Parenteral nutrition associated cholestasis: an American Pediatric Surgical Association Outcomes and Clinical Trials Committee systematic review

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1 Journal of Pediatric Surgery (2012) 47, Review articles Parenteral nutrition associated cholestasis: an American Pediatric Surgical Association Outcomes and Clinical Trials Committee systematic review Shawn J. Rangel a, Casey M. Calkins b, Robert A. Cowles c, Douglas C. Barnhart d, Eunice Y. Huang e, Fizan Abdullah f, Marjorie J. Arca b, Daniel H. Teitelbaum g, For the 2011 American Pediatric Surgical Association Outcomes and Clinical Trials Committee a Children's Hospital Boston, Boston, MA 02115, USA b Children's Hospital of Wisconsin, Medical College of Wisconsin, Milwaukee, WI 53005, USA c Columbia University College of Physicians and Surgeons, New York, NY 10032, USA d University of Utah/Primary Children's Medical Center, Salt Lake City, UT , USA e University of Tennessee Health Science Center, Memphis, TN 38105, USA f Johns Hopkins Children's Center, Johns Hopkins University, Baltimore, MD 21231, USA g C.S. Mott Children's Hospital, University of Michigan, Ann Arbor, MI 48109, USA Received 20 July 2011; revised 5 October 2011; accepted 6 October 2011 Key words: Parenteral nutrition associated cholestasis; Liver disease; Lipid emulsion Abstract Objective: The aim of this study was to review evidence-based data addressing key clinical questions regarding parenteral nutrition associated cholestasis (PNAC) and parenteral nutrition associated liver disease (PNALD) in children. Data Source: Data were obtained from PubMed, Medicine databases of the English literature (up to October 2010), and the Cochrane Database of Systematic Reviews. Study Selection: The review of PNAC/PNALD has been divided into 4 areas to simplify one's understanding of the current knowledge regarding the pathogenesis and treatment of this disease: (1) nonnutrient risk factors associated with PNAC, (2) PNAC and lipid emulsions, (3) nutritional (nonlipid) considerations in the prevention of PNAC, and (4) supplemental medications in the prevention and treatment of PNAC. Results: The data for each topic area relevant to the clinical practice of pediatric surgery were reviewed, evaluated, graded, and summarized. Conclusions: Although the conditions of PNAC and PNALD have been well recognized for more than 30 years, only a few concrete associations and treatment protocols have been established Elsevier Inc. All rights reserved. Corresponding author. Section of Pediatric Surgery, F3970 Mott Children's Hospital, Ann Arbor, MI Tel.: ; fax: address: dttlbm@umich.edu (D.H. Teitelbaum). Evidence-based medicine is a term applied to the practice of using the best current knowledge to one's individual practice and patients. Critical appraisal of the /$ see front matter 2012 Elsevier Inc. All rights reserved. doi: /j.jpedsurg

2 226 S.J. Rangel et al. literature is necessary to determine the reliability, validity, and applicability of the studies to clinical practice. The American Pediatric Surgery Association Outcomes and Clinical Trials Committee has undertaken a project to review current articles relevant to the practices of contemporary pediatric surgery. The primary objective of this endeavor is to summarize and critique the current literature to help the practicing pediatric surgeon. Parenteral nutrition (PN) has revolutionized the care of the neonate who is unable to sustain adequate growth by way of standard enteral means [1]. Long-term PN use was first described in a female neonate [2]; today more than 30,000 patients, young and old, depend on PN for survival. Parenteral nutrition associated cholestasis (PNAC) has been one of the most challenging disease processes associated with prolonged administration of PN. As PNAC progresses to PN-associated liver disease (PNALD), the process can lead to a high incidence of morbidity and mortality [3,4]. A number of recognized risk factors have been attributed to PNAC, and it is felt that the process may well be multifactorial. This review summarizes current knowledge on PNAC. The following topics were selected based on relevance to PNAC and potential causative or preventive strategies: I. Nonnutrient risk factors associated with PNAC II. PNAC and lipid emulsions III. Nutritional (nonlipid) considerations in the prevention of PNAC IV. Supplemental medications in the prevention and treatment of PNAC Under each of the 4 generalized headings, specific questions were answered based on the literature review. 1. Materials and methods The present study defined PNAC to be cholestasis attributable to PN use, with other parameters excluded. Parenteral nutrition associated liver disease was confined to those patients who developed long-term liver dysfunction and permanent injury to the liver. The authors identified questions relevant to pediatric surgical practice using the 4 general categories identified previously. Adult-related PNALD was not addressed in this review. PubMed, databases of the English literature (up to October 2010), and the Cochrane Database of Systematic Reviews were queried. The following search terms were used by the authors: PN, cholestasis, and liver disease. The following terms were then linked to the previously search elements: outcome, duration, sepsis, bacterial overgrowth, antibiotics, prematurity, surgery, trace elements, micronutrients, macronutrients, cycling, ursodiol, ursodeoxycholic acid, phenobarbital, cholecystokinin-octapeptide (CCK-OP), cholecystokinin, cholestyramine, taurourosodeoxycholic acid, erythromycin, prevention, and treatment. To answer each question, the literature was analyzed and graded according to the quality of the evidence available (Table 1). The subject matter was confined to the pediatric age group when making final summations. 2. Results 2.1. Nonnutrient risk factors associated with PNAC Modifiable risk factors for PNAC include sepsis, duration of PN, and enteric flora/bacterial overgrowth. Nonmodifiable risk factors include underlying surgical condition and prematurity/birth weight. Most available data regarding risk factors in the development of PNAC come from case series because randomized controlled trials (RCTs) are challenging owing to patient heterogeneity. For the purposes of this review, only the risk factors mentioned previously will be addressed Does prematurity or low birth weight increase the risk of developing PNAC? Multiple case series have shown that prematurity and/or low birth weight represents risk factors for PNAC [5-8]. A study of 267 infants receiving PN showed that infants born less than 32 weeks' gestation had a significantly higher rate of hyperbilirubinemia than those born at more than 36 weeks (13.7% vs 1.4%); in addition, those with a lower gestational age predicted a higher peak direct bilirubin level [9]. Using multivariate analysis, Beath et al [10] showed that young gestational age was associated with development of cholestasis. Another recent large case series of 1366 infants who received PN for 14 days or more reported direct hyperbilirubinemia in 29% [11]. In this study, logistic regression revealed that birth weight was closely related to the risk of developing PNAC, with the highest risk seen in the smallest neonates. Robinson and Ehrenkranz [12] performed a case-control study of 79 cholestatic infants and found a significantly increased incidence of small for gestational-aged infants in the cholestatic group as compared with the control group. Several reports raised questions as to whether prematurity or low birth weight was independent risk factors for cholestasis. In a prospective trial studying the effect of taurine on PNAC, the data showed no relationship between prematurity and PNAC [13]. In a study examining the effect of fluconazole prophylaxis in low-birth-weight neonates [14], the incidence of cholestasis was 31% overall and cholestatic infants showed significantly lower birth weights; however, a multivariate analysis failed to reveal a significant association between birth weight and the development of cholestasis. Similarly, Hsieh et al [15] found that gestational age and birth weight were not

3 Parenteral nutrition associated cholestasis Table 1 Rating of evidence/therapeutic evidence Rating of recommendation (note: technology assessment rating is parentheses) Translation of evidence to recommendations A = established as effective, ineffective, or harmful (or established as useful/predictive or not useful/predictive) for the given condition in the specified population B = probably effective, ineffective, or harmful (or probably useful/predictive or not useful/ predictive) for the given condition in specified population C = possibly effective, ineffective, or harmful (or possibly useful/predictive or not useful/ predictive) for the given condition in specified population U = data inadequate or conflicting. Given current knowledge, treatment (test predictor) is unproven. Level A rating requires at least 1 convincing class I study or at least 2 consistent, convincing class II studies. Level B rating requires at least 1 convincing class II study or at least 3 consistent class III studies. Level C rating requires at least 2 convincing and consistent class III studies. Rating of therapeutic article Class I: prospective, randomized, controlled clinical trial with masked outcome assessment, in a representative population The following are required: Primary outcome(s) is(are) clearly defined. Exclusion/inclusion criteria are clearly defined. Adequate accounting for dropouts and crossovers with numbers sufficiently low to have minimal potential for bias Relevant baseline characteristics are presented and substantially equivalent among treatment groups, or there is appropriate statistical adjustment for differences. Class II: prospective matched group cohort study in a representative population with masked outcome assessment that meets a-d above or an RCT in a representative population that lacks 1 of the criteria a-d. Class III: all other controlled trials (including well-defined natural history controls or patients serving as own controls) in a representative population, where outcome assessment is independent of patient treatment Class IV: evidence from uncontrolled studies, case series, case reports, or expert opinion 227 identified as independent risk factors in his study. The lack of correlation in these latter studies may be caused by other confounding factors having greater predictive weight in predisposing infants to PNAC What underlying surgical diagnoses are most closely associated with PNAC? Several studies have reported on the association between certain surgical disorders and the risk of developing PNAC [8]. In a prospective trial, Spencer et al [13] identified necrotizing enterocolitis (NEC) as being a significant predictor in the development of PNAC. The diagnoses of gastroschisis or intestinal atresia did not significantly predict the risk of PNAC; however, this may be caused by an insufficient number of infants in this latter group. Christensen et al [11] found that the highest risk of PNAC was seen in infants with surgical NEC, gastroschisis, or intestinal atresia and less so in infants with omphalocele or congenital diaphragmatic hernia [11]. The case-control study of Robinson and Ehrenkranz [12] showed that 51% of infants with NEC were cholestatic, whereas the incidence of NEC in the control group with no cholestasis was 7%. In their study of fluconazole prophylaxis, Healy et al [14] found that NEC was significantly associated with the development of cholestasis on univariate and multivariate analyses Does the duration of PN administration impact the development of PNAC? Multiple studies have supported the idea that duration of PN exposure is a risk factor in PNAC. Both Beale et al [6] and Pereira et al [9] showed that infants with cholestasis had significantly longer period of PN administration when compared with infants who did not develop cholestasis. The case-control study of Robinson and Ehrenkranz [12] also suggested a significant effect of PN exposure on the development of PNAC. Based on multivariate analysis, Healy et al [14] concluded that there was a significant association between PN duration and the development of cholestasis. A smaller study showed that the duration of PN was the only variable that predicted PNAC based on multivariate analysis [15]. In a study of percutaneously inserted central catheters in neonates, Hoang et al [16] showed that the duration of PN administration was a significant contributor to the development of cholestasis. Although no formal statistical analysis was performed on this aspect of their study of more than 1300 infants, Christensen et al [11] showed that the incidence of PNAC increased with longer exposure to PN, with the lowest incidence (14%) in those infants who received PN for 14 to 28 days and the highest incidence (86%) when PN was given for more than 100 days. A recent study has shown that prematurity influenced the development of PNAC far less than the

4 228 S.J. Rangel et al. duration of PN [17]. Infants who were small for gestational age were at an increased risk for PNAC and developed PNAC while receiving far less PN compared with premature infants [12]. There exists 1 study of 74 surgical neonates that showed a correlation between cholestasis with longer time on PN; however, multiple regression analysis eliminated the duration of PN as a predictor of hyperbilirubinemia [10]. This study included only surgical neonates where other variables may be more responsible for the development of PNAC Does the number of septic episodes impact development of PNAC? An association between sepsis and jaundice has been appreciated for many decades [18,19]. Pereira et al [9] showed a higher incidence of sepsis in infants who developed cholestasis (17.4%) compared with those who did not develop cholestasis (1.22%). Robinson and Ehrenkranz [12] also showed a significantly increased incidence of sepsis in cholestatic (80%) vs noncholestatic (34%) infants. Beath et al [10] showed that a higher number of septic episodes predicted an elevated bilirubin in patients undergoing surgery. Another study of 42 infants undergoing surgery showed that cholestasis occurred more quickly after the first documented infection and that it was rare for cholestasis to begin before the first infection [20]. The multivariate analysis of Hoang et al [16] showed that gramnegative septicemia had a significant correlation with cholestasis in neonates with percutaneously inserted central catheters receiving PN Can treatment of bacterial overgrowth decrease the risk or severity of PNAC? It has been postulated that gram-negative bacteremia may originate in the gastrointestinal tract in patients receiving PN. Several attempts to prevent PNAC by treating enteric flora have been made in adults and children. Capron et al [21] performed a randomized study evaluating metronidazole use in adults with Crohn disease who were receiving PN. After 30 days of PN, subjects who received metronidazole had improved alkaline phosphatase, γ-glutamyl transpeptidase (GGT), and alanine aminotransferase (ALT) levels compared with controls. A retrospective study of adults receiving PN showed that those treated with metronidazole had stabilization of serum liver enzymes, bilirubin, and albumin vs those without antibiotics [22], whereas a study of PN-receiving neonates administered 3 weeks of metronidazole resulted in improved levels of transaminases [23]. Another retrospective study assessed the use of oral gentamicin in low-birth-weight infants receiving PN and noted that the incidences of cholestasis and NEC were significantly lower in the gentamicin-treated group. Gentamicin treatment also was associated with stable direct bilirubin levels, whereas infants who were not treated with gentamicin developed significant increases in direct bilirubin. Although this study suggests a possible benefit of oral gentamicin, the results may be affected by the increased incidence of NEC in the control group, potentially acting as a confounding variable leading to cholestasis in this group [24] Summary of findings 1. There is disagreement in the available literature regarding the true role of prematurity as an independent risk factor in PNAC. Several studies (class III) suggest that prematurity is a risk factor for PNAC, but other studies (classes II and III) do not support this claim. 2. Necrotizing enterocolitis is a significant risk factor for PNAC (classes II and III). 3. Most the available data support the concept that PN duration is a significant predictor of developing PNAC (class III). 4. Studies support the concept that sepsis plays an important role in the development of PNAC (class III). 5. Although there are preliminary data in small studies that antibiotic treatment to prevent bacterial translocation may result in diminished hepatocyte damage, the data are currently insufficient to recommend routine use to prevent PNAC (class III, level U) (Fig. 1) Parenteral nutrition associated cholestasis and lipid emulsions Advanced PNAC has been shown to be one of the most significant risk factors associated with mortality in infants on long-term PN [25,26]. Evidence has implicated the fat component (also referred to as lipid emulsion) of PN as a potential causative factor for PNAC [27]. This section summarizes laboratory and clinical evidence to date that supports the contention that lipid emulsions contribute to PNAC and how manipulation of the administration and character of lipid emulsions may ameliorate or prevent PNAC Are there specific elements within standard lipid emulsions (soybean based) that incite cholestasis? Although the etiology of PNAC is not clear, most investigators have considered the cause to be multifactorial. However, cholestasis as a result of long-term lipid administration is widely accepted as a precursor to PNAC [28,29]. The use of soybean-based intravenous lipid emulsions (SLEs) has been speculated to be a contributing factor in the development of PNAC. Two characteristics of SLE have been implicated as etiologic factors in this process: phytosterol content and the proinflammatory nature of omega-6 fatty acids Phytosterols. Phytosterols are plant-derived steroid alcohols that are naturally occurring in plants. They are a component of the cell membrane, a role that is played by cholesterol in mammalian systems. Phytosterols are also a part of intravenous lipid components of PN and have been implicated in PNAC. Formulations of SLE contain high levels of phytosterols, and animal data would suggest that these agents may lead to impaired bile drainage

5 Parenteral nutrition associated cholestasis 229 OUTCOMES AND CLINICAL TRIALS COMMITTEE: SYSTEMATIC REVIEW 2011 Fig. 1 Summary of reviewed evidence on PNAC and PN liver disease. and hepatobiliary dysfunction. In a mammalian animal model, Iyer and colleagues [30] performed daily sterol injections into neonatal piglets and measured phytosterol accumulation in the serum, liver, and bile and compared them to nonexposed piglets. The sterol-treated piglets had significantly higher serum bile acid levels (an early marker

6 230 S.J. Rangel et al. for PNAC) and lower maximal bile acid accumulation. Furthermore, phytosterols caused a significant inhibition of secretory functions in isolated rat hepatocyte couplets [31]. Evidence from Carter et al [32] demonstrated that phytosterols contribute to bile acid induced hepatocyte damage by antagonizing a nuclear receptor critically involved in hepatoprotection from cholestasis. The studies by Ellagrd and Bindl noted a clinical association between high plasma phytosterol levels and PN, but these studies failed to link serum phytosterol levels with PNAC. Formulations of SLE do contain a reversed ratio of phytosterols to cholesterol when compared with the normal human diet [33]. In summary, SLE formulations contain high levels of phytosterols, and although animal data would suggest that these agents adversely affect bile acid clearance and subsequent hepatocyte damage, there is little to no clinical data to conclude that phytosterols are causative factors in the development of PNAC Inflammatory mediators. Soybean-based lipid emulsions are rich in omega-6 fatty acids, which have been shown to promote hepatocyte damage or induce hepatocyte apoptosis through a proinflammatory mechanism [34]. Thromboxanes derived from omega-6 fatty acids are mediators of platelet aggregation. In addition, the arachidonic acid liberated from thromboxanes contributes to the formation of prostaglandin E 2, a known immunosuppressant. This body of evidence suggests that a predominance of omega-6 fatty acids may be deleterious to hepatic function Does altering the administration schedule or dosing of soybean-based lipid emulsions decrease the frequency of PNAC? Some data suggest that the cumulative lipid infusion is an independent risk factor for the development of PNAC [35,36]. However, the potential advantages of reducing SLEs must be balanced with the necessity of using fat as a source of energy in the highly metabolic neonate and of providing fat mandatory for neural development. Another downside of lipid restriction is the potential development of essential fatty acid deficiency (EFAD). Meurling and Roos [37] showed that rats could develop EFAD within 10 days of receiving PN without lipids. Oshita et al [38] demonstrated that rats maintained with lipid-free PN developed significantly elevated liver enzymes, as well as the formation of steatohepatitis. Therefore, taking all fat out of the infusate is clearly not a durable solution. However, investigators have asked whether one can safely reduce the amount of lipid infused to decrease the incidence of PNAC. In the preterm infant, lipid is required to provide at least 0.5 g kg 1 d 1 to prevent EFAD [39], and the requirement for α-linoleic (the principal essential fatty acid) can often be achieved with as little as 1 g kg 1 d 1 for most infants and children [40]. However, many physicians use higher amounts of lipids in preterm infants as a source of energy delivery to promote adequate growth [39]. Most infants in the neonatal intensive care unit are unlikely to need longterm PN, and thus, lipid minimization strategies may not be necessary in many patients. However, neonates with pediatric surgical conditions (complicated gastroschisis, severe jejunoileal atresia, massive small bowel resection caused by NEC or malrotation) are at risk for PNAC because they will likely need long-term total parenteral nutrition (TPN) [11]. To date, there are no data to support the prophylactic use of a SLE reduction strategy in patients at risk for PNAC, although there are 2 compelling studies in patients on PN with hyperbilirubinemia, whereby a lipid minimization strategy was effective in improving cholestatic serum measurements (direct serum bilirubin). Cober and Teitelbaum [26] prospectively followed a group of infants with PNAC for 2 years on a SLE reduction protocol, defined as intravenous fat emulsion restriction (IFER) of approximately 1 g kg 1 d 1 2 to 3 times per week, and compared these infants to historical controls who received soybean-based lipids at 3 g kg 1 d 1. The authors reported a statistically significant reduction in the total bilirubin in the patients with IFER without detrimental infant growth. Although 8 infants in the IFER group developed mild EFAD (triene/tetraene ratio N0.5 but b0.2), this deficiency did not adversely affect the improvement in serum bilirubin. In a retrospective review of children referred to an intestinal rehabilitation and transplantation center at a single institution, Cowles and colleagues [41] demonstrated that a dedicated nutritional rehabilitation program can reverse PNAC in many children. Standard treatment consisted of cycling of PN, limiting SLE infusion, enteral stimulation, use of ursodeoxycholic acid, and surgical intervention when necessary. Total bilirubin level was used as the marker for PNALD. At referral, 76 of 93 children had a total bilirubin of 2.0 mg/dl or higher. Total bilirubin normalized in 57 of 76 children with elevated total bilirubin at referral; total bilirubin remained elevated in 19. Normalization of bilirubin was associated with a mortality of 5.2%, and transplantation was needed in 5.2%. Unfortunately, these data do not allow one to speculate as to which of the authors' alterations in nutritional support accounted for the improvement in PNALD. Taken together, therapeutic lipid restriction of the standard soybean-based lipid emulsion is indicated for neonates who have developed PNAC (grade C recommendation) Does the use of newer generation, non soybean-based lipid intravenous fat substrate decrease the frequency of PNAC? Since the introduction of SLEs 50 years ago, progress has been made in understanding the composition, dose, and clinical effects of parenteral lipids in neonatal patients. Although there are limited data to suggest that phytosterols and omega-6 fatty acids are the contributing factors to PNAC, there are reasonable data to suggest that use of lipid emulsions that do not contain phytosterols or less omega-6 fatty acids can reverse PNAC.

7 Parenteral nutrition associated cholestasis Fish oilbased intravenous lipid emulsions (Omegaven). Omegaven (Fresenius SE & Co, Bad Homburg, Germany) is a fish oil based lipid emulsion not currently approved for widespread use in the United States. It contains no phytosterols [33] and is derived from highly refined fish oil (10.0 g), eicosapentaenoic acid ( g), docosahexaenoic acid ( g), and α-tocopherol ( g) per 100 ml (see consumers/cmi/o/omegaven.pdf). Whether the effects of Omegaven are caused by the presence of anti-inflammatory omega-3 fatty acids or the absence of omega-6 fatty acids is unclear. When dosed appropriately, de Meijer et al [42] and Le et al [43] reported that fish oil based lipid emulsions contained sufficient amounts of essential fatty acids to prevent EFAD and can sustain growth in patients who are completely dependent on PN (class IV). However, close scrutiny of the linoleic acid levels reported in the patients in this study demonstrates that 5 of 10 children developed levels below 1000 μmol/l, which is typically the lower limit of normal. Thus, caution should be taken with any approach to modify lipid administration. To date, Omegaven for use in patients younger than 18 years of age is restricted to compassionate use only. Information on how to obtain Omegaven for clinical use can be obtained from Can_Obtain_Omegaven.pdf. There are a number of open compassionate use clinical trials in the National Institutes of Health clinical trial database (Table 2), and more than 60 institutions in the United States have used Omegaven under a compassionate use protocol in patients with PNALD [44]. A prospective clinical trial comparing Omegaven to a standard soybean oil lipid emulsion was recently suspended because of a mandate from the Food and Drug Administration (NCT ). This was not caused by adverse events in either arm. It is the only prospective prevention trial being performed in the United States to assess the effectiveness of a fish oil based lipid emulsion in neonates at risk for PNAC. However, there are several studies that have examined the role of Omegaven in the reversal of both PNAC and PNALD (Table 3). Despite the promise of Omegaven, however, the published literature is insufficient to provide a recommendation higher than grade C for its use in the treatment of PNAC or PNALD because a grade B rating requires at least 1 convincing class II study or at least 3 consistent class III studies, and these data do not currently exist Fish oilbased enteral lipid. To date, few data exist to support a strategy of lipid elimination with or without supplementation with enteral fish oil emulsions. In a retrospective review of a single-institution experience with the treatment of PNALD, Rollins and colleagues [45] reported that the temporary elimination of soybean-based lipid emulsion and supplementation of enteral fish oil (25 m gkg 1 d 1 ) improved PNAC. Four patients who were treated in this manner ultimately had resolution of PNAC. However, there are insufficient data to make a clinical recommendation 231 for the temporary addition of enteral fish oil along with soybean lipid infusion in the treatment of PNAC What is the evidence that a combination of lipid types results in a decline in PNAC? Over the past few years, a number of hybrid intravenous fats have been developed commercially. It has been suggested that a clinical benefit exists when a combination of soybean, medium-chain triglycerides, olive oil, and fish oil lipid emulsions (abbreviated SMOF) are used in PN therapy. In a single-center, randomized, double-blind study conducted by Goulet and colleagues [46], 28 children with short bowel syndrome dependent on PN were allocated to 1 of 2 groups. The experimental group received a combination lipid mixture SMOF lipid (containing 30% soybean oil, 30% mediumchain triglycerides, 25% olive oil, and 15% fish oil) (n = 15). Controls received standard soybean oil lipid (20% intralipid) (n = 13). The SMOF lipid was safe and well tolerated, decreased plasma bilirubin, and increased omega-3 fatty acids and α-tocopherol status without changing lipid peroxidation. These findings suggest that a mixture emulsion containing both soybean and fish oils offers a more balanced fatty acid profile with a concomitant reduction in PNAC. However, current data are insufficient to make a recommendation for the use of SMOF as the preferred lipid fraction in children with long-term PN dependence. Another approach to hybrid lipids has been to mix a dominant amount of olive oil (80%) with lowered amounts of soybean oil (20%) [47-49]. This has been shown to be a safe and effective way to deliver fat. Essential fatty acid deficiency has not been reported in these series; however, these have not been well studied in infants. Furthermore, a detailed analysis of the development of PNAC has not been extensively studied. There are insufficient data to recommend the use of SMOF or other hybrid lipids in the treatment of PNAC Summary of findings 1. Intravenous fat emulsion restriction 1 g/kg 2 to 3 times per week may reduce total bilirubin without detrimental effect on infant growth (class III, grade B). 2. Fish oil based lipid emulsions contain sufficient amounts of essential fatty acids to prevent EFAD and to sustain growth in patients who are completely dependent on PN (class IV). 3. Therapeutic lipid restriction of the standard soybeanbased lipid emulsion is indicated for neonates who have developed PNAC (class III, grade B). 4. Use of fish oil based lipid emulsions in children with PNAC and/or PNALD is safe and effective in reversing PNAC and/or PNALD (classes II and III, grade C). 5. There are insufficient data to recommend the use of temporary soybean lipid infusion with enteral fish oil in the treatment of PNAC. 6. There are insufficient data to recommend the use of SMOF or other hybrid lipids in the treatment of PNAC.

8 Table 2 Open compassionate use clinical trials for the use of Omegaven as listed in the NIH clinical trial database Institution Identifier Status Phase Aim Primary end points Investigator Date Opened CHOP NCT Available I Safety and efficacy of M. Mascarenhas, January 11 Omegaven with PNALD MBBS CH Cincinnati NCT Recruiting Reduction in ConjBili in PN ConjBili S. Kocoshsis, MD July 10 dependence and PNAC Children's and NCT Recruiting II RCT Omegaven vs standard ConjBili S. Albersheim, MD; December 10 Women's Health Centre British Columbia with established PNAC A.J. Singh, MD; R. Sherlock, MD CHLA NCT Recruiting Reduction in ConjBili in PN Rate of reduction of ConjBili R. Merritt, MD, PhD October 10 dependence and PNAC LIJ, New York NCT Recruiting II Reduction in ConjBili in PN Reduction of serum bilirubin R. Schanler, MD December 8 dependence and PNAC below 2 on 2 serial measures UCLA NCT Recruiting I Reduction in ConjBili in PN Time to reversal of PNAC K. Calkins, MD August 9 dependence and PNAC Kapiolani Medical NCT Recruiting III Decrease liver disease in Reduction of serum bilirubin L. Iwamoto, MD September 10 Center, Hawaii patient on long-term PN below 2 on 2 serial measures Vanderbilt NCT Recruiting IV Reversal of PNALD Resolution of conjugated W. Walsh, MD March 9 hyperbilirubinemia University of NCT Enroll by II Reversal of PNALD Progression to small bowel D. Mercer, MD, PhD April 9 Nebraska invitation transplant Baylor NCT Recruiting Compassionate use for PNAC Safety analysis S.A. Abrams September 8 Boston Children's NCT Recruiting II/III Reversal of PNALD Efficacy to reverse PNALD M. Puder, MD. PhD September 4 NIH indicates National Institutes of Health; ConjBili, conjugated bilirubin; CHOP, Children's Hospital of Philadelphia; CH, Children's Hospital; CHLA, Children's Hospital of Los Angeles; LIJ, Long Island Jewish; UCLA, University of California Los Angeles. 232 S.J. Rangel et al.

9 Parenteral nutrition associated cholestasis 233 Table 3 Published literature regarding the use of fish oil based lipid emulsions (FOBLEs) in the treatment of PNAC and liver disease Reference Type Findings Class [86] Case series 4 patients with ultra short bowel IV FOBLE (1 g kg 1 d 1 ) reversed or prevented PNAC in 4/4 [87] Case series 4 patients with PNALD, PN dependence, short bowel IV FOBLE (1 g kg 1 d 1 ) reversed or prevented PNAC in 3/4 [88] Case report Single patient with SBS caused by midgut volvulus IV FOBLE (1.5 g kg 1 d 1 ) reversed PNAC [89] Case series 2 patients with SBS, PN dependence, and PNALD IV FOBLE (1 g kg 1 d 1 ) reversed PNALD in 2/2 [90] Retrospective cohort study 18 patients with SBS and PNAC IV Median time to reversal of cholestasis was 9.4 wk n the FOBLE cohort compared with 44.1 wk in historical controls (soybean oil intralipid) [91] Prospective trial Open-labeled trial of a FOBLE in 42 infants with SBS with PNAC while receiving soybean oil based ILE. Subjects receiving fish oil based ILE experienced reversal of PNAC 6 times faster than those receiving soybean oil based ILE. PNAC reversed while receiving PN in 19 of 38 patients in FOBLE cohort vs 2 of 36 patients in the soybean oil cohort [92] Case report Infant with SBS and PNALD IV FOBLE (1 g kg 1 d 1 ) resolved PNAC and improved PNALD, PN discontinued after 7 mo SBS, short bowel syndrome; ILE, intravenous lipid emulsion. III 2.3. Nutritional (nonlipid) considerations in the prevention of PNAC Does the initial dosage, rate of advancement, and/ or goal protein load influence the development of PNAC independent of overall caloric intake? Overfeeding with carbohydrate and/or protein has been implicated in the development of PNAC, although neither component has been proven to be more cholestatic than another. As a general principle, caloric intake should be monitored and adjusted to optimize healthy growth and prevent overfeeding [50]. Although authoritative guidance documents do not reach total consensus in this regard, common practice for infants is to provide 100 to 120 kcal/kg as mixed fuel with dextrose at 11 to 12 mg kg 1 min 1, protein at 3.5 to 4.0 g kg 1 d 1, and lipids at 3 g kg 1 d 1 [50]. Early clinical trials that did not control for energy intake or feeding tolerance had suggested that withholding PN amino acid might prevent PNAC [51], but subsequent studies have found this earlier recommendation to be detrimental [52]. More recent attempts have been made to examine the impact of more aggressive feeding regimens on the development of PNAC with respect to protein loading, advancement, and daily goals. To determine whether different protein concentrations played a role in the development of PNAC, Vileisis et al [53] randomized 82 infants to receive PN with amino acid concentrations averaging 2.3 or 3.6 g kg 1 d 1. The incidence of cholestasis (conjugated bilirubin 2.0 mg/dl) was not significantly different between the groups, but the higher protein group averaged 20 fewer days of PN before the onset of cholestasis and had a significantly higher peak concentration of conjugated bilirubin. In addition, when patients were reanalyzed based on whether or not cholestasis had developed, infants with PNAC were found to have been exposed to significantly higher concentrations of dextrose in their PN solutions than those who did not. Nearly 2 decades later, Wilson and colleagues enrolled infants weighing less than 1500 g who were allocated to standard PN regimen (10% dextrose, a maximum of 2.5 g PN amino acid kg 1 d 1, a maximum of 2 g fat kg 1 d 1, and a caloric target of 70 kcal kg 1 d 1 by the end of the first study week) or to a more aggressive experimental feeding protocol (12.5%-15% dextrose, a maximum of 3.5 g PN amino acid kg 1 d 1, a maximum of 2 g kg 1 d 1 of fats, and a caloric target of 100 kcal kg 1 d 1 before the end of the first week) [54]. Enteral feeding was introduced for the control group once the infants were clinically stable and umbilical arterial catheters were removed. In the experimental group, enteral feeding was initiated before the third day of life at 0.5 ml/h and advanced as tolerated. The authors found no significant difference in timing to achieve full enteral feeding or in the incidence of PNAC between groups. However, the early enteral feeding may have prevented one to detect a difference between these study groups. In a recent randomized, prospective trial where other macronutrients were held in fixed concentrations, Clark et al tested whether PN amino acid initiated at 1.0 g kg 1 d 1 and advanced by 0.5 g kg 1 d 1 to a maximal rate of 2.5 g kg 1 d 1 would lead to a lower incidence of PNAC than initiating at

