Nutritional Management in Patients with Chyle Leakage: a Systematic Review

ORIGINAL ARTICLE Nutritional management in patients with chyle leakage: a systematic review

BR Steven1 and S Carey1,2

BACKGROUND/OBJECTIVES: To investigate all the available evidence assessing the effect of nutrition intervention on patients with chyle leakage and its effectiveness at reducing the need for surgical intervention. SUBJECTS/METHODS: A systematic review was undertaken of all English language studies using MEDLINE, Cinahl and Web of Science from January 1980 to September 2013. Case series were included because of limited available evidence. Exclusion criteria included animal studies, pediatrics and studies without nutritional intervention. Assessment of study quality was included. Because of the heterogeneity of the data, no meta-analysis was performed. RESULTS: Thirty-one articles were identified for analysis, all of which were retrospective case series studies. The data within these studies were greatly limited. A total of 550 subjects were identified from these studies, 72% of whom had a chyle leak successfully resolved without surgical intervention. However, there was no significant difference between the type of dietary intervention and the rate of resolution (χ2 = 11.14, P = 0.08). CONCLUSIONS: Although there is evidence to suggest that nutrition may have a role in the management of patients with chyle leakage, it is not possible to determine which dietary methods are most effective. More research is required before any guidelines for best practice can be established. European Journal of Clinical Nutrition (2015) 69, 776–780; doi:10.1038/ejcn.2015.48; published online 29 April 2015

INTRODUCTION The method of nutritional management commonly recommended Chyle leaks are a rare but potentially life-threatening condition, in among practitioners includes dietary fat restriction to reduce chyle 6 which chyle extravasates from the thoracic duct or one of its major flow, which is theorized to encourage the effusion to heal. This is branches, leading to chylous disorders such as chylothorax, used in conjunction with medium-chain triglyceride (MCT) chylous ascites, chyluria and chylopericardium. The potential supplementation. MCTs bypass the lymphatic system and enter 6 causes of a chyle leak are numerous, but they are typically caused the portal venous system directly. However, no consensus has by malignant neoplasms, specifically lymphoma,1 as well as been reached on the optimum method of management, with invasive surgery or penetrative trauma of the neck, chest or current guidelines being based on retrospective reviews of case abdomen.2–4 reports.11 Chyle is a lymphatic fluid flowing from the lymph channels of In addition to fat-free/low-fat diets and MCT supplementation, 5 the small intestine to the venous blood supply via the thoracic treatment options include enteral feeding, low-fat diets supple- duct.5 It is enriched with ingested dietary fats, specifically long- mented with the essential fatty acids (linoleic and linolenic chain triglycerides (LCT), which are bound to chylomicrons.5,6 acid),10,12 drainage of chyle to relieve pressure,11 pleurodesis,13,14 Postprandially, chyle becomes milky white and greatly increases in total parenteral nutrition (TPN) to provide bowel rest and reduce volume as a result of dietary fat ingestion,7 whereas in a fasted chyle output,11 drug therapy to reduce lymphatic flow15 and state, chyle becomes quite clear and reduces in volume.5 Because invasive surgical intervention to seal the leakage.16 Many of these chyle is a fat-enriched lymphatic fluid, it is rich in protein, fat, methods are often used in conjunction or used progressively as fat-soluble vitamins, lymphocytes, immunoglobulins and more conservative methods fail. electrolytes.4 Loss of this fluid may result in impaired wound Because of the lack of scientific consensus on the optimum healing, electrolyte abnormalities, dehydration, immune suppres- method of nutritional management for patients with a chyle leak, sion, nutritional deficiencies, prolonged hospitalization and the nutritional and medical practice employed varies between occasionally result in patient death.7,8 As many patients with a practitioners, and, as a result, it is unlikely that best patient health chyle leak have recently undergone surgery and/or suffered outcomes are consistently achieved. To consistently achieve severe trauma, they are already at significantly increased better patient health outcomes in those with chyle leakage, nutritional risk with increased protein and energy requirements evidence-based clinical practice guidelines need to be established. for wound healing,9 which is only exacerbated by nutrient losses However, with no available systematic reviews and a lack of from chyle leakage. evidence on the matter, this is currently not possible. The aim of The goal of nutritional management in chyle leakage is to this paper was to systematically review all the available evidence encourage healing of the damaged lymphatic vessels, along with assessing the effect of nutritional intervention on people with replacing chylous losses and meeting the patient's nutritional chyle leakage and its effectiveness at reducing the need for needs with adequate kilojoules, fluid, electrolytes and protein.10 surgical intervention.

