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Keywords:

  • atherosclerosis;
  • iliac artery;
  • kidney transplantation;
  • surgical anastomosis;
  • surgical staples

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conflict of interest
  8. References

Objectives:  To report our experience of arterial anastomosis with Nakayama's ring pin staplers (titanium staplers) after an endarterectomy in kidney transplantation of diabetic recipients with iliac atherosclerosis.

Methods:  In a series of 2126 kidney transplantations carried out between January 1998 and December 2008, 62 recipients received an endarterectomy during transplantation before renal arterial anastomoses as a result of severe iliac atherosclerosis. The renal arteries were anatomosed to hypogastric arteries through titanium staplers in 32 patients (group 1), or to external/common iliac arteries with conventional suturing in 30 patients (group 2). Perioperative outcomes of the two groups have been compared.

Results:  The mean artery anastomosis time in group 1 was considerably shorter than in the group 2 (6.4 min vs 17.3 min, P < 0.001). Group 1 showed a lower rate of delayed graft function (4.8% vs 27.5%, P = 0.004). No difference in Kaplan–Meier patient survival rate was found between group 1 and group 2 after follow up of 67 ± 28 months (P = 0.58). Graft survival rate (patient deaths included) was higher in group 1 than in group 2 (P = 0.04).

Conclusions:  Arterial anastomosis with a titanium stapler is more rapid than conventional suture. It can diminish the rate of delayed graft function and improve the graft survival rate in diabetic recipients with severe iliac atherosclerosis.


Abbreviations & Acronyms
CAD =

coronary artery disease

CsA =

cyclosporine

DGF =

delayed graft function

ESRD =

end-stage renal disease

HLA =

human leukocyte antigen

MMF =

mycophenolate mofetil

PNF =

primary non-function

PRA =

panel reactive antibody

Pred =

prednisolone

Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conflict of interest
  8. References

Diabetic nephropathy is the most common reason for renal failure and the need for renal replacement therapy worldwide.1 Most patients with type 2 diabetes will develop vascular complications with increasing duration of their disease. These might be either microvascular disease, such as diabetic retinopathy, nephropathy and neuropathy, or atherosclerotic macrovascular disease, including CAD, cerebrovascular and peripheral vascular disease.2 ESRD and diabetes are both high-risk factors for vascular calcification, a process that has been shown during the progression of atherosclerosis with calcification of intima and tunica media.3 Systemic artery atheroma and/or calcification, coronary artery atherosclerosis and arteriosclerotic obliterans are common complications of uremic renal transplant candidates with diabetes mellitus. It is technically difficult to carry out the arterial anastomosis for diabetic recipients with severe iliac atherosclerosis.

The metal ring pin stapler (also known as Nakayama's apparatus) was introduced in the early years of microsurgery for facilitating the anastomoses of small caliber arteries and vein.4 The ring pin stapler used clinically is made from titanium, so it is also known as a titanium stapler. We have used ring pin staplers for plastic operations of arteriovenous fistulas since 1985.5 After accumulating adequate experience, we have applied it to arterial anatomosis for renal transplantation since 1990,6 and then to arterial anastomosis after endarterectomy in diabetic renal transplant recipients with iliac atherosclerosis.7 The arterial anatomosis through a titanium stapler is rapid and accurate, with shorter warm ischemic time than that of the conventional suturing. There is no foreign material in the vascular lumen, with almost perfect coaptation of the intimal surface in the anastomotic line.8 Herein we report our results of renal transplantation in diabetic recipients with severe iliac atherosclerosis in which the arterial anastomoses were carried out by a titanium stapler after an endarterectomy.

Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conflict of interest
  8. References

