|Year : 2014 | Volume
| Issue : 2 | Page : 47-52
The effect of a late-evening protein-containing snack on nitrogen balance in cirrhotic patients
Ferial S.E. El-Kalla1, Loai O Mansor1, Hanan A El-Bassat1, Shaimaa Mishaal1, Jehan F Attia2
1 Departments of Tropical Medicine, Tanta University, Tanta, Egypt
2 Department of Clinical Pathology, Faculty of Medicine, Tanta University, Tanta, Egypt
|Date of Submission||11-Apr-2014|
|Date of Acceptance||17-Apr-2014|
|Date of Web Publication||31-Jul-2014|
Hanan A El-Bassat
Department of Tropical Medicine, Faculty of Medicine, Tanta University, Tanta
The aim of the study was to evaluate the effect of a late-evening protein-containing snack on nitrogen balance in cirrhotic patients.
Patients and methods
Thirty cirrhotic patients were divided into the following groups: group I, comprising 15 patients who received a late-evening 300-cal, 15-g protein-containing snack daily for 15 days; and group II, comprising 15 patients who received a late-evening supplement of amino acids (branched and essential) containing 22-g protein daily for 15 days. All patients were subjected to full history taking, clinical examination, and pelviabdominal ultrasound. Liver function tests, complete blood picture analysis, and estimation of blood urea and serum creatinine, urinary nitrogen loss, urea concentration in both serum and urine, and nitrogen balance were performed for all patients.
There was a significant increase in the mean level of serum albumin and red blood cell counts. The mean nitrogen balance significantly increased in both groups but more in patients who received branched chain amino acid (BCAA) supplementation. The mean serum ammonia significantly decreased in group II patients who received a late-evening BCAA supplementation, but not in patients of group I who received a late-evening protein-containing snack. There was no statistically significant difference in the levels of serum bilirubin or fasting blood glucose in either group.
The results of the present study suggest that late-evening snacking with either a small protein-containing meal or a BCAA supplement improves the level of alanine transaminase, aspartate aminotransferase, serum albumin, nitrogen balance, ammonia, urea, and the general condition of the patient. The patients receiving BCAAs respond better than the snack group. A BCAA mixture as a late-evening snack is a favorable nutritional intervention for liver cirrhosis patients to repair hypercatabolism and sarcopenia and improve their nutritional status, such as nitrogen balance and serum albumin. These results need to be further confirmed in a larger number of patients and for a longer period of time.
Keywords: cirrhosis, late-evening snack, sarcopenia
|How to cite this article:|
El-Kalla FS, Mansor LO, El-Bassat HA, Mishaal S, Attia JF. The effect of a late-evening protein-containing snack on nitrogen balance in cirrhotic patients. Tanta Med J 2014;42:47-52
|How to cite this URL:|
El-Kalla FS, Mansor LO, El-Bassat HA, Mishaal S, Attia JF. The effect of a late-evening protein-containing snack on nitrogen balance in cirrhotic patients. Tanta Med J [serial online] 2014 [cited 2019 Mar 20];42:47-52. Available from: http://www.tdj.eg.net/text.asp?2014/42/2/47/137797
| Introduction|| |
Cirrhosis is characterized by a state of accelerated starvation, with an early shift from glucose to lipid utilization for energy during the postabsorptive state. After an overnight fast, lipids account for 75% of the total calories utilized in cirrhotic patients, reflecting increased rates of ketogenesis and gluconeogenesis. In healthy participants, this metabolic profile develops only after 2 to 3 days of fasting As the rate of gluconeogenesis increases during starvation, there is an increased consumption of amino acids as a source of energy (protein catabolism) .
This accelerates skeletal muscle protein loss and reduces muscle protein synthesis, resulting in sarcopenia. Thus, cirrhosis is a state of anabolic resistance . The most common complication of cirrhosis is malnutrition comprising sarcopenia or loss of muscle mass and loss of fat mass or a combination constituting 'hepatic cachexia' . Sarcopenia adversely affects survival, quality of life, outcome after liver transplantation, and response to stress including infection and surgery .