1School of Clinical Nutrition, University of Sydney, Sydney, New South Wales, Australia and 2Nutrition and Dietetics Department, Royal Prince Alfred Hospital, Sydney, New South Wales, Australia. Correspondence: Dr S Carey, Royal Prince Alfred Hospital, Missenden Road, Camperdown, Sydney, New South Wales 2050, Australia. E-mail: [email protected] Received 7 January 2014; revised 24 August 2014; accepted 23 January 2015; published online 29 April 2015 Systematic review of chyle leaks BR Steven and S Carey 777 SUBJECTS AND METHODS Data analysis Search strategy A meta-analysis was not able to be performed because of the A computerized bibliographic search was performed using Title/Abstract heterogeneous nature of the studies. Because of the nominal nonpara- 2 searches and Medical Subject Headings (MeSHs) where appropriate, of the metric nature of the data, the χ -test was used to compare success rates Medline, Cinahl and Web of Science databases for publications from January between dietary treatment options, using the Statistical Package for Social 1980 to September 2013. Because of the variety of terminology used when Sciences version 17.0 (SPSS Inc, Chicago, IL, USA). Statistical significance describing chyle leaks, a comprehensive search was required to capture all was assumed at Po0.05. relevant articles. Search terms included the following: Chylous ascites (MeSH), chylothorax (MeSH), thoracic duct (MeSH), lymphatic vessels (MeSH) or chyl*, and therapeutics (MeSH), treatment outcome (MeSH), disease progression RESULTS (MeSH), survival analysis (MeSH), enteral nutrition (MeSH), parenteral nutrition A total of 7,198 citations were identified through the primary (MeSH),triglycerides(MeSH),mct,fat*,conservativeormanag*.Exclusions search (2285 from Medline, 4482 from Web of Science and 430 included animal studies, publications reported in another language other than English, studies containing pediatrics, individual case reports, studies without from Cinahl). After screening, 60 full-text articles were considered nutritional intervention, studies that did not report treatment outcomes and for review, 29 of which fell within the exclusion criteria, leaving 31 publications where the full text was not available. The reference lists of all suitable articles for analysis (Figure 1). The reference lists of these included articles were browsed to obtain additional studies. Because of the articles were browsed but did not identify any appropriate limited number of randomized trials, case review studies were included in this publications that were available in full text. systematic review. All of the identified articles were retrospective case series (Table 1). No randomized control trials involving nutritional Data extraction and quality assessment management were available. The highest score for scientific Each article was scored for its scientific quality by two researchers (BRS and quality was 3/11, with the majority of articles scoring 2/11, SC) on a scale of 0–11, using a quality assessment tool adapted from indicating the poor quality of evidence available. Sample size of 17 Heyland et al. Articles were appraised on their use of randomization, each study varied from 3 to 66 participants and from 18 to 89 blinding, intention-to-treat analysis, patient selection, description of years of age. patient outcomes and baseline comparisons for the groups of patients. From these articles, 550 patients having had received nutritional Data extraction was performed by one researcher (BRS). Extracted data fi included study design, participant characteristics, location of effusion, intervention for chyle leakage were identi ed. Reported methods diagnostic method used, drainage output, dietary intervention used, time of dietary intervention included fasting, TPN, enteral nutrition, to resolution and the incidence of surgical intervention. restriction of dietary fat/LCTs and MCT supplemented diets.

