Does remote sepsis influence the patency of microvascular anastomoses?

Britrs,h Journal y/ Plastic Surgery (1988). 41, 395-398 Ci 19BRThe Trustees of British Association of Plastic Surgeons

Does remote sepsis influence the patency of microvascular anastomoses? N. R. MCLEAN and H. ELLIS Department Department

of Plastic, Reconstructive and Burns Surgery, Queen Mary’s Hospital, Roehampton of Surgery, Westminster Hospital, London

Summary-A pyogenic abscess, even though remote from the artery, significantly occlusion rate of microvascular arterial anastomoses in the rat experimental model.

and Academic

increases the

varying concentrations of Pseudointo the subcutaneous tissues of the right axilla to produce a distant pyogenic abscess. It has previously been shown (De Haan et al., 1974) that these organisms are not normally present in the Sprague-Dawley rat. It was found that a suspension containing 2 x lo7 organisms gave a large acute inflammatory mass by 7 days. These animals were all systemically unwell and lost between 15 and 20% of their body weight within the first week. In a separate study it was found that 2 ml of sterile turpentine oil gave an acute aseptic inflammatory mass at one week. Seven days prior to end-to-end anstomoses of both femoral arteries, 60 female Sprague-Dawley rats were randomised to receive an injection into the right axilla of either (i) 2 ml suspension of Ps. aeruginosa containing 2 x lo7 organisms to produce a distant pyogenic abscess, (ii) 2 ml of sterile turpentine oil for a remote sterile abscess or (iii) 2 ml of sterile saline as controls. The animals were not restrained and were caged separately. Throughout the experiment they had free access to food and water. As stated previously, there was a random allocation and all groups were operated on concurrently by one microsurgeon. To prevent transmission of the organisms from one animal to another, all instruments were autoclave sterilised between cases. One week later the rats were anaesthetised with intraperitoneal sodium pentobarbitol, the groins shaved and the femoral vessels exposed via an oblique groin incision. The artery was mobilised from the inguinal ligament to the inferior epigastric vessel and the posterior branches ligated with 10/O prolene. The femoral artery was divided in Acland clamps, stripped of adventitia and flushed with heparinised saline. An end-to-end repair was performed using the posterior wall first technique. injected

Although Carrel (1908) and Guthrie (1908) discussed the subject of vascular anastomosis and organ transplant in the experimental situation, in the early part of this century, the first clinically successful free tissue transfer was reported by Seidenberg et al. in 1959. Their paper described free: jejunal transfer in mongrel dogs but included a case report of a one stage oesophageal reconstruction using vascularised small bowel following a laryngo-oesophagectomy performed in 1957. The reconstruction was successful but the patient died of a cerebra-vascular accident on the seventh postoperative day. Despite this work it took until the 1970s before the movement of tissues from one part of the body to another with the re-anastomosis of their supplying vessels at the recipient site became a routine and reliable reconstructive technique (Antia and Buch 1971, McLean and Buncke, 1972: Daniel and Taylor, 1973; O’Brienetal., 1973; Harii cited by O’Brien et al., 1974; O’Brien et al., 1974). In spite of technical advances, some free flaps still fail due to anastomotic occlusion in the early postoperative period. Many such cases may have local or distant sources of sepsis, where a transient bacteraemia could promote hypercoagulability (Calmpos et al., 1983, 1984) and thus occlusion of the microvascular anastomosis. It has already been shown that distant bacterial infection has a marked inhibitory effect on the hea.ling of skin, muscle and stomach wall (De Haan et al., 1974) and the purpose of this experimental study was to investigate the role of remote sepsis on the patency of microvascular anastomoses.

with

monas aeruginosa

Materials and methods In a preliminary study, female Sprague-Dawley rats, weighing between 300 and 400 grams, were 395