Patients' characteristics

Between January 1998 and December 2008, 2126 cadaveric renal transplantations were carried out at our centers (First Affiliated Hospital of Sun Yat-sen University and Zhujiang Hospital of Southern Medical Univerisity, Guangzhou, Guandong, China); 318 recipients were patients with type 2 diabetes, of which 62 recipients received an endarterectomy during transplantation before renal arterial anastomoses as a result of severe iliac atherosclerosis. The clinical data of these patients were retrospectively analyzed. The renal arteries were anastomosed to hypogastric arteries by titanium staplers in 32 patients (group 1), or to external or common iliac arteries with monofilament 6-zero polypropylene suture in a running fashion in 30 patients (group 2). The demographics and immunological factors of the two groups are listed in Table 1. All patients underwent a thorough preoperative evaluation, including medical history, physical examination and color Doppler ultrasound for iliac vessels. Computed tomography and/or arteriography were carried out when abnormalities were found on ultrasound. Criteria for lower extremity peripheral vascular disease included claudication or ulceration with large vessel disease on flow studies (ankle-brachial index and pulse-volume recording), major amputation (excluding toe amputation), operative bypass procedures and percutaneous angioplasty.9 Patients with diffuse, symptomatic aortoiliac atherosclerosis or peripheral arterial atherosclerosis of the lower extremities were excluded from the waiting list of transplantation or considered candidates for pretransplant vascular bypass/percutaneous angioplasty. Patients who underwent vascular bypass surgery simultaneously with kidney transplantation were excluded from analysis because of the complexity of the surgery. Mean follow up of the patients was 67 ± 28 months (range 6–115 months).

Table 1.  Patients' characteristics and immunological data
ParametersGroup 1Group 2P-value
(n = 32)(n = 30)
Age (years) ± SD59.6 ± 9.061.0 ± 7.10.49
Sex distribution, male : female28 : 426 : 41.0
Donor age (years) ± SD27.5 ± 4.827.6 ± 5.11.0
Cold ischemia time (hours) ± SD10.2 ± 3.59.7 ± 3.90.56
HLA mismatch ± SD2.9 ± 1.33.2 ± 1.30.44
PRA level >10%, % (n)15.6% (5)20.0% (6)0.75
Immunosuppression  0.60
 FK506/MMF/Pred (n)2117
 CsA/MMF/Pred (n)1113
Coronary artery diseases, % (n)43.8% (14)53.3% (16)0.61
Peripheral vascular disease, % (n)9.4% (3)16.7% (5)0.47

Technique of endarterectomy

For atheromatous plaque limited to the internal iliac artery, endarterectomy was carried out by the eversion technique.10 A vascular clamp is applied to the internal iliac artery at its origin; after division of the internal iliac artery distally, the proper plane of endarterectomy is established and developed circumferentially by dissection between the atheromatous core and the artery adventitia using a dissecting spatula. With traction on the atheromatous core, the arterial adventitia is turned back on itself and dissection is continued until the atheroma is removed. The vessel wall is then drawn back distally into a normal position for anastomosis to the renal graft artery. Before anastomosis, the artery clamp is released momentarily to flush out trapped debris and the vessel lumen is flushed out with heparinized saline.

If there is significant ostial stenosis of the internal iliac artery, an endarterectomy should be carried out at the bifurcation of iliac arteries. A longitudinal arteriotomy on the junction of common and external iliac arteries is made. Endarterectomy of the iliac arteries is next carried out using a dissecting spatula to separate the adventitia from the media. Special care must be taken to thoroughly correct any stenosis of the origin of the internal iliac artery and to avoid an intimal flap of the iliac artery. The latter can be prevented by an intimal tacking stitch placed circumferentially at the proximal and distal end of the endarterectomy. Before the artery is closed with a continuous 5-0 polypropylene suture, any tags of residual media are removed and thorough flushing of all vessels is carried out. Heparin (50 units/kg) is given intravenously before clamping the iliac arteries. After release of the vascular clamps, heparin is reversed with protamine. All recipients received low-dose aspirin therapy (100 mg/day) after transplantation.

Technique of anastomosis by titanium stapler

Nagayama's ring pin stapler system (Fig. 1) was manufactured by Shandong Xinhua Medical factory (Zibo, China). Detailed descriptions of the techniques of renal arterial anastomosis by titanium stapler have been reported by the present authors and others.6,8,11 Nagayama's method is shown in Figure 2. Briefly, two titanium rings are put on a pair of ring holders, one of the pins on the ring should be aimed at the marker on the ring holder (Fig. 2a). The vessel end of the hypogastric artery is passed through the titanium ring, its edge is everted by a hook (Fig. 2b). The everted vessel end is impaled on the small pins by the pressing pin head (Fig. 2c). The two ring holders are brought together. Caution in the position of the pins should be used, it should pass the everted edges of the arteries without slanting or overlapping (Fig. 2d). The head of the ring holders are compressed with a crushing clamp to make the two arteries tightly linked (Fig. 2e). Two ring holders are separated in parallel to each other, unlocked and withdrawn, (Fig. 2f) and the anastomosis procedure is completed. The photographs taken during the operation are shown in Figure 3. If there is a discrepancy between the diameter of the renal artery and the diameter of the inferior epigastric artery, an aortic patch from which the renal artery arising can be used. It is trimmed to an appropriate size and fixed on the stapler.

image

Figure 1. Nagayama's ring pin stapler system consists of titanium rings, a pair of ring holders, hook, pressing pin head and crushing cramp.

