Living Related Segmental Bowel Transplantation: From Experimental to Standardized Procedure

doi:10.1097/01.sla.0000232555.02880.84

Journal List > Ann Surg > v.244(5); Nov 2006

Ann Surg. 2006 November; 244(5): 694–699.

doi: 10.1097/01.sla.0000232555.02880.84.

PMCID: PMC1856585

Living Related Segmental Bowel Transplantation

From Experimental to Standardized Procedure

Enrico Benedetti, MD,^* Mark Holterman, MD,^† Massimo Asolati, MD,^* Stefano Di Domenico, MD,^* José Oberholzer, MD,^* Howard Sankary, MD,^* Herand Abcarian, MD,^‡ and Giuliano Testa, MD^*

From the *Division of Transplantation, †Division of Pediatric Surgery, and ‡Department of Surgery, University of Illinois at Chicago, Chicago, IL.

Abstract

Introduction:

Living donor bowel transplantation has recently emerged as a valuable alternative to cadaver bowel transplant. We herein present our single-center experience with this procedure.

Materials and Methods:

From April 1998 to October 2004, 12 living donor intestinal transplants were performed in 11 patients (7 males, 4 females; average age, 26 years). Four of the patients were children under 5 years. A segment of distal ileum 150 to 180 cm long in pediatric recipients and 200 cm long in adult was used. The immunosuppressive protocol consisted of induction with thymoglobulin and maintenance with tacrolimus with or without mycophenolate mofetil and steroids.

Results:

All donors recovered well and did not experience any early or late complications. The overall 1- and 3-year patient survival was 82% with a graft survival of 75%. In the last 8 patients, transplanted after January 2000, the 1-year patient and graft survival has been 100% and 88%, respectively. The median hospital stay was 36 days (range, 13–290 days). During the first year after transplant only, the patient who received a totally mismatched graft experienced one episode of rejection (8%). All the surviving patients are currently supported by enteral diet without fluid requirements.

Conclusions:

Living donor bowel transplantation is a valuable strategy in the treatment of irreversible intestinal failure. The results have improved over the years thanks to increased experience of the team.

Intestinal transplantation represents the most physiologic alternative to long-term total parenteral nutrition (TPN) in patients affected by irreversible intestinal failure (IF). Although TPN can allow survival in patients with IF, it is plagued by high cost and significant morbidity and mortality, and it is associated with poor quality of life.¹ However, mostly because of historically suboptimal results of bowel transplantation, only patients with IF experiencing life-threatening complications from TPN are usually considered suitable candidates for small bowel transplant. With the introduction of more potent immunosuppressive medications and a better control of infectious complications, the results of intestinal transplantation have been gradually improving in the last decade, and the procedure has been widely accepted as an effective option in the treatment of selected pediatric and adult patients affected by irreversible IF with life-threatening complications from TPN.^2,3

Most of the intestinal transplants have been performed using intestinal graft obtained from cadaver donors. The use of living donor bowel grafts can add some important advantages with acceptable risks for the donors. To date, only 32 small bowel transplants (3.3% of the total) have been performed from living donor versus 957 from deceased donors.^4,5 Intestinal Transplant Registry data suggest that patient and graft survival rates after living donor bowel transplant are similar to those obtained with cadaver organs.⁵

The use of living donors in intestinal transplantation is still controversial, and some authors suggest that it may not improve access to organs for patients waiting for an intestinal transplant.⁶ However, living donor intestinal transplantation offers substantial potential advantages that make it theoretically quite attractive. This strategy makes the transplant an elective procedure with minimization of waiting time, reduces the cold ischemia, and allows HLA matching.

Our experience, herein reported, suggests that living-related small bowel transplantation (LR-SBTX) is an effective strategy in the treatment of patients with irreversible IF and may provide an alternative to cadaveric intestinal transplantation.

PATIENTS AND METHODS

We studied 11 patients with irreversible IF who underwent 12 LR-SBTX at the University of Illinois at Chicago, between April 1998 and April 2004 (Table 1).