Records identified through Additional records identified database searching through other sources (n = 7198) (n = 0) Identification Records after duplicates removed (n = 6277)

Records screened Records excluded (n = 6218) Screening (n = 6277)

Full-text articles excluded, with reasons Full-text articles assessed (n =29) for eligibility (n =60) • 2 case reports

Eligibility • 5 containing children • 22 without nutritional intervention Studies included in qualitative synthesis (n = 31)

Studies included in quantitative synthesis Included (meta-analysis) (n = 0)

Figure 1. Literature search and selection of articles.

Table 1. Case series studies of nutritional interventions among patients with chyle leakage.

Publication (n = 31) Methods score Participants Diet Days until leak resolved with conservative % requiring surgical treatmenta intervention

Alexiou et al.39 2 21 TPN x̄ = 17 (7–36) 19 Allaham et al.34 2 5 TPN x̄ = 8(7–9) 40 Assumpcao et al.25 2 47 TPN M = 15 (9–28) 0 Bolger et al.26 2 11 TPN x̄ = 35 (14–42) 27 Bonavina et al.35 2 3 TPN Did not resolve conservatively 100 Capocasale et al.27 2 8 TPN and MCT diet x̄ = 12.3 (5–16) 0 Cerfolio et al.40 1.5 47 TPN and MCT diet M = 7(2–15) 72 (80% TPN, 45% MCT) de Gier et al.18 2 11 TPN and MCT diet x̄ = 21 (9–30) 18 Dugue et al.41 2 23 TPN x̄ = 9(3–17) 39 Evans et al.19 2 23 TPN and MCT diet Eight patients required 414 weeks to 23 resolve. Three required 411 months. Fahimi et al.28 2 12 MCT diet 58 Izzard et al.42 2 11 MCT Diet x̄ = 8.1 (4–26) 0 Kaas et al.20 2 12 Enteral MCT diet or 25 TPN Lagarde et al.29 2 20 TPN x̄ = 920 Le Pimpec-Barthes 1.5 26 MCT Diet o7 days for 5, 7–14 days for 9, 18 days for 1 42 et al.30 Malik et al.36 2 7 TPN M = 7.5 (4-32) 14 Merigliano et al.33 3 19 TPN M = 21 (20–28.5) 64 Nishigori et al.43 1.5 9 Normal, low fat or x̄ = 6.2 (fasted), 2.5 (normal), 4 (MCT) 0 fasted Nussenbaum et al.21 2 15 TPN and MCT diet x̄ = 9.8 (3–25) 20 Roh et al.3 1.5 4 MCT diet x̄ = 9.75 (4–16) 0 Roh et al.22 2 13 TPN and MCT diet x̄ = 8.73 (5–20) 15 Seow et al.31 2 36 TPN x̄ = 16 20 Shah et al.44 3 33 TPN or elemental x̄ = 7(5–11) 62 enteral Shimizu et al.13 2 26 TPN M = 8(4–35) 19 Singh et al.45 2 6 Fat-free diet x̄ = 14.75 (12–18) 25 Spiro et al.46 2 16 Low-fat diet 4–25 63 Takuwa et al.14 2 37 Low-fat diet M = 10 (5–27) 6 Tulunay et al.37 3 24 TPN and MCT diet M = 28 (11–60) MCT; M = 10 (5–66) TPN 29 (11% MCT, 40% TPN) van der Gaag et al.2 2 66 TPN and low-fat diet M = 3.5 (1–16) 0 Worthington et al.23 2 8 TPN and MCT diet Did not resolve 100 Zhou et al.47 2 4 Low-fat diet M = 15.5 (7–34) 25 Abbreviations: MCT, medium-chain triglyceride; TPN, total parenteral nutrition. aDays reported as mean (x)/median̄ (M) and range.

Table 2. Comparison of success rates between dietary methods

Diet Publication Subjects Resolved Failed Percent successfully treated Days to resolution with non-surgical therapy

Normal 43 2 2 0 100% 2–3 MCT diet 3,23,27,28,30,37,40,42 119 92 27 77.3% 4–60 Low fat 2,14,43,45–47 58 44 14 75.9% 4–34 TPN 2,13,25–27,29,31,33–37,39–41,44 270 181 89 68.5% 3–66 Enteral 42,44 19 12 7 63.2% MCT and TPN 18–23 76 59 17 77.6% 2–30 NBM 43 6 6 0 100% 4–12 Total 550 396 154 72% Abbreviations: MCT, medium-chain triglyceride; NBM, nil by mouth; TPN, total parenteral nutrition. No statistically signiﬁcant difference in the rate of successful resolution between groups (χ2 = 11.14, P = 0.08).

Six publications reported the use of both TPN and MCT non-nutritional treatments were used alongside dietary interven- supplementation, usually indicating TPN when MCT supplementation. These included the use of chemical pleurodesis, diuretics and tion alone has failed, and these subjects have been combined as a somatostatins (octreotide). However, these treatments were not separate group.18–23 The use of TPN and MCTs were the most used consistently among patients either within or between common interventions, with TPN having a slightly lower success studies. As a result, it is likely that they have confounded the rate compared with MCT supplementation (Table 2). However, results by modifying health outcomes among those patients who there was no statistically signiﬁcant difference between any of the received those therapies. Because of the poorly descriptive nature dietary methods and the rate of resolution of a chyle leak of the available literature, these confounding treatments could not (χ2 = 11.14, P = 0.08). Within the studies, several conservative, be adjusted for.

