Pediatric Intestinal and Multivisceral Transplantation
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Intestinal failure in infants and children is a devastating condition. Total parenteral nutrition (TPN) is the treatment of choice for patients with intestinal failure. Advancements in neonatal care, nutritional support, and surgical techniques have improved the survival of children with intestinal failure. However, intestinal transplantation remains one of the treatment options for this condition.
Intestinal and multivisceral transplantation provides an alternative for patients who have life-threatening complications of TPN. Recent improvements in surgical technique, the monitoring and diagnosis of rejection, and cytomegalovirus (CMV) prophylaxis and the development of improved immunosuppression have paved the way for significant improvements in patient and graft survival rates. This article reviews the current status of intestinal and multivisceral transplantation, with emphasis on the authors’ experience at the University of Miami.
Carrel performed the first experimental intestinal transplantation in 1902. [1] Half a century later, in 1959, Lillehei demonstrated successful intestinal autotransplantation after cold preservation. [2] Experimental multivisceral transplantation (termed polysplanchnic transplantation) was pioneered by Starzl in 1960. [3] The earliest attempts at clinical intestinal transplantation were unsuccessful because of what appeared to be insurmountable barriers: graft rejection and infectious complications. [4, 5]
The first successful intestinal transplantations occurred in the late 1980s. Grant reported successful intestinal transplantation in pigs with cyclosporine use in 1988. [6] Starzl reported the first clinical successful multivisceral transplantation in 1987. [7] In 1988, Goulet and Deltz independently reported the first successful isolated intestine transplantations. [6] Grant reported the first combined liver and intestine transplantation under cyclosporine-based immunosuppression in 1990. [8] Starzl, Todo, and Tzakis pioneered intestinal transplantation with tacrolimus in the early 1990s. [7, 9, 10, 11, 12] As a result, the number of centers performing the procedures increased. [13, 14]
The intestinal and multivisceral transplantation program at the University of Miami was started in 1994. Through May 2012, 349 intestinal transplantations have been performed, including 309 primary intestinal transplantations (80 isolated intestine, 36 combined liver-intestine, 28 modified multivisceral, and 165 multivisceral transplantations) and 40 retransplantations (16 isolated intestine, 2 combined liver-intestine, 5 modified multivisceral and 17 multivisceral transplantations).
Short bowel syndrome is often the result of extensive intestinal resection for multiple pathophysiologies, such as volvulus, trauma, tumor, and thrombosis. An inadequate absorptive surface results in an inadequate energy intake and malabsorption of vitamin B-12 and other vitamins. Calcium and magnesium deficiencies can lead to neurologic complications such as encephalopathy, tetany, and convulsions. Intestinal failure with hyperalimentation causes liver failure. Patient with long-term hyperalimentation usually have complications, including line sepsis, thrombosed veins, and liver dysfunction. [15]
No database reports the exact incidence of short bowel syndrome. However, the incidence is estimated to be 3-5 patients per 100,000 births per year. [16, 17]
The causes of intestinal failure include the following:
Mesenteric thrombosis
Volvulus
Trauma
Pseudoobstruction
Microvillus inclusion disease
Massive resection of the intestine
At the University of Miami, all patients with intestinal failure that necessitated transplantation had TPN-related complications, and most had concurrent TPN-induced liver failure. The causes of intestinal failure and the number of patients affected are as follows:
Gastroschisis – 42
Necrotizing enterocolitis – 39
Mesenteric thrombosis – 35
Volvulus – 30
Hirschsprung disease – 19
Intestinal atresia – 19
Trauma – 18
Pseudo-obstruction – 17
Desmoid tumor – 16
Crohn disease – 13
Megacystic microcolon -12
Microvillus inclusion – 10
Others – 39
Retransplant – 40
Extensive resection of the small bowel can cause short bowel syndrome. Extensive loss of the intestinal mucosa surface results in an inadequate absorptive surface. An inadequate caloric intake and malabsorption of vitamins, including vitamin B-12, can result in severe malnutrition and neurological symptoms. Inadequate electrolyte absorption (eg, calcium, magnesium) also results in severe neurological complications, including encephalopathy, tetany, and convulsions.
All patients who received intestinal or multivisceral transplants at the University of Miami had life-threatening TPN-related complications, such as sepsis, central vein thrombosis, and cholestatic TPN-induced liver failure.
