“Korotkov demonstrated that, in each specific case, one can preoperatively be aware of so-called collateral circulation efficiency.”
—Vladimir A. Oppel, 19061
“Whatever may be said of the method, great credit is due to Korotkov for first calling attention to the importance of making accurate observations before operating for aneurysm, with a view of determining the efficiency of the collateral circulation after temporary obliteration of the main artery.”
—Rudolph Matas, 19112
At the dawn of the 20th century, it became possible to surgically access areas of the body that were previously off limits. The dynamic progress of surgical science, specifically in the form of improved anesthesia, aseptics, and antiseptics, provided the prerequisites for the complete treatment of arterial injuries using vessel suturing. In the spirit of the times, some surgeons attempted to restore blood flow in the injured vessel itself using direct surgical techniques, whereas others made efforts to improve extremity blood supply through the development of arterial collaterals. The former approach was pioneered by the Nobel Prize winning surgeon Alexis Carrel, who developed techniques to directly suture or repair the injured vessel. Nikolai Korotkov (Fig. 1), a Russian surgeon who did not expect breakthroughs in direct vessel repair “in the near future,” belongs in the latter camp or those recognizing the value of collateral circulation to maintain limb viability following disruption of the axial artery or arteries.
The names of these two surgeons are well known, although Carrel is famous for the development of the vessel suturing technique, whereas Korotkov was the first to discover the method of auscultation to measure systolic and diastolic blood pressures. Few people are aware that this method was developed in the course of his creative search for the answer to a primary question in the clinical management of trauma: is it possible to determine preoperatively whether an extremity will remain viable or succumb to gangrene following arterial ligation of an injury. Many well-known surgeons, such as Antonio Scarpa, Nikolai Pirogov, Richard von Volkmann, August Bier, Pierre Delbet, and Rudolph Matas, focused on the management of aneurysms, but it was Korotkov who dedicated his career to studying the importance of collateral circulation in the setting of extremity vascular trauma and its role in preserving the limb.
Korotkov was familiar with the works of Carrel and wrote, “Welcoming the attempts to save the vessel lumen, I cannot help but get rid of a certain degree of skepticism concerning this fact.”3 His skepticism was associated with the high thrombosis rate after direct vessel repair which—at that time—was being developed decades before the use of the anticoagulant heparin. These factors may have been why there was an almost a 50-year delay between the first vessel suture and its wider adoption in surgical practice. The question remains: how did it happen that a Russian military surgeon, whose contributions laid the groundwork for innovations in vascular surgical science, is still known mainly to internists and cardiovascular specialists more than 100 years after he discovered the method of auscultation to measure arterial pressure?
Nikolai Sergeevich Korotkov was born on February 26, 1874, in the small country town of Kursk 500 km to the south of Moscow, into a merchant family. He finished public school and entered the medical faculty of Kharkov University, from which he transferred to Moscow University, graduating with honors in 1898. Professor Alexander A. Bobrov, one of the preeminent Russian surgeons of the time, noted the abilities of the young graduate and his craving for knowledge. Korotkov was engaged for the position of an acting resident surgeon without pay.4,5 Very soon after in 1900, Korotkov voluntarily joined a Red Cross unit directed by I. P. Aleksinski, one of Bobrov’s students, that was going to China to aid the injured in the Boxer Rebellion of 1899 to 1901. After this tour of duty, he returned to Moscow. When his residency was over, Korotkov was invited by another outstanding Russian surgeon, Sergey Fedorov (also a former student of Bobrov), to the Military Medical Academy in Saint Petersburg. There, Korotkov started work as an unpaid assistant (similar to a resident or instructor) in the surgical clinic.5–10
As early as 1903, Korotkov began studying actively for a doctoral degree. It should be noted that the professor who proctored Korotkov’s examination in physiology was Ivan Petrovich Pavlov, the 1904 Nobel laureate in Physiology or Medicine for studies on digestion. Unfortunately, defense of the thesis was precluded by the outbreak of the Russo-Japanese war in 1904 to 1905, for which Korotkov again volunteered. The long expedition of several thousand kilometers to the eastern front in Harbin, China, along with subsequent hard labor as a Red Cross senior surgeon undermined his health, and Korotkov fell ill with pulmonary tuberculosis. Having passed all dissertation examinations, he temporarily stopped work on the thesis to take care of his health.
