Historical Perspective

Surgical ligation of the GSV above or below the knee has been practiced for many centuries, starting with Paulus of Aegina in 660 a.d. However it was not until the nineteenth century before the effect of ligation on the vein itself and on the venous hemodynamic situation became better understood.

In 1861, Langenbeck3 described in detail what exactly happened with a vein after surgical ligation. He noticed that a vein had a very important regeneration capacity and that a new vein channel could be formed after ligation or extirpation of a piece of vein:

In one case of very large varix of the great saphena in a young man

I had extirpated the enlarged vein in the length of three inches and ligated the upper and lower ends. One year later I found, in the region of the scar tissue of the extirpation, a new vein channel of the thickness of the quill of a crow's feather, which again joined the both ends of the fully functioning saphena.

Looking at his detailed description now, one and a half centuries later, this could be considered as the first real

Figure Stitch Varicose Vein
FIGURE 26.1 Prominent recurrent varicose veins with venous ulcer in a 32-year-old man who underwent comprehensive saphenofemoral junction ligation and stripping of the great saphenous vein above the knee 8 years earlier.

description of formation of new veins after ligation (which could possibly lead to recurrence of varicose veins later on).

Throughout the nineteenth century, surgical treatment of varicosity of the GSV was limited to simple ligation and transection at a site in the thigh where there were relatively few tributaries. Therefore it was obvious that, if recurrence occurred, the cause was situated at the site of ligation in the thigh. In the beginning of the twentieth century, Homans4 introduced saphenofemoral junction ligation in the groin. He advocated ligation of all tributaries to the terminal portion of the saphenous vein to prevent restoration of venous continuity through a collateral network in the groin. From that time, the theory of recurrence through preexisting collateral veins gained ascendancy over the earlier theory of recurrence through growth of new vessels. Ever since, inadequate operation by the previous surgeon was claimed to be the main cause of recurrence. Only a minority believed that recurrence also could occur after accurately performed saphenofemoral ligation through formation of new vessels. In explaining the genesis of this phenomenon, Sheppard5

previous ligation of the Great Saphenous vein (GSV) and all tributaries at the saphenofemoral junction, without stripping the GSV. A new vein (arrow) is bulging at the anteromedial side of the common femoral vein (CFV) and continues downward as a very tortuous vein, connecting again with the retained GSV trunk. If the above knee GSV has been stripped, it may connect with any other superficial vein remnant.

previous ligation of the Great Saphenous vein (GSV) and all tributaries at the saphenofemoral junction, without stripping the GSV. A new vein (arrow) is bulging at the anteromedial side of the common femoral vein (CFV) and continues downward as a very tortuous vein, connecting again with the retained GSV trunk. If the above knee GSV has been stripped, it may connect with any other superficial vein remnant.

hypothesized that, "under the influence of the high femoral pressure, the capillaries and venules in the granulation tissue (of the newly forming scar) developed into dilated tortuous channels."

Starnes et al.6 described a radiological type of recurrence of varicose veins, which could occur even after skillful high ligation. He was convinced that ascribing all thigh recurrences to a missed venous branch at the time of high ligation of the saphenofemoral junction was too simple an explanation. In four out of six cases with clinical recurrence vari-cography demonstrated the presence of a new, tortuous segment of vein at the site of the previous operation. The proximal and distal cut ends of the GSV or one of its branches had been rejoined by new vessels, described as "a zigzag of recurrent vein joining the remnant of the GSV with the femoral vein."

During the period 1950 to 1980, Glass7-9 led surgeons to focus again on recurrence of varicose veins after surgery through "regrowth of veins." He published his clinical and experimental work concerning this problem, in 1987 mentioning the term neovascularization for the first time.7 In this study, a series of patients with venous ulceration due to GSV insufficiency were treated in stages. First, a transection of the GSV was performed in the lower part of the thigh and all side branches at that site were ligated. In a second stage, individually timed for each patient by healing of the ulcer, the SFJ was ligated in combination with stripping of the GSV. During the same operation the ends of the vein at the site of the original transection in the lower thigh were excised together with the tissue intervening between them. The excised specimen was examined by injecting normal physiologic solution into the distal segment. Continuity between the proximal and distal cut end had been reestablished through small vessels after 40 weeks and through larger dilated vessels after 64 weeks. The histological examination showed organization of the blood clot starting soon after the operation, with blood vessels moving in from the surrounding tissue. At six weeks, there was recanalization of the thrombus occluding the vein and vessels started to grow from the transected vein end. At 18 weeks it could be observed that new vessels between the cut ends were arranged in a parallel formation. At 40 weeks, continuity of the vein had been completely restored through small vessels, which were continuous with the transected vein ends. The new vessels were very thin-walled with muscular tissue. At the site of the previously closed vein end it seemed to be reopened, establishing a new connection with the surrounding tissue. He hypothesized that one of the important triggers for restoration of continuity was a large pressure difference in a vein proximal and distal to the site of transection.

He also studied the gross anatomy and histology at the level of the SFJ during reexploration of the groin.8,9 In the majority of limbs a newly formed vessel or complex of vessels was found in connection with the former saphenous stump proximally and with varicose veins on the thigh distally. Macroscopic examination revealed several lumens in an irregular mass of vein tissue and cords or bands traversing the lumen, which suggested that the vessels were newly formed and not preexisting. Large lymph nodes were often in close proximity to them. The histology confirmed the macroscopic findings: an irregular vessel wall with a varying thickness at different points of the circumference, often with several lumens. Also typical was the presence of many small vessels close to the newly formed vessel and in neighboring lymph nodes. These studies clearly indicated that neovascu-larization had played an important role in recurrent saphe-nofemoral incompetence after a correctly performed SFJ ligation.