TABLE 1. Demographics of Living Donor Bowel Transplant Recipients

Intestinal Donor Protocol

Potential donors were initially screened based on history and physical as well as ABO compatibility. Only candidates at excellent surgical risk and ABO compatible were considered. If more than one donor was deemed suitable, the one with the best HLA match was chosen. In the pediatric group (5 transplants in 4 recipients), we had 4 one-haplotype match and one full mismatch; in the adults (7 transplants in 7 patients), there were 3 one-haplotype match, 3 full-match, and 1 identical twin.

All the chosen donors were living related. In the initial 7 donors, a preoperative selective angiography of the superior mesenteric artery (SMA) was performed to study the vascular supply of the cecum, ileocecal valve, and terminal ileum and to exclude any vascular abnormality. In the last 5 donors, the evaluation of the abdomen and of the splanchnic vasculature was performed with CT scan imaging and combined angiography with 3-dimensional reconstruction.⁷

Mechanical preparation of the intestinal graft was performed 1 day prior to surgery. Two doses of 45 mL of phosphosoda were given 4 hours apart on the afternoon before the surgery. Three doses of neomycin 1 g and metronidazole 500 mg were given 18, 17, and 10 hours prior to surgery per os. A single preoperative dose of antibiotic prophylaxis with intravenous cefoxitin 2 g IV was also administered.

The donor operation has been previously described in details.^8,9 Briefly, the donor’s small bowel is measured in its entire length from Treitz to ileocecal valve. Then, after controlling the position of the vascular arcades of the last portion of the terminal ileum, the 200 cm (for adult recipients) or 150 to 180 cm (for pediatric recipients) of bowel destined to become the graft is measured, starting from 20 cm from the ileocecal valve. Lastly, the remainder of the bowel is measured again to assure that at least 60% is left for the donor.

The location of the distal branch of the SMA supplying the future segmental graft is identified with palpation and transillumination. All the major branches of the SMA supplying the jejunum and proximal ileum are left intact. The margins of the segmental graft are “marked” with a Prolene suture proximally and Dexon distally. The mesentery is then divided in a “V”-shaped fashion with the tip of the V at the vessel take-off and extending toward the stitches marking the segment of ileum to become the graft. Lastly, the small bowel is divided proximally and distally using a GIA stapler.

Once the vessels are transected and the graft removed, the vessels stumps are oversewn with 5-0 polypropylene sutures in running fashion, and the donor intestinal continuity reestablished with a functional end-to-end stapled anastomosis. The ileal graft is flushed through the artery with cold University of Wisconsin solution until clear return from the vein is obtained. Postoperatively, the donor will recover in the transplant unit until ready for discharge. The donors are thereafter monitored for possible periodically to detect any possible complications in the short and long term.

Intestinal Recipient Protocol

Potential recipients are screened with standard preoperative evaluation to establish candidacy. Only patients with life-threatening complications from TPN and no hope for intestinal rehabilitation are considered. One exception was made for a potential recipient affected by ultra-short bowel syndrome with an available identical twin as a donor: in this case, the transplant was carried out in the absence of serious complication from TPN. All the other recipients were on TPN from 5 to 13 months preoperatively and experienced multiple episodes of bacterial or fungal sepsis. TPN-related cholestasis with total bilirubin >3 mg/dL was present in all these patients. Two pediatric patients were transplanted because of complete loss of central venous access. One of the pediatric patients underwent combined living donor liver and bowel transplant due to TPN-related cirrhosis. All the patients had ultra-short bowel syndrome defined as total lack of small bowel with only duodenum/colon remaining.

In the 4 children, the indication to intestinal transplantation was IF due to gastroschisis in all cases. In the 7 adults, the causes of IF were trauma in 3 patients, superior mesenteric thrombosis in 2 patients, Churg Strauss syndrome in 1 patient, and midgut volvulus in the last patient. The median recipient age was 26 years, ranging from 18 months to 50 years. Patient demographics are summarized in chronologic order in Table 1.

The adult recipients received as bowel preparation [1/4] of a gallon of Golytely or multiple fleet enemas to clean the colon if the GI tract was not in continuity. Intravenous vancomycin (1 g q 12 h) and piperacillin (3 g q 6 h) for 5 days were used as antibacterial prophylaxis.

The recipient procedure was completed in a standardized fashion as described by Gruessner and Sharp.⁸ Donor and recipient’s dissections were timed to minimize cold ischemia time. As a result, our average cold ischemia time was 10 minutes. After exposing the infra-renal vessels, the ileal graft was transplanted suturing the distal SMA and SMV branches in an end-to-side fashion to the aorta and the inferior vena cava, respectively. Particular attention was given to the orientation of the graft vessels to avoid rotation and the possibility of a thrombosis. The aorta was clamped with 2 separate spoon clamps, and an arteriotomy about 1.5 times the size of the diameter of the mesenteric artery of the graft was created. The anastomosis was then fashioned with interrupted 6.0 or 7.0 Prolene sutures. A bull dog clamp was then applied on the mesenteric artery and the clamps placed on the aorta were released. This maneuver is particularly useful for controlling the orientation of the mesenteric artery and obtaining perfect hemostasis at the site of the anastomosis. Next, a Satinsky clamp was applied to the cava and a large cavotomy was performed. The vein anastomosis was performed with 6.0 Prolene in continuous fashion. The graft was then reperfused and the alignment of the vessels was controlled. The average warm ischemia time was about 30 minutes. In no occasion was there a need to use a vascular graft. The intestinal continuity was immediately reestablished. Proximally, the graft was anastomosed to the recipient’s duodenum and distally to the stump of the colon in a double layer fashion. Both these anastomoses are functional end-to-end constructed by joining the lateral walls of the terminal portions of both intestines. A temporary loop ileostomy 10 cm proximal to the ileocolostomy was performed in all patients to monitor graft output and to allow easy access for endoscopic surveillance and biopsies. The loop ileostomy is fashioned on a rod. The enterotomy is performed on a transverse plane on the proximal side of the loop. In this way, the access to the proximal end of the graft is facilitated fro the numerous protocol endoscopies.

In all pediatric patients, the closure of the abdomen was achieved with the use of an absorbable mesh followed by a split-thickness skin graft after 4 to 6 weeks (Fig. 1). In 1 adult patient transplanted for IF due gunshot injury, the extensive loss of abdominal wall was treated using the same strategy.¹⁰ All the other adult patients underwent primary closure of the abdomen taking advantage of the relative small size of the segmental ileal graft.

FIGURE 1. Abdominal closure with absorbable mesh after living donor bowel transplant in pediatric recipients.

Postoperatively, antiviral prophylaxis in children (CMV and EBV) was carried out with intravenous gancyclovir for the first 3 week followed by oral gancyclovir until 1 year posttransplant. In adults, the antiviral prophylaxis consisted of perioperative IV gancyclovir (5 mg/kg q12 hours for 14 days) followed by PO gancyclovir for 3 months. Immunosuppressive protocol consisted of induction with Thymoglobulin (1.5 mg/kg) given once preoperatively and 2 to 3 times postoperatively until therapeutic levels of tacrolimus were reached. Maintenance immunosuppression consisted of tacrolimus and steroids in the first 5 adults and 3 children, whereas the last 3 patients (2 adults, 1 child) were treated with Tacrolimus and mycophenolate mofetil with early steroid discontinuation at postoperative day 6. The tacrolimus dose was adjusted to achieve serum levels of 15 to 20 ng/mL during the first month, 10 to 15 ng/mL during the second and third months, and 5 to 10 ng/mL thereafter.

Patients underwent a weekly magnified video-endoscopy with protocol biopsy through the stoma for the first 2 months for the detection of rejection episodes (Fig. 2). Thereafter, biopsy was performed once a month in adults and twice a month in children until 6 months posttransplant, when the ileostomy was routinely reversed. If clinically indicated, further biopsies after ileostomy reversal were performed using the colonoscopic approach. Acute rejection confirmed by biopsy was treated with steroid boluses following by Thymoglobulin for steroid-resistant rejections.

FIGURE 2. Serial magnified video-endoscopies of living donor bowel transplant graft with demonstration of intestinal villi (original magnification ×25).

After transplantation, the absorptive function of the segmental graft was monitored serially through d-xylose and fecal fat absorption studies. All the clinical information related to donor and recipients was carefully reviewed retrospectively after IRB approval.

RESULTS

Donor Outcomes

All 12 donors had uneventful recovery with an average hospital stay of 4 days: no technical complications were observed. Donors experienced moderate diarrhea during the first 2 months that resolved in all cases by the third months and did not recur thereafter.

Donor vitamin B12 levels remained within normal limits. Body weight decreased in only 3 patients in the postoperative period. The average median weight loss was 2.5 kg (range, 0–5 kg). No donor reported changes in lifestyle, work habits, or psychosocial conditions after the small bowel donation.

Recipient Outcomes

The overall 1- and 3-year patient survival is 82% (9 of 11), with a 1- and 3-year graft survival of 75% (9 of 12). In the last 8 patients, transplanted after January 2001, the 1-year patient and graft survival has been 100% and 88%.

Early in our experience, an intestinal graft was removed 6 weeks after transplant for diffuse ischemic injury related to octreotide administration for acute pancreatitis; examination of the graft after removal failed to show technical, immunologic, or infectious complications. Nine months later, the patient died of TPN-related complications. Another patient died 3 months after transplantation due to systemic aspergillosis with a functioning intestinal graft.

One pediatric patient experienced steroid resistance acute rejection 1 month after intestinal transplant with a full HLA mismatched graft from the grandmother. He was treated with 5 doses of Thymoglobulin obtaining reversal of the acute rejection. Three months later, he developed EBV-related posttransplant lymphoproliferative disease within the intestinal graft. Graft enterectomy with withdrawal of the immunosuppressive therapy was immediately carried out. Six months later, the patient was disease free and was reevaluated for retransplant. Unfortunately, by then he had TPN-induced cirrhosis, requiring a combined liver and bowel transplant for treatment. The patient’s mother, who was previously unable to donate because pregnancy, volunteered as a donor. Upon evaluation, the child was found to have positive cross-match due to a donor-specific anti-HLA antibody (anti-A3, shared by mother and grandmother). Attempts to convert the cross-match to negative by plasmapheresis failed. Therefore, the procedure was staged performing initially the segmental liver transplant (segment 2–3 of the mother liver) to take advantage of the well-known resilience of the liver in the face of preformed antibodies. The cross-match became immediately negative and a successful living donor bowel transplant from the mother was carried out a week later. The patient is currently doing well, on full enteral feeding and with good liver function.¹¹ He did not experience either rejection or recurrent posttransplant lymphoproliferative disease. All the other patients did well and did not experience any technical complications. The median hospital stay was 36 days with a range of 13 to 290 days.

During the first year posttransplant, acute rejection was diagnosed only in the pediatric patient already mentioned who received full mis-matched graft (1/11, 9%). Two additional late acute rejection episodes were documented in 2 adult patients in relation to overt noncompliance at 1.5 and 4 years after transplant.

One patient developed CMV enteritis 4 months after SBTx. The CMV status was positive to positive, and he was successfully treated with intravenous gancyclovir. We did not encounter any other significant infectious complications in adults. However, all the pediatric patients experienced at least 1 central line sepsis posttransplant.

Feeding was started through jejunal feeding tube on postoperative day 4 with an elementary diet at a low rate, and TPN was discontinued as soon as the patients tolerated an oral diet with an average of 8 days (range, 4–15 days). Fat-soluble vitamin levels and Shilling tests normalized within the first month after transplantation. Fat absorption, documented by fecal studies, was abnormal 1 month after transplant but normalized within 6 months. The d-xylose absorption test was also abnormal early after the transplant but progressively improved to reach normal value within 6 months. All the adult patients recovered their baseline (pre-TPN) weight and maintained it. In our pediatric recipients, average height increased from 82.5 to 97.5 cm while the mean weight increased from 11.4 to 14.2 kg.

The ileostomies were reversed 4 to 6 months after transplantation without technical complications. After the ileostomy take-down, the patients did not require any supplemental intravenous hydration. After ileostomy reversal, the number of bowel movements stabilized between 2 and 5 per day. All the patients received Imodium at high doses (4–6 mg PO q 6 h) since the second week posttransplant; the antidiarrheal medications are continued indefinitely. All the patients are currently supported by full enteral diet without fluid requirement, except 1 pediatric patient that still require some additional IV fluids. This child had only a short rectal stump residual after the original resection as opposed to the other patients who had at least the sigmoid colon preserved.

DISCUSSION

Patients with irreversible IF and who are TPN dependent have poor quality of life and reduced long-term survival.^1,6 Intestinal transplantation is the treatment of choice for these patients whose life expectancy is jeopardized by the complications of TPN.^12–14

Because of improved results of intestinal transplantation in the most recent years, the number of patient listed has gradually increased and almost reached 200 patients in the United States in 2004. The median time to transplant is more than 240 days, and children of any ages wait longer for intestine transplant than adults. Approximately three fourths of the patients awaiting intestinal transplant are children and the majority of them are less than 5 years of age.

Despite the relative short waiting time, the waiting-list mortality is the highest in solid organ transplant, averaging 30% per year in the pediatric population of age 0 to 5 years.⁴ It must be noted that almost all the deaths on the waiting list occur in candidates for combined liver-bowel transplant. Comorbidities (particularly line infection and sepsis) may cause a significant delay in the timing of transplantation in these patients. In addition, most patients are referred for intestinal transplant late in the course of their disease with already developed end-stage liver disease (ESLD), which constitutes the major risk for early mortality on the waiting list. Indeed, a large subset of patients, adults and pediatrics, are referred for combined liver-intestine transplantation with a lower probability of being transplanted and a higher mortality rate.^4–5 Given the small number of patients waiting for bowel transplantation in the United States (only 180–200 currently), the number of potentially available cadaver donors should easily satisfy the demand. However, delay in transplantation persists, maybe because of inadequate ability of offering suitable organs by organ procurement agencies.

LR-SBTx virtually eliminates the waiting time, and can therefore reduce the mortality rate on waiting list and minimize the risk of progression of liver disease to ESLD with obvious advantages especially for pediatric patients. Furthermore, the recent introduction of combined liver-bowel transplant from our group may allow timely treatment even for patient affected by combined intestinal and hepatic failure.¹¹

Moreover, LR-SBTx is an elective procedure and can be performed when the donor and the recipient conditions are optimal and the donor bowel preparation can be easily performed, leading to a decreased risk of infectious complications.

In a previous analysis of 50 SBTx in pediatric recipients, it was shown that preservation time was the most significant factor in inducing bacterial translocation.¹⁵

Additional mucosal injury can be triggered by hemodynamic instability of the donor and subsequent splanchnic hypoperfusion. LR-SBTx virtually eliminates this risk and can be performed with a very short cold ischemic time. Our preliminary data suggest a reduced incidence of infectious complications in LR-SBTx.¹⁶

An immunologic advantage can be also theoretically obtained with LR-SBTx, since optimal HLA matching can be reached between related donor and recipient. Given the relatively small size of the world experience with living donor bowel transplant, it is not possible to come to a final conclusion in relation to the role of HLA matching. The excellent results obtained in the setting of recipients of fully matched intestinal graft are suggestive of a potential benefit. However, at this stage, there are no data available to demonstrate any beneficial effect of HLA matching in bowel transplantation. Recent series of cadaver bowel transplants in leading centers have reported a low rejection rate despite poor HLA matching.