After returning to Saint-Petersburg in 1905, Korotkov left for Siberia to work as a physician in the Vitimsko-Olekminsky district (1908–1909). After defending his thesis in 1910, he returned to Siberia as a doctor of medicine (MD, PhD) in Lensk, where he treated gold miners in the camps. On his return from Siberia in 1913, World War I broke out and Korotkov filed a request to enter the theater of war. He was sent to Tsarskoe Selo (now the town of Pushkin near Saint-Petersburg), where he served as a surgeon at a recently established hospital. He devoted all energies to the care of injured and sick there against the backdrop of revolutionary Russia. Being in delicate health, he endured the October Revolution of 1917 and died in 1920 of progressing pulmonary tuberculosis.9,11
COMBAT EXPERIENCE AS A SOURCE OF THESIS MATERIAL
There is no doubt that Korotkov’s activity as a military surgeon turned the young scientist to the in-depth study of collateral blood flow and ways to save the extremity in the setting of major vascular injury. Two travels to the theater of war—first to the Russian Far East and later to Harbin, China—enabled the acquisition of valuable data on the diagnosis and treatment of traumatic aneurysms, as each case was thoroughly investigated, analyzed, and registered.
The taste for investigation was born during his first trip in 1900 to 1901, which resulted in a serious scientific work on traumatic aneurysms of extremities and neck. It was not long before an opportunity to evaluate his capabilities in treating this kind of pathology presented itself when the hospital in Blagoveshchensk (on the way to Khabarovsk) was opened. As S.E. Popov wrote, the field hospital was established in a deserted two-story old house; 40 beds were placed on the upper floor.11 To make the house with log walls suitable for operative work, Korotkov and two other surgeons on the team sheathed surfaces with cardboard and oilcloth, which were thoroughly disinfected with formalin. On the first day of hospital work, 32 patients were admitted.11 One was a soldier with a gunshot wound of the thigh, with injury to both the femoral artery and vein and severe blood loss. At that moment, the question arose in the head of the future surgical scientist: was it possible to ligate the injured vessels to control hemorrhage and still maintain limb viability, and if so, how could one preemptively evaluate or predict the outcome of such an approach? In this influential case, despite Korotkov’s concerns regarding the need for amputation, the injury was managed with vessel ligation, with resultant maintenance of perfusion and limb viability, and the soldier recovered.
A spiritual mentor of Korotkov, Nikolai Pirogov—one of the greatest surgeons in the history of medicine and founder of scientific war surgery—devoted his thesis entitled “Is the ligation of the abdominal aorta in inguinal aneurysm an easy and safe procedure?” to the possibility of abdominal aorta ligation.12 In this work, Pirogov advised thorough auscultation of aneurysm in doubtful cases of diagnosis. The surgeon Korotkov did not fail to take advantage of this advice, and using the Riva-Rocci blood pressure cuff, he could hear the sounds, which were later known as “Korotkov sounds.”6,8,9,11 As he later wrote:
“The unpredictable results of operations are unpleasant for the physician and even more unpleasant for the patient. Therefore, it would be advisable to seek the basic signs by which it is possible to know whether after the ligation of the artery the patient would be dead or alive.”13
Thus, uncertain surgical approach prompted the discovery of an evaluation method for collaterals development based on the method of auscultation to measure arterial pressure.
On his second trip in 1904 to 1905, Korotkov was already an experienced war surgeon and served as senior doctor of the St. George community sanitary unit of the Red Cross. There, at the 2nd Harbin Hospital in China, Korotkov had the opportunity to take care of all injured admissions with aneurysm. Five days after hospital deployment, Korotkov dealt with the first patient with traumatic aneurysm of the right axillary artery.11 A 26-year-old soldier wounded by a rifle bullet to the right shoulder joint who presented with sustaining pains and incomplete anesthesia and paresis of the right upper extremity. A large pulsating tumor was palpated in the axilla. The radial pulse was weak, and a blowing systolic murmur was auscultated. After Korotkov ligated the arteries above and below the aneurysm, all pains were gone, the arm remained alive, and, eventually, extremity function improved.3 This first, already sensible, case of care of an injured soldier with aneurysm served as the base for Korotkov’s doctoral thesis in 1910.
