NUTRITION REVIEWS IN GASTROENTEROLOGY, SERIES #10

Nitrogen Balance: Revisiting Clinical Applications in Contemporary Practice

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Proteins play vital roles in metabolic reactions in both healthy and critically ill adults. Nitrogen balance (NB) studies serve as a key metric for protein metabolism. Despite its introduction in nutrition research in the early 20th century, NB studies remain underutilized in the hospital setting. The methodology of a NB calculation can be complex and there are specific limitations when it is applied in several clinical scenarios including burn injury, renal disease, and trauma. Overall, NB assessments remain a valuable tool in assessing the adequacy of nutrition support as achieving a positive NB has been associated with improved clinical outcomes. The aims of this review are to delineate NB calculations in hospitalized patients and provide insights into its limitations and adaptations in special populations.

Introduction

Proteins are composed of long chains of amino acids with functions ranging from catalyzing metabolic reactions to providing support for cellular structures.1 Balancing adequate intake with protein degradation is therefore crucial to maintaining metabolic functions. Because proteins are the only macronutrient that contain nitrogen, NB studies serve as a surrogate for protein metabolism.2 The earliest attempts to calculate daily protein requirements in health date back to the 1860s-1870s, although these reports were largely based on dietary surveys of working men.2,3 Published in 1911, Chittenden was one of the first to utilize a NB assessment on 108 healthy subjects; he suggested 56 g of daily protein intake, close to modern-day recommendations.4 By the 1940s, NB was incorporated into many nutrition studies, including assessments of malnourished populations in postwar Denmark and Germany.5 In modern nutrition literature, NB or equilibrium is defined as a balance of protein degradation and accretion in most non-stressed adults.

Despite the abundant NB studies in unstressed populations, NB remains underutilized in critically ill and hospitalized patients. Yet, these patients experience significant physiologic stress and their protein requirements fluctuate frequently. NB assessment in these patients allows for more precise delivery of nutrition support. The critique of underlying methodology and applications of NB in specific clinical scenarios, such as hemodialysis and burn injury, have been published.6–9 The aim of this review is to provide updated clinical insights in the interpretation of NB studies in hospitalized adults and to summarize its use in select patient populations.

Definition of Nitrogen Balance

As nitrogen is a fundamental component of amino acids, a NB study calculates the difference between nitrogen intake and output and reflects the loss or gain of total body proteins. When more nitrogen is excreted than taken in, this is considered negative NB or a catabolic process; the reverse is considered positive NB or anabolic. In an unstressed adult, the nitrogen intake is almost entirely from protein via an enteral or parenteral route. Nitrogen losses include the excretion of urine urea with additional losses via feces and dermal layers.1 

Goals for Nitrogen Balance 

The general goal of NB is usually determined as -4 to +4 g nitrogen/day.10 This target is difficult to achieve in a hypercatabolic state. Hence, for critically ill patients, the goal is to provide enough nutrition support to minimize nitrogenous losses, which may blunt catabolism of lean tissue. Importantly, net balance or zero NB is not always the only target for protein supplementation, because patients suffering from chronic malnutrition or starvation may demonstrate pathologic adaption, where the body relies on muscle atrophy to provide amino acids for metabolic needs and to reestablish the balance.11 Hence, one should assess a patient’s clinical state such as muscle atrophy, body composition and strength, to eliminate the possibility of a falsely positive balance study. Importantly, without meeting the global caloric requirements, patients with sufficient protein intake still experience muscle degradation, because the muscle breakdown provides metabolites for other tissues. Thus, both adequate protein and caloric supplementation is necessary to suppress muscle breakdown.12

There is no strong evidence to support unlimited protein supplementation. Apart from the deleterious effect of excess protein in liver disease, renal insufficiency, and inborn errors of urea metabolism, a high protein supplementation may cause false positivity in the NB calculation.13 Previous studies, as well as the 2016 and 2021 American Society of Parenteral and Enteral Nutrition (ASPEN) guidelines, have recommended 1.5-2 g/kg of actual body weight (ABW) of daily protein as sufficient for nitrogen retention.14–17 In practice, protein support can be increased to 2.5 g/kg/d in critically ill trauma patients with severe nitrogen deficits and normal liver and renal functions.10 In non-obese patients receiving frequent intermittent hemodialysis or continuous renal replacement therapy, the protein goal can also be increased by 0.2 g/kg/d to a maximum of 2.5 g/kg of ABW per day. In obese critically ill patients, the protein goal is recommended as 2-2.5 g/kg of ideal body weight per day.17

In a dynamic patient, NB usually achieves a steady state after 48 hours of a constant nutritional regimen.18 Therefore, a steady intake or provision of calories and protein is required prior to NB assessment. To assess the adequacy of protein support, it is recommended to calculate a NB at 24 to 48 hours after the initiation of nutrition support with weekly assessments in those at risk for malnutrition, critically ill or with impaired healing.10 

Calculation Methods

The classic formula to calculate NB is: 


NB (g/d) = protein intake (g/d)/6.25 – urinary urea nitrogen (UUN)(g/d) – 4

Protein intake – In this formula, the estimated constants simplify the calculations, but carry inherent errors. The nitrogen input is calculated by dividing the protein intake in grams per day by 6.25, a constant based on the early determination that the average nitrogen content of proteins is approximately 16 percent (1/0.16 = 6.25).10,19 There are two sources of error here. First, all foods contain non-protein nitrogen such as free amino acids, nucleotides, and choline, and only a small amount of these carry the same metabolic effects of protein.19 These nitrogen sources thus should be excluded for NB calculations; however, the exact proportion of these sources in the common diet and in nutritional supplements is not well understood. Secondly, the nitrogen content varies by the molecular weight of the amino acids taken in. Therefore, the actual nitrogen content of proteins range from 13 to 19 percent, which is equivalent to conversion factors of 5.26 to 7.69.19 It is undoubtedly impractical to comb through the protein sources for a patient ingesting varying food groups daily. One may consider altering the constant for patients who receive solely commercially available feeding formula or parenteral nutrition, because the commercially available formulas also vary by their amino acid contents.10,20 However, in a classic review by Dickerson, the amino acid content in varying products would result in a 1g maximum error in NB for a patient with 120g daily protein intake, a relatively small impact unless patients have significantly high protein requirements.

Urinary nitrogen loss – The remainder of the NB equation accounts for the nitrogen losses via urine (UUN – 2 g) and other losses (- 2 g). To obtain the UUN, the patient’s urine is collected for a 24-hour period. Because of the various extrapolations used in a NB calculation, it is recommended to adhere to the 24-hour collection for accuracy. To assess the completeness of urine collection, one can calculate the estimated creatinine clearance (CrCl) and compare it with the one derived from the Cockroft-Gault equation. A significantly lower CrCl from urinary volume suggests incomplete collection.10 

The UUN can be measured in most laboratories, but it underestimates total urinary nitrogen (TUN) excretion because TUN also includes molecules such as ammonia.1,21 The classic formula assigns 2 grams as an estimation of the difference between UUN and TUN. However, in critically ill patients, the non-urinary nitrogen loss tends to increase due to increased protein catabolism.10,22 Dickerson, et al. studied the TUN in trauma patients using pyrochemiluminescence and proposed that UUN/0.85 is a more accurate estimation of urine urea loss:22 

 
NB (g/d) = protein intake (g/d)/6.25 – UUN (g/d)/0.85 – 2

As 60% of non-urinary nitrogen loss is in the form of ammonia in critically ill patients,21,23 this estimation does not apply for patients with significant open wounds, diarrhea, renal insufficiency or end stage liver disease.

Extrarenal losses – The final subtraction of 2 grams arises from nitrogen losses via skin, soft tissues, and feces. Skin and soft tissue loss is approximately 0.5 g/d in sedentary people, and an average of 1.6 g/d nitrogen is excreted in stool.1 These generalized values, however, are based on small studies that measured nitrogen loss in non-stressed adults. Nitrogen loss from skin has been measured from desquamated cells, nail clippings and hair. It is directly correlated with body surface area and has been calculated as 5 mg/kg body weight in a comfortable environment.24 In addition to cutaneous loss, there is also nitrogen loss from sweat, which varies by gender, race and ambient temperature. There have been several measurements reported via physiological studies in the 1960s and 1970s. An average dermal and sweat nitrogen loss of 6 mg/kg at temperatures of 6-22°C, and 15 mg/kg at 25-30°C.25 For fecal nitrogen loss, it can differ based on the amount of nitrogen in dietary intake. Regardless, there is an obligatory nitrogen loss due to baseline metabolism and enzyme proteins, which was estimated to be 7-10 mg nitrogen per kg of body weight.26,27

