R.O. Datiashvili and A.R Lein
RESTORATION OF LYMPH DRAINAGE AFTER EXTREMITY
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REPLANTATION ABSTRACT A clinical analysis of 171 major extremity replantations was carried out. From one month to 2.5 years after surgery, direct lymphographic studies of replanted limbs were done in 17 patients (16 upper limbs and one lower limb). Despite a complete disruption of lymphatic drainage, replanted limbs underwent adaptive and compensatory structural changes of the lymphatic system in the post-replantation period; first, with regeneration of cutaneous vessels and then (after six to eight weeks postoperatively) with regeneration of lymphatic collecting vessels. Such changes led to improvement as early as four to six weeks postoperatively and subsequently to restoration of lymphatic drainage in the replanted limb. The rate and extent of lymphatic recovery depends largely on the surgical techniques used in replantation.
Although more than 20 years have passed since the first successful salvage of a complete limb amputation, it is still generally accepted that many problems remain in major extremity replantations. Replantation aims at restoring practically all anatomic and functional structures in an amputated limb: bony skeleton, arteries, veins, muscles, and nerves. However, in the course of extremity replantation, lymphatic vessels are not restored. The role of lymph circulation in normal organ and systemic activity and function is well known. Lymphographic studies have shown that the main reason for post-traumatic lower limb edema, often persisting for up to three to eight years in a very acute form, is transport disorder of major and smaller lymphatic vessels.1 Certainly, few lymph vessels are damaged by ordinary injury, while amputations completely disrupt lymphatic drainage. Important questions are: What sort of lymph circulation disorders take place after replantation? Can lymphatic drainage be restored in replanted limbs, and what are its mechanisms? The literature offers limited reports concerning these questions. Nevertheless, some previous experimental studies are interesting. Lapchinsky et al.,3 Kirpatovsky and colleagues,4 and Chachques et al.5 have studied the mechanisms of lymph drainage restora-
tion in various experimental models, including dogs, rabbits, and rats. Indirect and direct lymphography have been used, as well as radioisotope and histologic techniques. The general consensus is that, following replantation, the lymphatic system in the extremities undergoes structural changes, in particular, the development of a superficial lymphatic network that contributes to the gradual stabilization of lymphatic drainage and the disappearance of edema as early as one month after surgery. A deeper network of lymphatic vessels begins to form between four and eight months postoperatively. Chachques and colleagues5 attribute a principal role in the mechanism of lymph drainage restoration to the opening of physiologic lymphovenous anastomoses, while Kirpatovsky and colleagues4 believe that the formation of new lymphatic vessels is due to endothelial growth. Chachques et al. note that the course of postoperative lymphatic edema has a cyclic character, with four distinct periods: 1) stasis (first postoperative day); 2) lymph distribution through diffusion alone (up to the tenth postoperative day); 3) transition (up to the fifteenth postoperative day); and 4) restoration of lymphatic circulation (after the fifteenth postoperative day).
Department of Emergency Microsurgery, USSRAMS National Surgical Research Center, Moscow, USSR Reprint requests. Dr. Datiashvili, Dept of Emergency Microsurgery, National Research Center of Surgery, USSR Academy of Medical Science, Abrikosovsky 2, 119874 Moscow, USSR Accepted for publication April 17, 1990 Copyright© 1990 by Thieme Medical Publishers, Inc., 381 Park Avenue South, New York, NY 10016. All rights reserved.
325
OCTOBER 1990
MATERIALS AND METHODS
RESULTS
In our Emergency Microsurgery Service at the USSR National Surgical Research Center, between 1976 and 1989, we performed 171 major extremity replantations in 167 patients. Fourteen were at the shoulder level; four at the elbow joint; 90 in the forearm; 50 at the wrist; two in the thigh; and 11 in the shin. One hundred and twenty patients (71.9 percent) had extremely severe injuries—crushes, avulsions, and complex traumas consisting of combinations of avulsions and crush injuries. Zones of crushing extended up to 20 cm along the length of the extremity. Upper extremities were replanted in 16 cases, and the lower extremity in one case (Table 1). The patients ranged in age from 15 to 50 years. Two of them had incomplete and 15 had complete traumatic amputations. During surgery, the limb was debrided of all nonviable structures and shortened according to the required amount of excised soft tissue. The maximum shortening was 20 cm for the upper extremity and 17 cm for the lower. Thus, these replantations significantly disturbed normal anatomic structures, including the lymphatic vessels. To define the mechanisms involved in lymph drainage recovery, we performed lymphographies in 17 patients at various time periods after replantation. Lymphographies were generally performed between one month and 2.5 years after replantations. In one patient, the procedure was performed twice, at one and 5.5 months after surgery. The lymphatic vessels were isolated through small (1.0 to 1.5 cm) incisions on the dorsal wrist or foot; 3 to 5 ml of water-soluble contrast material (50 percent verographine solution) were introduced, followed by roentgenography or electroroentgenography of the extremity under x-ray and TV control.
