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J Vasc Surg Cases Innov Tech
J Vasc Surg Cases Innov Tech
Journal of Vascular Surgery Cases, Innovations and Techniques
2468-4287
Elsevier

S2468-4287(24)00148-5
10.1016/j.jvscit.2024.101564
101564
Editorial
A classic article that has never been read in English
Pappou Emmanouil MD, PhD a
Sorber Rebecca MD b
Reifsnyder Thomas MD treifsn1@jhmi.edu
c∗
a Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY
b Department of Surgery, University of WA School of Medicine, Seattle, WA
c Department of Vascular Surgery, Johns Hopkins School of Medicine Faculty, Baltimore, MD
∗ Correspondence: Thomas Reifsnyder, MD, Division of Vascular Surgery, Johns Hopkins Bayview Medical Center, 4940 Eastern Ave, Bayview Medical Offices, Level 03, Baltimore, MD 21224 treifsn1@jhmi.edu
03 7 2024
10 2024
03 7 2024
10 5 10156416 5 2024
31 5 2024
© 2024 The Author(s)
2024
https://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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pmcThe article “Le traitement de l'ischémie artérique par la greffe veineuse longue” or “Treatment of arterial ischemia by use of a long vein graft” written by the French vascular surgeon Jean Kunlin in 1951 is acknowledged as the first published series of lower extremity bypasses. Despite its seminal nature and frequent reference, no English translation has ever been made available, and even the original French language article is challenging to locate. This fascinating manuscript identifies many of the issues that limb salvage surgeons have continued to debate over the subsequent 60 years. Among their many astute observations, Kunlin et al noted that long bypasses do work; autogenous saphenous vein is an ideal conduit, although alternative autogenous vein may also be used; inflow and outflow arteries are unaffected if a vein bypass occludes; good outflow leads to better patency; angiography is necessary for operative planning; hyperemia of the foot accompanies successful revascularization; and small veins may work, but will be flow limiting. They describe myointimal hyperplasia of vein grafts and hypothesize that progression of atherosclerosis contributes to late bypass failure.

From a technical standpoint, the authors' description of an anastomosis varies little from today's standard. Although the article is somewhat dated, we felt that an English version publication was better late than never, because it makes for fascinating reading. Where possible, this translation uses contemporary language and the manuscript style has been modified to more closely resemble current publishing standards. Owing to space limitations, we have not included text, or tables that are repetitive, or included any angiograms owing to the inability to reproduce them legibly because of the age of the original article.

Treatment of arterial ischemia using a long vein graft

Kunlin J, Bitry-Boély C, Volnié, Beaudry, Leriche R.

Paris, France, 1951

In 1912, our division chief R. Leriche proposed that atherosclerotic occlusion of the lower extremity arteries could be bypassed with vein. In 1948, we finally undertook this project, and the problems we encountered came as no surprise. J. Goyanes was the first surgeon to successfully bypass a human artery in 1906 when he resected a popliteal artery aneurysm and replaced it with popliteal vein. In subsequent years, many have attempted to reproduce this feat, yielding a few isolated successes. However, lower extremity bypass has not yet become commonplace and in none of the successful cases has the bypass been longer than a few centimeters. Additionally, no one has attempted to use this procedure to remedy ischemia due to atherosclerotic peripheral arterial disease. The typical burden of atherosclerotic disease along with our poor understanding of its pathogenesis and natural history have prevented any attempts at surgical treatment.

The discovery and purification of heparin and warfarin have made the surgical treatment of vascular disease feasible. During thromboendarterectomy, as described by Juan Cid Dos Santos, not only are old thrombus and atherosclerotic plaque removed, but also a portion of the arterial wall. It seems more logical to replace the diseased vessel with autologous vein—a biologic conduit which would maintain its viability from the intraluminal arterial blood. Theoretically, it should be easier to maintain the patency of a transplanted vein that has intact endothelium than an endarterectomized vessel that has been denuded of its intima.

Several questions arose when we contemplated proceeding with lower extremity bypass using autologous vein: (1) Can atherosclerotic vessels hold suture? (2) If the bypass failed would thrombus propagate into the inflow or outflow vessels? (3) Would the compliance mismatch between the venous conduit and the artery lead to stenosis? With these concerns in mind, we performed our first lower extremity bypass.