One can assess protein requirement by measuring the nitrogen balance between intake and excretion, in which intake represents nutritional nitrogen and excretion represents the sum of measured urinary nitrogen plus an estimate of cutaneous and gastrointestinal losses .
Achievement of a positive nitrogen balance is widely considered to be the primary goal of nutritional support. Indeed, improved nitrogen balance calculations over time in response to nutrition is the single nutritional variable most consistently associated with improved outcome during critical illness .
Increasing caloric intake alone is inadequate to reverse sarcopenia . A potential strategy for reversing sarcopenia of cirrhosis is extending the duration of the postprandial (fed) state, when muscle protein breakdown (MPB) is suppressed and protein synthesis is stimulated. As the postabsorptive phase is the longest between dinner and breakfast, this period of time may offer the best opportunity to reverse anabolic resistance. A late-evening snack (LES), which shortens the duration of this prolonged physiological fasting, may potentially preserve skeletal muscle mass by both reducing the mobilization of amino acids from skeletal muscle (decreased MPB) and increasing the rate of skeletal muscle protein synthesis. LES is a simple, safe, and inexpensive intervention, but may exacerbate symptoms of gastroesophageal reflux, aggravate pre-existing sleep disturbances, and worsen glucose intolerance .
Liquid dietary supplements, high-carbohydrate foods (e.g. rice ball, bread and jam, oral glucose), and branched chain amino acid (BCAA)-enriched supplements have all been used as an LES.
BCAA-enriched LES may be more effective than high-carbohydrate LES, as BCAAs not only serve as substrates for protein synthesis but are also important regulators of protein synthesis .
| Patients and methods|| |
The protocol of this study was approved by the Tanta Ethical Committee and written informed consent was taken from all patients. Thirty cirrhotic patients were recruited from the Tropical Medicine Department, Tanta University, Egypt. All patients gave informed consent to participate in the study. They were divided into the following:
(1) Group I: this group comprised 15 patients who received a late-evening 300-cal, 15-g protein-containing snack daily for 15 days.
(2) Group II: this group comprised 15 patients who received a late-evening supplement of amino acids (branched and essential) containing 22-g protein daily for 15 days.
Child B or C cirrhotic patients.
Patients with diabetes, hepatic encephalopathy, renal dysfunction, or hepatocellular carcinoma were excluded from the study.
All patients were subjected to full history taking, thorough clinical examination, pelviabdominal ultrasound, liver function tests, complete blood picture analysis, and estimation of blood urea, serum creatinine, urinary nitrogen loss, and urea concentration in both serum and urine.
To determine the nitrogen balance of a patient three samples are required:
S1 = the first sampling of serum.
S2 = serum sampling after 24.
S3 = sample of the 24-h urine. The urine is diluted 50×, and the result has to be multiplied 50× .
(1) Reagents were pipetted into numbered tubes as shown in [Table 1], and then mixed and incubated for 10 min at room temperature.
(2) The tubes were shaken immediately after addition of reagent B and incubated 10 min at 25°C (room temperature).
(3) Within 2 h the absorbance of samples and standard was measured against blank at 600 nm.
Nitrogen balance calculation
Nitrogen balance is the measure of nitrogen input with the nitrogen output subtracted from it.
Nitrogen intake is calculated using the given protein intake (proteins contain about 16% of nitrogen).
Eighty percent of nitrogen is excreted through the urine as urea; the remaining 20% is excreted as creatinine, NH4+, and uric acid.
Nitrogen balance = nitrogen intake − nitrogen loss.
Nitrogen loss = urinary urea nitrogen + 4 (nonurinary loss of nitrogen).
The collected data were organized, tabulated, and statistically analyzed using the statistical package for the social sciences (SPSS, version 19; SPSS Inc., Chicago, Illinois, USA). Sex was presented as number and percentage and the observed difference of distribution by sex was tested using the c2 -test. Other numerical variables were presented as range, mean, and SD. The observed differences in mean values of each variable between studied groups were tested using Student's t-test. The differences in mean values before and after intervention within each group were tested using paired Student's t-test. The level of significance was determined at P value less than 0.0.
| Results|| |
Demographic characteristics of the studied groups
(1) Group I: this group consisted of eight (53.3%) male and seven (46.7%) female patients, nine Child B and six Child C.
(2) Group II: this group consisted of 11 (73.3%) male and four (26.7%) female patients, eight Child B and seven Child C.
There were 23 ascitic patients in both groups.
[Table 2] shows the comparison between the two groups for the studied parameters.
The mean body weight in group I decreased from 73.53 to 71.20 kg (P = 0.045) and in group II from 67.8 to 64.8 kg (P = 0.001), both groups showing statistical significance. The comparison of the mean of the two groups before and after the snack was statistically insignificant (P = 0.178 and 0.136).
The mean red blood cell (RBC) count in group I increased from 3.39/μl before the introduction of the LES to 3.48/μl at the end of the study (P = 0.141) with no statistical significance. In group II the mean was 3.23/μl before and 3.45/μl after (P = 0.030) with statistical significance. The comparison between mean RBCs of the two groups before and after LES administration was not statistically significant (P = 0.419 and 0.846).
The mean white blood cell (WBC) count in group I increased from 4.52 to 4.58/μl (P = 0.422), with no statistical significance. In group II the mean WBCs increased from 4.45 to 4.57/μl (P = 0.109), with no statistical significance. The comparison between the mean WBCs of the two groups before and after snacking was statistically insignificant (P = 0.925 and 0.987).
The mean platelet count in group I decreased from 107.13 to 106.67/μl (P = 0.756). In group II the mean platelet count increased from 83.87 to 83.93/μl (P = 0.984), with no statistical significance. The comparison between the mean of the two groups before and after the snack was statistically insignificant (P = 0.160 and 0.176).
The mean blood urea in group I decreased from 41 to 37 mg/dl (P = 0.288), with no statistical significance. In group II the mean decreased from 40.33 to 29.2 mg/dl (P = 0.003), with statistical significance. The comparison between the mean of the two groups before and after the snack was statistically insignificant (P = 0.836 and 0.093).
The mean blood ammonia level in group I increased from 19.47 to 19.80 mmol/l (P = 0.825) with no statistical significance. In group II the mean decreased from 23.8 to 20.33 mmol/l (P = 0.007), which was statistically significant. The comparison of the mean of the two groups before and after the snack gave insignificant results (P = 0.338 and 0.826).
The mean nitrogen balance increased from -15.47 to -10 (P = 0.005) in group I, and in group II the mean increased from -13.24 to -5.91 (P = 0.003), with statistical significance. The comparison of the mean of the two groups before and after the snack gave statistically insignificant results (P = 0.228 and 0.068).
The mean fasting blood sugar level in group I increased from 78.47 to 83.6 mg/dl (P = 0.178), and in group II the mean increased from 76.20 to 83 mg/dl (P = 0.182), both showing statistical insignificance. The comparison of the mean of the two groups before and after the snack was statistically insignificant (P = 0.414 and 0.852).
The mean bilirubin level in group I decreased from 1.79 to 1.75 mg/dl (P = 0.150) and in group II the mean decreased from 1.76 to 1.73 mg/dl (P = 0.262), both groups showing no statistical significance. The comparison of the mean bilirubin level between the two groups before and after the snack was statistically insignificant (P = 0.924 and 0.969).
The mean alanine transaminase (ALT) in group I decreased from 28.4 to 26.07 U/l (P = 0.073), with no statistical significance. In group II the mean decreased from 28.93 to 25.87 U/l (P = 0.002), with statistical significance. The comparison between the mean of the two groups before and after the snack gave statistically insignificant results (P = 0.829 and 0.939).