Twelve patients showed recovery of major lymph drainage in the replanted limbs. Among four patients examined in the earliest postoperative period (four to six weeks), contrast material in the lymphatic collecting vessels above the level of replantation was found at two to 43 days and at 48 days, respectively, after replantation at the wrist-joint level. At longer postoperative periods, lymphatic collecting vessels above the replantation level were not filled in two patients: in one, at 3.5 months after replantation at the shoulder and in the other, at 7.5 months after replantation at the middle third of the forearm. In two cases, lymphography was not possible because of thinning of the lymphatic vessels in the dorsal wrist. A comparative analysis of the lymphography data showed that, in the early post-replantation periods, lymphatic vessels distal to the level of tissue connection revealed hypertension, manifested by dilated vessel lumens, crimped vessels, and accelerated perivascular diffusion of contrast material. Lymph diffusion from the distal part of ruptured collecting vessels formed sacciform lacunae in the replantation zone, and further diffusion progressed to the proximal collecting vessel end. On lymphograms, the lymphatic neovessels appeared crimped and dilated, compared to normal, and had unusual forms, e.g., sacculation (Fig. 1), or vine-shaped (Fig. 2) or ball-shaped (Fig. 3) structures. With later postoperative examinations, the vessels were clearer and their lumens more contracted. However, the lumens of new lymphatic vessels still remained somewhat dilated over time (Figs. 4, 5). On lymphographic examination, restoration of the major lymphatic collecting vessels was observed, even in very shortened replanted limbs. For example, one of our female patients had her forearm shortened
Table 1.
Patient Distribution by Level of Extremity Replantation and Type of Injury Type of Injury
Level of Replantation
Cut
Laceration
Arm Forearm: Upper third Middle third Lower third Wrist joint Shin Total 326
*A combination of various injuries, mainly crush with avulsion.
Crush
Avulsion
Complex*
Total
4 4 5 1 17
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JOURNAL OF RECONSTRUCTIVE MICROSURGERY/VOLUME 6, NUMBER 4
Figure 1. Lymphogram of the right upper limb; a 44year-old patient, four-and-a-half months after hand replantation.
Figure 3. Lymphogram of the left upper limb; a 26year-old patient, five-and-a-half months after hand replantation; total shortening of the limb is 12 cm.
Figure 2. Lymphogram of the left upper limb; a 44year-old patient, 43 days after hand replantation; total shortening of the limb is 7 cm.
Figure 4. Electroroentgenolymphogram of the left upper limb; a 44-year-old patient, seven months after hand replantation.
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RESTORATION OF LYMPH DRAINAGE/DATIASHVILI, LEIN
327
Figure 5. Lymphogram of the right upper limb; a 21year-old patient, two years after replantation at the lower third forearm.
by 12 cm (see Fig. 3) and, in another patient, the shin was shortened by 17 cm (Fig. 6).
DISCUSSION
328
In major replantations, one of the characteristic sequela of unrestored lymphatic vessels in the postoperative clinical picture, is edema of the replanted limb. We categorize the following components in the pathogenesis of post-replantation edemas: post-traumatic, postanoxic, venous, lymphatic, and inflammatory. Each of these components has specific characteristics, permitting judgement about the degree of predominance in each particular case. For example, edema of the replanted segment will be most manifest with a lymphatic component, while predominance of a traumatic component will result in acutely edematous segments above the replantation line. Inflammatory edemas are characterized by skin hyperemia and tissue infiltration, especially around sutures. Over time, replanted limb edemas will regress and disappear. In our observations, the time needed for resolution of edemas depends on three main factors: the quality of postoperative wound healing; the age; and individual patient characteristics. With an uneventful postoperative period and primary wound healing,
OCTOBER 1990
Figure 6. Lymphogram of the right lower limb; a 16year-old patient, one-and-a-half years after foot replantation; total shortening of the limb is 17 cm.