Case report

A 54-year-old man presented with nocturnal rest pain and dry gangrene of his left foot. On examination he had a femoral pulse, but no distal pulses and his foot was edematous. Three years earlier he had undergone a lumbar sympathectomy followed by a femoral endarterectomy and amputation of his left great toe. His severe ischemic symptoms returned after about 2 years. Considering the failure of his previous procedures, leg amputation seemed unavoidable. As a final effort, the patient was offered the novel procedure of lower extremity bypass using saphenous vein. He was admitted to the hospital and underwent angiography which confirmed a superficial femoral artery occlusion with reconstitution of his popliteal artery. On June 3, 1948, the bypass was performed. The result was incredible: the leg became hyperemic with a palpable pedal pulse and the gangrenous wound healed in 2 weeks. The patient's nocturnal rest pain disappeared and he was able to walk without left leg claudication, subsequently unmasking short distance claudication in his right leg. He requested a bypass for that leg as well, which we performed with equally good results.

A retrospective report of the results of the first 17 lower extremity bypasses for the treatment of peripheral arterial disease

Surgical technique

Preoperative routine blood work includes a coagulation panel. Prophylactic antibiotics are administered particularly if there is an open wound on the leg. The patient is positioned supine on the operating room table with the affected limb in external rotation. The knee is slightly bent and supported by a sandbag, with the thigh abducted 20° to 25°. The operation begins by exposing the popliteal artery from a medial approach. Depending on the preoperative angiogram, either the above knee or the below knee portion is exposed. The tendons of the sartorius, gracilis, and semitendinosus muscles may be divided if necessary. Additionally, the medial head of the gastrocnemius muscle may be divided to enhance exposure of the vessel.

Once patency of the popliteal artery is confirmed, a vertical groin incision is made and the common femoral artery and saphenofemoral junction are dissected out. If the vein is adequate then the incision is extended distally and the vein harvested. It is wise to obtain several centimeters more than one is expected to need. When harvesting, carefully tie off the side branches flush with the vein. Once the vein is removed, irrigate with normal saline to confirm that there are no leaks. Since the vein tends to spasm when removed, it can be flushed or soaked in 1% procaine which tends to relax it.

Next the popliteal artery dissection is completed. Self-retaining retractors work nicely to maintain exposure. Double loop (Potts) all the side branches with catgut sutures and tighten slightly. Potts the popliteal artery with vessel loops both proximally and distally to the proposed site of the anastomosis. This not only helps lift the vessel out of its bed making the anastomosis easier to sew, but also obviates the need to clamp the vessel. Next, use a long vascular clamp or metal rod and make a tunnel either in the subcutaneous tissue or just deep to the sartorius muscle and pass the saphenous vein through this. Avoid any twisting of the vein as this may lead to thrombosis. Make sure the vein is reversed so the valves do not restrict flow. Tunneling is important for two reasons: (1) it keeps most of the vein out of the wound and (2) it places most of the vein in intimate contact with surrounding tissues allowing neovascularization of the vein wall, ensuring that it remains a living biologic conduit.

The distal anastomosis is performed first. The proximal end of the saphenous vein is spatulated for about 3 cm and sewn end-to-side to the popliteal artery (Fig 1). By performing the anastomosis end to side and keeping all the arterial branches intact, the original native arterial flow is maintained should the bypass thrombose. This is particularly true with an autogenous graft, as thrombus does not propagate into the outflow artery if the bypass occludes. Were the anastomosis end-to-end, the native arterial circulation would be rendered worse than preoperatively if the bypass thrombosed. Additionally, an end-to-end anastomosis creates a smaller connection between the two vessels (Figs 2 and 3).Fig 1 The popliteal artery with vessel loops controlling the artery and temporary ligatures on the arterial branches. The spatulated vein graft is already tunneled and ready to be anastomosed.

Fig 2 To spatulate the vein, cut along the dotted line, including a branch if possible.

Fig 3 Depiction of an end-to-side anastomosis with an enlarged lumen vs end-to-end, which is slightly stenosing.