The mean aspartate aminotransferase (AST) in group I decreased from 41.07 to 36.67 U/l (P = 0.113). In group II the mean decreased from 44.2 to 37.6 U/l (P = 0.011) with statistical significance. The comparison between the mean of the two groups before and after the snack was statistically insignificant (P = 0.640 and 0.840).
The mean albumin in group I increased from 2.63 to 2.71 g/dl (P = 0.017), which is statistically significant. In group II the mean albumin increased from 2.61 to 2.69 g/dl (P = 0.003), which is statistically significant. The comparison between the mean of the two groups before and after the snack was statistically insignificant (P = 0.912 and P = 0.907).
| Discussion|| |
Patients with cirrhosis lack adequate glycogen stores because of liver atrophy and develop a severe catabolic state on fasting. After an overnight fast, patients with cirrhosis have a marked decrease in glucose oxidation, with enhanced fat and protein catabolism similar to that observed in healthy participants after 2-3 days of starvation . To avoid such nocturnal starvation, energy supplements have been developed  and are recommended as LESs by the American Society for Parenteral and Enteral Nutrition .
The mean RBC count increased at the end of the study, with statistical significance among the patients in the BCAA group. Another study by Nakaya et al.  found that the RBC count significantly increased among patients receiving a BCAA supplement but not in the snack group (who received ordinary food containing 210 kcal protein, 9 g protein and 5 g fat vitamins trace elements). In a study on athletes by Ohtani et al. , it was found that BCAA supplementation significantly improved physiological markers such as RBC count, hemoglobin, hematocrit, serum albumin, fasting glucose, and a decrease in creatinine phosphokinase (P < 0.05), suggesting increased hematopoiesis and glycogenesis, and rapid alleviation of muscle inflammation. This may also explain the increase in platelet count among our patients from the BCAA group.
There was a statistically significant decrease in ALT and AST levels among the patients in the BCAA group after the introduction of the LES, which was in agreement with previous studies by Nakaya et al.  and Koreeda et al. . This may be explained by the finding that BCAAs, specifically leucine, are potent stimulators of hepatocyte growth factor production .
Accordingly, BCAAs not only provide substrates for protein synthesis but also accelerate the biochemical machinery, which facilitates liver regeneration, compensating for progressive liver cell death.
Patients from both groups showed a statistically significant increase in serum albumin levels. Similar findings were reported by Nakaya et al. , Habu et al. , and Koreeda et al. . The level of serum albumin significantly increased with a LES and BCAA supplementation. This may be explained by the view that BCAA regulates albumin synthesis at a subcellular level. A low BCAA level impairs synthesis of proteins such as albumin . Tsien et al.  and Marchesini et al.  have stated that administration of BCAA supplementation to cirrhotic patients reduces MPB in the short term and increases serum albumin levels and improves patient survival in the long term.
In a study by Fukushima et al.  daytime administration improved nitrogen balance and Fischer's ratio; however, both were further significantly improved with nocturnal administration. At 3 months, a significant increase in serum albumin level was observed in patients receiving nocturnal BCAAs but not daytime BCAAs. It is possible that daytime BCAAs are used primarily as calories, whereas nocturnal BCAAs may be preferentially used for protein synthesis.
The favorable effect of BCAA on liver regeneration and nutritional state of the body is related to their stimulatory effect on protein synthesis, secretion of hepatocyte growth factor, glutamine production, and inhibitory effect on proteolysis . The simultaneous activation of mammalian target of rapamycin (mTOR) signaling in the liver, a well-demonstrated effect of BCAAs, promotes albumin synthesis in the liver .
In this study there is significant decrease in body weight in both groups. This is in disagreement with the results of Nakaya et al.  who found that body weight was slightly but significantly increased in the BCAA group but not in the snack group. Our explanation is that the weight loss in our patients may be due to use of diuretics on hospitalization as 23 patients had ascites and lower-limb edema. This study showed a decrease in the level of blood urea in both groups with statistical significance in the BCAA group. This was in agreement with the study by Nakaya et al. , which showed that the serum blood urea level significantly decreased in the BCAA group between baseline and end of the study.