edemas of replanted segments disappear as early as four to six weeks. In contrast, with secondary wound healing and the formation of extensive rough postoperative scarring, limb edemas persist for three to five months and longer. In young patients, especially pediatric cases, edemas disappear much faster than in patients in the 45- to 50-year range. This is evidently due to different degrees of regeneration and compensation, such as the opening of physiologic lymphovenous anastomoses, and would explain the wide variations in the recovery of lymphatic circulation in replanted limbs. The compensatory and adaptive postoperative changes in the lymphatic system lead to a relatively rapid recovery (within four to six weeks) and restoration of lymphatic drainage in the replanted limb. The main mechanism of recovery is regeneration of lymphatic collecting vessels in the limb. Adequate lymphatic drainage through the major collecting vessels begins about five to eight weeks after replantation. Comparisons of clinical lymphographic data confirm the conclusions of experimental studies regarding the role of lymphatic neovessels of the skin in restoring lymphatic drainage in replanted limbs,4 especially in the early postoperative period. According to our observations, the appearance of contrast material in the major lymphatic vessels is practically a guarantee of the absence of edema in the replanted limb. However,
Downloaded by: National University of Singapore. Copyrighted material.
JOURNAL OF RECONSTRUCTIVE MICROSURGERY/VOLUME 6, NUMBER 4
RESTORATION OF LYMPH DRAINAGE/DATIASHVILI, LEIN
SUMMARY Clinical observations and lymphographic data showed that patients with major extremity replanta-
tions sustain compensatory and adaptive structural changes of the lymphatic system, despite complete disruption. Regeneration first affects the cutaneous and then the collecting lymphatic vessels. Such changes lead to a relatively rapid recovery four to six weeks after surgery, and to subsequent compensation of lymph drainage in the replanted limb. The rate and extent of the compensation depend on the adequacy of debridement, with excision of nonviable tissues at the time of replantation, as well as on the age and characteristics of individual patients.
REFERENCES Chepelenko GV: Lymphography in diagnostics of post-traumatic acute and chronic lymph drainage disorders. Vestnik khirurguii 4:78, 1985 (in Russian). Tamai S, Hori Y, Tatsumi, et a\.\ Major limb, hand and digital replantations. World I Surg 3:17, 1979. Lapchinsky AG, Sedov W, Medvedeva GV, Tarasov NF: Restoration of lymph circulation after extremity replantations in dogs. In TransplantatsiyaOrganoviTkanei, ed I, vol 42. Moscow, 1965, pp 75-86 (in Russian). Kirpatovsky ID, Satyukova GS, Kiprensky YV: Some characteristics of blood and lymph circulation recovery in replanted limbs and modelling of such replantations in experiments. In Peresadka Konechnostei, Moscow, 1973, pp 38-46 (in Russian). Chachques JC, Mitz V, de Vernejoul P, et a\:. Etude experimental de la circulation lymphatique apres reimplantation de membres. Ann Chir Plast Esthet 28:195, 1983
329
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in some patients, despite recovery of major lymphatic drainage confirmed by lymphography, edema persisted, especially in cases of rough scarring of the skin in the replantation zone, i.e., an unfavorable condition for regeneration of cutaneous lymphatic vessels. An adequate excision of nonviable tissue at the time of replantation is of paramount importance for a full-scale recovery of lymphatic drainage in the replanted limb. We believe that the apposition of viableto-viable tissue creates optimal conditions for the regeneration of both cutaneous and collecting lymph vessels. This is demonstrated especially by observations of extensive shortening of up to 17 cm in the replanted extremities where, despite significant disturbances of normal anatomic structures and proportions, we noted lymphographic recovery of the major lymphatic vessels and full restoration of lymphatic drainage. Lymphographs of patients examined at relatively long periods after surgery (showing the distinct outline of new lymphatic vessels and their rather narrow lumens) allow statements to be made in clinical cases about a true anatomic restoration of such vessels, with formation of vascular wall elements.
