Microsurgical lymphovenous treatment of lymphedema" A. anastomosis for critical review PATIENTS

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1 Microsurgical lymphovenous treatment of lymphedema" A anastomosis for critical review Peter Gloviczki, M.D., Jack Fisher, M.D., Larry H. Hollier, M.D., Peter C. Pairolero, M.D., Alexander Schirger, M.D., and Heinz W. Wahner, M.D., Rochester, Minn. Lymphovenous anastomoses (LVA) offer ideal physiologic treatment for lymphedema, and our experimental data support late patency. Between Jan. 1, 1982, and.april 1, 1986, 18 patients underwent operation for chronic lymphedema; LVA could be performed in 14 patients (10 women and four men). Six patients had secondary lymphedema of the upper extremity. One of eight patients with lymphedema of the lower extremity had filariasis, and seven had primary lymphedema. Mean follow-up was 36.6 months (range: 5 to 57 months). Limb drcmnference and volume, number of postoperative episodes of cellulitis, and lymphoscintigraphy were used to assess results. Improvement occurred in three upper extremities and two lower extremities. There was no change in five extremities, and in four patients the edema progressed. One patient with primary lymphedema and four of seven patients with secondary lymphedema improved. Only one of five patients benefited from one anastomosis; however, all patients with more than two anastomoses improved. Lymphoscintigraphy was performed in 10 patients. No lymphatic channel was visualized before operation in three patients, and at operation none was fi~und. In four other patients lymph channels localized by lymphoscintigraphy were identified during operation. Significant improvement was docmnented by lymphoscintigraphy in one patient after operation, and this patient had permanent improvement 30 months later. Patients with primary lymphedema had disappointing results, but four of :seven patients with secondary lymphedema benefited from LVA, especially if several anastomoses could be performed. Lymphoscintigraphy appears to be a suitable method of both identifying patent lymph channels before surgery and determining fimction of LVA afi:er operation. However, presently objective data to prove the clinical efficacy of this operation are lacking. (J Vase SURG 1988;7: ) The large variety of operations that have been suggcsted to treat lymphedcma serve as testimony of our frustration to deal with this difficult clinical problem. Improvement in microsurgical technique has allowed lymph nodes or lymph vessels to be anastomosed to veins and transplantation of lymph vessels to improve lymphatic transport of the extremity. 1-~ Direct lymphovenous anastomoses (LVA) have been performed since 1969,1 but clinical results have bccn inconsistent. Either the follow-up period has been short or concomitant excisional operations have made evaluation of function of LVA difficult?,4's'9 Recent publications from China ~4,~s report unusually From the Sections of Vascular Surge U and Plastic and Reconstructive Surgery, the Department of Surgery, the Division of Cardiovascular Diseases and Internal Medicine, and the Department of Laboratory Medicine, Mayo Clinic and Mayo Foundation. Presented at the Eleventh Annual Meeting of the Midwestern Vascular Surgical Society, Chicago, Ill., Sept , Reprint requests: Peter Gloviczki, M.D., Section of Vascular Surgery, Mayo Clinic, 200 1st Street S.W., Rochester, MN good results, with improvement in more than 70% of patients as long as 4.5 years after operation. Encouraged by these clinical reports and the results of our previous experimental work, 2,I6 we undertook a clinical study to evaluate the effectiveness of this operation and determine if lymphoscintigraplay was effective in judging patcncy and function of LVA. PATIENTS Between Jan. 1, 198;2, and April 1, 1986, LVA was attempted in 18 patients with chronic lymphedema of the extremity. In four patients exploration only was performed, since patent lymph vessels could not be found for anastomosis. In 14 patients (10 women and four men), successful LVA could be performed. Six of these 14 patients (five women and one man) had secondat T lymphedema of the upper extremity. The mean age of the patients who had upper extremity lymphedema was 54 years (range 42 to 67 years). All female patients had lymphedema 647

2 648 Gloviczki et al. Journal of VASCULAR (- v~n f!j f Cephalic " ---~ /~y ~ / Basilta vein saphenous~ ~,Median cubita~ Vei~ Fig. 1. Incision sires used on the upper (A) and lower (B) extremid, to anastomose lymph vessels to superficial veins. after mastectomy, whereas the one male patient had previous axillat3/lymph node dissection and radiation treatment for Hodgkin's disease. The median duration of lymphedema in these patients was 4.5 years (range 1.5 to 10 years). Eight patients (three men and five women) had lymphedema of the lower extremity with a median duration of edema of 6 years (range 2 to 25 years). Six patients had lymphedema praecox, one patient had prima U lymphedema tarda, and one patient had filariasis. The follow-up was complete in all patients and ranged from 5 to 57 months (mean 46.2 months). M1 patients who underwent operations had failed medical management that consisted of prolonged periods of intermittent