Predictors of Enteral Autonomy in Children with Intestinal Failure:A Multicenter Cohort Study

Faraz A. Khan, MD1, Robert H. Squires, MD2, Heather J. Litman, PhD1, Jane Balint, MD3, Beth A. Carter, MD4,

Jeremy G. Fisher, MD1, Simon P. Horslen, MB, ChB5, Tom Jaksic, MD, PhD1, Samuel Kocoshis, MD6, J. Andres Martinez, MD7,

Soden, MD10, Debra Sudan, MD11,

, MD14, Paul W. Wales, MD, MSc15,

al Failure Consortium*

ht to determine the cumulative incidencecharacteristics associated with enteral

iatric Intestinal Failure Consortium wasntestinal diseases during infancy withy was defined as PN discontinuation

(16.2-51.5) months. Enteral autonomy(43%) patients died or underwent trans-

sis identified necrotizing enterocolitis (NEC; OR 2.42, 95% CI 1.33-4.47), care atPN Parenteral nutritionan IF site without an associated intestinal transplantation program (OR 2.73, 95% CI 1.56-4.78), and an intactileocecal valve (OR 2.80, 95% CI 1.63-4.83) as independent risk factors for enteral autonomy. A second model(n = 144) that included only patients with intraoperatively measured residual small bowel length found NEC(OR 3.44, 95% CI 1.36-8.71), care at a nonintestinal transplantation center (OR 6.56, 95% CI 2.53-16.98),and residual small bowel length (OR 1.04 cm, 95% CI 1.02-1.06 cm) to be independently associated with enteralautonomy.Conclusions A substantial proportion of infants with IF can achieve enteral autonomy. Underlying NEC, pre-served ileocecal valve, and longer bowel length are associated with achieving enteral autonomy. It is likelythat variations in institutional practices and referral patterns also affect outcomes in children with IF. (J Pediatr2015;167:29-34).

See editorial, p 6 andrelated article, p 35

Intestinal failure (IF) is characterized by the reduction of functional intestinalmass necessary to meet nutrient, electrolyte, and fluid requirements.1,2 Themost common cause of IF in children is a loss of intestine attributable to

congenital or acquired conditions that results in short bowel syndrome.3 Theinstitution of multidisciplinary care of patients with IF has reduced mortalitysubstantially,4 but significant morbidity remains for affected infants. Long-term use of parenteral nutrition (PN) is associated with multiple serious compli-cations, including mechanical, infectious, hepatic, and metabolic disease, as wellas financial and psychosocial morbities.5-9 Achievement of enteral autonomyavoids the significant morbidity associated with long-term dependence on PNand is therefore the primary aim of modern management of IF.10

From the 1Boston Childrens Hospital, Boston, MA;2Childrens Hospital of Pittsburgh of University ofPittsburgh Medical Center, Pittsburgh, PA; 3NationwideChildrens Hospital, Columbus, OH; 4Texas ChildrensHospital, Houston, TX; 5Seattle Childrens Hospital,Seattle, WA; 6Cincinnati Childrens Hospital MedicalCenter, Cincinnati, OH; 7Monroe Carrell Jr. ChildrensHospital, Nashville, TN; 8Childrens Hospital andMedicalCenter, Omaha, NE; 9University of California, SanFrancisco, Benioff Childrens Hospital, San Francisco,CA; 10Childrens Hospital Colorado Medical Center,Denver, CO; 11Duke Childrens Hospital and HealthCenter, Durham, NC; 12Childrens Memorial Hospital,Chicago, IL; 13Motts Childrens Hospital, Ann Arbor, MI;14Mattel Childrens Hospital University of California, LosAngeles, Los Angeles, CA; and 15Hospital for SickChildren, Toronto, Ontario, Canada

*A list of members of the Pediatric Intestinal FailureConsortium is available at www.jpeds.com (Appendix).

Supported by the National Institutes of Health/NationalInstitute of Diabetes and Digestive and Kidney Diseases(1 R21 DK081059-01). C.D. was funded in part from theEunice Kennedy Shriver National Institute of Child Healthand Human Development (K24HD058795 andK24DK104676-06). The authors declare no conflicts ofinterest.

0022-3476/$ - see front matter. Copyright 2015 Elsevier Inc.