RESTORATION OF LYMPH DRAINAGE AFTER EXTREMITY
Downloaded by: National University of Singapore. Copyrighted material.
REPLANTATION ABSTRACT A clinical analysis of 171 major extremity replantations was carried out. From one month to 2.5 years after surgery, direct lymphographic studies of replanted limbs were done in 17 patients (16 upper limbs and one lower limb). Despite a complete disruption of lymphatic drainage, replanted limbs underwent adaptive and compensatory structural changes of the lymphatic system in the post-replantation period; first, with regeneration of cutaneous vessels and then (after six to eight weeks postoperatively) with regeneration of lymphatic collecting vessels. Such changes led to improvement as early as four to six weeks postoperatively and subsequently to restoration of lymphatic drainage in the replanted limb. The rate and extent of lymphatic recovery depends largely on the surgical techniques used in replantation.
Although more than 20 years have passed since the first successful salvage of a complete limb amputation, it is still generally accepted that many problems remain in major extremity replantations. Replantation aims at restoring practically all anatomic and functional structures in an amputated limb: bony skeleton, arteries, veins, muscles, and nerves. However, in the course of extremity replantation, lymphatic vessels are not restored. The role of lymph circulation in normal organ and systemic activity and function is well known. Lymphographic studies have shown that the main reason for post-traumatic lower limb edema, often persisting for up to three to eight years in a very acute form, is transport disorder of major and smaller lymphatic vessels.1 Certainly, few lymph vessels are damaged by ordinary injury, while amputations completely disrupt lymphatic drainage. Important questions are: What sort of lymph circulation disorders take place after replantation? Can lymphatic drainage be restored in replanted limbs, and what are its mechanisms? The literature offers limited reports concerning these questions. Nevertheless, some previous experimental studies are interesting. Lapchinsky et al.,3 Kirpatovsky and colleagues,4 and Chachques et al.5 have studied the mechanisms of lymph drainage restora-
tion in various experimental models, including dogs, rabbits, and rats. Indirect and direct lymphography have been used, as well as radioisotope and histologic techniques. The general consensus is that, following replantation, the lymphatic system in the extremities undergoes structural changes, in particular, the development of a superficial lymphatic network that contributes to the gradual stabilization of lymphatic drainage and the disappearance of edema as early as one month after surgery. A deeper network of lymphatic vessels begins to form between four and eight months postoperatively. Chachques and colleagues5 attribute a principal role in the mechanism of lymph drainage restoration to the opening of physiologic lymphovenous anastomoses, while Kirpatovsky and colleagues4 believe that the formation of new lymphatic vessels is due to endothelial growth. Chachques et al. note that the course of postoperative lymphatic edema has a cyclic character, with four distinct periods: 1) stasis (first postoperative day); 2) lymph distribution through diffusion alone (up to the tenth postoperative day); 3) transition (up to the fifteenth postoperative day); and 4) restoration of lymphatic circulation (after the fifteenth postoperative day).
Department of Emergency Microsurgery, USSRAMS National Surgical Research Center, Moscow, USSR Reprint requests. Dr. Datiashvili, Dept of Emergency Microsurgery, National Research Center of Surgery, USSR Academy of Medical Science, Abrikosovsky 2, 119874 Moscow, USSR Accepted for publication April 17, 1990 Copyright© 1990 by Thieme Medical Publishers, Inc., 381 Park Avenue South, New York, NY 10016. All rights reserved.
325
OCTOBER 1990
MATERIALS AND METHODS
RESULTS
In our Emergency Microsurgery Service at the USSR National Surgical Research Center, between 1976 and 1989, we performed 171 major extremity replantations in 167 patients. Fourteen were at the shoulder level; four at the elbow joint; 90 in the forearm; 50 at the wrist; two in the thigh; and 11 in the shin. One hundred and twenty patients (71.9 percent) had extremely severe injuries—crushes, avulsions, and complex traumas consisting of combinations of avulsions and crush injuries. Zones of crushing extended up to 20 cm along the length of the extremity. Upper extremities were replanted in 16 cases, and the lower extremity in one case (Table 1). The patients ranged in age from 15 to 50 years. Two of them had incomplete and 15 had complete traumatic amputations. During surgery, the limb was debrided of all nonviable structures and shortened according to the required amount of excised soft tissue. The maximum shortening was 20 cm for the upper extremity and 17 cm for the lower. Thus, these replantations significantly disturbed normal anatomic structures, including the lymphatic vessels. To define the mechanisms involved in lymph drainage recovery, we performed lymphographies in 17 patients at various time periods after replantation. Lymphographies were generally performed between one month and 2.5 years after replantations. In one patient, the procedure was performed twice, at one and 5.5 months after surgery. The lymphatic vessels were isolated through small (1.0 to 1.5 cm) incisions on the dorsal wrist or foot; 3 to 5 ml of water-soluble contrast material (50 percent verographine solution) were introduced, followed by roentgenography or electroroentgenography of the extremity under x-ray and TV control.