compression with pneumatic pumps and elastic support. Preoperative evaluation of the lymphatic system included lymphoscintigraphy in eight patients and contrast lymphangiography in three. The venous circulation was evaluated with Doppler measurements, plethysmography, and contrast venography (five patients). In selected patients CT scanning was done to exclude malignancy. Limb circumference and volume, the number of postoperative episodes ofcellulitis, and lymphoscintigraphy (four patients) were used to assess results. Since lymphedema may cause pain and significant disabiliw with emotional, cosmetic, and social problems, patient satisfaction was also evaluated. Circumferential measurements were obtained on the upper extremity at the level of the wrist, the forearm (10 cm distal to the olecranon process), and the arm (10 cm proximal to the olecranon process). On the lower extremity, the ankle, calf (10 cm distal to the patella), and thigh (10 cm proximal to the patella) were measured. Limb!volume was measured on the upper extremity by means of the water displacement method as described by Stillwell. 17 To evaluate the differences in volume or in circumference, percentage decrease oflymphedema was calculated according to the method of Raines et al. t8 The following formula was Used: Decrease = preop - postop measurement 100 preop - contralateral normal limb measurement The method of lymphoscintigraphy, which was performed with technetium 99m-labeled antimony sulfur colloid, has been previously described by us."9

3 Volume 7 Number 5 Ma x, 1988 Microsurgical lymphovenous anastomosis 649 Table I. Results of lymphovenous anastomosis operations in 14 patients with lymphedema Extremity Type of edema Result Duration Age of edema No. of No No. (yr) Sex Upper Lower Primary Secondary (yr) anastomoses Improved change Poor 1 57 F F M F F F ~ F F F F F M M M Imaging with a y-camera was performed immediately after injection and again at 1 and 3 hours. Quantitative lymphoscintigraphy was performed with an on-line computer, and the disappearance of the colloid from the injection site, appearance at inguinal or axillary lymph nodes, and accumulation in the liver were quantitated. The lymphedema was classified as improved if three of the following were present: a permanent decrease in edema and a reduction in the number of episodes of cellulitis, the edema became softer, or if the patient was satisfied with the result. There was no change if circumferential or volume measurements were unchanged (less than 10%) and the number of episodes of cellulitis did not decrease. The result was poor if edema increased and there were more episodes of cellulitis. Fisher's exact test and the Wilcoxon rank sum test were used for statistical analysis of the data. METHOD All operations were performed with thc patients under general anesthesia. Fig. 1 illustrates the sites of incisions used to explore lymph vessels and the subcutaneous veins. All anastomoses in this series of patients were performed between the superficial lymphatics and superficial veins. The most frequent incision in the upper extremity was a transverse skin incision at the level of the elbow crease, whereas the incision used most frequently in the lower extremity was just distal to the inguinal ligament on the medial aspect of the upper thigh. If several anastomoses could be performed in this area, no further skin incisions were made. However, if patent usable lymph vessels could not be found, then an additional inci- sion was made at the medial aspect of the upper arm or in lymphedema of the lower extremity, at the medial aspect of the calf[ In one patient, three anastomoses were performed just above the wrist. To visualize the lymph vessels, 2 to 4 ml of patent blue dye was injected after induction of anesthesia about 10 to 15 cm distal to the incision site subcutaneously. Careful dissection of the subcutaneous space was performed down to the level of the fascia, and all vascular structures, including small arteries, veins, and lymphatic channels, were identified and preserved. Clamps were not placed on the lymphatic vessels to avoid trauma, but the small veins were clamped if there was back flow of blood from the venous side. Heparin was used for local irrigation. End-to-end or end-to-side lymphovenous anastomoses were performed with a technique described in detail previously? 6 An operating microscope with five to 25 times magnification, 10-0 or 11-0 monofilament nonabsorbablc sutures, and atraumatic microvascular technique were used for the anastomosis. The diameter of lymph vessels ranged from 0.5 to 1.5 ram, whereas the sizes of the veins ranged from 2 to 4 mm. Four to 12 interrupted sutures were needed to perform a tension-free LVA. Continuous local heparin irrigation was used throughout thc procedure, and the adventitia of the lymph vessels was not stripped to carefully preserve nutrient blood supply to the lymph vessel wall. After completion of the anastomosis, the passage of lymph, which was stained with blue dye, was instantly observed under the operating microscope, If dye did not reach the area, the passage of dear lymph could be confirmed by the Acland 2 test. After completion of the procedure, the skin was dosed with subcuticular Vicryl stitches.