Nitrogen balance significantly increased in both groups of this study but more in the BCAA group. This is a very important finding as improved nitrogen balance calculations of improvement over time in response to nutrition is the single nutritional variable most consistently associated with improved outcome during critical illness . The improved nitrogen balance in the case of the protein-containing LES is explained by cirrhotic patients exhibiting increased protein requirements to achieve balanced nitrogen metabolism  and with the BCAAs can be explained by the fact that BCAAs not only serve as substrates for protein synthesis but are also important regulators of protein synthesis .
In the study by Nakaya et al.  nitrogen balance had significantly increased in the BCAA group by the end of the study, but not in the snack group. The suggested explanation here was that the BCAA group was taking more protein (13.5 g protein and 3.5 g fat for 3 months).
The timing of administration of BCAA seems to be important. When cirrhotic patients were given BCAA granules after each meal (12 g/day), there was no significant improvement in the nitrogen balance. However, when they were given 8 g of BCAAs at bedtime a significant recovery of the nitrogen balance and a significant improvement in serum albumin levels were observed [16,18]. With LES, a significant increase in nitrogen balance has been reported compared with daytime supplementation  or no LES at all .
In this study, there was no improvement in the level of ammonia among patients in group I, but there was a significant decrease in the level of ammonia in group II patients. This may be explained by the finding that BCAAs are used for ammonia degradation in skeletal muscles of cirrhotic patients . In patients with cirrhosis, the skeletal muscle becomes a major organ for ammonia disposal via glutamine synthesis ; therefore, reversal of sarcopenia may enhance nonhepatic ammonia removal with subsequent improvement in hepatic encephalopathy.
Other studies have reported no significant change in plasma ammonia concentrations when BCAA LES was administered to people with cirrhosis with normal or mildly elevated serum ammonia concentrations at baseline [18, 25, 26]. These studies, however, did not use clinical outcome measures, and the well-known discord between plasma ammonia and the severity of encephalopathy suggests that LES may have an indirect effect on hepatic encephalopathy (HE) by reversing sarcopenia. This is supported by the observation that malnourished patients have more severe and frequent HE .
It has been found that normal protein diets have been given safely to patients with hepatic encephalopathy . Thus, restriction is rarely required but, if necessary, usually for no more than 48 h . Because long-term protein restriction promotes catabolism of body proteins and protein energy malnutrition (PEM), it must be combined with BCAA supplementation and increased intake of insoluble dietary fiber-rich vegetables to improve and prevent constipation.
In this study, fasting plasma glucose levels were not significantly different between the two groups. This was in accordance with the results of Nakaya et al.  who reported that LESs did not affect fasting blood glucose significantly in either group. Also, Fukushima et al.  demonstrated that there was no significant difference in fasting plasma glucose in both short-term and longer-term studies. No potential adverse effects to LESs appeared in our study, which is in agreement with the results of Marchesini et al. .
The goal of giving the late-evening protein-containing snack was to achieve a positive nitrogen balance. In this study the nitrogen balance becomes less negative. This may be due to the short period of this study or the poor nutritional state of our patients before starting the LES as the mean total calorie intake was 895 kcal/day and protein intake was 35 g/day, which were severely low.
| Conclusion|| |
The results of the present study suggest that late-evening snacking with either a protein-containing small meal or a BCAA supplement improves the level of ALT, AST, serum albumin, nitrogen balance, ammonia, and urea, and the general condition of the patient. The patients receiving BCAAs showed a better response compared with the snack group. A BCAA mixture as an LES is a favorable nutritional intervention for liver cirrhosis to repair malnutrition, hypercatabolism, and sarcopenia, which are the most common complications of cirrhosis and improve the nutritional status, such as nitrogen balance and serum albumin. These results need to be further confirmed on a larger number of patients and over a longer period of time.
| Acknowledgements|| |
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[Table 1], [Table 2]