Abstract
Context: The impact of mechanical ventilation on energy expenditure after spinal cord injury (SCI) is sparse. The objective of this case-series is to measure 15-minutes resting metabolic rate (RMR) to determine 24-hours measured-RMR (m-RMR) using QUARK indirect calorimeter (IC) and; compare the m-RMR with estimated RMR (e-RMR) using four commonly used predictive equations (Harris-Benedict, Mifflin St-Jeor, Henry and Schofield).
Findings: We measured the RMR of four patients with SCI (one male and three female; mean age: 58.3 years) all with complete tetraplegia (ISNCSCI A) twice in a one-week interval using an IC with two sampling flow settings during a six month period. The median (IQ) of all m-RMRs was 1094 (340.2) kcal/day. The median m-RMR was 40.1% lower than the median calculated with four different e-RMRs using predictive equations. All four predictive equations overestimated RMR in SCI patients requiring mechanical ventilation by 4.1–61.1% (Harris-Benedict: 28.8–60.6%; Mifflin St-Jeor: 6.9–61.1%; Henry: 4.1–58.9% and; Schofield: 6–54.6%).
Conclusion/clinical relevance: There is a high variability of e-RMR and m-RMR in patients with SCI who are dependent on mechanical ventilation. The use of predictive equations may lead to over-estimation of energy requirements. To avoid overfeeding we recommended measuring RMR using IC wherever possible. A further study with a larger sample size is needed due to the small number of subjects in our case-series. Development of a validated RMR equation in the SCI population is warranted
Keywords: Spinal cord injury centers, Resting metabolic rate, Indirect calorimetry
Introduction
Survival after spinal cord injury (SCI) when mechanical ventilatory support is required has greatly improved.1 One element considered as part of this improvement is enteral tube feeding which is recommended when there is evidence of dysphagia; however, limited literature is available to guide the clinician about the optimal energy requirements.2 Predictive equations utilizing the subject’s age, sex, weight and/or height have been proposed to estimate resting metabolic rate (e-RMR).2–5 When used in the SCI population, these predictive equations tend to overestimate measured requirements by 5–32%, especially in patients with tetraplegia, ultimately leading to obesity.6 In mechanically ventilated patients, overfeeding may result in the storage of excessive carbohydrates in fat tissue, leading to increased production of carbon dioxide (CO2) and increased requirement for ventilation.7
The objective of this study was to compare measured RMR (m-RMR) with e-RMR in four SCI patients totally dependent on invasive ventilatory support. Our hypothesis is that the estimated e-RMR using predictive equations2–5 overestimates the energy requirements of SCI patients that require mechanical ventilation.
Methods
The RMR measurements were carried out in a SCI centre in the United Kingdom. All four patients were on continuous invasive pressure support ventilation delivered via cuff inflated non-fenestrated tracheostomy tubes.
After obtaining informed consent, the RMR (m-RMR) was measured in four patients (one male and three female; median age 72) with complete (International Standards for Neurological Classification of Spinal Cord Injury: A8) tetraplegia (C2 to C4 level). m-RMR was measured while the patients were alert and ventilated via tracheostomy tube using ambient air. (FiO2: 21%) No additional oxygen was used during any measurements.
Oxygen consumption (VO2), carbon dioxide (CO2) production (VCO2), respiratory quotient (RQ; RQ = VO2/VCO2), and m-RMR were determined with Quark Indirect Calorimeter (IC) by two clinicians. (SW and PS) The Quark IC (Cosmed, Rome, Italy) is a breath-by-breath system for gas exchange measurements. The machine measures O2 and CO2 from the heat and moisture exchange filter (HME) on a single limb, dry active exhalation valve circuit of the ventilator. The HME is located proximal to the patient’s tracheostomy tube. Ventilation flow is measured by an attached flow sensor which is connected between patient’s ventilator circuit and the Quark IC device. The flow sensor is located between the HME and the active exhalation valve of patient’s ventilator circuit (Elisée 150, Resmed, Didcot, United Kingdom). Before each measurement the Quark IC was calibrated according to manufacturer instructions. As normal room air contains less than 0.03% of CO2, FCO2 can be assumed to be equal to FeCO2.9 The m-RMR was calculated from measured VCO2 and VO2 values using Weir’s equation.10
The m-RMR was assessed during a fasting state where nutritional support was stopped for a minimum of 4 hours prior to data collection. The overall measurement time was 20 minutes for each session. A stable period of five minutes minimum in m-RMR was considered as a valid measurement. The stability was defined as <10% and <5% deviations from the mean RQ and VO2 values, respectively. RMR data were only considered valid when RQ values were between 0.7 and 0.9. The patient’s peripheral blood oxygen saturation was monitored during the RMR measurements with a portable non-invasive pulse oxymeter (Beneview T5, Huntingdon, Cambridgeshire, United Kingdom).
Blood samples for determination of serum albumin, and serum C-reactive protein (CRP) were measured. Elevated CRP >15mg/L and body temperature >37.5°C were considered signs of infection and subject’s m-RMR was excluded.
The RMR was assessed twice within a one week interval with two sampling flow settings during September 2017 to September 2018. The two m-RMR were averaged before being entered into the database. The m-RMR values were compared to the e-RMR values calculated using four different predictive equations includingHarris-Benedict,2 Schofield,3 Mifflin St-Jeor4 and Henry5 equations.
Results
The demographic characteristics, blood biochemistry, clinical, nutritional and energy expenditure data of the patients are summarized in Table 1. All of the patients’ nutritional needs were met by enteral tube feeding. They received a mean calories intake of 1530 kcal/day (19.9 kcal/kg/day) and a mean protein intake of 78.5 g/day (1 g/kg/day) at the time of measurements. The median serum albumin was 30 g/L.