4 650 Gloviczki et al. journal of VASCULAR SURGERY E 50 O >2 E 40 ID Q. 30 o 20 O O E "-1 e ~ B-gA ~ 51 y.o. male I I I Wrist Forearm Arm Site of measurement Fig. 2. Changes in upper limb circumference in a 51-year-old man with secondary, lymphedema. Six lymphovenous anastomoses were performed. Excellent early and moderate late results 4 years later. Postoperative elastic compression, leg elevation, and intermittent pneumatic compressions were used to augment lymph flow through the anastomosis. RESULTS One to six LVAs could be performed in 14 patients. In one patient five anastomoses were performed during two different procedures. Table I demonstrates the results of the operations and suggests a correlation between clinical improvement and the number of anastomoses. Improvement occurred in three upper extremities and two lower extremities. There was no significant change in ~ve extremities, and in four the lymphedema progressed during the follow-up period. One patient with prima U lymphedema and four of seven patients with secondary lymphedema improved. However, the difference between the two groups was not significant (p = 0.26). Only one of five patients who had one LVA improved. In contrast, all four patients who had more than two anastomoses improved. The mean duration of preoperative lymphedema was 7.2 years in the patients who showed improvement and 15.7 years in those who had poor results (p = 0.50). Five of the 14 patients had recurrent episodes of cellulitis before operation. After operation cellulitis disappeared in four patients and was reduced in one. One patient who had no preoperative cellulitis developed it after operation (case 4). Patient 6 had several episodes for many years; she is now 4 years and 2 months after the operation and is free of cellulitis. Patient 1 had at least five documented episodes before surge U but none since the operation. Fig. 2 demonstrates changes in the circumference of the limb of a 51-year-old man (case 3) who had axillary lymph node dissection and radiation therapy for Hodgkin's lymphoma. Calculated percentage decrease in edema at the wrist level was 92% immediately after operation and 81% at 4 years. When measured at the forearm level, the initial decrease was 72%, but was only 23% at 4 years. Fig. 3 demonstrated excellent result at 3 months in a 55-year-old man who had positive serologic findings for filariasis (case 7). Although his lymphedema decreased from a 77% improvement at 3 months to only 31% at 1 year, he continues to have a good result. Lymphoscintigraphy was performed on 10 patients--eight before operation and four after operation. In four patients the lymph channels, which were localized by lymphoscintigram before operation, were identified during the operation. In three patients no lymph channels were visualized before operation, and at exploration, no lymph vessel could be identified. In the four patients who had postoperative lymphoscintigraphy, this test documented significant improvement 1 month after surgery with continued permanent clinical improvement at 30 months (case 9). Two of the remaining patients had no change, and the last patient had a poor result.

5 Volume 7 Number 5 May 1988 Microsu,aical Iymphovenous anastomosis 651 Fig. 3. A, A 55-year-old man with lymphedema of the right lower extremity caused by filariasis. Four lymphovenous anastomoses were performed at the medial aspect of the upper thigh. B, Excellent results 3 months after operation. The result of lymphoscintigraphy correlated well with the clinical findings in all patients who had this study. DISCUSSION Lymphcdcma is a chronic, progressive condition that develops if the lymphatic load exceeds the transport capacity of the lymphatic system. In its early phase (grade 1) the lymphedema is entirely reversible. 21 Restoring normal lymphatic transport at this time could cure the disease. As lymphedema progresses, irreversible changes occur as a result of tissue fibrosis, chronic interstitial inflammation, and a poor proteolytic and phagocytic function of the macrophages (grade 2). Reconstitution of normal lymphatic transport in grade 2 disease may theoretically give relief but not cure. Repeated episodes of inflammation and fibrosis eventually destroy the collecting lymphatic channels, thereby making microsurgical treatment impossible. Therefore, it appears that the most favorable anatomic conditions of the lymphatics are present at the early stage of the disease. Unfortunately, it also means that the more significant the lymphedema, the less the chances are that restoration of the canalicular function of the lymphatic system will result in reversal of changes in the tissues. In our study patients with primary lymphedema had disappointing results. We