Our own series, although small, represents the largest single-institution experience (12 cases of the 32 reported worldwide) and has the merit of using standardized technique and immunosuppressive protocol. In our series, we encountered only one episode of rejection during the first year posttransplant (9%), which compares very well with rejection rates in cadaver bowel transplant. According to registry data, 56% of the graft failures in cadaver bowel transplant are secondary to acute rejection, an event that has not occurred inour experience with LR-SBTx.⁴ Interestingly, we did not document any acute rejection during the first year after transplant in patients receiving an intestinal graft with at least one haplotype match, suggesting a beneficial effect of HLA matching. The 2 episodes of late acute rejection were related to overt noncompliance with immunosuppressive therapy, admitted by the patients and confirmed by laboratory testing. With the obvious limitation of the small number of cases performed, the favorable results in terms of rejection rates may be reasonably attributed to the short ischemia time and the better HLA matching.

Finally, the smaller segmental grafts can reduce the size-match problem at least in adult patients with a retracted abdominal cavity due to multiple laparotomies, loss of abdominal wall, or severe adhesions.

The goal of LR-SBTx is to achieve an acceptable survival rate and TPN independence for the recipient without compromising the health status of the donor.

Even though the donor does not undergo the operation to improve his own health status, potential psychologic benefits of intestinal donation have been suggested.⁶

This may be particularly rewarding for parents donating to their sick child, helping in reducing their feeling of helplessness.

The first living donor small bowel transplantation using a standardized technique was performed by Gruessner¹² and has constituted the conceptual and technical bases for the 12 living donor small bowel transplants performed at our center. The length of the graft is a balance between patient and donor needs. We found that a graft of 200 cm in adult recipients and 150 to 180 cm in pediatric recipients is sufficient to obtain TPN independence. This amount of bowel corresponds to approximately 40% of the total bowel length in the donor. Preservation of the last 20 cm of the terminal ileum is critical in preventing lipid and/or vitamin B12 malabsorption. We have previously reported our excellent track record with segmental ileal resection in our bowel transplant donor, with no significant technical complications.⁹ The period of partial intestinal insufficiency that can be characterized by increased number of bowel movements, weight loss, and vitamin B12 deficiency has been limited in time (4–6 weeks), causing minimal discomfort for the donors. At the present time, no donor is complaining of diarrhea, new onset of food intolerance, weight loss, or signs of vitamin B12 malabsorption.

Our patient and graft survivals are comparable with current results with cadaver bowel transplant, supporting the clinical applicability of LR-SBTx.⁵ All the recipients were weaned off from TPN, which was discontinued at an average of 8 days after transplantation. Although intravenous fluid administration was required during the first months, the segmental graft underwent complete functional adaptation within 6 months, leading to a stable weight, normal nutritional parameters with unrestricted general diet, and improved quality of life.¹⁷ All pediatric recipients showed improvement in growth, level of activity, and interaction with peers.

Of note, living-related bowel transplantation is also cost-effective: based on Medicare data, the procedure becomes effective from the first year posttransplantation and, when successful, provides optimal rehabilitation in these patients.¹⁸

CONCLUSION

Our experience suggests that LR-SBTx is technically feasible and it is associated with very low morbidity for the donors and acceptable outcomes for the recipients. The option should be considered in bowel transplant candidates with an available donor at low surgical risk. We think that if the donor is an identical twin or a HLA-identical sibling, LR-SBTx is the procedure of choice. However, our data suggest that if the donor has at least one haplotype match, the rejection rate is very low. In pediatric patients, LR-SBTx may be an attractive alternative to cadaver bowel transplant to reduce the mortality on the waiting list, especially in children less than 5 years of age. Pediatric patients affected by combined intestinal and hepatic failure may also benefit from combined living donor liver/bowel transplant. Of course, further study in a larger number of recipients is needed to confirm our initial findings.

Footnotes

Reprints: Enrico Benedetti, MD, FACS, 840 South Wood Street, Suite 402, Chicago, IL 60612. E-mail: Enrico/at/uic.edu.

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