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image

Figure 2. Arterial anastomosis with Nagayama's ring pin stapler system.

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image

Figure 3. Arterial anastomosis with Nagayama's ring pin stapler system. (a) Roll up the internal iliac artery on the titanium ring of 6 mm in diameter and fix it on the staplers. (b) The donor renal artery is fixed on another titanium ring. (c) Put together the two rings and compress them with a crushing cramp to make the two vessels join tightly. (d) Withdraw the ring holders, and arterial anastomosis is completed.

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Statistical analysis

Results are expressed as numerical values and percentages for categorical variables, and as mean ± standard deviation for continuous variables. Statistical analyses were carried out with spss software for Windows (version 16.0; SPSS, Chicago, IL, USA). Comparisons were based on Fisher's exact test for categorical data and the t-test for normally-distributed continuous data. The Mantel–Cox log–rank test was used to compare Kaplan–Meier patient and graft survival between groups. Results were considered significant when the P-value was less than 0.05.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conflict of interest
  8. References

No significant difference was noted between group 1 and group 2 in term of demographics and immunological factors, as shown in Table 1.

The artery anastomosis time in group 1 was significantly shorter than in the group 2 (6.4 ± 2.3 min vs 17.3 ± 5.1 min, P < 0.001). Group 1 showed a lower rate of DGF (4.8% vs 27.5%, P = 0.006). Group 1 also showed lower rates of PNF (0% vs 10.0%, P = 0.107) and acute ischemic extremity (0% vs 10.0%, P = 0.107), although the difference was not statistically significant. A comparable rate of graft arterial stenosis was observed in the two groups (Table 2).

Table 2.  Main results of kidney transplantation
 Group 1Group 2P-value
(n = 32)(n = 30)
Artery anastomosis time (min)6.4 ± 2.317.3 ± 5.1<0.001
Primary non-function, % (n)0% (0)10.0% (3)0.11
Delayed graft function, % (n)6.3% (2)36.7% (11)0.004
Acute ischemic extremity, % (n)0% (0)10.0% (3)0.11
Graft arterial stenosis, % (n)6.3% (2)10.0% (3)0.67

No difference in Kaplan–Meier patient survival rate was found between group 1 and group 2 after follow up of 67 ± 28 months (P = 0.583; Fig. 4). The graft survival rate (patient deaths included) was significantly higher in group 1 than in group 2 (P = 0.040; Fig. 5).

image

Figure 4. Patient survival curves in renal transplant recipients of severe atherosclerosis with renal graft arteries end-to-end anastomosed to hypogastric arteries through a titanium stapler after an endarterectomy (group 1), or end-to-side anastomosed to iliac arteries after an endarterectomy (group 2), log–rank P = 0.58.

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image

Figure 5. Graft survival curves in renal transplant recipients of severe atherosclerosis with renal graft arteries end-to-end anastomosed to hypogastric arteries through a titanium stapler after an endarterectomy (group 1), or end-to-side anastomosed to iliac arteries after an endarterectomy (group 2), log–rank P = 0.04.

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Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conflict of interest
  8. References

The major obstacle to kidney transplantation in diabetic uremic patients is macrovascular diseases, including coronary artery disease, aorto-iliac and peripheral vascular disease. Macrovascular atheroma and/or calcification will cause technical difficulty in graft arterial anastomosis, insufficient blood perfusion of the renal graft, exacerbation of ischemia of lower extremities and more cardiovascular complications during the perioperative period.

The current study shows that arterial anastomosis through a titanium stapler after an endarterectomy in diabetic renal transplant recipients with iliac atherosclerosis can achieve a better clinical outcome than through a conventional suture in an end-to-side anastomosis fashion, including less DGF and PNF, and higher renal graft survival rate. The rate of acute ischemic extremity post-transplant was also lower, although the difference was not statistically significant.