Once the vessels are prepared for the anastomosis, a U-stitch is placed in the heel of the vein and then in the proximal end of the popliteal arteriotomy (Fig 4). Next, run the suture in a horizontal mattress fashion to the mid-point of the anastomosis (Fig 5). Now place a similar U-stitch into the toe of the vein and the distal end of the arteriotomy. Make sure the spatulated vein is pulled tight when placing the second suture otherwise the anastomosis will bleed. This suture then is run in a horizontal mattress fashion back to the middle of the anastomosis to meet the first suture. Make sure the suture bites are close together and approximate endothelium of the vein to endothelium of the artery. Before tying the first sutures start another layer of suture which is a simple baseball stitch oversewing the previously made suture line. Once all the suture has been placed, flush the vessel with normal saline and temporarily loosen the vessel loops to flush the artery. Now the suture can be tied and the anastomosis checked by flushing saline through the proximal end of the vein (Fig 6). All vessel loops are released and the vein graft gently clamped. The proximal or femoral anastomosis is now performed in a similar fashion. While working on the anastomosis, the tissues should be kept moist with saline.Fig 4 The heel and toe U sutures are placed at the start of the anastomosis.

Fig 5 The first layer of running horizontal mattress suture.

Fig 6 The completed two-layered anastomosis.

Although we prefer ipsilateral saphenous vein, it is not always available or adequate. In one case we used contralateral saphenous vein. If use of contralateral vein will be necessary, in order to save time during the bypass, we recommend harvesting the vein a few days earlier and refrigerating it. In addition to saphenous vein, femoral vein had to be used in one patient. In one case no saphenous vein was available and ipsilateral femoropopliteal vein was used. This cannot be recommended, as the patient has gone on to suffer severe and persistent postoperative edema. Lastly, in one patient we used a homograft. This graft was harvested a week before the procedure and refrigerated in a solution of normal saline and penicillin.

Five thousand units of heparin are administered at the beginning of the operation. Since we anticoagulate the patient postoperatively, the dissection is performed while fully anticoagulated in order to force meticulous hemostasis. The partial thromboplastin time (PTT) is checked throughout the procedure and heparin redosed appropriately. The PTT is kept two to three times normal. Although heparin can be administered in a variety of ways, we prefer a continuous drip: 3000 units in 500 mL of D5NS to run at 240 mL/hour or approximately 1500 units/hour. Additional heparin boluses may be given depending on the PTT, which should be checked hourly and every 2-3 hours once stable. Start oral warfarin on the night of surgery if possible or the next morning at a dose of 5 mg daily. Once the international normalized ratio is approaching or greater than 2, the heparin is stopped. All patients respond differently to heparin and warfarin, so the above are average doses and should be modified according to the individual's response.

Results

From June 1948 to October 1949, 17 lower extremity bypasses were performed varying in length from 15 to 52 cm. The configurations were as follows: common femoral to popliteal (n = 12), external iliac to popliteal (2), superficial femoral to popliteal (1), common iliac to popliteal (1), and common femoral to superficial femoral (1). Sixteen of the bypasses were constructed of autogenous vein and one was made of homograft. Two (12%) patients died: one on postoperative day 3 with a patent bypass and the other on postoperative day 11 secondary to an infected bypass that ruptured. Four patients had to be re-explored for bleeding. In three patients, small arterial branch bleeding was found and in one the distal anastomosis was bleeding. This anastomosis was performed with a single layer of suture; since we have started using a double layer technique, no anastomosis has bled. There were five (29%) early graft failures, two of which ruptured and three thrombosed. The two patients who survived ruptured bypasses included one hypertensive patient who returned 2 months postoperatively with a pseudoaneurysm at the distal anastomosis. On exploration the sutures had pulled through and torn the popliteal artery, requiring ligation of the bypass. The other ruptured graft was the patient in whom we used homograft. This conduit had a thin-walled varicosity, which was simply ligated at the time of implantation; on re-exploration this portion of the bypass had ruptured, requiring bypass ligation.