The recipients of isolated intestinal transplants had short bowel syndrome with severe central vein thrombosis and line sepsis. Liver functions were preserved.
The recipients of liver and small bowel transplants had short bowel syndrome and cholestatic TPN-induced liver failure. Total bilirubin levels were usually higher than 15 mg/dL.
The recipients of multivisceral transplants had short bowel syndrome and cholestatic TPN-induced liver failure. In addition, they usually had a history of surgery, abdominal trauma, motility disorders, tumors, and other etiologies.
The role of TPN in short bowel syndrome is established, and long-term TPN is the treatment of choice for these patients because of its well-documented long-term safety. [18] A subset of patients with short bowel syndrome cannot tolerate TPN because of frequent episodes of catheter-associated sepsis, catheter-associated vascular thrombosis, or TPN-induced cholestasis. This is the subset of patients who need intestinal or multivisceral transplantation.
Line infection is the most common cause of fever and chills for patients with TPN. Gram-positive bacteria are the common pathogens. TPN-induced liver failure is the most common cause of jaundice in TPN therapy. If liver failure progresses, intestinal transplantation or intestinal and liver transplantation is indicated. See Etiology for the causes of intestinal failure and the experience at the University of Miami.
Liver function test findings must be carefully evaluated for derangements that suggest the need for biopsy evaluation. If significant fibrosis, macrosteatosis, or cirrhosis is present on liver biopsy findings, then liver transplantation is necessary. Evaluation of renal function is critical because of the need for long-term use of tacrolimus postoperatively.
For isolated intestinal transplantation in patients with normal anatomy, the superior mesenteric artery (SMA) of the donor is procured with the aortic cuff. The portal vein is cut above the confluence of the superior mesenteric and splenic vein. If a right replaced hepatic artery from the SMA is present, the SMA is cut distal to the takeoff of the replaced hepatic artery. The SMA of the donor is anastomosed to the recipient SMA or the abdominal aorta. The portal vein of the donor is anastomosed to the portal vein or the inferior vena cava of the recipient.
For liver and intestinal or multivisceral transplantation, the celiac trunk and SMA are procured with the abdominal aorta and thoracic aorta. The inferior vena cava is procured from the iliac vein bifurcation to above the diaphragm. The anastomosis is performed between the donor abdominal aorta and the recipient abdominal aorta in an end-to-side fashion.
Transplantation is contraindicated if the recipient has active infection such as pneumonia, sepsis, or fungal infection. Because of the immunosuppressive medication used in the postoperative period, the infection must be controlled by antibiotics or antifungal therapy before transplantation.
Lifelong immunosuppression after transplant is necessary. The patient and family need to have commitment for the compliance of the medication. If patient does not want to take medications, transplantation is contraindicated.
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Seigo Nishida, MD, PhD Professor of Clinical Surgery, Miami Transplant Institute, Department of Surgery, University of Miami, Leonard M Miller School of Medicine
Seigo Nishida, MD, PhD is a member of the following medical societies: American College of Surgeons, American Society of Transplant Surgeons, Society for Surgery of the Alimentary Tract, Society of University Surgeons, Transplantation Society, Japan Surgical Society
Disclosure: Nothing to disclose.
Andreas G Tzakis, MD, PhD Professor of Surgery, University of Miami, Leonard M Miller School of Medicine
Andreas G Tzakis, MD, PhD is a member of the following medical societies: American Association for the Study of Liver Diseases, American College of Angiology, American College of Surgeons, American Medical Association, American Society of Transplant Surgeons, American Spinal Injury Association, International College of Surgeons, Society of University Surgeons
Disclosure: Nothing to disclose.
David M Levi, MD Professor of Clinical Surgery, Department of Surgery, Division of Liver and Gastrointestinal Transplantation, Division of General Surgery, Jackson Memorial Hospital, Miller School of Medicine, University of Miami
David M Levi, MD is a member of the following medical societies: Alpha Omega Alpha, American Association for the Study of Liver Diseases, American College of Surgeons, American Society of Transplant Surgeons, Phi Beta Kappa, International Liver Transplantation Society, Transplantation Society
Disclosure: Nothing to disclose.
Tomoaki Kato, MD Associate Professor of Clinical Surgery, Department of Surgery, Division of Liver and Gastrointestinal Transplantation, Miller School of Medicine, University of Miami
Tomoaki Kato, MD is a member of the following medical societies: American Gastroenterological Association, American Medical Association, American Society of Transplant Surgeons
Disclosure: Nothing to disclose.
