G.A. Ilizarov embarked upon his remarkable medical career as a general physician in the small industrial town of Kurgan, east of the Ural Mountains in Siberia of the former Soviet Union. The year was 1944, and the majority of his patients suffered musculoskeletal injuries following the Second World War. Antibiotics, though available in the western world, were scarce in Siberia where chronic osteomyelitis with bone deficiencies such as nonunions and deformities were so common that Ilizarov found himself practicing orthopedics of necessity. In part through serendipity and in part through his own genius and tenacity, he developed the method still used today that bears his name.
Using modular ring external fixators with transosseous wires tensioned to the rings to stabilize the bone fragments, Ilizarov introduced the concept of “local bone regeneration” using minimally invasive surgery. His method salvaged limbs, avoiding amputation, and returned completely disabled patients to normal activity. Eventually his clinical success spread by word of mouth throughout the Communist Block. By 1981, a group of Italian orthopedic surgeons learned of his technique, mastered it and subsequently published it in didactic textbooks.
The ASAMI is created
G.A. Ilizarov at home in Kurgan, Siberia, in September 1988.
In order to disseminate the device and the technique, these Italian orthopedic surgeons organized national societies throughout the world under the title of the Association for the Study and Application of the Methods of Ilizarov (ASAMI). More recently, the method was introduced to North America, where it has been adopted primarily by pediatric orthopedic surgeons for limb lengthening. Some American orthopedic surgeons have expanded their practice to include the Ilizarov method for adults with severe deformities such as nonunions and bone deficiencies from trauma and infections or tumors.
Many research centers have utilized the method to study bone formation. Coincidentally, these efforts corroborated Ilizarov’s own research and in part extended insights into the regeneration of both bone and soft tissues under mechanical distraction. Ilizarov first introduced this method both experimentally and clinically over his 40-year career in Siberia.
Distraction osteogenesis involves mechanical stretching, using external fixation of the reparative process invoked by a low-energy osteotomy. Ilizarov’s approach implies that this process is regenerative, rather than reparative. Consequently, he referred to the new bone as “regenerate.” His clinical successes saving the limbs of thousands of patients with conditions that traditionally resulted in amputation revolutionized the current practice of modern orthopedic surgery.
Distraction osteogenesis has been successfully used to regenerate bones deficient from congenital conditions and failures in formation such as hemimelias acquired from fractures or infections during childhood that stopped normal bone growth; and from intercalary bone defects, where large segments of a bone have been lost due to open fracture. Also treatable through this method are osteomyelitis and a variety of local tumors or dysplasias of bone. Bone deformities and discontinuities (e.g., nonunions) have also been corrected with this technique. The procedure has been successful with patients of nearly any age, from early childhood to middle-aged adults.
The actual length of new bone produced from a single procedure can be as much as 18 to 20 cm per limb segment. This astounding growth translates to sometimes extending an individual bone by over 100% of its initial baseline length. Multiple lengthening sites are also capable of simultaneously producing new bone segments, which lengthens the limb even more rapidly. The new bone lengths are usually of equivalent cross-section and quality to the local site in the host bone. Bone production seems to be highly successful in these procedures, but soft tissue growth and preservation of normal joint function may limit the clinical applications.
In sync with orthopedics’ history
In order to appreciate the monumental contributions of Ilizarov to the field of orthopedic surgery, it is important to relate his achievements to precedent events historically. To fully grasp Ilizarov’s contribution to the medical science of orthopedics, it is necessary to chronicle milestones as far back as the turn of this century. Three areas — limb lengthening, external fixation and bone regeneration — can be traced from the earliest orthopedic ideas through the time of Ilizarov’s discoveries.
Codivilla reported the first successful lengthening of deformed limbs in 1905. He published results of 26 lengthenings using an osteotomy of the cortex and acute traction force through a calcaneal pin under narcosis. Although he did attain 3 to 8 cm of length in many patients, complications included seizures and death. Codivilla emphasized the need to determine the appropriate force to stretch the soft tissues, especially muscle, in order to maintain normal function.
Spontaneous bony healing
In 1908, Magnuson examined the potential for spontaneous bony healing following acute lengthening. He used a step-cut in the bone and internal fixation with “absorbable” ivory pegs in both animal experiments and clinical trials. Shock and death complicated the method, but he demonstrated that large, local vessels and nerves could tolerate up to 2 inches of acute lengthening.
Ombredanne employed the first use of an external fixator for limb lengthening in 1912. He lengthened an oblique osteotomy at a “gradual” rate of 5 mm/day for eight days. Reported complications included skin necrosis and infection. In 1921, Putti slowed the rate of distraction even further, to 2 to 3 mm/day for 30 days. After his initial experience using stretched piano wires for skeletal traction, Putti introduced a monolateral fixator he called the “osteoton,” which incorporated half-pin fixation. He published a series of 10 cases of femoral lengthening following infected fractures from war injuries. Putti’s improvements on the orthopedic technique reportedly resulted in an average lengthening of 3 to 4 inches.