European Journal of Clinical Nutrition (2015) 776 – 780 © 2015 Macmillan Publishers Limited Systematic review of chyle leaks BR Steven and S Carey 779 Drainage output between patients on conservative treatment compromise and demonstrative of clinical outcomes in hospita- compared with invasive treatment was poorly reported and could lized patients. not be effectively analyzed. Where reported, drainage outputs Because of the lack of evidence on this topic, the method of were recorded as peak 24-h rates either after diagnosis or after management is currently up to each individual practitioners’ cessation of oral intake. Patients who underwent surgical judgement, and their opinion on what is considered a need for intervention typically had greater peak 24-h drainage rates than surgery is highly variable.33 As a result, it is hard to interpret what those whose leaks resolved conservatively,3,12,13,19–21,24–31 but no constituted failure in conservative management, when surgery statistical analysis was available to determine significance. In some was often indicated consistently early in some publications, for cases, patients with exceedingly high peak drainage outputs up to example, after 10 days of continued leakage,34 whereas in other 3 L per day resolved with conservative treatment alone,19,24,26 cohorts conservative management continued as long as there was whereas a patient with a peak output as low as 245 ml per day evidence that the leakage was still reducing, in some cases for up failed to resolve conservatively and required surgical intervention.32 to 2 months.37 The differences between patients who failed No measures of nutritional status, such as changes in lean body conservative management versus those who resolved conserva- mass, were reported in any of the publications. However, three of tively may have more to do with the judgement of the attending the subjects in this review had chyle leakage that persisted for physician, rather than the severity of the patient’s condition. As 411 months,21 whereas seven studies reported leaks lasting the effects of long-term chyle leakage are highly detrimental to 1–2 months.19,26,31,33,34–36 Given the nature of chyle leakage, it is the health of the patient, including an increased risk of possible that these patients suffered from significant nutritional malnourishment and immune compromise,7,8 it is reasonable to compromise, and early surgical intervention may have resulted in assume that dietary intervention may not be as effective as better health outcomes for these patients. reported if the patients’ health is allowed to become significantly compromised as a result of long-term conservative therapy. Furthermore, surgery in malnourished and immuno-compromised DISCUSSION patients is associated with many adverse outcomes, including Overall, the evidence demonstrating the appropriate method of infection, impaired wound healing, increased length of stay and nutritional management for patients with chyle leakage is increased risk of mortality.38 Thus, it may often be in the patient’s inadequate, with case series comprising the strongest available best interests to surgically intervene early if there is a risk that data. Nutritional modification is vital in these patients to prevent conservative therapy may fail or be prolonged. nutritional compromise, but there is insufficient evidence to Despite this, the results of this systematic review indicate demonstrate whether and when nutritional intervention can proportionately more patients required surgery if they received replace surgically invasive management as a method of therapy. TPN compared with an MCT supplemented diet. However, it Very few conclusions can be drawn from the available evidence would be ill advised to presume that TPN is a less effective due to many limitations. The sample size of these publications is treatment. TPN was often indicated by the patients’ attending very small (x̄ = 19), and, even with all of the available participants practitioner when drainage outputs were considered too high to compiled together, only the TPN and MCT diet groups had 4100 resolve with dietary fat restrictions alone or when more participants. Little was to be gained from comparing the normal, conservative methods had failed.2,18–23,37 Consequently, patients enteral or nil by mouth interventions due to the small sample sizes on TPN typically had more severe chyle leaks than those on an (o6), and this strongly impairs the capacity to make judgements MCT or low-fat diet and were more likely to require surgery about their effectiveness as a treatment. The available publications regardless of dietary treatment. Given the inherent risks involved were highly heterogeneous in nature. Although almost all of the in TPN,32 it is important for practitioners to evaluate the risks and cases of chyle leaks were caused by iatrogenic physical trauma, benefits of this treatment, as a failed TPN intervention introduces they were diverse in the location and severity of damage to the increased risk of morbidity in addition to the possibility of poor lymphatic structures. Furthermore, dietary interventions were surgical outcomes if long-term chyle leakage occurs. described in minimal detail, such as ‘MCT diet’ or simply ‘TPN’, The absence of high-quality studies investigating the outcomes without any information regarding the nutrient composition of of nutritional management in this population is the major issue the corresponding TPN solutions or diet or how the patient’s affecting this review. Retrospective analyses are highly limited in energy and nutrient requirements were calculated. Thus, the their methods and the data that are reported. Further research is nutrient intake between subjects undergoing the same interven- required before the method of best practice can be established. tion may be vastly different. The use of other conservative Future research should consider as follows: (i) whether and how interventions, such as chemical pleurodesis and octreotide the rate of drainage output upon diagnosis and after the cessation therapy, may have improved chyle leak recovery outcomes of feeding can demonstrate the likelihood of successful resolution; independent of diet. However, the inconsistent use of these (ii) whether adequate nutrition can prevent or treat malnourish- therapies both within and between the studies inhibits the ment and immunodeficiency that has occurred due to chyle capacity to assess their influence on patient outcomes and further leakage, and how; (iii) changes in nutritional markers of health increased the heterogeneity of the data. status during conservative therapy, for example, changes in lean None of the available studies reported any assessment of body mass; (iv) whether successful conservative resolution is nutritional status or risk of malnutrition in their patients during affected by the location and severity of lymphatic damage; (v) hospitalization and treatment. Because of the increased likelihood whether non-nutritional conservative therapies, such as pleurod- of nutritional compromise in patients with a chyle leak,7,8 it is esis and octreotide, are beneficial in chyle leak management and imperative to assess the patients’ nutritional status to determine finally; and (vi) whether the response to conservative therapy the necessity and effectiveness of nutritional intervention. This differs between effusions caused by trauma compared with data is lacking from these studies and further exemplify the poor malignancies. quality of the available evidence on this subject. Analysis of Although there is evidence to suggest that nutrition may have a patient health outcomes between intervention methods is not role in the management of patients with chyle leakage, currently possible as a result of this. Relevant methods of nutritional the evidence is insufficient to determine which dietary methods assessment would include changes in body weight, triceps are most effective, and more research is required before any skinfold thickness, mid-arm circumference and hand grip guidelines for best practice can be established. Until this time, strength.18 All of these can be used as evidence for the loss of clinicians should ensure that patients with a chyle leak achieve lean body mass, which is a strong indicator of nutritional and maintain good nutritional status. This would expectedly entail

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