NEOVASCULARIZATION: TODAY'S EVIDENCE

Sonographic Evidence

Duplex scanning can provide the necessary anatomical and functional information about the nature of recurrence and has become the investigation of choice in patients with recurrent varicose veins. Jones et al.10 found that neovascularization at the SFJ was the most common cause of recurrence in 113 legs two years after stripping of the GSV. Typical serpentine tributaries arising from the ligated SFJ were detected in 52% of limbs. Another duplex-based prospective study revealed some degree of neovascularization in 14% of 177 limbs already at one year after flush saphe-nofemoral or saphenopopliteal junction ligation.11 The clinical relevance of finding neovascularization on postoperative duplex ultrasound was examined in a long-term follow-up study at the same institution almost five years (56 months) after the varicose vein operations.12 In 68% of limbs with clinically obvious recurrent varicose veins, neovasculariza-tion (with new veins of >4 mm diameter, pathological reflux, and connected to recurrent varicose veins) was present at the site of the saphenous ligation on duplex examination, whereas in limbs without recurrent varicose veins this degree of neovascularization was seen in only 9% of cases (see Figure 26.3). A reintervention was proposed to all patients with disabling recurrent varicose veins and obvious neovascu-larization on duplex examination. Fifteen reinterventions were performed. In all 15 reinterventions, newly formed vessels were present exactly at the site of the previous saphe-nous ligation, which confirmed the duplex findings in all of them. Histological examination of the excised tissue in some of the reoperated cases illustrated the presence of typical tortuous veins (see Figure 26.4). These findings demonstrate the clinical relevance of duplex-detectable neovascularization in the long-term follow-up after varicose vein operations.

Histopathological Evidence

Nyamekye et al.13 provided further evidence that neovas-cularization was the cause of recurrence. Histological examination of the venous tissue blocks, excised during groin reexplorations, showed neovascularization in 27 of 28 blocks, characterized by vein tortuosity, small size, and mural asymmetry and lack of intramural nerves on immu-nohistologically S100 stained sections. The authors drew attention to the fact that a negative demonstration of a focal structure, such as a mural nerve seen on S100 stained sections, is never entirely convincing and that a more useful tool for the diagnosis of neovascularization was not yet available. In spite of this warning, the findings of his study

FIGURE 26.3 Proportional incidence of different degrees of neovascularization according to duplex ultrasound scanning of the groin at long-term follow-up in limbs with and without recurrent varicose veins. Grade 0: no neovascularization; Grade 1: tiny new vein <4 mm; Grade 2: tortuous new connecting vein with a diameter >4 mm and with pathological reflux.

FIGURE 26.3 Proportional incidence of different degrees of neovascularization according to duplex ultrasound scanning of the groin at long-term follow-up in limbs with and without recurrent varicose veins. Grade 0: no neovascularization; Grade 1: tiny new vein <4 mm; Grade 2: tortuous new connecting vein with a diameter >4 mm and with pathological reflux.

FIGURE 26.4 Histological section of an excised tissue block in the groin showing tortuous newly formed veins within the scar tissue (Masson's trichrome stain, original magnification x40).

were cited in many instances as the final histological description of neovascularization.

The causality of recurrence was further investigated by van Rij et al.14 by correlating findings from duplex ultrasound scans before operation with histological findings in specimens taken from the groin at operation and resin casts made from some of the excised tissue blocks (see Figure 26.5). Neovascular channels of variable size, number, and tortuosity accounted for the ultrasound appearances in the vast majority of examined specimens. These new vessels connected to the CFV at the site of the previous SFJ. At

FIGURE 26.5 Vascular casts of recurrent refluxing saphenofemoral junction (SFJ) specimens, showing the connecting network of vessels. In both specimens there are abundant tortuous vessels. Casts injected from the SFJ show resin present in the connecting network of vessels. Notice the variation in size of the abundant tortuous vessels in both specimens. A: Though several channels are larger, there are more than 100 channels running in a similar proximal distal direction. B: Three large-diameter channels dominate the cast; however, there are also small channels present in continuity. Note the injecting cannula (distal). Scale bars: A, 5 mm; B, 10 mm. (Reprinted from AM van Rij, GT Jones, GB Hill, P Jiang. Neovascularization and recurrent varicose veins: more histologic and ultrasound evidence, J Vasc Surg. 2004. 40: 296-302, Copyright 2004, with permission from The Society for Vascular Surgery.)

FIGURE 26.5 Vascular casts of recurrent refluxing saphenofemoral junction (SFJ) specimens, showing the connecting network of vessels. In both specimens there are abundant tortuous vessels. Casts injected from the SFJ show resin present in the connecting network of vessels. Notice the variation in size of the abundant tortuous vessels in both specimens. A: Though several channels are larger, there are more than 100 channels running in a similar proximal distal direction. B: Three large-diameter channels dominate the cast; however, there are also small channels present in continuity. Note the injecting cannula (distal). Scale bars: A, 5 mm; B, 10 mm. (Reprinted from AM van Rij, GT Jones, GB Hill, P Jiang. Neovascularization and recurrent varicose veins: more histologic and ultrasound evidence, J Vasc Surg. 2004. 40: 296-302, Copyright 2004, with permission from The Society for Vascular Surgery.)

Research on the Pathophysiology of Saphenofemoral Recurrence and the Role of Neovascularization

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