BRITISH JOURNAL OF PLASTIC SURGERY

396 On average, 8 interrupted 10/O prolene sutures were required. After clamp release, haemostasis was achieved by gentle pressure. Patency was assessed at 30 minutes by observing for expansile pulsation distal to the anastomotic site (Acland, 1972) and by the use of the flicker and milking test. One week later the groins were re-explored and the anastomoses inspected for patency. Thrombosed specimens were immersed in form01 saline. Patent vessels were cannulated proximally and gently irrigated with a fixative prior to being removed. Specimens were stained with haematoxylin and eosin and the Brown-Bren stain to show the presence of Ps. aeruginosa. Bacteriological specimens were taken from the groin wounds at the anastomotic site. Blood cultures were also taken. In four of the thrombosed anastomoses in the pyogenic abscess group the thrombus was sent for ultrasonic disintegration prior to culture. A total of 16 animals died in the study; one control, nine with aseptic abscesses and six in the group with distant pyogenic abscesses. In the last two groups all the animals died after injection but before the operation and were replaced with new ones. Results were assessed for statistical significance by use of the x? test. Results One week postoperatively 39 of the 40 control anastomoses were patent (Table 1). This was not significantly influenced by the sterile abscess, where 35 anastomoses were patent at seven days (x’= 1.62, p =0.203). The occlusion rate, however, was significantly increased in those animals with a pyogenic abscess, even though remote from the artery (x’ = 20.92, p < 0.001). In the patent vessels of all three groups the histological appearances showed necrosis of the tunica media with denucleation of the smooth muscle cells. In some cases the sutures had caused a scalloped effect and there was evidence of subintimal hyperplasia both proximal and distal to the anastomotic site. An infiltrate of acute inflammatory cells was often seen in the vessel wall (Figs 1 and 2). In the thrombosed vessels in all the groups there was disruption of the vessel wall with complete occlusion of the lumen, which was filled with organising thrombus (Fig. 3). Many of the thrombi were recanalising by 7 days. We were unable to demonstrate the presence of pseu-

Post-operative

Table 1.

patency rates

Group

Number patent

Control

39/40

Sterile abscess

35/40 (p = 0.203)

Septic abscess

IO/40 (p
domonas in the thrombus using the Brown-Bren stain. Pseudomonas aeruginosa could always be cultured from the axillary focus of sepsis but was never grown from swabs of the groin wounds at the anastomotic site nor from blood cultures (Table 2). None of the control animals with a superficial wound infection had occlusion of the underlying anastomosis. Two grew coliform organisms and in three, staphylococcus species was cultured. In no case was Ps. aeruginosa grown despite an intensive bacteriological study. Significantly more animals in the distant pyogenic abscess group developed a local wound infection. In all the wound swabs only a scanty growth of organisms was demonstrated. As all these animals were systemically unwell, it may be that their defences against bacterial infection were depressed by the chronic septic abscess. In the four thrombi sent for ultrasonic disintegration no pseudomonas was grown although in one of them there was scanty growth of coliforms. We were unable to demonstrate the presence of pseudomonas in either the thrombi or the vessel walls using the Brown-Bren stain. On one occasion the turpentine abscess became infected due to the animal biting itself. A scanty growth of staphylococcus was obtained. Both anastomoses in this animal were occluded by thrombus. In five of the animals in the study the anastomoses required to be revised on the table; all these revised anastomoses were patent at 7 days. Discussion While sterile abscesses had no effect on the success of microvascular anastomoses in this study, the occlusion rate was significantly increased to 20 of 40 anastomoses in those animals with a distant pyogenic abscess, in spite of the fact that organisms from the abscess were never found at the anastomotic site. This was not in keeping with the previous study on abdominal wounds, which showed the organism present in 50% of the wounds (De Haan et al., 1974).

DOES REMOTE SEPSIS INFLUENCE

THE PATENCY

OF MICROVASCULAR

Fig. 2

Fig. 1

397

ANASTOMOSES?

Fig. 3

Figure I --Normal rat femoral artery stained with haematoxylin and eosin (magmfication x 40). Figure 2-Patent anastomosis in ammal wtth a distant pyogenic abscess stained with haematoxylin and eosin (magnification x 40). There is some medial necrosis and scalloping of the vessel wall related to the sutures. Figure 3GThrombosed anastomosts in animal with distant pyogenic abscess stained with Brown-Bren stain (magnification x40). Lumen completely occluded by organising thrombus. No evidence of pseudomonas in the specimen.