The idea of a latency period to promote bone formation was introduced by Abbott in 1927. While preserving periosteum, he performed a step-cut osteotomy followed by a latency period prior to distraction via a spring-loaded, force-controlled device. He reported his clinical results of six tibia lengthenings as being from 3 to 5 cm, with spontaneous bone healing. He also introduced the concept of releasing skin around the pins to avoid pain.
Long-term Abbott technique results
Fifteen years later, Brockway and Fowler reported their long-term follow-up of 105 lengthenings using the Abbott technique. They employed a five-day latency period and a distraction rate of 1 to 1.5 mm/day. Prolonged casting until healing followed the skeletal fixation-distraction period. A 5-cm lengthening required a total treatment time of one to two years. This duration is equivalent to about three to four months per centimeter.
In 1936, Anderson reported his method of femoral lengthening using wires tensioned to external stirrups attached to a heavy frame. A two-part body cast was connected after the lengthening, so that the patient remained bedridden for the entire treatment. The periosteum, like the bone, was cut obliquely, and the lengthening was performed daily at 1.5 to 2 mm/day He later introduced the technique of percutaneous osteotomy by manual osteoclasis.
Using an intramedullary rod
In 1956, Bost and Larsen published their series of 23 patients who underwent femoral lengthening over an intramedullary rod. This orthopedic innovation avoided the deformity commonly associated with conventional external pin devices. After cutting the periosteum, an osteotomy was performed using a power saw or Gigli saw. Although some femurs united spontaneously by “stretching callus,” delayed unions were frequent.
The authors questioned the significance of a latency period prior to distraction, but could not determine the cause of the delayed unions. However, they did realize that the longer a bone was lengthened, the longer it took for union and the greater the likelihood of nonunion. They observed that lengthening a congenital shortening was more difficult than lengthening an acquired shortening. They believed that the problem was due to the soft tissues that were less elastic in the former conditions.
Ring first employed the concept of distraction physeolysis in 1958. He used a turnbuckle external fixator to distract the radial and ulnar growth plates of 20 puppies. In doing so, he observed that the growth plate fractured, but the periosteal tube remained intact and gave rise to a shell of new bone. Similarly, Fishbane and Riley performed limb lengthening via trans-physeal traction, but used a ring external fixator. In 1976, the duo were the first in the United States to refer to Ilizarov’s work.
The biology behind the technique
Dr. James Aronson stands in front of the World War II memorial in Kurgan, Siberia, home of Dr. Ilizarov, during his trip there in 1988. The memorial is significant not only because it denotes the time when Ilizarov started his groundbreaking work, but it also signified the end of World War II and the beginning of the Cold War.
Significant advances in the understanding of the biology of distraction osteogenesis emerged in 1968, when Kawamura presented data from more than 150 animal lengthenings and 74 clinical applications. Both bone formation and soft tissue response to lengthening were measured using histology, histochemistry, plethysmography (blood flow), pharmacological agents and neurotomies. The surgical technique utilized a mid-diaphyseal, subcutaneous osteotomy. Based on experimental data, he demonstrated that periosteum was less damaged if stripped as a tube circumferentially, beyond the eventual lengthening goal. The periosteum and other soft tissues (muscles, nerves and vessels) seemed to tolerate up to a 10% lengthening limit. Peripheral blood flow diminished as the rate of lengthening increased, an effect that could be reversed by pre-administration of diazepam.
In patients ages 8 to 15, bony union was 100% (16/16), if peripheral blood flow increased beyond 70% of baseline. Delayed unions occurred in six out of seven patients whose blood flow increased less than 70%. Using the experimental results to guide clinical techniques, the average lengthening was 2.7 cm. Although this was relatively low compared to Ilizarov’s standards, they noted faster healing time (one to two months per centimeter) and a higher union rate than previously reported.
Although Kawamura emphasized care of soft tissues by slower distraction rates and a subperiosteal, drill-osteotome, osteoclasis technique, he did not seem to appreciate the importance of a latency period or of gradual daily distraction as advocated by Ilizarov.
Substituting the Wagner method
The Wagner method of lengthening replaced the Anderson technique among pediatric orthopedists during the 1970s and early 1980s. His method, which utilized a monolateral fixator that allowed patient mobility, as well as a three-stage plan to expedite treatment and maximize function, became the standard of care. Wagner purposely cut periosteum, fascia and other constraining tissue to minimize resistance. This variation in technique limited the lengthening to 6 or 7 cm and used relatively rapid daily rates of 1.5 to 2 mm, as tolerated by the unanesthetized patient. Next, he bone grafted the defect as a planned procedure.
The mid-diaphyseal osteotomy was made with an oscillating saw and a special internal fixation plate replaced the external fixator after the distraction goal was achieved. Muscle and joint function took precedence over spontaneous bone formation.
In 1982, Alho published an article on experimental osteotaxis distraction. Alho’s article focused on demonstrating osteoblastic bone formation from the endosteal surfaces, as well as the periosteal tube. He also cited Ilizarov’s work. For the first time, research outside of Ilizarov’s own laboratory had reproduced this new phenomenon, distraction osteogenesis.
Monolateral, half-pin frames
Although Ilizarov often attributed special biological effects to the ring external fixator with tensioned wires, distraction osteogenesis and even bone transportation can be successfully accomplished using monolateral, half-pin frames or even intramedullary rods. Ilizarov emphasized the importance of frame stability for successful bone healing. Most modern monolateral fixators are stable enough to distract the osteogenic zone but are limited by an inherent cantilever design, which imparts eccentric loads to the bone and may result in undesirable angulation of the lengthened segment. Gross frame instability should be avoided, as it results in either premature consolidation or fibrocartilage nonunion. The surgeon’s experience and preference determines the choice of an external fixator. Other factors to be considered include the complexity of the problem, the patient’s ability and tolerance and the number of sites requiring treatment.
Ilizarov’s three major contributions involve extended limb lengthening, skeletal reconstruction and bone transportation. The method of limb lengthening has been advanced in several ways: multiple simultaneous sites, extended lengthening goals allowed by protection of adjacent joints and gradual stretching in a function-oriented frame, spontaneous bone bridging without grafting, internal fixation or secondary operations and simultaneous deformity correction.
The method of skeletal reconstruction encompasses the treatment of nonunions, deformities (bony and soft tissue) and arthrodiastasis (mobilization of joint contractures). Nonunions have been treated successfully with minimally invasive percutaneous techniques. Deformities have been corrected gradually, in any plane (simple deformity) or a combination of planes (complex deformity), by innovative external fixation constructs that allow for stable mechanical control and movement of the bony fragments.
Bony deformities and nonunions are healed by distraction osteogenesis and the mechanical axis of the limb is restored to normal. Articular deformities are corrected by gradual stretch of soft tissues via transosseous external fixation with special distraction hinges to protect hyaline cartilage against excessive compression.
Bone transportation: a true breakthrough
The method of bone transportation is perhaps the most unique innovation. Major intercalary defects in bone substance have been regenerated while restoring bony integrity and alignment with this method. In utilizing this technique, bone grafts are not necessary and limb length can be regained. Chronic focal, segmental and cavity osteomyelitis have all been treated by bone transportation by excising the osteomyelitic bone and regenerating the resultant defect. In cases of cavity osteomyelitis, the partial defect can be regenerated using transverse or oblique transport whereas in most cases of segmental defects, axial transport is carried out along the longitudinal axis of the bone. Bone transportation has been used to salvage limbs that would otherwise require amputation, since the defects generally exceed the volume of available autograft.
Clearly, the biology and modular system of external fixation developed by Ilizarov have revolutionized orthopedic care. The biology has certain limitations, including slower osteogenesis in adults, delayed or absent growth from muscles during lengthening at the critical rate for distraction osteogenesis, rebound phenomenon in both muscles and primary collagenous tissues such as ligaments and capsules, and joint stiffness secondary to prolonged external fixation. Pin tract inflammation and infection contribute to the discomfort, stiffness and possibly to the poor response of muscle, as well as occasionally impinging on neurovascular structures.
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This series of radiographs of Ilizarov’s work demonstrates the elongation of the humerus of an achondroplastic dwarf. The arm was lengthened at two sites.
Research is underway in many centers to discover therapeutic innovations to accelerate bone formation, promote muscle growth and even to avoid transcutaneous fixation. Since intramedullary rods have been compatible with distraction osteogenesis, the natural solution to avoid external fixation pins would be to develop a growing intramedullary rod. This is perhaps one of the more exciting potential areas for future research in the application of distraction forces at different rates to regenerate both ligaments (Aston recreated a cruciate ligament by distraction histogenesis in the stifle joint of 13 dogs) and articular cartilage.
Ilizarov died in 1992. His fellow citizens fondly referred him to as the “magician from Kurgan.” Those who had the opportunity to meet him know that he cared deeply for his patients and dedicated his life to improving care of musculoskeletal problems.
James Aronson, MD, is chief of pediatric orthopedics at Arkansas Children’s Hospital, director of the Laboratory for Limb Regeneration Research at Arkansas Children’s Hospital Research Institute, and a professor of orthopedic surgery at the University of Arkansas.