ICV Ileocecal valve

IF Intestinal failure

ITx Intestinal transplantation

NEC Necrotizing enterocolitis

PIFCon Pediatric Intestinal Failure Consortiumwas achieved in 118 (43%); 3plantation. Multivariable analydependence on parenteral nutrition (PN) >60 days. Enteral autonom>3 months.Results A total of 272 infants were followed for a median (IQR) of 33.5David Mercer, MD8, Susan Rhee, MD9, Jeffrey A. Rudolph, MD2, Jason

Riccardo A. Superina, MD12, Daniel H. Teitelbaum, MD13, Robert Venick

and Christopher Duggan, MD, MPH1, for Pediatric Intestin

Objectives In a large cohort of children with intestinal failure (IF), we sougof achieving enteral autonomy and identify patient and institutionalautonomy.Study design A multicenter, retrospective cohort analysis from the Pedperformed. IF was defined as severe congenital or acquired gastroi

6 (13%) remained PN dependent and 118All rights reserved.

http://dx.doi.org/10.1016/j.jpeds.2015.03.040

RSB Residual small bowel length

29

THE JOURNAL OF PEDIATRICS www.jpeds.com Vol. 167, No. 1Data describing the cumulative incidence of enteral auton-omy in pediatric IF are relatively sparse, with estimatesranging between 42% and 86%.3,11,12 In addition, the processof intestinal adaptation from intestinal resection to a theoret-ical plateau phase in bowel adaptation is controversial andhas been reported variably in the literature to occur within1-3 years in children.13,14 The extent of adaptive response isinfluenced by several factors, such as the age of the patientat the inciting event leading to IF, magnitude, and locationof bowel loss,14,15 presence of an intact ileocecal valve(ICV),9,16 residual colon in continuity,9,16 composition,timing and advancement of enteral feeds, and the luminalenvironment (ie, absence of bacterial overgrowth).17-19 How-ever the interpretation of these published data is limitedbecause of variability in patient populations studied, criteriaused to define IF, duration of patient follow-up, and charac-teristics of patient management, among other factors.Because of these gaps in the literature, a multi-institutional

collaborative (the Pediatric Intestinal Failure Consortium[PIFCon]) was established.20 The current study was per-formed as an ancillary analysis of data collected by PIFCon,to more accurately track intestinal adaptation and achieve-ment of enteral autonomy. Our specific aims were tomeasurethe cumulative incidence of enteral autonomy and identifypatient and institutional characteristics associated withachieving enteral autonomy.

Methods

We performed a multicenter retrospective cohort studyamong the PIFCon. The group was initiated in June 2006 asa collaboration among 14 sites with established multidisci-plinary programs for treatment of pediatric IF; 9 of the 14 sitesalso had affiliated intestinal transplantation (ITx) programs.After Institutional Review Board approval was obtainedfrom each participating center, records of patients who metinclusion criteria were reviewed retrospectively. Infants withIF were included if they had severe congenital or acquiredgastrointestinal diseases, were younger than 1 year of age,and required prolonged support with PN (defined as $60of 74 consecutive days). This specific PN duration was chosento allow for brief interruptions such as loss of intravenous ac-cess or perioperative cessation. Participants at 13 sites met theage and PN criteria between January 2000 and December2004, whereas at 1 site the end date for study entry wasextended to December 2005. Data were collected throughDecember 2006 for 13 sites andDecember 2007 at the remain-ing site to allow at least a 2-year follow up for all children.Baseline clinical data were collected at study inclusion; subse-quent clinical data were collected at 1, 3, 6, 9, and 12 monthsafter study enrollment and annually thereafter. The results ofthe original study have been previously published.20

The outcome variables for the current study were theachievement of enteral autonomy (defined as discontinua-tion of PN for >3 consecutive months with maintenance ofacceptable growth variables), persistent dependence on PN,30and the combined outcome of death or undergoing intestinalor multivisceral transplantation. Statistical analysis was con-ducted using SAS version 9.3 (SAS Institute, Cary, NorthCarolina). Categorical data are summarized as frequencycounts and percentages. Continuous data are shown asmean SD when normally distributed, and nonparametricdata are presented as median and IQR. Cumulative incidencecurves with adjustment for competing risks for the 3 mainoutcomes were plotted.21 Potential factors associated withachievement of enteral autonomy were evaluated by the useof bivariate analysis. Variables that reached statistical signif-icance in the bivariate analysis (P < .2) or were deemed clin-ically relevant were selected for inclusion in multivariablelogistic regression models to identify independent patientand institutional characteristics associated with achievementof enteral autonomy. Intraoperative measurements of resid-ual small bowel length (RSB) were available for a limitednumber of subjects, so 2 multivariable models were created:one considering the entire dataset and 1 for only those withRSB measurements. Post-hoc analysis was performed toidentify the threshold RSB predicting probability of enteralautonomy with the greatest combined sensitivity and speci-ficity using a receiver operating characteristic curve. Cumu-lative incidences of enteral autonomy for patients withdifferent diagnoses were compared using Grays test.22

Results

Select patient demographic and baseline characteristics aresummarized in Table I. The 272 infants who met studyinclusion criteria were followed for a median of nearly3 years. Complete enteral autonomy was achieved in 118(43%) by the end of the study follow-up period; 36 patients(13%) remained partially or exclusively PN dependent, and118 (43%) patients died (n = 58), underwent intestinal/multivisceral transplantation (n = 50), or underwenttransplant and then died (n = 10). The cumulativeincidences of enteral autonomy, PN dependence, and death/transplantation with adjustment for competing risk bystudy follow-up period are depicted in Figure 1, A.Patient, clinical, and institutional factors associated with

enteral autonomy on bivariate analysis are shown inTable II. Children who achieved enteral autonomy by theend of the follow-up period were slightly older at the timeof study inclusion, were more likely to have necrotizingenterocolitis (NEC) as the underlying diagnosis, hadpreserved ICV, and had significantly longer intraoperativelymeasured RSB compared with those not achievingautonomy. Conversely, patients cared for at a PIFCon sitewith an affiliated intestinal/multivisceral transplantprogram and those with more advanced liver disease (asevidenced by higher baseline direct and total bilirubinlevels and a higher aspartate aminotransferase to plateletratio)23 were less likely to achieve enteral autonomy.Multivariable logistic regression analysis using forward se-

lection in the full cohort (n = 272) found that children withKhan et al

July 2015 ORIGINAL ARTICLESan underlying diagnosis of NEC (OR 2.42, 95% CI 1.33-4.47)and those with an intact ICV (OR 2.80, 95% CI 1.63-4.83)were more than 2 times more likely to achieve enteral auton-omy than infants with other underlying diagnoses or an ab-sent ICV. Children cared for at an IF site without anassociated intestinal transplant program also were signifi-cantly more likely to achieve enteral autonomy (OR 2.73,95% CI 1.56-4.78). The multivariable odds of achievingenteral autonomy in infants receiving human milk was 1.92

Table I. Baseline characteristics in 272 infants with IF

Characteristics n (%) or median (IQR)

Age at study entry, d 63 (61-73)Gestational age, wk (n = 264) 34 (30-36)Months in study (n = 271) 33.5 (16.2-51.5)Male sex 156 (57%)Race (n = 254)

White 210 (82%)Black 30 (12%)Asian 13 (5%)Other 1 (

Table II. Bivariate relationships between select baseline demographic and clinical factors and the achievement of enteralautonomy in 272 children with IF

CharacteristicsAchieved enteral

autonomy (n = 118)Did not achieve

enteral autonomy (n = 154) P value*

Gestational age, wk (n = 264) 34 (29, 36) 34 (31, 36) .56Gestational age

July 2015 ORIGINAL ARTICLESdisease severity.3,16 Authors who have reported greater ratesof weaning from PN support generally have included infantswith less severe manifestations of IF. In some instances, acombination of RSB and duration of PN dependence wereused to define IF, inherently meaning a heterogeneous pop-ulation of patients with varying disease severity.9,24-26 More-over, review of pediatric IF literature tracking outcomesreveals that several previous investigators, reporting excellentoutcomes, either did not comment on the severity of liverdysfunction in the studied population or conversely had arelatively smaller proportion of patients with evidence ofcholestasis, as opposed to the 74% prevalence of cholestasisseen in this cohort.1,9,17,27-29

The natural history of the adaptive response after bowelresection is unclear, as some observational studies suggestmaximal adaption occurs within 24-36 months of the initialinsult. Therefore, the probability of weaning off PN wasthought to drastically decrease beyond this time frame.3,14

Children in this present cohort, however, continued todemonstrate achievement of enteral autonomy well beyond3 years after the initial insult leading to IF. These data supportcontinued efforts at intestinal rehabilitation even in childrenwith very short RSB. This observation may be explained bythe significant potential for the gastrointestinal tract to pro-gressively lengthen in infants and young children.30