Jose R Nery, MD Medical Director, Good Samaritan Community Health Care Center
Jose R Nery, MD is a member of the following medical societies: American Society of Transplant Surgeons, International Liver Transplantation Society, Transplantation Society
Disclosure: Nothing to disclose.
Juan Madariaga, MD
Juan Madariaga, MD is a member of the following medical societies: American Medical Association, American Society of Transplant Surgeons, Medical Society of the State of New York, Society of Surgical Oncology
Disclosure: Nothing to disclose.
G Patricia Cantwell, MD, FCCM Professor of Clinical Pediatrics, Chief, Division of Pediatric Critical Care Medicine, University of Miami Leonard M Miller School of Medicine/ Holtz Children’s Hospital, Jackson Memorial Medical Center; Medical Director, Palliative Care Team, Holtz Children’s Hospital; Medical Manager, FEMA, South Florida Urban Search and Rescue, Task Force 2
G Patricia Cantwell, MD, FCCM is a member of the following medical societies: American Academy of Hospice and Palliative Medicine, American Academy of Pediatrics, American Heart Association, American Trauma Society, National Association of EMS Physicians, Society of Critical Care Medicine, Wilderness Medical Society
Disclosure: Nothing to disclose.
Phillip Ruiz, Jr, MD, PhD Professor of Pathology, Department of Pathology and Surgery, Miller School of Medicine, University of Miami
Phillip Ruiz, Jr, MD, PhD is a member of the following medical societies: American Association for the Advancement of Science, American Association of Immunologists, American Society for Clinical Pathology, American Society of Nephrology, American Society of Transplant Surgeons, American Society of Transplantation, Clinical Immunology Society, Florida Medical Association, New York Academy of Sciences, Pan-American Medical Association of Central Florida, Southern Medical Association, United States and Canadian Academy of Pathology
Disclosure: Nothing to disclose.
Mary L Windle, PharmD Adjunct Associate Professor, University of Nebraska Medical Center College of Pharmacy; Editor-in-Chief, Medscape Drug Reference
Disclosure: Nothing to disclose.
Brian F Gilchrist, MD Surgeon-in-Chief of Pediatric Surgery, The Floating Hospital for Children at Tufts-New England Medical Center; Associate Professor, Department of Surgery, Tufts University School of Medicine
Brian F Gilchrist, MD is a member of the following medical societies: American College of Surgeons, American Pediatric Surgical Association, Society for Surgery of the Alimentary Tract
Disclosure: Nothing to disclose.
Stuart M Greenstein, MD Professor of Surgery, Albert Einstein College of Medicine; Consulting Surgeon, Department of Surgery, Division of Transplantation, Montefiore Medical Center
Stuart M Greenstein, MD is a member of the following medical societies: American Association for the Advancement of Science, American College of Surgeons, American Society of Transplant Surgeons, American Society of Transplantation, Association for Academic Surgery, International College of Surgeons, Medical Society of New Jersey, National Kidney Foundation, New York Academy of Sciences, Southeastern Surgical Congress
Disclosure: Nothing to disclose.
Casimir F Firlit, MD, PhD Director of Reconstructive Urology, Neuro-Urology and Fetal Urology at SSM Cardinal Glennon Children’s Medical Center.
Casimir F Firlit, MD, PhD is a member of the following medical societies: American Academy of Pediatrics, American College of Surgeons, American Medical Association, American Society of Transplant Surgeons, American Urological Association, Illinois State Medical Society
Disclosure: Nothing to disclose.
John F Thompson, MD Professor of Pediatrics, Director of Division of Pediatric Gastroenterology and Nutrition, University of Miami Miller School of Medicine
John F Thompson, MD is a member of the following medical societies: Alpha Omega Alpha, American Gastroenterological Association, and North American Society for Pediatric Gastroenterology and Nutrition
Disclosure: Nothing to disclose.
Acknowledgments
The authors gratefully acknowledge Jose Martinez, MD, for his support involving endoscopy and patient care. The authors also acknowledge Joseph Tector, MD, for his support of this manuscript. The authors would also like to thank Debbie Weppler, RN, for her contribution of intestinal patient management and data collection.
Pediatric Intestinal and Multivisceral Transplantation
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