Twelve patients showed recovery of major lymph drainage in the replanted limbs. Among four patients examined in the earliest postoperative period (four to six weeks), contrast material in the lymphatic collecting vessels above the level of replantation was found at two to 43 days and at 48 days, respectively, after replantation at the wrist-joint level. At longer postoperative periods, lymphatic collecting vessels above the replantation level were not filled in two patients: in one, at 3.5 months after replantation at the shoulder and in the other, at 7.5 months after replantation at the middle third of the forearm. In two cases, lymphography was not possible because of thinning of the lymphatic vessels in the dorsal wrist. A comparative analysis of the lymphography data showed that, in the early post-replantation periods, lymphatic vessels distal to the level of tissue connection revealed hypertension, manifested by dilated vessel lumens, crimped vessels, and accelerated perivascular diffusion of contrast material. Lymph diffusion from the distal part of ruptured collecting vessels formed sacciform lacunae in the replantation zone, and further diffusion progressed to the proximal collecting vessel end. On lymphograms, the lymphatic neovessels appeared crimped and dilated, compared to normal, and had unusual forms, e.g., sacculation (Fig. 1), or vine-shaped (Fig. 2) or ball-shaped (Fig. 3) structures. With later postoperative examinations, the vessels were clearer and their lumens more contracted. However, the lumens of new lymphatic vessels still remained somewhat dilated over time (Figs. 4, 5). On lymphographic examination, restoration of the major lymphatic collecting vessels was observed, even in very shortened replanted limbs. For example, one of our female patients had her forearm shortened
Table 1.
Patient Distribution by Level of Extremity Replantation and Type of Injury Type of Injury
Level of Replantation
Cut
Laceration
Arm Forearm: Upper third Middle third Lower third Wrist joint Shin Total 326
*A combination of various injuries, mainly crush with avulsion.
Crush
Avulsion
Complex*
Total
4 4 5 1 17
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JOURNAL OF RECONSTRUCTIVE MICROSURGERY/VOLUME 6, NUMBER 4
Figure 1. Lymphogram of the right upper limb; a 44year-old patient, four-and-a-half months after hand replantation.
Figure 3. Lymphogram of the left upper limb; a 26year-old patient, five-and-a-half months after hand replantation; total shortening of the limb is 12 cm.
Figure 2. Lymphogram of the left upper limb; a 44year-old patient, 43 days after hand replantation; total shortening of the limb is 7 cm.
Figure 4. Electroroentgenolymphogram of the left upper limb; a 44-year-old patient, seven months after hand replantation.
Downloaded by: National University of Singapore. Copyrighted material.
RESTORATION OF LYMPH DRAINAGE/DATIASHVILI, LEIN
327
Figure 5. Lymphogram of the right upper limb; a 21year-old patient, two years after replantation at the lower third forearm.
by 12 cm (see Fig. 3) and, in another patient, the shin was shortened by 17 cm (Fig. 6).
DISCUSSION
328
In major replantations, one of the characteristic sequela of unrestored lymphatic vessels in the postoperative clinical picture, is edema of the replanted limb. We categorize the following components in the pathogenesis of post-replantation edemas: post-traumatic, postanoxic, venous, lymphatic, and inflammatory. Each of these components has specific characteristics, permitting judgement about the degree of predominance in each particular case. For example, edema of the replanted segment will be most manifest with a lymphatic component, while predominance of a traumatic component will result in acutely edematous segments above the replantation line. Inflammatory edemas are characterized by skin hyperemia and tissue infiltration, especially around sutures. Over time, replanted limb edemas will regress and disappear. In our observations, the time needed for resolution of edemas depends on three main factors: the quality of postoperative wound healing; the age; and individual patient characteristics. With an uneventful postoperative period and primary wound healing,
OCTOBER 1990
Figure 6. Lymphogram of the right lower limb; a 16year-old patient, one-and-a-half years after foot replantation; total shortening of the limb is 17 cm.