His theory was tested and confirmed later in the management of a 25-year-old soldier who was admitted with a rifle wound to the left popliteal area and a constant murmur increasing with systole. Korotkov made the diagnosis of a traumatic aneurysm with arteriovenous fistula and noted that the pulse in the posterior tibial artery in the injured leg was weak with an arterial occlusion pressure of pressure 60 mm Hg. In contrast, the arterial occlusion pressure of the uninjured leg was 110 to 115 mm Hg. “On pressing art. popliteae at the site of its junction with vein, the exsanguinated foot becomes colored at 40 mm Hg; the cuff was applied on the lower leg muscles.”3 Immediately after the resection of arteriovenous fistula, the arterial pressure at the posterior tibial artery was 40 mm Hg, which confirmed the suggestions by Korotkov and the reliability of his preoperative examination.
Korotkov described in detail “the method of preoperative measurement of arterial collaterals efficiency”:
“If, after previous extremity exsanguination, we compress a major artery above the site of exsanguination, and then remove pressing bandage, at the same time continuing artery compression, then reactive hyperemia in peripheral areas of the leg will appear only in case blood enters a peripheral portion of the artery through collaterals; and taking this into account, hyperemia of peripheral areas of the extremity would guarantee viability of the extremity in postoperative period. Thus, having changed bandage application for temporary artery compression, we could judge about presence or absence of collaterals in a clinical sense; adding the blood pressure measurement in distant areas of the extremity, we could judge about collateral flow efficiency in every given case.”3
In the Russo-Japanese war, Korotkov got the experience of examining patients using his method and surgical care for 35 patients with aneurysms. On average, patients arrived to the Harbin hospital within 2 weeks of injury and were operated on within 3 to 4 weeks. He described 44 cases, nearly half of which featured arteriovenous aneurysms, in his doctorate thesis “The Experience of Measuring Arterial Collateral Efficiency” (Table 1).3,11
Korotkov performed preoperative measurements of peripheral arterial pressure in almost all patients with aneurysms. He wrote, “The patient, having traumatic arterial-venous aneurysm of femoral artery and vein, had arterial pressure in an uninjured leg = 120 mm Hg and in an injured leg = 35 mm Hg. Another patient N.M., who also suffered from traumatic arterial-venous aneurysm at the border of the middle and lower thirds of the thigh, had arterial blood pressure in an uninjured leg = 105 mm Hg and in an injured leg = 50 mm Hg.”3 He repeated these measurements before and after each operation, thoroughly analyzing and checking them. Currently, we perform the same measurements in admitted patients with suspected extremity vascular injuries, that is, when comparing ankle pressure in uninjured and injured extremities, whereas Korotkov actually performed so-called arterial pressure index measurements. He invented a special longer cuff for the purpose of measuring ankle pressure in anterior and posterior tibial arteries. Korotkov noted that every time an artery was ligated above and below an aneurysm, arterial pressure in the peripheral or distal portion decreased more than twofold but eventually increased by 15 to 20 mm Hg in the first postoperative day because of the effect of collateral circulation. By carrying out numerous pressure measurements in dramatically ischemic extremities, he found that, to save viability, it is sometimes sufficient for peripheral arterial pressure to be even less than 30 mm Hg. Thus, because of the developed and high-sensitivity method of auscultation, Korotkov made a critical discovery—he could quantitatively estimate compensation abilities of the vascular system to restore circulation while a main artery was ligated, thus anticipating the later work of German surgeons Adolf Henle, Erich Lexer, and Hermann Coenen with adequate prognostic evaluation of collaterals reserves. The abovementioned arterial pressure threshold, below which one should not carry out artery ligation, has been corroborated by many investigators across the past century.14
CONTRIBUTION TO THE WORLD OF MEDICINE
At all times, in striving to help patients, scientists worked out ways of solving problems that seemed to be momentous for the generations and, to a large extent, specified treatment approaches years before their widespread adoption. This was the case with the method of measuring arterial collaterals efficiency developed by Korotkov.15,16 As described in his initial report to the Military Medical Academy in November 1905, the method’s logic was elegant:
“The cuff of Riva-Rocci is placed on the middle third of the upper arm; the pressure within the cuff is quickly raised up to complete cessation of circulation below the cuff. Then, letting the mercury of the manometer fall, one listens to the artery just below the cuff with a children’s stethoscope. At first, no sounds are heard. With the falling of the mercury in the manometer down to a certain height, the first short tones appear; their appearance indicates the passage of part of the pulse wave under the cuff. It follows that the manometric figure at which the first tone appears corresponds to the maximal pressure. With the further fall of the mercury in the manometer one hears the systolic compression murmurs, which pass again into tones (second). Finally, all sounds disappear. The time of the cessation of sounds indicates the free passage of the pulse wave; in other words, at the moment of the disappearance of the sounds, the minimal blood pressure within the artery predominates over the pressure in the cuff. It follows that the manometric figures at this time correspond to the minimal blood pressure.”15
It enabled one, for the first time, to define indications for aneurysm removal with vessel ligation based on preoperative examination using noninvasive techniques. Years later, more adequate diagnostic methods appeared, such as continuous wave Doppler examination, duplex scanning, angiography, and computed tomography angiography. These diagnostic tools allow accurate imaging without detailed physical examination, although in the case of suspected extremity arterial injury, a routine method of distal arterial pressure measurement—more commonly using continuous wave Doppler and the injured extremity index—has proven to be the mainstay of screening and diagnosis.17–19
The pioneering work of Korotkov was confirmed and extended by Vladimir Oppel and his students, who used the described method of measuring blood pressure in both basic science experiments and clinical practice.20 Noninvasive and accurate, the method has become widespread. In the case of treating a patient with arteriovenous aneurysms in the axillary region, who was examined by Korotkov and operated on three times by Oppel, the technique of ligating axillary veins after arterial ligation and isolation of the aneurysm led to a secondary theory—that of “reduced circulation,” or promoting simultaneous vein-artery ligations. The study results were presented in Oppel’s fundamental work, “The Collateral Circulation,” published in 1911.20,21
Oppel highly praised Korotkov’s contribution to the interpretation of collateral circulation mechanisms in the presence of injured vessels. In particular, he noted that Korotkov was the first to pay special attention to arterial pressure variations distal to ligation sites, giving a definition to “conducted pulse,” that is, taking pulse by palpation distally, which developed afterward in case of sufficient collateral support.
In Korotkov’s thesis, in addition to the significant discovery of “sounds” when arteries are ligated (described as early as 1905), another serious, almost prophetic, message for future investigations was presented.15 He raised a question about using pharmacotherapy to improve peripheral circulation in the extremity. Considering the main means of improving peripheral circulation after artery ligation to be cardiac muscle functioning and capillary resistance, Korotkov suggested the use of digitalis as a medication increasing systolic output, as well as peripheral vasodilator amyl nitrite to dilate small capillaries. Realizing that gangrene can develop after major artery ligation because of slowly developing collaterals, he proposed maintaining extremity perfusion with solutions, such as saline or preferably, saline with “some oxygenated nutrient solutions.” He wrote, “In order to keep the extremity alive, long-term artificial circulation is unlikely to be necessary, short-term lavage will suffice, though it may be repeated.”3
In a record of competitors for doctoral degrees, Korotkov’s achievements contained the following: “In 1900, he translated Prof. [Eduard] Albert’s “The Diagnosis of Surgical Diseases” from German. In 1905, he suggested a new method of measuring blood pressure in humans.”3 Thus, a century in advance, briefly and clearly great Russian surgeons S.P. Fedorov, V.A. Oppel, and N.N. Petrov—Korotkov’s rivals—foretold of their student’s scientific work. Korotkov set fundamental and applied issues for himself and medicine as a whole, the resolution of which laid the groundwork for further developments in the diagnosis and treatment of patients with vascular injury and disease.
More than 100 years later, the legacy of Korotkov—whose few but revolutionary works have been appreciated by physicians and scientists globally—is still in need of further understanding and analysis by contemporary surgeons.21,22 To pay tribute to the outstanding scientist on the 100th anniversary of the discovery of the method of auscultation to measure arterial pressure, a memorial tablet was established at S.P. Fedorov’s Hospital Surgery Clinic in Saint-Petersburg, where this method was discovered and announced for the first time (Fig. 2). A memorial stele was also constructed at the Academy site at Bogoslovskoye cemetery, where Korotkov was buried (Fig. 3). One of the streets within the Military Medical Academy, where Korotkov worked, is named after him (Fig. 4).
The authors declare no conflicts of interest. The views in this article are those of the authors and do not reflect official positions of their governments or the US Air Force or Department of Defense.