Table 2.

Animals

with

a local

wound

infection.

GWlp Control (5) Control (I 7) Sterile abscess Sterile abscess Septic abscess Septic abscess Septic abscess Septic abscess Septic abscess Septic abscess Septic abscess Septic abscess Septic abscess Septic abscess Septic abscess Septic abscess Septic abscess Septic abscess Septic abscess

(1) (9)

(1) (3) (3) (6) (10) ( I 1) (13) (14) (15) (I 6) ( ! 6) (17) (17) (18) (19)

Skin flora on(R) B Haemolytic streptococcus (R) Corynebacterium on (R) Corynebacterium on (R) Stuph. rpidermidir on (R) Staph. nureus on (L) Staph. crurrus and coliforms (R) Stuph. rpidermidis on (L) Proteus and Staph. epidernzidl~ on t L) and (R) Proteus on (L) and (R) Staph. species on (R) Staph. species on (L) Coliforms on (L) and (R) Coliforms on (L) Coliformson (R) Staph. species on (L) Staph. species on (R) Staph. spectes on (L) Staph. species on (L) and (R)

F’ourteen of the occlusions occurred bilaterally in seven animals, which could point to a systemic factor being involved in the aetiology of the anastomotic thrombosis. Although dehydration could explain some of these failures, it has been shown that animals with an acute septic or aseptic inflammatory focus have normal blood urea and haemoglobin levels (De Haan et al., 1974). Endotoxaemia is known to cause occlusion of small vessels and further studies are under way in this

Patent Patent Patent Patent Thrombosed Thrombosed Patent Thrombosed Thrombosed Thrombosed Patent Patent Thrombosed Patent Thrombosed Thrombosed Patent Thrombosed Patent

laboratory to elucidate the effect of a transient bacteraemia and endotoxaemia on the patency rate of small vessel anastomoses. In conclusion, although the exact mechanism of anastomotic failure remains uncertain, these results demonstrate that septic foci anywhere in the body may promote occlusion of a microvascular anastomosis and should therefore be eliminated prior to reconstructive surgery involving the microvascular transfer of free tissue.

398 Acknowledgements We wish to thank the departments of Medical Photography at the Westminster Hospital and Queen Mary’s Hospital, Mrs Kathryn Savage for typing the manuscript and the department of Medical Computing, Westminster Hospital. for the statistical analysis. This work was supported by a locally organised grant from the South West Thames Regional Health Authority.

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OF PLASTIC SURGERY

infection on wound healing. Surgery, Gvneco1og.r and Obstetrics, 138, 693. Guthrie, C. C. (1908). Some physiologic aspects of blood-vessel surgery. Journal of the American Medical Association, 51, 1658. McLean, D. H. and Buncke, H. J. (1972). Autotransplant of omentum to a large scalp defect, with microsurgical revascularization. Plastic and Reconstructive Surgery, 49,268. O’Brien, B. McC., MacLeod, A. M., Hayhurst, J. W. and Morrison, W. A. (1973). Successful transfer of a large island flap from the groin to the foot by microvascular anastomoses. Plastic and Reconstructive Surgery, 52, 271. O’Brien, B. McC., Morrison, W. A., Ishida, H., MacLeod, A. M. and Gilbert, A. (1974). Free flap transfers with microvascular anastomoses. British Journal of Plastic Surgery, 27,220. Seidenberg, B., Rosenak, S. S., Hurwitt, E. S. and Sam, M. L. (1959). Immediate reconstruction of the cervical esophagus by a re-vascularised isolated jejunal segment, Annals of’ Surgery, 149, 162.

The Authors Neil R. McLean, FRCS, Senior Registrar in Plastic Surgery, Department of Plastic, Reconstructive and Burns Surgery. Queen Mary’s Hospital, Roehampton, London SW 15 5PN. Harold Ellis, CBE, DM, MCh, FRCS, Professor of Surgery, Academic Department of Surgery. Westminster Hospital, Page Street Wing, London SW 1P 2AP. Requests

for reprints

to Mr N. R. McLean

Paper received 18 June 1987. Accepted 8 December 1987 after revision