Certain IF diagnoses have been suspected previously to beassociated with overall worse outcomes. Although Georgesonet al29 reported no differences in the probability of weaningfrom PN in those with NEC compared with other diagnoses,our data suggest that infants with NEC are not only morelikely to achieve enteral autonomy compared with patientswithout NEC, but do so more rapidly, adjusted for RSB, sta-tus of ICV, and institution where care is provided. It ispossible that previous investigators did not identify this asso-ciation due to smaller number of patients studied and/orhigh rate of associated morbidities of prematurity.Previous studies have demonstrated improved outcomes

for patients with IF transferred to specialized centers at arelatively early phase of their illness.31 In contrast, wefound that being referred to or cared for at a center withtransplantation capability was associated with lower ratesof enteral autonomy, even after we adjusted for RSB, statusof the ICV, and underlying diagnosis. One possible expla-nation for this finding is the selection biases inherent in aretrospective study (ie, a tendency to refer only the mostseverely ill children to sites with transplant capacity).This is supported by our findings that patients at trans-plantation sites had shorter RSB, were more likely to bepremature, and of very low birth weight, compared withpatients at nontransplantation sites. Alternatively, ourfindings might be the result of a philosophical predisposi-tion away from intestinal rehabilitation towards transplan-tation at these sites. This is perhaps suggested by thecomparable measures of cholestasis and some but not allmeasures of liver dysfunction. The nature of availabledata limit further characterization of this association;large, prospective studies are warranted to better identifyPredictors of Enteral Autonomy in Children with Intestinal Failurethe influence of institutional and referral patterns on pa-tient outcomes.Previous studies have identified RSB as a major factor in

determining whether a patient with short bowel syndromewill wean off PN support.3,19 Before the widespread imple-mentation of PN support among infants requiring significantbowel resections, Wilmore et al32 reported 100% mortalityfor infants with less than 40 cm RSB without ICV. On the ba-sis of data from this more recent cohort, a threshold value of41 cm or greater appears to be best predictive of the ability towean off from PN support, although as mentioned previ-ously, RSB less than this are no reason to abandon effortsat rehabilitation. Previous investigators have reportedimproved rates of survival and successful intestinal rehabili-tation in patients with IF with an intact ICV.9,11 Theimproved outcomes seen in patients with IF with an intactICV and therefore at least some terminal ileum may in partbe attributable to the significantly greater adaptive potentialof distal small bowel. Other factors such as a preserved ileo-gastric reflex33 and over all slower transit of luminal contentsthrough the distal small bowel are likely contributory. RSBand the status of ICV can therefore be used to risk stratifychildren with IF, identify those likely to require prolongedPN support and are thereby likely to experience greater levelof IF-related morbidity.Although the correlation between humanmilk feeding and

enteral autonomy did not achieve statistical significance,available evidence suggests not only mode (enteral nutritionvs PN) but also the content of enteral nutrition has an influ-ence on outcomes in IF.10,18 The lack of a statistically signif-icant association of the use of human milk with enteralautonomy in this cohort may be attributable to the small pro-portion of children who received human milk and the possi-bility of confounders (differences in institutional practicesand severity of illness, among other factors). Because of theseveral advantages afforded by human milk over commer-cially prepared formulas, including the presence of secretoryIgA, amino acids, numerous growth factors, and other com-ponents which bolster systemic and mucosal immuneresponse and likely assist intestinal adaptation, the use of hu-man milk as the primary type of enteral nutrition for infantswith IF should still be strongly considered in the absence ofspecific intolerance.34

The large, geographically diverse cohort of infants whowere followed for amedian duration of approximately 3 yearsenhances the validity and generalizability of our findings.This study is, however, limited by its retrospective designand incomplete data collection of some variables. Since thecollection of these data, improvements in IF management(eg, alterations of the dose and type of intravenous fattyacid emulsions, ethanol locks for central line-associatedbloodstream infection prophylaxis, and more) have been re-ported, which in part may explain the relatively small numberof patients dependent on PN at the end of the study follow-up period. Even though all the participating sites had inde-pendent multidisciplinary programs for management of IF,there were likely variations in patterns of clinical practice: A Multicenter Cohort Study 33

within and between the participating centers, which maypartly be responsible for the association noted betweenenteral autonomy and care at specific IF programs. Nonethe-less, these data can serve as effective bench marks for futureprospective multicenter studies needed to further improveoutcomes in children with IF. n

Submitted for publication Sep 29, 2014; last revision received Feb 27, 2015;

16. Quiros-Tejeira R, Ament M, Reyen L, Herzog F, Merjanian M, Olivares-

Serrano N, et al. Long-term parenteral nutritional support and intestinal

adaptation in children with short bowel syndrome: a 25-year experience.