End-to-end renal arterial anastomosis might have some benefits in recipients with iliac atherosclerosis. Under the circumstances, of severe iliac atherosclerosis in which the arterial elasticity, rate and velocity of blood flow have been impaired, end-to-end anastomosis with a hypogastric artery might have hemodynamic advantages compared with end-to-side anastomosis with external or common iliac arteries. A hypogastric artery after an endarterectomy can provide adequate blood supply to the renal graft.12,13 Furthermore, unlike the end-to-side anastomosis technique, the end-to-end technique will not exacerbate the impaired blood supply of lower extremities, which might contribute to the lower rate of acute ischemic extremity in group 1.

The positive clinical outcomes of group 1 seem to be correlated with the advantages of arterial anastomosis with a titanium stapler. First, compared with conventional suturing anastomosis, anastomosis with a titanium stapler is rapid and simple.6–8,11 Second, the rigid titanium ring and the equal intervals between staplers lead to almost perfect coaptation of the intimal surface in the anastomotic line, with no malformation or stenosis of anastomotic stoma.6,8 Third, there is no foreign material in the vascular lumen with everted anastomosis, and the handling of the vessel end is atraumatic with the avoidance of intimal damage. Under scanning electron microscope, no microemboli or leukocyte infiltration were found.8 Fourth, there are fewer anastomotic complications. The titanium ring was placed to evert the wall of the vessel end, and the everted vessel edges were compressed as well as united tightly with less anastomotic bleeding.11 Finally, the benefits of easy application and speed were obvious when creating an anastomosis between the inferior epigastric artery and a lower pole artery using a ring of 2 mm in diameter.

In the present study, the arterial anastomosis time with staplers is less than half of the anastomosis time with conventional suturing. Another group of titanium stapler users reported similar anastomosis speed.11 A longer warm ischemia time increased the probability of PNF and DGF.14–16 DGF is one of the most important predictors of poor short- and long-term graft survival.17

Renal artery stenosis usually arises close to the surgical anastomosis. An anastomotic stenosis is most likely related to trauma to the donor or recipient vessels during harvesting, clamping or suturing, and usually arises early after transplantation. Small, subtle intimal flaps or subintimal dissections of the vascular wall precede intimal scarring and hyperplasia that result in narrowing or occlusion of the lumen.18,19 So, in theory, anatomosis with a titanium stapler will put an end to anastomotic stenosis. Ye et al. found that the incidence of renal artery stenosis appeared to be lower when arterial anastomoses were applied with the titanium ring pin stapler.11 However, in the present study, the rates of graft arterial stenosis in the two groups were similar. The main reason accounting for this difference might be, in the case of heavily diseased vessels with atheroma of the recipients in group 2, a broad rim anastomosis using a heavier suture was used, and the trimmed cuff of aorta attached to the renal artery was relatively larger than the usual size. We never found any infectious complications specific to the titanium stapler in group 1. Two reasons might account for this phenomenon. First, although the titanium stapler is foreign material, but as a result of its metal property, the bacteria cannot invade it. Second, the titanium stapler is situated just outside the arterial lumen.

However, there are different opinions about what kinds of anastomosis technique should be selected in renal transplantation. Sutherland et al. reported that among patients with end-to-end hypogastric artery anastomosis, the incidence of renal graft artery stenosis was significantly greater when an endarterectomy was required to render the hypogastric artery suitable for use, and treatment of transplant renal artery stenosis in patients with end-to-end hypogastric artery anastomosis is more difficult and results in a higher morbidity rate than treatment in the external iliac artery group.20 Droupy et al. also reported that end-to-side anastomosis on the external iliac artery is associated with a lower rate of arterial stenosis than end-to-end anastomosis on the internal iliac artery in renal transplant recipients with iliac artery atheroma requiring an endarterectomy.21

There are severe shortcomings of anastomosis with a titanium stapler. Although we have tried renal venous end-to-side anastomosis to the external iliac vein with titanium staplers,8 it had no advantage compared with suturing anastomosis of two veins. It is inconvenient to use a titanium stapler in kidney grafts with multiple renal arteries, although we had experience of carrying out conjoined anastomosis between two renal arteries before implantation. Furthermore, obvious artifacts would appear in the image of computed tomography of the renal graft. Because the rigid titanium ring is a circular staple, it is unsuitable for pediatric transplantation, in which an interrupted anastomosis is desirable to allow vascular growth with age and avoid anastomotic stenosis. Another mechanical vessel anastomosis apparatus, the non-penetrating vascular closure staple system, has been reported to be a suitable alternative to conventional suture in pediatric vascular surgery.22,23