10 234 S.J. Rangel et al. 1.5gkg 1 d 1 and advancing by 1.0 g kg 1 d 1 to a maximal rate of 3.5 g kg 1 d 1 [55]. The study found that these groups did not differ in cholestasis, which was defined as a conjugated bilirubin greater than 5 mg/dl. Although this would suggest that a more aggressive regimen is safe and well tolerated, the trial examined outcomes over a relatively short duration of PN therapy, and the results may not be applicable to infants requiring PN longer than 1 month. Steinbach et al [56] examined factors associated with PN administration that may be associated with the development of cholestasis in a cohort of 122 neonates on PN. The authors found that neonates developing PNAC were exposed to PN for a longer period of time, received a higher dose of parenteral amino acids, and were less often on enteral nutrition by the seventh day of life. Higher doses of amino acids given earlier in the PN course were not associated with PNAC. In a recent case-controlled study of 25 cholestatic (serum total bilirubin 2.0 mg/dl) and 25 noncholestatic PNdependent premature neonates weighing between 600 and 1000 g, Blau et al [57] analyzed PN macronutrient compositions to determine whether different amounts of protein concentrations and protein/nonprotein calorie ratios played a role in the development of PNAC. The only parameters that differed significantly between the groups were the duration of PN therapy and length of hospital stay. Neither protein concentrations nor protein-to-nonprotein calorie ratios of the PN solutions were statistically different between the 2 groups. These data would collectively suggest that the duration and total cumulative dosage of parenteral amino acids are the primary associated factor with the development of PNAC Which amino acid formulations are associated with a decreased incidence of PNAC? Early concerns that adult PN formulations contained an inappropriate macronutrient composition for neonates and children and that these non-physiologic formulations may increase the incidence of PNAC in pediatric patients led to the development of formulations specifically designed for children. Two popular infant-specific PN formulations created to mimic the amino acid profile of premature infants are Aminosyn PF (APF; Abbott, North Chicago, IL) and TrophAmine (TA; B. Braun, Bethlehem, PA). In the first clinical study comparing the relative effectiveness of the 2 pediatric amino acid formulations in reducing PNAC (defined as a conjugated serum bilirubin 2 mg/dl), the courses of 70 infants younger than 1 year who received TPN for at least 14 days were reviewed by Forchielli et al [33]. The type of PN solution administered (APF or TA), along with other potential risk factors for PNAC such as previous surgery, sepsis, extracorporeal membrane oxygenation (ECMO), prematurity, and nitrogen/calorie intake were all not significant only the length of TPN administration was significant. In a more contemporary case-control cohort study by Wright et al, the authors examined PN-associated risk factors for the development of PNAC in infants receiving APF or TA and parenteral solutions [58]. The use of APF, in addition to birth weight and duration of PN, were significant risk factors for the development of PNAC Does supplementation of standard PN solutions with beneficial amino acids lead to a reduction in the incidence and/or severity of PNAC? It has been suggested from animal studies that certain amino acids (eg, methionine, phenylalanine, tyrosine, and tryptophan) may be hepatotoxic, whereas others (eg, glutamine and taurine) may be hepatoprotective. These observations, in concert with biochemical data indicating a relative deficiency of these macronutrients during prematurity or critical illness, has led to clinical studies investigating the efficacy of supplementing standard PN solutions with conditional amino acids. Taurine plays a multitude of functions in the liver, such as osmoregulation, membrane stability, and antioxidation. It is also a principal amino acid used to conjugate and eliminate bilirubin and may therefore play a role in preventing cholestasis. Spencer et al [13] examined the effect of taurine supplementation (comparing infants receiving APF or TA vs adult crystalline amino acid solutions) on neonates receiving PN as part of a secondary analysis involving 236 neonates from a prospective, multicenter study of 7 institutions. Although taurine supplementation decreased the level of conjugated bilirubin compared with the nonsupplemented group, this did not reach statistical significance (0.50 mg/dl vs 3.45 mg/dl, P =.07). However, a significant decrease in PNAC was found with supplementation in the cohort of neonates with NEC (4.04 mg/dl vs 8.29 mg/dl, P b.01), a subgroup at particularly high risk for PNAC. The experimental basis for adding glutamine to PN solutions has been driven by promising animal data suggesting a multitude of hepatoprotective roles. Glutamine may protect against PN-related hepatic dysfunction by improving gut immunity, attenuating PN-associated gut hypoplasia, preventing PN-related depletion of gut-derived immunoglobulin, and reducing septic complications [59,60]. In a randomized, placebo-controlled trial of 22 patients, Duggan et al [61] showed no difference on the duration in PN or peak conjugated bilirubin concentration in infants younger than 12 months who were supplemented with enteral glutamine compared with those who were not. A recent randomized trial demonstrated a significant reduction in the levels of ALT and total bilirubin but no difference in time to enteral feedings or duration of PN in patients receiving parenteral glutamine supplementation [62]. Neither of these trials found a significant difference in mortality, episodes of septic complications or other measures of morbidity. Because of the distinct differences in administration of glutamine efficacy between enteral and parenteral, it is possible future studies may better or firmly address this question.