could demonstrate improvement in only one patient who had patent lymph vessels up to the groin ]but who had proximal occlusion at the aortoiliac level. A good result was obtained in one patient who had filariasis. Other authors 1 'rid4 have noted similarly good rcsuks in patients with this disease. Three of six patients with secondary lymphedema of the upper extremity showed long-term improvement. It appears, as predicted by othcrs, 3'4a4 that the number of anastomoses correlates well with the outcome of the procedure. All patients who showed striking initial improvement after the operation had some recurrence of lymphedema, even if the degree of swelling was less than before the opcration. This confirms the findings of Puckett et al., s who demonstrated that with time, lymphatic pressure decreases and flow diminishes through the anastomosis in chronic lymphedema. Our results are less impressive than those published by our Chinese colleagues. 14,1s One of the reasons is that the etiology was different. In the study of Huang Gong-Kang et al. ~4 50% of the paticnts had filariasis. In our group we had only one such patient. Despite favorable results published in the literature, s'4,8,9,14ds further mddence is needed to support

6 652 Gloviczki et al. Journal of VASCULAR SURGERY this operation. Circumferential and volume measurements are not always reliable, and because of the nature of the disease, some of the data used to evaluate the outcome are subjective. Most authors are reluctant to perform postoperative lymphangiograms because of concern that pulmonary, embolization of the oily contrast media Occurs. At this points despite promising results that were obtained with lympho: scintigraphy, objective evidence of the patency of LVA could not be demonstrated: Therefore, although we believe that the operation has value in selected patients with obstructive secondary lymphedema, clinical evidence to prove the effectiveness of this procedure is still lacking. REFERENCES 1. Yamada Y. The studies on lymphatic venous anastomosis in lymphedema. Nagoya J Med Sci 1969;32: Gloviczki P, LeFloch P, Hidden G. Anastomoses lymphaticoveineuses experimentales. J Chir (Paris) 1979;116: , O'Brien BM, Chair LA, Hurwitz pj. Microlymphatic surgery. Orthop Clin North Am 1977;8: O'Brien BMcC, Shafiroff BB. Microlymphaticovenous and resectional surgery in obstructive lymphedema. World J Surg 1979;3: Puckett CL, Jacobs GR, Hurvitz JS, Silver D. Evaluation of lymphovenous anastomoses in obstructive lymphedema. Plast Reconstr Surg 1980;66: , Olszewski WL. Physiology, and microsurgen, of lymphatic vessels in man. Lymphology 1981;14: Clodius L, Piller NB, Casley-Smith JR. The problems of lymphatic microsurgery for lymphedema. Lympholog T 1981; 14: Krylov V, Milanov N, Abalmasov K. Microlymphatic surgery, of secondary lymphoedema of the upper limb. Ann Chir Gynaecnl 1982;71: Nieuborg L. The role of lymphaticovenous anastomoses in the treatment of postmastectomy oedcma. Offsetdruk, kerij Kanters BV. Alblasserdam: Jamat S. Indications and success of surgical approaches to filarial elephantiasis. Lymphology 1985v18:164.! I. Dandapat MC, Mohapatro SK, Mohant T SS. Fitarial lymphoedema and elephantiasis of lower limb: a review of 44 cases. J Surg 1986:74: Baumeister RG, Siuda S, Bohmert H. Moser E. A microsurgical method for reconstruction of interrupted lymphatic pathways: autologous lymph-vessd transplantation for treatment of lymphedemas. Scand J Plast Reconstr Surg 1986: 20: Campisi C. Tosatti E, Casaccia M, et al. Microchirurgla dei linfatici. Minerva Chir 1986:41: Huang Gong-Kang, Hu Ru-Qi, Liu Zong-Zhao, Shen Yao- Liang, Lan Tie-De, Pan Gong-Ping. Microlymphaticovenous anastomosis in the treatment of lower limb obstructive lymphedema: analvsis of 91 cases. Plast Reconstr Surg 1985: 76: Jia-Kai Zhu, Guo-Zhong Yu, Jun-~ Liu, Shui-Fa Pang, Zen- Guo Lao, Hai-Yun Tang. Recent advances in microlymphatic surgery in China. Clin Orthop 1987;215: Gloviczki P, Hollier LH, Nora FE, Kaye MP. The natural history of microsurgical lymphovenous anastomoses: an experimental study. J VASe SURG 1986;4: Stillwelt GK. Management of arm edema. In: Stoll BA, ed. London: Heinemann Medical, 1977: Raines JK, O'Connell TF Jr, Kalisher L, Darling RC. Selection of patients with lymphedema for compression therapy. Am J Surg 1977;133: Vaqueiro M, Gloviczki P, Fisher J, Hollier LH, Schirger A, Wahner HW. Lymphoscintigraphy in lymphedema: an aid to microsurgery. J Nud Med 1986;27: Acland R. Signs of patency in small vessel anastomosis. Surgery 1972;72: Casley-Smith JR, Foldi M, Ryan TJ, et al. Summary of the 10th International Congress of Lymphology Working Group discussions and recommendations, Adelaide, Australia, Aug , Lymphology 1985;18: