- Email: [email protected]
Shortage of Donors for Intestinal Transplantation in São Paulo, Brazil
Shortage of Donors for Intestinal Transplantation in São Paulo, Brazil I.L. Calil, G.M. Andrade, F.H. Galvao*, A.Z.A. Leite, R.A. Pecora, A.W. Lee, and L.A.C. D’Albuquerque Department of Gastroenterology, University of São Paulo, São Paulo, Brazil
ABSTRACT Background. The number of deceased organ donors has decreased slightly over the past 4 years. Although the pool of intestinal transplantation candidates is relatively small, donor allocation is challenging because of the inability to maintain the donor in a good condition and the complexities involved in making a suitable weight match between donors and recipients. Our goal was to analyze the epidemiologic profile of potential donors based on the organs offered by the regional Organ Procurement Organization from Hospital das ClinicasUSP (OPO/HC-USP) and attempt to estimate possible matches and program viability. Methods. We retrospectively analyzed information from the OPO/HC-USP database regarding organs offered over the past 7 years as well as patients listed in our program. Data were collected regarding donor characteristics (eg, sex, age, race, body mass index, blood type, cause of death) and medical care details (eg, intensive care unit stay, use of vasopressor agents and antibiotics). Results. In this time period, there were 18,103 brain death notifications in the state of São Paulo; 5,202 (35%) became viable donors, resulting in 5,201 (99%) effectively used livers and kidneys. Most potential donors were male, in their 40s, white, and had blood type O. Only 3 potential donors from OPO/HC-USP would have reached the established minimum criteria for intestinal donation over these 7 years.
S
INCE THE INTRODUCTION OF parenteral nutrition (PN) in the late 1960s, PN has been the mainstay of therapy for patients with intestinal failure; contemporary multicenter studies, however, suggest that 1% to 26% of patients who are permanently PN-dependent develop severe complications and are therefore considered for intestinal transplantation (ITx) indications [1,2]. In adults, 5-year patient survival for those with PN failure (ie, complications that are considered indications for ITx) is 73% [2]. ITx is a consolidated therapy for intestinal failure and may dramatically improve patient survival. Despite continued improvements in the field of ITx, the long-term survival of intestinal allograft recipients remains inferior compared with survival rates in other forms of solid organ transplantation [3]. This outcome may be due to the susceptibility of the intestinal graft to warm and cold ischemia and immunologic injury starting during the process of brain death [4,5]. Inflammation of the intestine causes profound structural deterioration and increased permeability [6,7], and this injury is exacerbated by warm and cold ischemia during the preservation phase [8]. After engraftment into the 0041-1345/16 http://dx.doi.org/10.1016/j.transproceed.2015.10.081
450
recipient, reperfusions of the allograft completes the cascade. This process, termed ischemia/reperfusion injury, is closely related to early postoperative complications such as sepsis and acute rejection [9,10]. A clear description of donor criteria to discriminate between acceptable and unacceptable intestinal grafts is not available. This oversight could lead to the underutilization of intestinal grafts. Fischer-Fröhlich et al [11] reported on adequate studies exploring intestinal graft selection criteria; the majority of studies are single center and personal experiences. The US Organ Procurement and Transplantation Network [12] has defined a set of empiric donor-based criteria (Table 1). The justification for these network criteria is to help the transplantation team identify quality
*Address correspondence to Flavio Henrique Ferreira Galvao, MD, PhD, Laboratory of Experimental Transplant Surgery, LIM37, Liver Transplantation Division, University of São Paulo School of Medicine, Av. Dr. Arnaldo 455, Room 3210, 01246-903 São Paulo, SP, Brazil. E-mail: [email protected] ª 2016 by Elsevier Inc. All rights reserved. 360 Park Avenue South, New York, NY 10010-1710
Transplantation Proceedings, 48, 450e452 (2016)
INTESTINAL TRANSPLANTATION DONORS
donors. The goal of the present study was to analyze the epidemiologic profile of potential donors based on the organs offered by the regional Organ Procurement Organization from Hospital das Clinicas-USP (OPO/HC-USP) and to estimate possible matches and program viability. METHODS Brazil is the largest country in South America, and it performs approximately 1,500 liver transplantations per year. In 2010, the National Transplant System approved 2 centers to perform ITx in São Paulo. This state has a population of 44 million people, 15 million of whom live in the capital, São Paulo City. There are 9 organ procurement organizations in São Paulo state, and the biggest is located at Hospital das Clinicas de São Paulo. Despite almost doubling the annual number of liver transplant procedures in the last 10 years and improvements in notification, donor care, and organ procurement, indicators regarding donor profile and intestinal donor viability are still lacking. We retrospectively analyzed information from the OPO/HC-USP database on organs offered between January 2007 and December 2014, as well as from patients listed in the ITx program. Data regarding donor description profile (eg, sex, age, race, body mass index, blood type, cause of death), in addition to details related to medical care (eg, intensive care unit stay, use of vasopressors, antibiotic use) and laboratory values, were collected.
451 Table 2. Donor Characteristics From OPO/HC-USP, 2007e2014 Characteristic
Value
Age, y Male sex, no. (%) Race, no. (%) White Pardo African American Asian Weight, kg Height, cm BMI, median, kg/m2 Blood type, no. (%) O A B AB Plasma sodium, mEq/dL Use of pressor agents, no. (%) Norepinephrine, median dose, mg/kg/min Dobutamine, median dose, mg/kg/min Dopamine, median dose, mg/kg/min ICU stay, median, d
0.2e83 (46) 627 (59) 555 (52) 360 (34) 134 (13) 14 (1) 7e180 (75) 50e195 (168) 26 508 (48) 384 (37) 125 (12) 34 (3) 111e219 (153) 909 (94) 880 (95)e0.28 26 (3)e5 69 (7)e5.19 4
Unless otherwise indicated, values are given as minimum-maximum (medium). Abbreviations: BMI, body mass index; ICU, intenstive care unit; OPO/HCUSP, Organ Procurement Organization from Hospital das Clinicas-USP.
RESULTS
From January 2007 to December 2014, there were 18,103 brain death notifications in the state of São Paulo; 5,202 (28.7%) became viable donors, resulting in 5,201 (99%) effectively used livers and kidneys. From the OPO/HC-USP, these numbers were 2,918, 1,063 (36.4%), and 991 (93%), respectively. Most donors were white men; common blood types were O and A, respectively, and the donor’s median intensive care unit stay was 4 days (Table 2). When we analyzed the laboratory data, there was a high rate of vasoactive drug use (4% with >2 drugs), high serum creatinine levels (27.2% measured >2 mg/dL), and high serum sodium levels (13.4% measured >170 mEq/L) (Table 3). Table 1. OPTN Donor Criteria Acceptance for an Intestinal Graft
Body proportion is also very important to avoid mismatch in ITx, mainly because recipients who remain with the abdominal wall opened have lower survival than those who can close. Our patients on the transplant list had a mean weight of 59.8 kg with a mean body mass index of 21.75 kg/m2; the mean weight of the donors was 73 kg, with a mean body mass index of 26.1 kg/m2 (Table 4). In this scenario, we found that only 3 potential donors from OPO/HC-USP would have reached the established minimum criteria for intestinal donation over these 7 years. DISCUSSION
An important development has been reached concerning understanding the minimum criteria for ITx donation. This knowledge supports a lower rate of ischemia/reperfusion
Criteria
Brain death CIT <9 h Donor age <50 y Other organs (except for intestine) retrieved AST and ALT <500 U/L Last serum sodium measurement <170 mEq/L Serum creatinine <2 mg/dL (if the donor is aged >1 y; <1 mg/dL if the donor is aged <1 y) Negative virology results (HIV, HBsAg/cAb, HCVAb) Maximum of two vasopressors Resuscitation <15 min in cardiac arrest after BD declaration
Criteria
OPO/HC-USP
Mazariegos et al
Age >50 y Anti-HCV-positive Anti-HBc-positive ASTor ALT >500 U/L Sodium >170 mEq/dL Use of >2 vasopressor agents Creatinine >2 mg/dL
38 0.12 8 2.6 13.4 4 27.2
32 27 1 1.4 0.2 1.2 5.2
Abbreviations: ALT, alanine aminotransferase; AST, aspartate aminotransferase; CIT, cold ischemic time; HbsAg/cAb, hepatitis B surface antigen/core antibody; HCVAb, hepatitis C virus antibody; HIV, human immunodeficiency virus; OPTN, US Organ Procurement and Transplantation Network.
Values are given as %. Abbreviations: ALT, alanine aminotransferase; AST, aspartate aminotransferase; HBc, hepatitis B core antigen; HCV, hepatitis c virus; OPO/HC-USP, Organ Procurement Organization from Hospital das Clinicas-USP.
Table 3. Comparative Database From OPO/HC-USP and Mazariegos et al [12]
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CALIL, ANDRADE, GALVAO ET AL
Table 4. Comparative Analysis Between Body Biometrics of the Donors and OPO/HC-USP Recipients Size Match
Donor
Recipient
Weight, kg Height, cm BMI, kg/m2
73 18.1 170 20 26.1 4.7
59.8 6.19 166 11 21.75 3.82
Data are given as mean SD. Abbreviation: OPO/HC-USP, Organ Procurement Organization from Hospital das Clinicas-USP.
injury and, consequently, a better survival of intestinal grafts. The 10-year graft survival rate of 43% [13] indicates that more research is needed to improve the benefits of this transplantation option. ITx is a highly complex procedure that depends on a health system that is well structured by the caregiver to achieve long-term monitoring of the recipient. Thus, Brazil needs network improvements to health care in all aspects, including in the care of donors. Progressive knowledge in intestinal rehabilitation, care for the parenteral catheters, new nutritional formulations that are less harmful on the liver, and intestinal lengthening surgeries are possible reasons for the current reduction in ITx indications [13]. When transplantation is inevitable, other proposals should be considered, such as reducing the intestinal graft for placement in the receiver cavity. This technique decreases the donor restrictions regarding body mass disparity. Other possible techniques include the living donor intestine. Research in this direction is improving, especially in countries in which deceased donations are scarce due to religious reasons. Our transplantation group works closely with the government to improve the quality of donors, educate health professionals about the entire process of ITx, and increase the number of intestinal rehabilitation programs in the country. CONCLUSIONS
The appropriate proportion between the donor and the recipient is considered critical to the successful outcome of the transplant, and this requirement restricts the pool of donors. In our assessment, the analysis of donor and recipient weight limited the supply of donors. In the
OPO/HC-USP, we found only 3 donors with the minimum characteristics to be a appropriate donor for ITx. It would be advisable that Brazilian health authorities dedicate financial and logistics efforts toward improving donor care in order to increase the probabilities of better donor-receipient matches.
REFERENCES [1] Squires RH, Duggan C, Teitlelbaum DH, et al. Natural history of pediatric intestinal failure: initial report from the Pediatric Intestinal Failure Consortium. J Pediatr 2012;161:723e728.e2. [2] Pironi L, Joly F, Forbes A, et al. Long-term follow-up of patients on home parenteral nutrition in Europe: implications for intestinal transplantation. Gut 2011;60:17e25. [3] Fishbein TM. Intestinal transplantation. N Engl J Med 2009;361:998. [4] Zweers N, Petersen AH, van der Hoeven JA, et al. Donor brain death aggravates chronic rejection after lung transplantation in rats. Transplantation 2004;78:1251. [5] Jassem W, Koo DD, Muiesan P, et al. Non-heart-beating versus cadaveric and living-donor livers: differences in inflammatory markers before transplantation. Transplantation 2003;75:1386. [6] Koudstaal LG, ’t Hart NA, Ottens PJ, et al. Brain death induces inflammation in the donor intestine. Transplantation 2008;86:148e54. [7] Koudstaal LG, ’t Hart NA, van den Berg A, Olinga P, van Goor H, Ploeg RJ, et al. Brain death causes structural and inflammatory changes in donor intestine. Transplant Proc 2005;37: 448e9. [8] Thuijls G, de Haan JJ, Derikx JP, et al. Intestinal cytoskeleton degradation precedes tight junction loss following hemorrhagic shock. Shock 2009;31:164. [9] Varga J, Stasko P, Toth S, Pristasova Z, Bujdos M, Pomfy M. Development of jejunal graft damage during intestinal transplantation. Ann Transplant 2009;14:62. [10] Tilney NL, Guttmann RD. Effects of initial ischemia/ reperfusion injury on the transplanted kidney. Transplantation 1997;64:945. [11] Fischer-Fröhlich CL, Konigsrainer A, Schaffer R, et al. Organ donation: when should we consider intestinal donation. Transpl Int 2012;25:1229. [12] Mazariegos GV, Steffick DE, Horslen S, et al. Intestine transplantation in the United States, 1999-2008. Am J Transplant 2010;10:1020. [13] Grant D, Abu-Elmagd K, Mazariegos G, Vianna R, Langnas A, Mangus R, et al. Intestinal Transplant Association. Intestinal transplant registry report: global activity and trends. Am J Transplant 2015;15:210e9.
ABSTRACT Background. The number of deceased organ donors has decreased slightly over the past 4 years. Although the pool of intestinal transplantation candidates is relatively small, donor allocation is challenging because of the inability to maintain the donor in a good condition and the complexities involved in making a suitable weight match between donors and recipients. Our goal was to analyze the epidemiologic profile of potential donors based on the organs offered by the regional Organ Procurement Organization from Hospital das ClinicasUSP (OPO/HC-USP) and attempt to estimate possible matches and program viability. Methods. We retrospectively analyzed information from the OPO/HC-USP database regarding organs offered over the past 7 years as well as patients listed in our program. Data were collected regarding donor characteristics (eg, sex, age, race, body mass index, blood type, cause of death) and medical care details (eg, intensive care unit stay, use of vasopressor agents and antibiotics). Results. In this time period, there were 18,103 brain death notifications in the state of São Paulo; 5,202 (35%) became viable donors, resulting in 5,201 (99%) effectively used livers and kidneys. Most potential donors were male, in their 40s, white, and had blood type O. Only 3 potential donors from OPO/HC-USP would have reached the established minimum criteria for intestinal donation over these 7 years.
S
INCE THE INTRODUCTION OF parenteral nutrition (PN) in the late 1960s, PN has been the mainstay of therapy for patients with intestinal failure; contemporary multicenter studies, however, suggest that 1% to 26% of patients who are permanently PN-dependent develop severe complications and are therefore considered for intestinal transplantation (ITx) indications [1,2]. In adults, 5-year patient survival for those with PN failure (ie, complications that are considered indications for ITx) is 73% [2]. ITx is a consolidated therapy for intestinal failure and may dramatically improve patient survival. Despite continued improvements in the field of ITx, the long-term survival of intestinal allograft recipients remains inferior compared with survival rates in other forms of solid organ transplantation [3]. This outcome may be due to the susceptibility of the intestinal graft to warm and cold ischemia and immunologic injury starting during the process of brain death [4,5]. Inflammation of the intestine causes profound structural deterioration and increased permeability [6,7], and this injury is exacerbated by warm and cold ischemia during the preservation phase [8]. After engraftment into the 0041-1345/16 http://dx.doi.org/10.1016/j.transproceed.2015.10.081
450
recipient, reperfusions of the allograft completes the cascade. This process, termed ischemia/reperfusion injury, is closely related to early postoperative complications such as sepsis and acute rejection [9,10]. A clear description of donor criteria to discriminate between acceptable and unacceptable intestinal grafts is not available. This oversight could lead to the underutilization of intestinal grafts. Fischer-Fröhlich et al [11] reported on adequate studies exploring intestinal graft selection criteria; the majority of studies are single center and personal experiences. The US Organ Procurement and Transplantation Network [12] has defined a set of empiric donor-based criteria (Table 1). The justification for these network criteria is to help the transplantation team identify quality
*Address correspondence to Flavio Henrique Ferreira Galvao, MD, PhD, Laboratory of Experimental Transplant Surgery, LIM37, Liver Transplantation Division, University of São Paulo School of Medicine, Av. Dr. Arnaldo 455, Room 3210, 01246-903 São Paulo, SP, Brazil. E-mail: [email protected] ª 2016 by Elsevier Inc. All rights reserved. 360 Park Avenue South, New York, NY 10010-1710
Transplantation Proceedings, 48, 450e452 (2016)
INTESTINAL TRANSPLANTATION DONORS
donors. The goal of the present study was to analyze the epidemiologic profile of potential donors based on the organs offered by the regional Organ Procurement Organization from Hospital das Clinicas-USP (OPO/HC-USP) and to estimate possible matches and program viability. METHODS Brazil is the largest country in South America, and it performs approximately 1,500 liver transplantations per year. In 2010, the National Transplant System approved 2 centers to perform ITx in São Paulo. This state has a population of 44 million people, 15 million of whom live in the capital, São Paulo City. There are 9 organ procurement organizations in São Paulo state, and the biggest is located at Hospital das Clinicas de São Paulo. Despite almost doubling the annual number of liver transplant procedures in the last 10 years and improvements in notification, donor care, and organ procurement, indicators regarding donor profile and intestinal donor viability are still lacking. We retrospectively analyzed information from the OPO/HC-USP database on organs offered between January 2007 and December 2014, as well as from patients listed in the ITx program. Data regarding donor description profile (eg, sex, age, race, body mass index, blood type, cause of death), in addition to details related to medical care (eg, intensive care unit stay, use of vasopressors, antibiotic use) and laboratory values, were collected.
451 Table 2. Donor Characteristics From OPO/HC-USP, 2007e2014 Characteristic
Value
Age, y Male sex, no. (%) Race, no. (%) White Pardo African American Asian Weight, kg Height, cm BMI, median, kg/m2 Blood type, no. (%) O A B AB Plasma sodium, mEq/dL Use of pressor agents, no. (%) Norepinephrine, median dose, mg/kg/min Dobutamine, median dose, mg/kg/min Dopamine, median dose, mg/kg/min ICU stay, median, d
0.2e83 (46) 627 (59) 555 (52) 360 (34) 134 (13) 14 (1) 7e180 (75) 50e195 (168) 26 508 (48) 384 (37) 125 (12) 34 (3) 111e219 (153) 909 (94) 880 (95)e0.28 26 (3)e5 69 (7)e5.19 4
Unless otherwise indicated, values are given as minimum-maximum (medium). Abbreviations: BMI, body mass index; ICU, intenstive care unit; OPO/HCUSP, Organ Procurement Organization from Hospital das Clinicas-USP.
RESULTS
From January 2007 to December 2014, there were 18,103 brain death notifications in the state of São Paulo; 5,202 (28.7%) became viable donors, resulting in 5,201 (99%) effectively used livers and kidneys. From the OPO/HC-USP, these numbers were 2,918, 1,063 (36.4%), and 991 (93%), respectively. Most donors were white men; common blood types were O and A, respectively, and the donor’s median intensive care unit stay was 4 days (Table 2). When we analyzed the laboratory data, there was a high rate of vasoactive drug use (4% with >2 drugs), high serum creatinine levels (27.2% measured >2 mg/dL), and high serum sodium levels (13.4% measured >170 mEq/L) (Table 3). Table 1. OPTN Donor Criteria Acceptance for an Intestinal Graft
Body proportion is also very important to avoid mismatch in ITx, mainly because recipients who remain with the abdominal wall opened have lower survival than those who can close. Our patients on the transplant list had a mean weight of 59.8 kg with a mean body mass index of 21.75 kg/m2; the mean weight of the donors was 73 kg, with a mean body mass index of 26.1 kg/m2 (Table 4). In this scenario, we found that only 3 potential donors from OPO/HC-USP would have reached the established minimum criteria for intestinal donation over these 7 years. DISCUSSION
An important development has been reached concerning understanding the minimum criteria for ITx donation. This knowledge supports a lower rate of ischemia/reperfusion
Criteria
Brain death CIT <9 h Donor age <50 y Other organs (except for intestine) retrieved AST and ALT <500 U/L Last serum sodium measurement <170 mEq/L Serum creatinine <2 mg/dL (if the donor is aged >1 y; <1 mg/dL if the donor is aged <1 y) Negative virology results (HIV, HBsAg/cAb, HCVAb) Maximum of two vasopressors Resuscitation <15 min in cardiac arrest after BD declaration
Criteria
OPO/HC-USP
Mazariegos et al
Age >50 y Anti-HCV-positive Anti-HBc-positive ASTor ALT >500 U/L Sodium >170 mEq/dL Use of >2 vasopressor agents Creatinine >2 mg/dL
38 0.12 8 2.6 13.4 4 27.2
32 27 1 1.4 0.2 1.2 5.2
Abbreviations: ALT, alanine aminotransferase; AST, aspartate aminotransferase; CIT, cold ischemic time; HbsAg/cAb, hepatitis B surface antigen/core antibody; HCVAb, hepatitis C virus antibody; HIV, human immunodeficiency virus; OPTN, US Organ Procurement and Transplantation Network.
Values are given as %. Abbreviations: ALT, alanine aminotransferase; AST, aspartate aminotransferase; HBc, hepatitis B core antigen; HCV, hepatitis c virus; OPO/HC-USP, Organ Procurement Organization from Hospital das Clinicas-USP.
Table 3. Comparative Database From OPO/HC-USP and Mazariegos et al [12]
452
CALIL, ANDRADE, GALVAO ET AL
Table 4. Comparative Analysis Between Body Biometrics of the Donors and OPO/HC-USP Recipients Size Match
Donor
Recipient
Weight, kg Height, cm BMI, kg/m2
73 18.1 170 20 26.1 4.7
59.8 6.19 166 11 21.75 3.82
Data are given as mean SD. Abbreviation: OPO/HC-USP, Organ Procurement Organization from Hospital das Clinicas-USP.
injury and, consequently, a better survival of intestinal grafts. The 10-year graft survival rate of 43% [13] indicates that more research is needed to improve the benefits of this transplantation option. ITx is a highly complex procedure that depends on a health system that is well structured by the caregiver to achieve long-term monitoring of the recipient. Thus, Brazil needs network improvements to health care in all aspects, including in the care of donors. Progressive knowledge in intestinal rehabilitation, care for the parenteral catheters, new nutritional formulations that are less harmful on the liver, and intestinal lengthening surgeries are possible reasons for the current reduction in ITx indications [13]. When transplantation is inevitable, other proposals should be considered, such as reducing the intestinal graft for placement in the receiver cavity. This technique decreases the donor restrictions regarding body mass disparity. Other possible techniques include the living donor intestine. Research in this direction is improving, especially in countries in which deceased donations are scarce due to religious reasons. Our transplantation group works closely with the government to improve the quality of donors, educate health professionals about the entire process of ITx, and increase the number of intestinal rehabilitation programs in the country. CONCLUSIONS
The appropriate proportion between the donor and the recipient is considered critical to the successful outcome of the transplant, and this requirement restricts the pool of donors. In our assessment, the analysis of donor and recipient weight limited the supply of donors. In the
OPO/HC-USP, we found only 3 donors with the minimum characteristics to be a appropriate donor for ITx. It would be advisable that Brazilian health authorities dedicate financial and logistics efforts toward improving donor care in order to increase the probabilities of better donor-receipient matches.
REFERENCES [1] Squires RH, Duggan C, Teitlelbaum DH, et al. Natural history of pediatric intestinal failure: initial report from the Pediatric Intestinal Failure Consortium. J Pediatr 2012;161:723e728.e2. [2] Pironi L, Joly F, Forbes A, et al. Long-term follow-up of patients on home parenteral nutrition in Europe: implications for intestinal transplantation. Gut 2011;60:17e25. [3] Fishbein TM. Intestinal transplantation. N Engl J Med 2009;361:998. [4] Zweers N, Petersen AH, van der Hoeven JA, et al. Donor brain death aggravates chronic rejection after lung transplantation in rats. Transplantation 2004;78:1251. [5] Jassem W, Koo DD, Muiesan P, et al. Non-heart-beating versus cadaveric and living-donor livers: differences in inflammatory markers before transplantation. Transplantation 2003;75:1386. [6] Koudstaal LG, ’t Hart NA, Ottens PJ, et al. Brain death induces inflammation in the donor intestine. Transplantation 2008;86:148e54. [7] Koudstaal LG, ’t Hart NA, van den Berg A, Olinga P, van Goor H, Ploeg RJ, et al. Brain death causes structural and inflammatory changes in donor intestine. Transplant Proc 2005;37: 448e9. [8] Thuijls G, de Haan JJ, Derikx JP, et al. Intestinal cytoskeleton degradation precedes tight junction loss following hemorrhagic shock. Shock 2009;31:164. [9] Varga J, Stasko P, Toth S, Pristasova Z, Bujdos M, Pomfy M. Development of jejunal graft damage during intestinal transplantation. Ann Transplant 2009;14:62. [10] Tilney NL, Guttmann RD. Effects of initial ischemia/ reperfusion injury on the transplanted kidney. Transplantation 1997;64:945. [11] Fischer-Fröhlich CL, Konigsrainer A, Schaffer R, et al. Organ donation: when should we consider intestinal donation. Transpl Int 2012;25:1229. [12] Mazariegos GV, Steffick DE, Horslen S, et al. Intestine transplantation in the United States, 1999-2008. Am J Transplant 2010;10:1020. [13] Grant D, Abu-Elmagd K, Mazariegos G, Vianna R, Langnas A, Mangus R, et al. Intestinal Transplant Association. Intestinal transplant registry report: global activity and trends. Am J Transplant 2015;15:210e9.