Chronic kidney disease confers a high risk of cardiovascular morbidity and mortality. This risk greatly exceeds the risk of progressing to end-stage renal disease, and it appears to be particularly elevated when chronic kidney disease and diabetes are comorbid.24 A notable proportion (48%) of asymptomatic type 2 diabetic renal transplant candidates have significant coronary artery disease.25 Routine screening recipients for coronary artery disease before renal transplantation in diabetic candidates is suggested, but the methods for screening are controversial. Clinical symptoms, as well as the cardiovascular risk profile, are not valid predictors of CAD in diabetic patients with chronic renal failure, and coronary angiography in all diabetic patients with ESRD before renal transplantation is recommended for perioperative risk stratification and proper patient management in general.26 This recommendation was confirmed by a recently published article that found only angiographic CAD was predictive of subsequent major adverse cardiac events in diabetic patients with ESRD.27 Myocardial revascularization (coronary artery bypass grafting or percutaneous transluminal coronary angioplasty) can be carried out with acceptable short- and long-term results in patients with renal disease who have renal transplantation either before or after the revascularization procedure.28 In order to diminish the incidence of cardiovascular complications and thereby optimize patient survival, we believe it is more rational to screen and treat patients for CAD before renal transplant.

In conclusion, the diabetic renal transplant candidates with iliac atherosclerosis are of high risk for CAD, peripheral vascular disease, difficult anastomosis of graft artery and DGF. It is pivotal to screen CAD and peripheral arterial disease, and then treat them before transplantation. A hypogastric artery after an endarterectomy can provide adequate blood supply to the renal graft. Arterial anastomosis with a titanium stapler is more rapid than conventional suture. It can diminish the rate of DGF and improve the graft survival rate in diabetic recipients with severe iliac atherosclerosis.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conflict of interest
  8. References
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    Ye G, Mo HG, Wang ZH, Yi SH, Wang XW, Zhang YF. Arterial anastomosis without sutures using ring pin stapler for clinical renal transplantation: comparison with suture anastomosis. J. Urol. 2006; 175: 63640; discussion 640.
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    Galazka Z, Szmidt J, Nazarewski S et al. Kidney transplantation in recipients with atherosclerotic iliac vessels. Ann. Transplant. 1999; 4: 434.
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    Szostek M, Kosieradzki M, Chmura A et al. Does “second warm ischemia time” play a role in kidney allograft function? Transplant. Proc. 1999; 31: 10378.
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    Fervenza FC, Lafayette RA, Alfrey EJ, Petersen J. Renal artery stenosis in kidney transplants. Am. J. Kidney Dis. 1998; 31: 1428.
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    Bruno S, Remuzzi G, Ruggenenti P. Transplant renal artery stenosis. J. Am. Soc. Nephrol. 2004; 15: 13441.
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    Sutherland RS, Spees EK, Jones JW, Fink DW. Renal artery stenosis after renal transplantation: the impact of the hypogastric artery anastomosis. J. Urol. 1993; 149: 9805.
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    Droupy S, Eschwege P, Hammoudi Y, Durrbach A, Charpentier B, Benoit G. Consequences of iliac arterial atheroma on renal transplantation. J. Urol. 2006; 175: 10369.
  • 22
    Zeebregts CJ, Kirsch WM, van den Dungen JJ, Zhu YH, van Schilfgaarde R. Five years' world experience with nonpenetrating clips for vascular anastomoses. Am. J. Surg. 2004; 187: 75160.
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    Calles-Vazquez Mdel C, Viguera FJ, Sun F, Uson JM, Uson J. Vein and artery growth after anastomosis with vascular closure staple clips vs interrupted polypropylene suture: application in pediatric vascular surgery. J. Pediatr. Surg. 2005; 40: 142835.
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    Patel T, Charytan DM. Cardiovascular complications in diabetic kidney disease. Semin. Dial. 2010; 23: 16977.
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    Ramanathan V, Goral S, Tanriover B et al. Screening asymptomatic diabetic patients for coronary artery disease prior to renal transplantation. Transplantation 2005; 79: 14538.
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    Koch M, Gradaus F, Schoebel FC, Leschke M, Grabensee B. Relevance of conventional cardiovascular risk factors for the prediction of coronary artery disease in diabetic patients on renal replacement therapy. Nephrol. Dial. Transplant. 1997; 12: 118791.
  • 27
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