the nose 1759 by Hallowell who repaired a wound in the brachial and with uncertain results [3]. artery by hand suture. In 1802, Jones studied the healing process in vascular injuries in animals and stressed the importance of the neointima that was regenerated at the suture site [3]. Revascularization techniques before the advent of microsurgery The advent of microsurgery Since the beginning of recorded history, various suture mate- rials have been used [3, 5–7]. The earliest reports of surgical A few notable developments in the and sutures date in 3000 BC in ; the oldest known surgery paved the application of microsurgical techniques. In suture is found in a mummy from 1100 BC. A detailed 1718, Jean Louis Petit (1674–1750), with the assistance and

1 3 European Journal of Orthopaedic Surgery & Traumatology (2019) 29:247–254 249 constructive genius of the mechanic Peron, developed a tour- niquet that did not compress the region through which large and were passing, and it could be defated as necessary. The apparatus used a screw for compression of the limb, compression was better localized, once applied it could be held frm in place without the help of an assistant, and it could also be left in place if secondary bleeding was feared. This tourniquet allowed the application of complex surgical techniques without the fear of hemorrhagic shock from massive bleeding [8]. The Dominican monks Salvino D’Amato of Florence and Alessandro della Spina of Pisa are often accredited with the invention of the spectacles at the end of the thirteenth cen- tury [9] and subsequently used extensively since the four- teenth century. Others refned the construction of optical lenses; Hans Lippershey, Hans Janssen and his son Zacharias Janssen of Middelburg were the most famous spectacle mak- ers of the late sixteenth century. Antonie van Leeuwenhoek (1632–1723), a Dutch merchant, invented in the 1670s the single-lens microscope and made possible the direct inspec- tion of muscle fbers, nerves and arteries. Carl Zeiss (Fig. 2) and Ernst Abbe perfected and made available in the level of mass production the compound microscope in the late nineteenth century and thus provided the necessary opti- cal equipment for direct visualization of small arteries and Fig. 2 Carl Zeiss (1816–1888) perfected the compound microscope nerves [9]. (Felix Auerbach’s book Das Zeisswerk und die Carl Zeiss Stiftung in Jena, 1907) The advent of the optical binocular loupes was also a milestone in the advent of microsurgery. Charles Louis Chevalier (1804–1859) constructed a magnifcation loupe clinical practice for all surgical staf members, and Charles in 1840s. In 1876, Edwin Theodore Saemisch developed Chamberland invented the steam sterilizer, known as the the frst simple loupe for surgical use. Carl Wilhelm Von autoclave in 1881; the autoclave was used to clean surgical Zehender used a new compound binocular device in 1886, tools and kill bacteria by heated water to 140 degrees Cel- and Westien added a light source on a headband [9]. sius for approximately 20 min [1, 2, 5]. These innovations At the same time the advent of anesthesia made feasible provided for the advent of microsurgical techniques in the to extend the surgical time, and sterilization and antimicro- twentieth century [1, 2]. bial methods provided for reduced risks in com- plex and major operations. In 1842, the American physician removed two tumors from a patient with the Microsurgery in the twentieth century use of for a painless operation, and in 1846 Morton and Warren used ether through inhalation to induce The beginning of the twentieth century brought several perioperative anesthesia in the Massachusetts General Hos- achievements that initiated the revolution of microsurgery. pital. The use of , followed by oth- In 1902, Alexis Carrel (Fig. 3) frst performed the vascu- ers shortly after and the administration through an inhalation lar end-to-end anastomosis with a 3-stay suture technique, machine was eventually implemented [1, 2, 5]. The problem which remains a fundamental technique of vascular surgery of infection started to solve with the introduction of anti- up to now. Goyanes in 1906 and Lexer in 1907 performed sepsis by in 1867. Based on the contemporary autogenous grafting, and Guthrie in 1912 