Nitrogen Balance and Clinical Outcomes

Table 1. Sample Calculation of Additional Nitrogen Loss in Burn Patients
Calculate additional nitrogen loss for a
5-foot-6-inch, 70kg adult patient with
burn injuries of 20% BSA:
• BSA is 1.82 m2

Day 1-3:
0.3 x 1.82 m2 x 20 = 10.9 g nitrogen loss per day
Day 4 onward:
0.1 x 1.82 m2 x 20 = 3.6 g nitrogen loss per day

The objective of a NB measurement is to provide guidance on adequate protein supplementation to mitigate the hypercatabolism of illness. However, the actual effect of a positive NB on patient outcomes is difficult to study due to the heterogeneity of patient populations. Individual studies tend to have limitations of small study sizes or short study durations. In a retrospective study of 40 neurologic intensive care unit (ICU) patients, Kim, et al. found that a positive NB was associated with less neurological deterioration and shorter ICU and hospital stays.28 Zhu, et al. conducted a meta-analysis that included eight observational studies of 1409 critically ill patients. A positive change in NB on subsequent studies was associated with patient survival, demonstrating the impact of repeated hospital measurements.29 In a retrospective study of  99 critically ill patients with COVID-19 infections, both the survivor and the non-survivor groups had similarly negative NB, but the survivor group had consistently higher NB values than the non-survivor group.30 However, in a small randomized controlled trial (RCT) of 40 ICU patients comparing a protein-fortified versus a standard diet, there was no difference of skin alterations (secondary outcome of interest) despite a higher NB in the protein-fortified group.31 Lastly, in a RCT of 120 ICU patients receiving standard (0.8 g/kg/day protein) or high protein (1.2 g/kg/day protein) parenteral nutrition, the high protein group had better forearm muscle mass, grip strength, and fatigue score on day 7 as well as a higher NB on day 3.32 Overall, the current data suggest a potential benefit in survival, hospital outcomes, and muscle preservation among individuals with a positive or improved NB, although more rigorous trials are needed.

Special Scenarios

Burn – In burn patients, body fluid and protein losses are highly dynamic in the first week post-injury, especially for those suffering burns on more than 15% of the body surface area (BSA).28 The fluid loss tends to be the greatest in the first 24-48 hours post-burn, peaking at approximately 20 g per 10% total surface area.33,34 Based on this, Waxman, et al. proposed that the average daily nitrogen loss on post-burn days 1-3 is estimated as nitrogen loss (g/d) = 0.3 (g/m2) x BSA (m2) x % burn; and on post-burn days 4 and onward as nitrogen loss (g/d) = 0.1 (g/m2) x BSA (m2) x % burn.33 This equation can be used to calculate an additional nitrogen loss in the NB equation. Table 1 provides an example of calculated daily nitrogen losses with the BSA calculated using the Mosteller formula.35 

Table 2. Nitrogen Balance Calculations for Patients Receiving CRRT
Nitrogen loss on CRRTNitrogen losses (g/day) = effluent urea nitrogen losses
(g/day) + amino acid loss via effluent (g/day) + urine
urea nitrogen (g/day) + insensible nitrogen losses
(0.031 g/kg/day x weight in kg)
Effluent urea nitrogen = total effluent ultrafiltrate
volume (L) Å~ average ultrafiltrate urea nitrogen (g/L)
The total effluent ultrafiltrate volume = sum of dialysate
volume + replacement fluid volume + removed
ultrafiltration
In terms of calculating the average ultrafiltrate urea nitrogen concentration, Scheinkestel described a method of
collecting 20 mL dialysate every eight hours and measuring the nitrogen concentration in the mixed 60 mL sample.37

Open abdomen – The open abdomen leads to abdominal fluid and protein loss from the exposed viscera. In a small cohort study of 25 critically ill surgical patients, the average abdominal fluid loss ranged from 2.2 to 3.0 L per day between post-operative day 1 and day 5 with a daily abdominal fluid nitrogen loss of 3.5 g + 1.7 g per 24 hours, or 1.9 g + 1.1 g per liter of abdominal fluid. This translated to an average underestimation of 3.5 g/d nitrogen loss in the study cohort when not accounting for the abdominal fluid losses.36 Overall, one should consider nitrogen losses from abdominal and other body fluids when losses are significant.