11 Parenteral nutrition associated cholestasis In summary, evidence is currently lacking to support the routine supplementation of conditional amino acids as a strategy to prevent PNAC in infants and children receiving PN. However, there is class III evidence that supplementation of TA may reduce incidence of PNAC in certain highrisk populations such as those with NEC Which trace elements and other nonprotein micronutrients should be supplemented or avoided to reduce the incidence or severity of PNAC? Much focus has been placed on the role of trace elements and other nonprotein nutritional elements in the pathogenesis and possible prevention of PNAC. With respect to the former, a number of studies have reported the effects of manganese toxicity in children on long-term TPN [63,64].In these studies, children with impaired liver function were found to have significantly higher manganese levels; a significant correlation was found between whole-blood manganese levels to aspartate aminotransferase (AST) (r = 0.63, P 0.001), and total plasma bilirubin was characterized [63]. The potential hepatotoxicity of manganese was further supported in a RCT comparing 2 different trace element solutions on the incidence and severity of PNAC on infants receiving PN. The formulations differed mainly in their concentrations of manganese (1.0 mmol kg 1 d 1 vs 0.02 mmol kg 1 d 1 ). Although there was no difference in the proportion of patients who developed cholestasis, infants in the high-manganese arm had significantly higher conjugated bilirubin levels, suggesting more severe PNAC. Given the paucity of clinical evidence characterizing conditions associated with manganese deficiency, these observations have led some to recommend the omission of manganese from trace element solutions [65]. Copper is an essential nutrient in humans, with deficiencies resulting in anemia, neutropenia, skeletal abnormalities, and other clinical manifestations. In this regard, copper supplementation is essential in PN to prevent an adverse effect of deficiency. Balance studies indicate that copper requirements in TPN amount to 0.3 mg/d in the adult. For infants and children, the estimated requirement is 20 μg kg body weight 1 d 1. However, recent evidence suggests that potentially toxic copper accumulation can occur in patients with chronic cholestasis, and this is independent from the total duration of PN administration [66]. Because current data suggest that copper deficiencies develop in children on chronic PN, it is recommended that standard trace element solutions containing copper be given. With the development of confirmed PNAC, one should consider reducing copper administration in half to the PN regimen; however, insufficient evidence supports any additional reduction in copper. In addition, copper levels and a complete blood count should be closely monitored after such reductions because of the known association of copper deficiency and lethal pancytopenia. Supplementation of PN formulations with choline has been proposed because plasma levels of this nutrient are 235 significantly decreased in many patients receiving long-term home PN [67]. Furthermore, low-choline status has been associated with both hepatic morphologic and hepatic aminotransferase abnormalities [67]. In a small clinical trial of 15 patients, Buchman et al [67] randomized patients to receive either their usual TPN formulation or TPN, to which 2 g of choline chloride had been added. Serum ALT decreased significantly in the choline group after 6 weeks, and AST was significantly decreased in the choline group by week 24. The serum alkaline phosphatase was significantly reduced in the choline group after the second week, and the total bilirubin remained unchanged during the study, suggesting that although beneficial to PN-associated increases in hepatic enzymes, choline may not have a benefit to PNAC. Importantly, no available clinical source of choline is currently available for such supplementation Does early or trophic feeding in patients who can tolerate it lead to a reduction in the severity or incidence of PNAC? Cholestasis appears to develop more frequently in those children who are unable to tolerate any enteral feeding compared with those who are partially enteral fed. These observations have formed the motivation for studying the impact of early feeding on the incidence and severity of PNAC. In a clinical trial of neonates weighting 500 to 1500 g, Slagle et al randomized infants to PN plus early hypocaloric enteral feeding beginning the first week of life for 10 days or to PN only for 20 days [68]. The mean conjugated bilirubin was significantly higher in the PN-only group (n = 24) compared with those fed early enteral formula (n = 22), but none of the infants developed cholestasis by 29 days of life. Similarly, McClure and colleagues [69] studied infants weighing less than 1750 g but extended the period of testing to the first 6 weeks of life. Infants were randomly assigned to begin PN plus early hypocaloric enteral feeding or PN only. The early enteral group required an average of 11.5 fewer days of PN (P b.01) than the PN-only group, but the mean maximum conjugated bilirubin did not differ. Al-Hathlol et al [70] randomly allocated 52 infants (b30 weeks' gestational age) in the first week of life to receive either mixed-fuel PN or an amino acid-free PN. Those assigned amino acid-free PN were also started on enteral feeding with whey protein at 1 g kg 1 d 1 and advanced daily by increments of 0.5 g/kg until protein intake reached 2.5 to 3.0 g kg 1 d 1. Later, whey protein was replaced gram for gram with protein contained in infant formula. No instances of PNAC were observed in the amino acid-free PN group (0/17), whereas 7 (58%) of 12 infants in the mixed-fuel PN group had PNAC (P_0.001), defined as conjugated bilirubin greater than 3 mg/dl (51.3 μmol/l). However, the investigators did not control for tolerance for enteral feeding, and infants only remained in the experimental group if they tolerated early enteral feeding. Thus, the infants measured in this group were likely less critically ill

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