Three bypasses thrombosed in the early postoperative period. One thrombosed at the time of implantation due to lack of outflow. That patient had not had a preoperative angiogram and at the time of his above knee amputation was found to have a small thrombosed popliteal artery aneurysm. Another was an external iliac to popliteal bypass which thrombosed on postoperative day 3. His incision subsequently became infected and he underwent an above knee amputation a month later. He died a year later with gangrene of the contralateral leg secondary to Buerger's disease. The last thrombosis occurred on postoperative day 12 when the foot became cool and the bruit disappeared from the proximal anastomosis. This thrombosis was probably due to slow flow in this bypass which was 47 cm in length. Of the five surviving patients with early failure of their bypasses, two required above knee amputation and the other three returned to their preoperative degree of ischemia.

Ten patients were discharged with a patent bypass. Eight of the 10 had a palpable pulse in the foot. Since discharge, 3 of these 10 patients had thrombosis of their bypasses at an average time of 13.7 months (range, 7-18 months). In one case, angiography showed that the entire popliteal artery was occluded, so the patient had a sympathectomy. He can now slowly walk about 400 meters but has no rest pain. In another, angiography showed the above knee popliteal artery to be occluded, but the below knee popliteal artery to be patent. A redo bypass would have been possible, but because of wounds on his leg he underwent an above knee amputation roughly 6 months later. The third late bypass failure was a 33 cm long graft that occluded 7 months postoperatively leading to an above knee amputation. Of the seven successes, all but once are asymptomatic and have intact feet. One patient has a small (3 mm) bypass that is flow limiting and still claudicates at about 300 to 400 meters.

Pathophysiology of bypasses performed for chronic ischemia

After the bypass has been completed the foot becomes hyperemic. After several hours the pedal pulses become palpable. After several days the pulse is at its maximum and then regresses a bit. This phase likely corresponds to structural changes in the bypass wall from inflammation and neovascularization of the transplanted vein. In two patients, the foot cooled after a couple of days despite a patent bypass. Neither of these patients had a prior sympathectomy and we suspect vasoconstriction was the cause. We have not seen it in a patient with prior sympathectomy and with the institution of antispasmodic therapy no further instances have occurred.

A bruit is heard near the proximal anastomosis and extends several centimeters into the bypass. This bruit is loudest just after implantation and decreases with time as the vein adapts to becoming an arterial conduit. The bruit disappears over several months and also disappears with thrombosis of the graft. In one patient a subtle change in the bruit occurred a few days prior to thrombosis. In another patient with a 2-year-old bypass there was a bruit over the distal anastomosis which on arteriography was found to be aneurysmal.

The structural changes in an arterialized vein graft are known from experimental studies by Villard and Tavernier, by Carrel and Guthrie, and by Moure. Additionally, there have been clinical cases of graft placement after aneurysm resection that shed light on the structural changes in arterialized vein. During reoperations either for postoperative bleeding or impending thrombosis, we made some observations about vein grafts. The reversal of the initial vein spasm with local anesthetic leads to vein dilation that is complete after several hours; upon exploration for bleeding 5 hours postoperatively the vein was quite dilated. On postmortem exam, a bypass that had been in place for 50 hours was a dark red color and there was a perigraft hematoma although the vein wall remained smooth and intact. Examination of a vein graft 4 days after it had thrombosed showed the vein wall to be wine-stained, thickened and adherent to the surrounded tissue. The thrombus was densely adherent to the endothelium and the inflow and outflow arteries were patent. A month later at amputation, pathologic examination revealed a thrombus meniscus at the end of the vein graft in addition to multiple suture abscesses at the distal anastomosis which was destroying the vein wall. Lastly, a 16 month old bypass which had thrombosed 4 days earlier had the structure of an artery and the thrombus and neointima could be removed as in a standard thromboendarterectomy. Histology showed the classic picture of a well-incorporated bypass with arterialization of a vein graft with myointimal hyperplasia and thrombosis.