Renal impairment – Patients with significant renal impairment accumulate nitrogen in the body as urea. Given its water solubility, the amount of urea in the body can be estimated by body water content and blood urea nitrogen (BUN).10,21 Dickerson proposed an adjusted formula that takes BUN fluctuations into consideration: 


Body urea nitrogen accumulation = 0.6 x weight x (BUN2 – BUN1) x 0.01 

BUN1 and BUN2 are the two serum urea nitrogen values before and after the urine collection. Generally, a change in BUN greater than 5 mg/dL correlates to a meaningful change in NB.10 In this case, the final NB equation is:


NB (g/d) = protein intake (g/d)/6.25 – (UUN(g/d)/0.85) – (0.6 x weight x (BUN2 – BUN1) x 0.01)– 2

Renal replacement therapy – In patients receiving continuous renal replacement therapy (CRRT) or intermittent hemodialysis (iHD) the calculation of nitrogen losses requires an assessment of the protein and amino acid losses in the dialysate in addition to the accumulation of BUN (in iHD). Ostermann, et al. previously summarized the studies utilizing NB in hemodialysis patients.6,8 During CRRT the amino acid losses can be estimated as 1.5 g/day for an ultrafiltration flow rate of 1 L/h and 2 g/day for an ultrafiltration flow rate of 2 L/h. In iHD, nitrogen loss is calculated through the urea nitrogen accumulation (UNA), because patients with renal insufficiency have decreased capacity to excrete urea and the change in BUN during the 24-hour urine collection requires assessment. Hence, the equation for nitrogen loss while on dialysis is listed below in Tables 2 and 3.6,7,37

Compared to the UNA in a patient with renal disease but not on dialysis, the calculations above incorporate the accumulated urea that has been removed from dialysis and the weight change after dialysis. 

Liver dysfunction and hyperammonemia – The liver captures serum ammonia and converts it to urea, which is then excreted mainly through the kidneys. In both acute and chronic liver dysfunction, there is marked decrease in ammonia uptake by the liver. The muscle uptake of ammonia increases roughly in a linear relationship to the arterial ammonia level and converts ammonia into glutamine.38 Hence, it is expected that calculation of urinary nitrogen loss underestimates the total nitrogen loss. However, there are no clear studies on its significance in nutritional practice or NB measurement.

Metabolic acidosis – In metabolic acidosis, the kidneys secrete more ammonia into the renal tubules to bind hydrogen ions and increase hydrogen excretion. Consequently, the ammonia excretion can increase 5 to 10-fold from the baseline of 5-10% of total urine nitrogen.21 The NB equation therefore has additional losses that are not routinely measured. This process can be reversed by correcting the underlying acidosis.

Extracorporeal membrane oxygenation (ECMO)
For patients receiving ECMO for circulatory support, there is a theoretic concern of protein sequestration in the ECMO circuit, thus affecting the calculation of NB and underestimating protein losses. Estensen, et al. conducted an ex vivo study on macro- and micronutrient disposition in ECMO models and concluded that there was no significant difference in protein concentration over 24 hours on ECMO versus in regular circuits.9 This indicates that the protein loss via ECMO is minimal. However, another ex vivo study found that among the medications of similar lipophilicity, there was significantly lower concentration of protein-bound medications after 24 hours of ECMO circulation, inferring protein loss via sequestration in the ECMO circuit.39 Pelekhaty, et al. studied measured NB in two cohorts of patients on venovenous-ECMO (VV-ECMO) and found that both non-obese and obese patients on VV-ECMO had elevated urine nitrogen excretion and negative NB despite nutrition and protein supplementation based on 2016 ASPEN guidelines. This indicated that patients on VV-ECMO may have high levels of catabolism and require more protein supplementation than currently recommended.40,41 Currently, there is no proposed adjustment of NB calculation in the critical care and nutrition society guidelines.42,43 However, based on the studies, one may consider actively monitoring the NB in this population and supplement more than 2 g protein/kg per day from the standard recommendations.

Conclusions

Nitrogen balance has been widely used for decades to provide individualized nutrition support in highly dynamic patients with multiple acute and chronic medical conditions. This review highlights the various clinical circumstances that one may consider when applying the NB equations in acutely ill patients. While we acknowledge the inherent flaws and inaccuracy of NB calculation, this method still holds significant value for patients in complex metabolic states. 

References

References

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