edemas of replanted segments disappear as early as four to six weeks. In contrast, with secondary wound healing and the formation of extensive rough postoperative scarring, limb edemas persist for three to five months and longer. In young patients, especially pediatric cases, edemas disappear much faster than in patients in the 45- to 50-year range. This is evidently due to different degrees of regeneration and compensation, such as the opening of physiologic lymphovenous anastomoses, and would explain the wide variations in the recovery of lymphatic circulation in replanted limbs. The compensatory and adaptive postoperative changes in the lymphatic system lead to a relatively rapid recovery (within four to six weeks) and restoration of lymphatic drainage in the replanted limb. The main mechanism of recovery is regeneration of lymphatic collecting vessels in the limb. Adequate lymphatic drainage through the major collecting vessels begins about five to eight weeks after replantation. Comparisons of clinical lymphographic data confirm the conclusions of experimental studies regarding the role of lymphatic neovessels of the skin in restoring lymphatic drainage in replanted limbs,4 especially in the early postoperative period. According to our observations, the appearance of contrast material in the major lymphatic vessels is practically a guarantee of the absence of edema in the replanted limb. However,
Downloaded by: National University of Singapore. Copyrighted material.
JOURNAL OF RECONSTRUCTIVE MICROSURGERY/VOLUME 6, NUMBER 4
RESTORATION OF LYMPH DRAINAGE/DATIASHVILI, LEIN
SUMMARY Clinical observations and lymphographic data showed that patients with major extremity replanta-
tions sustain compensatory and adaptive structural changes of the lymphatic system, despite complete disruption. Regeneration first affects the cutaneous and then the collecting lymphatic vessels. Such changes lead to a relatively rapid recovery four to six weeks after surgery, and to subsequent compensation of lymph drainage in the replanted limb. The rate and extent of the compensation depend on the adequacy of debridement, with excision of nonviable tissues at the time of replantation, as well as on the age and characteristics of individual patients.
REFERENCES Chepelenko GV: Lymphography in diagnostics of post-traumatic acute and chronic lymph drainage disorders. Vestnik khirurguii 4:78, 1985 (in Russian). Tamai S, Hori Y, Tatsumi, et a\.\ Major limb, hand and digital replantations. World I Surg 3:17, 1979. Lapchinsky AG, Sedov W, Medvedeva GV, Tarasov NF: Restoration of lymph circulation after extremity replantations in dogs. In TransplantatsiyaOrganoviTkanei, ed I, vol 42. Moscow, 1965, pp 75-86 (in Russian). Kirpatovsky ID, Satyukova GS, Kiprensky YV: Some characteristics of blood and lymph circulation recovery in replanted limbs and modelling of such replantations in experiments. In Peresadka Konechnostei, Moscow, 1973, pp 38-46 (in Russian). Chachques JC, Mitz V, de Vernejoul P, et a\:. Etude experimental de la circulation lymphatique apres reimplantation de membres. Ann Chir Plast Esthet 28:195, 1983
329
Downloaded by: National University of Singapore. Copyrighted material.
in some patients, despite recovery of major lymphatic drainage confirmed by lymphography, edema persisted, especially in cases of rough scarring of the skin in the replantation zone, i.e., an unfavorable condition for regeneration of cutaneous lymphatic vessels. An adequate excision of nonviable tissue at the time of replantation is of paramount importance for a full-scale recovery of lymphatic drainage in the replanted limb. We believe that the apposition of viableto-viable tissue creates optimal conditions for the regeneration of both cutaneous and collecting lymph vessels. This is demonstrated especially by observations of extensive shortening of up to 17 cm in the replanted extremities where, despite significant disturbances of normal anatomic structures and proportions, we noted lymphographic recovery of the major lymphatic vessels and full restoration of lymphatic drainage. Lymphographs of patients examined at relatively long periods after surgery (showing the distinct outline of new lymphatic vessels and their rather narrow lumens) allow statements to be made in clinical cases about a true anatomic restoration of such vessels, with formation of vascular wall elements.