Angiography

Angiography is crucial to appropriate planning for lower extremity bypass for peripheral arterial disease. It is most important to confirm patency of the runoff vessels. After bypass the collateral circulation is less well visualized. This is certainly due to the histologic changes in collateral vessels as described by Leriche. One would think that the collateralization to the outflow vessel would be better visualized after bypass due to increased pressure in the vessel; however, we have not observed this. Angiograms performed after late thrombosis indicates that progression of disease is a major factor contributing to this complication. Graft thrombosis has never caused inflow artery obstruction. Lastly, after graft thrombosis the collateral circulation resumes it function and appears to be largely unchanged from before the bypass.

Ten patients had good runoff and all 10 had palpable pulses immediately postoperatively. Two had bypass complications requiring bypass ligation. Of the eight successes followed long term, two thrombosed late (16 and 18 months). In the seven patients with poor runoff, three thrombosed early, one died, and one had a bypass complication requiring ligation. None of these patients had palpable pedal pulses after their bypasses although two of them remained patent after discharge. One of these thrombosed at 7 months from the index operation.

Although the comparison of two different treatments in the same individual is not ideal since the disease burden may vary between extremities, some conclusions can be drawn. In one patient with bilateral superficial femoral artery occlusions, one leg was treated with a bypass and the other with lumbar sympathectomy. The bypassed leg has a normal foot and no claudication while the leg with the sympathectomy has a hot, dry foot and persistent claudication.

Discussion

This is the first published series of lower extremity bypasses and although small, some tentative conclusions can be made. The best indication for a leg bypass is complete occlusion of the femoral artery with reconstitution of the popliteal artery with good runoff. As shown by Leriche, these are the same patients that do well with atherectomy and sympathectomy. Considering our limited experience with lower extremity bypass and relatively short follow up, the gold standard for treatment of peripheral arterial disease should not change. However, if sympathectomy does not generate the desired result, then leg bypass should be considered.

What we have learned from this series is that bypasses of great length can remain patent and patients with good runoff fare better than those with distal disease. Additionally, we have learned diseased vessels hold suture well and do not tend to thrombose. From a technical standpoint we attribute our success to the use of an end to side spatulated anastomosis with everting sutures and intima-to-intima apposition. The ability to anticoagulate also clearly helped. One probably does not need to be as aggressive with anticoagulation as in this series, but currently no one has enough experience to determine the appropriate dose to prevent thrombosis while still limiting bleeding.

One of the most significant problems we encountered was finding suitable vein to use as a conduit for bypass grafting. Frequently veins were found to be varicose or sclerotic, causing us to abandon the operation for lack of suitable vein in three cases. Femoral or common femoral vein may be utilized if an additional short segment of vein is needed. Homografts may be a good solution since size matching of the graft would be superior; however, homografts with or without immunosuppression have not yet been shown to have patency equivalent to autogenous vein. If adequacy of homograft patency can be demonstrated in the future, then the creation of “vein banks” would make lower extremity bypass an easier and more successful operation. There may be other limb salvage applications for lower extremity bypass: limb conservation after tumor resection and bypassing traumatic wounds through an extra-anatomic pathway.

This small series demonstrates the feasibility of using vein to bypass occluded lower extremity arteries. Due to the small size of this series, it is difficult to predict the future role of lower extremity bypass in treating peripheral arterial disease. The immediate results are quite gratifying, but because of myointimal hyperplasia and progression of underlying disease, late occlusions are always possible. It is important to remember that atherosclerosis is not cured by this procedure: the bypass is only a palliative intervention designed to ameliorate the lower extremity ischemia.

Disclosures

None.

The editors and reviewers of this article have no relevant financial relationships to disclose per the Journal policy that requires reviewers to decline review of any manuscript for which they may have a conflict of interest.
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Further readings

1. Leriche B. Kunlin J. Possibilite de greffe veineuse de grande dimension (15 a 47 cm) dans les thromboses arthrielles etendues C B Seances Acad des Sci 227 1948 939 940
2. Kunlin J. Le traitement de l’arterite obliterante par la greffe veineuse Arch Malad Coeur 3 1949 371
3. Arnulf G. Chirurgie arterielie, Monographie 1950 Masson
4. Fontaine R. Ilubinont J. Buck P. Rivaux B.R. Kim M. Le traitesnent des obliterlations arterielles par auto—greffes fraiches et segmentaires de veines Acta Chir Belg IV 1950 397