described the work of (1822–1895 AD) on the microbial replantation of amputated limbs in dogs. Later, Carrel and theory of infection and the success of Guthrie performed organ transplantations (heart, kidney and (1818–1865 AD) on the treatment of gynecological infec- ovary) in the laboratory. Carrel was awarded a Nobel Prize tions, he used in elective surgery soaking of the patient’s for medicine and for his surgical technique in the skin, his hands, instruments and dressings, and spraying anastomosis of arteries in 1912 [1, 2]. the air around with . Subsequently, Gustav The application of the surgical microscope appeared in Adolf Neuber of Kiel implemented sterilization rules in his 1921 in the University of Stockholm; Carl-Olof Siggesson

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manufactured a microscope equipped with coaxial illu- mination for use as a colposcope or otoscope; this is still used today. In 1953, Harms in Tubingen and Barraquer in Buenos Aires used the microscope for eye surgery. Jacob- son and Donaghy in Vermont worked together to apply the operating microscope to intracranial microvascular surgery such as thromboendarterectomy and surgery. Yasargil from Zurich joined the Donaghy group to learn the basic techniques of microneurovascular surgery [10]. In 1958 in Japan, a historic and challenging replantation of an amputated extremity was done by Onji and Tamai; this inaugurated the microsurgical reimplantation of an injured limb. In 1959, Walz was the frst to use of the operating microscope in fallopian tube surgery. In 1962, Malt and McKhann in Boston, successfully performed the Fig. 3 Alexis Carrel (1873–1944) performed the frst end-to-end vas- cular anastomosis (US Library of Congress’s Prints and Photographs world’s frst replantation in a 12-year-old boy with division) a mangled arm by a train accident. In 1964, Ito in Japan reported the funicular suture of the peripheral nerve. In 1963, the hand surgeons Harold Kleinert and Mort Kas- dan performed the frst revascularization of a partial digit [3, 10]. Revascularization of a nonviable amputation of the and index fnger of a 3-year-old girl was successful performed in 1972 at Duke University [11]. One of the frst thumb replantations of a completely amputated thumb in the USA took place in 1973 at Duke University Medical Center with Urbaniak and Soucacos who successfully reattached the thumb of a 16-year-old male whose thumb was completely severed in a water skiing accident when thumb was retrieved after being submerged for 4 h under water [11]. In 1965, Lougheed performed a thrombectomy of the internal carotid artery, and Pool, Rand and Jannetta reported the use of micro- techniques for intracranial aneurysm surgery [10]. In 1967, Donaghy and Yasargi succeeded a bypass operation for an embolism of the middle cerebral artery by means of a superfcial temporal artery to middle cerebral artery anastomosis. The hallux-to-thumb transfer by Cobbed in East Grinstead was performed in April of 1968. In 1972 at the Tokyo Metropolitan Hospital, Harii and Ohmori Jr. began microvascular surgery and successfully performed a temporal free fap transfer; this was the frst free skin fap transfer ever performed. In 1974, Taylor and his colleagues Fig. 4 Carl-Olof Nylén (1892–1978), the father of microsurgery performed vascularized fbula grafts to the tibia [3, 10]. (Stockholm, Sweden: Biografskt Galleri A–B; 1939) Other technological innovations of the era that facili- tated and expanded even more the feld on which microsur- Nylén (1892–1978) (Fig. 4), the father of microsurgery, gical techniques could be applied were the use of vascular built the frst surgical microscope. At frst he used it for clips and microclips, vascular stents, laser and artifcial operations in animals, and later he used it to operate on vascular allografts [12]. In the last 40 years, many institu- a patient with chronic otitis who had a labyrinthine fs- tions around the world absorbed and incorporated the new tula. Nylen’s microscope was soon replaced by a binocular techniques in their educational curricula ofering fellow- microscope, developed by his colleague Gunnar Holmgren ships and making microsurgical techniques wide spread. in 1922 [1, 10]. In 1951, Littmann of the Carl Zeiss Co.

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Tissue engineering and regenerative blockade and regional anesthesia techniques is the prem- medicine ise that a sensory block is achieved by interrupting the function of nerve fbers along the nerve’s pathway through In 1975, the frst in vitro cultivation of keratinocytes by certain pharmacological interventions, such as the injec- Rheinwald and Green was achieved, followed by cultured tion of local anesthetic close to the targeted nerves. First, autologous epithelium in 1979. In 1981, Bell developed Plato and Aristotle considered that , like pleasure, is the composite living skin equivalent, and in 1982, Yannas an emotion expressed by the human soul and not one of developed the collagen–glycosaminoglycans (GAG)-based the senses. However, in seventeenth century, Descartes dermal matrix. In 1988, cell transplantation in synthetic developed the concept of the biologic function of pain biodegradable polymers was achieved, and in 1994, Britt- and the neural connections from the periphery to the cen- berg used the chondrocyte culture and transplantation [13]. tral nervous system and brain [18, 19]. Pressure on nerves These advents provided a background for the booming of to produce local anesthesia may well be of Egyptian or microsurgery and tissue transplantation in the modern era. ancient-Greek origin, which in fact was the frst regional Currently, novel advents are changing the of micro- anesthesia technique for surgical interventions [18, 19]. surgery. Tissue engineering with living cells, biocompat- After Ambroise Paré gave a good description of the use ible materials and suitable biochemical (growth factors) of compression for amputations [18, 19], in 1784, Moore, and physical (cyclic mechanical loading) factors promises a young English surgeon, tried to improve the previously to create tissue-like structures to fll gaps of destroyed tis- described compression method; he reported that complete sues after trauma. insensibility and loss of power of the whole leg could Another signifcant advent was the establishment of occur after half-an- hour compression to the sciatic nerve regenerative medicine. The term was frst used by Leland [20]. The term regional anesthesia was frst introduced by Kaiser to describe the use of stem cells and their ability to the American neurosurgeon Cushing in 1901 after describ- diferentiate into any tissue in order to replace damaged ing pain relief by the use of peripheral nerve block. The tissue in patients with chronic diseases [14]. From 1995 great pioneer, however, of modern regional anesthesia was to 1998, a team led by Michael West achieved the frst Labat, a French physician who described the essence and isolation of human embryonic stem and human embry- best practice of successful peripheral nerve blocks [21, onic germ cells [14]. In 2008, Paolo Macchiarini and his 22]. colleagues performed the frst tissue engineered trachea A breakthrough in modern regional anesthesia was made transplantation. Adult stem cells were extracted from the in 1841 when Jayne created the framework for the modern patient’s bone marrow, grown into a large population and hypodermic syringe for the delivery of various medications matured into cartilage cells using an adaptive method [23]. The decisive step in the development of regional anes- originally devised for treating osteoarthritis [15]. In 2014, thesia was done by Koller in 1884, a Czech physician who surgeons led by Kurimoto at the Institute of Biomedical frst used local anesthesia in eye operations at the Vienna Research and Innovation Hospital in Kobe of Japan, trans- general hospital [24]. The next year, Halsted performed planted a sheet of retinal pigment epithelium cultivated the frst brachial plexus nerve block [25]; Halsted, his stu- from undiferentiated cells into an eye of an elderly woman dents and fellow physicians experimented on each other and [16]. Such methods are still in an experimental stage, but demonstrated that as local anesthetic could produce the horizons opened by them in the and safe and efective local anesthesia when injected near the microsurgery cannot be overemphasized. nerves. Max Kappis, a German surgeon, described poste- rior approaches to the lower seven cervical nerves for the purposes of cervical and brachial plexus nerve block, and described paravertebral block of the thoracic nerves and Regional anesthesia the frst four lumbar nerves in 1908 [26]. At the same year, Bier, a German surgeon described the intravenous regional Evolution of regional anesthesia techniques further added anesthesia for upper extremity interventions (Bier’s block) to the advent of microsurgery [17–34]. Compared to gen- [27]. In 1911, Hirschel, another German surgeon, performed eral anesthesia, not only are peripheral nerve blocks asso- the frst brachial plexus nerve block by using an axillary ciated with signifcant pain control during surgery but also approach [28]. At the same time, Kulenkampf, also Ger- with substantial sympathetic blockade. Augmentation of man surgeon reported his frst experience on brachial plexus blood fow and reduction in certain pro-thrombotic coagu- nerve block via the supraclavicular approach [29]. In 1962, lation factors are the major benefts of the technique in the Greenblatt and Denson [30] constructed a small portable context of microsurgery [17]. Essential to current neural transistor-based device similar in design and appearance to modern nerve stimulators used for peripheral nerve blocks;