J Pediatr 2004;145:157-63.

17. Kaufman S, Loseke C, Lupo J, Young R, Murray N, Pinch L, et al. Influ-

ence of bacterial overgrowth and intestinal inflammation on duration of

parenteral nutrition in children with short bowel syndrome. J Pediatr

1997;131:356-61.

18. Bines J, Francis D, Hill D. Reducing parenteral requirement in children

with short bowel syndrome: impact of an amino acid-based complete in-

fant formula. J Pediatr Gastroenterol Nutr 1998;26:123-8.

THE JOURNAL OF PEDIATRICS www.jpeds.com Vol. 167, No. 1Reprint requests: Christopher Duggan,MD,MPH, Center for Nutrition, Division

of Gastroenterology, Hepatology and Nutrition, Boston Childrens Hospital,

333 Longwood Avenue, Boston, MA 02115. E-mail: christopher.duggan@

childrens.harvard.edu

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Appendix

Members of the PIFCon include (by site):Childrens Hospital of Pittsburgh (Pittsburgh, PA): Cart-

land Burns, MD, George Mazariegos, MD, Sharon Lawlor,MBA, Tamara Haller, BS, Marcia Kurs-Lasky, MS, StevenH. Belle, PhD, MScHyg, Anita Nucci, PhD, RD, Jane AnneYawarski, RN, Danielle Sebbens, DNP, CRNP, Rhonda Cun-ningham, BA; Boston Childrens Hospital (Boston, MA):Daniel Kamin, MD, Tom Jaksic, MD, PhD, Heung BaeKim, MD, Sharon Collier, RD, LD, Melanie Connolly, RD,LD; University of Michigan (Ann Arbor, MI): Pamela Brown,MD, Michele Johnson, LD, Robert Drongowski, MA;Nationwide Childrens Hospital (Columbus, OH): ChristinaValentine, MD, Steven Teich, MD, Beth Skaggs, BA; UCLA(Los Angeles, CA): Martin G. Martin, MD, MPP, Patty Beck-with, RD, CDE, James Dunn, MD, PhD, Douglas G. Farmer,MD, Laurie Reyen, RN, MN; UCSF (San Francisco, CA):Diana Farmer, MD, Sang-Mo Kang, MD, Lane Bower, RD;University of Nebraska (Omaha, NE): Dean L. Antonson,MD, Steve C. Raynor, MD, Brandy Sunderman, RD, Kris Sei-

Figure 2. Receiver operating characteristic curve analysis ofthreshold RSB associated with achievement of enteral au-tonomy. The threshold of 41 cm for residual bowel lengthyields the greatest combined value of sensitivity (78.3%) and1-specificity (29.8%). The thresholds of 36 cmand 38 cmhavea sensitivity of 81.7% and 34.5% and 33.3%, respectively.

July 2015 ORIGINAL ARTICLESpel, BA; Vanderbilt (Nashville, TN): Brent Polk, MD, MarthaBallew, MEd, RD; Texas Childrens Hospital (Houston, TX):Mary Brandt, MD, Saul Karpen, MD, PhD, Sara Philips, RD,Kristin Brown, RD, Alejandro De La Torre, BA; ChildrensHospital, Denver (Denver, CO): Sara Fidanza, NP, KristinBrown, RD; Seattle Childrens Hospital (Seattle, WA): Fran-ces Malone, ARNP, PhD, Patrick Healey, MD, Jorge Reyes,MD, Cheryl Davis, RD; Cincinnati Childrens Hospital Med-ical Center (Cincinnati, OH): Greg Tiao, MD, JacquelineWessel, RN; Childrens Memorial Hospital (Chicago, IL):Valeria Cohran, MD, Kimberley Kazmerski, RD, Lisa Keys,BSN, RN, CCTN, Margaret Peggy Richard, RN; Universityof Calgary: David Sigalet, MD, PhD, Calgary, CA; and EmoryUniversity (Atlanta, GA): Conrad Cole, MD.Predictors of Enteral Autonomy in Children with Intestinal Failure: A Multicenter Cohort Study 34.e1

Predictors of Enteral Autonomy in Children with Intestinal Failure: A Multicenter Cohort StudyMethodsResultsDiscussionReferencesAppendix