1 3 252 European Journal of Orthopaedic Surgery & Traumatology (2019) 29:247–254 however, the neurostimulation technique was frst described amputations. For cases that face more complex problems, and documented by Perthes [31] at the beginning of the the surgeon should be aware of other alternative tech- twentieth century. Greenblatt and Denson’s device deliv- niques, such as transpositional microsurgery, various ered a square-wave impulse of 0.1 ms in duration at 1-Hz other secondary reconstructive procedures, and today frequency, with an adjustable output of 0.3 to 30 V [30]. In the options of tissue engineering. After 5 full decades of the early nineties, ultrasound systems were introduced in the microsurgery, the words of James R. Urbaniak “…there is practice of peripheral nerve blocks and revolutionized the no end to the world of microsurgery…” ring true, as the implementation of regional anesthesia techniques in surgery history of microsurgery is once more marked by a signif- and microsurgery [32]. cant milestone. Currently, composite tissue allotransplantation (CTA) or vascularized composite allotransplantation (VCA) has intro- The latest historical milestone duced new options and challenges to reconstructive micro- in microsurgery: composite tissue surgery. Transplantation of a vascularized limb or its compo- allotransplantation (CTA) or vascularized nents is defned as composite tissue allotransplantation. The composite allotransplantation (VCA) frst hand allotransplantation was performed by Dubernard in Lyon France on September 23, 1998 [52]. Ten years later, While the origin of microsurgery is rooted in the early inno- in 2008, Biemer, Hoehnke and colleagues performed the frst vations of vascular surgery and the introduction of intraop- bilateral upper arm allotransplantation in Germany [53]. The erative magnifcation in the nineteenth century, the hallmark initial success of these procedures led to a focused interest of microsurgery, microsurgical replantation and revasculari- on the potential of CTA [53–56]. zation became a reality in 1962 with frst replantation of a This new area in surgery has been made possible by the completely amputated arm in a 12-year-old in Boston by advent of microvascular surgery combined with advances Malt and McKhann [35]. This initiated a deluge of eforts in our knowledge of transplantation immunology. Hand to promote replantation microsurgery around the world, transplants, as a composite tissue allograft, difer from solid including the frst experimental eforts by Buncke; Buncke’s organ transplants, since they consist of several types of tis- work established many of the primary principles in micro- sue such as bone, muscle, cartilage, tendon, skin, nerves and surgery [36]. Shortly after Komastsu and Tamai successful vessels, with diferent antigenicities. As such, composite tis- replantation of a completely amputated thumb in 1965 [37], sue allotransplantation is faced by three major obstacles. The replantation surgery spread through the world at various frst is acute rejection that is the most frequent complication centers with successful replantations reported in Durham, of allotransplantation. Acute rejection occurs without excep- North Carolina, USA (Urbaniak, Soucacos) [11], Zurich, tion at least once within the frst year of transplantation and Switzerland (Meyer) [38], Munich, Germany (Biemer) [39] may lead to early graft loss. The second is chronic rejection and Athens, Greece (Soucacos, Anastasiou, Beris) [40, 41], that is a poorly characterized process that occurs late after with survival rates of more than 80–90%. allotransplantation. The third is the necessary chronic immu- The frst free tissue transfer is considered the groin fap nosuppression that may lead to drug side efects such as transfer by Daniel and Taylor in 1973 [42]. Shortly after, in opportunistic , diabetes, osteonecrosis, malignan- the 1970s, several surgeons focused on defning new donor cies or organ failure. Methods to reduce immunosuppression sites, including the scapular fap (Gilbert) [43], latissimus requirements include tolerance and chimerism. Chimerisms dorsi musculocutaneous fap (Baudet) [44], latissimus dorsi refect the ability of two genetically distinct types of cells to free fap (Marko Gondina) [45] and recently the perforator be able to coexist in a single organism. These three issues fap (Alexander Georgescu) [46]. Other landmark microsur- have dominated the debate in the hand surgery community gical transplantations include the toe-to-thumb procedure regarding the life-enhancing benefts and ethics of human (Buncke) [47], partial toe transfers (Foucher) [48] and many hand transplantation [53–56]. more. Alongside the advances in microvascular surgery, The outcomes of this procedure are still being deter- microsurgeons from USA (Julia Terzis) [49], Italy (Brunelli) mined, and details of all composite tissue allotransplanta- [50] and Austria (Millesi) [51] focused on fascicular nerve tions are maintained in the «International Registry on Hand repair and grafting. and Composite Tissue Transplantation» . The ethical aspects Even though today replantation surgery has become of using chronic immunosuppression for a condition that is a routine, it still remains a delicate and demanding sur- not life-threatening have also been debated in the surgical gery that requires adequate expertise in microsurgical communities. Consequently, the future of hand transplants techniques. The indications for replantation procedures and other composite tissue allografts lies in the development have been well established including formulated guide- of less toxic immunosuppressive drugs and/or safer methods lines for digits, hand, upper extremity and lower extremity of tolerance induction, such as chimerism [53–57].

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