Table 1. Characteristics of the four patients.
| Patient 1 | Patient 2 | Patient 3 | Patient 4 | Median (IQ) | |
|---|---|---|---|---|---|
| Sex | Female | Female | Male | Female | |
| Ethnicity | Caucasian | Caucasian | Asian | Asian | |
| Age (years) | 77 | 74 | 32 | 50 | 72 (34.8) |
| Weight (kg) | 65.8 | 93 | 73.2 | 59.4 | 76.6 (22.1) |
| Height (m) | 1.52 | 1.58 | 1.6 | 1.6 | 1.59 (0.25) |
| Body mass index (kg/m2) | 28.5 | 37.3 | 28.6 | 23.2 | 28.6 (10.5) |
| Smoker | No | No | No | No | – |
| Onset of spinal cord injury (SCI) (days) | 230 | 163 | 368 | 212 | 221 (158.3) |
| Onset of mechanical ventilation (months) | 7.6 | 5.4 | 12 | 7.1 | 7.4 (5.1) |
| Mode of nutrition support | PEG | NG | PEG | PEG | – |
| Serum albumin (g/L) | 30 | 28 | 35 | 30 | 30 (5.3) |
| C-reactive protein (mg/L) | 10 | 11 | 15 | 14 | 12.5 (4.5) |
| Temperature (oC) | 37.1 | 37.3 | 37.3 | 37.2 | 37.3 (0.18) |
| Level of SCI | C2 | C4 | C2 | C3 | – |
| ISNCSCI grade | A | A | A | A | – |
| O2 saturation (%) | 96 | 95 | 95 | 96 | 95.5 (1) |
| Oxygen consumption VO2 (mL/min) | 176 | 139 | 200 | 145 | 160.5 (53.5) |
| Carbon dioxide production VCO2 (mL/min) | 143 | 121 | 154 | 119 | 132 (31.8) |
| Vital capacity (mL) | 0 | 400 | 0 | 0 | – |
| Respiratory quotient RQ | 0.87 | 0.87 | 0.77 | 0.82 | 0.85 (0.09) |
| m-RMR (kcal/day) | 1185 | 973 | 1366 | 1003 | 1094 (340.2) |
| kcal/kg/day | 18 | 10.5 | 18.6 | 16.9 | 17.5 (6.4) |
PEG: Percutaneous endoscopic gastrostomy feeding.
NG: Nasogastric tube feeding.
ISNCSCI: International Standards for Neurological Classification.
m-RMR: measured resting metabolic rate.
kcal – kilocalorie.
The median blood oxygen saturation for all patients was 95.5% (IQ: 1) during all assessments. Median VO2 was 160.5 mL/min (IQ: 53.5), median VCO2 was 133 mL/min (IQ: 31.8) and median RQ was 0.85 (IQ: 0.09). The level of SCI, onset of SCI and values of m-RMR in all four patients are summarized in Table 2. The median m-RMR was 1094 kcal/d (IQ: 340.2), which is equivalent to 14.3 kcal/kg/day. Overall, the m-RMR was 40.1% less than e-RMR.
Table 2. comparison of the values of measured (m-RMR) and estimated (e-RMR) resting metabolic rate in four SCI patients require mechanical ventilation.
| Patient | e-RMR (HB) kcal/day | e-RMR (MS) kcal/day | e-RMR (Henry) kcal/day | e-RMR (Schofield) kcal/day | m-RMR kcal/day |
|---|---|---|---|---|---|
| 1 | 1526 | 1267 | 1234 | 1256 | 1185 |
| 2 | 1491 | 1377.4 | 1508.3 | 1503 | 973 |
| 3 | 1651 | 1578 | 1632 | 1713 | 1366 |
| 4 | 1611 | 1616 | 1594 | 1523 | 1003 |
| Median (IQ) | 1568.5 (141.3) | 1477.7 (311.9) | 1551.2(319.9) | 1513 (347.8) | 1094 (340.2) |
| % difference between e-RMR and m-RMR | 43.3 | 35.1 | 41.8 | 38.3 |
e-RMR: estimate resting metabolic rate.
HB: Harris Benedict equation; MS: Mifflin-St-Jeor equation; Henry: Henry equation; Schofield: Schofield equation.
m-RMR: resting metabolic rate measured by Quark RMR.
kcal: kilocalorie.
SCI: spinal cord injury.
All four predictive equations overestimated RMR by 4.1–61.1% (Harris-Benedict: 28.8–60.6%; Mifflin St-Jeor: 6.9–61.19%; Henry: 4.1–58.9% and; Schofield: 6–54.6%).
Discussion
In this case series, the m-RMR in mechanically ventilated SCI patients is 40.1% (and up to 61.1%) less than the e-RMR calculated using predictive equations designed for the general populations. This is in agreement with the existing published literature.11,12
This study has a number of limitations. First, our sample size of four patients is small and not typical of the general SCI population (75% of our samples were female) but the results are very consistent and the difference compared with e-RMR values is clear. Second, we were not able to account for differences in the duration of SCI, which may influence RMR due to change in body composition after SCI. Indeed, studies have reported muscle mass is correlated to the length of an SCI.2 Finally, due to the nature of clinical case report and availability of clinical resources, it was not possible to ensure overnight fasting of 8 hours. Patients were fasted at least 4 hours to minimize the effect of diet-induced thermogenesis. We did not include SCI-specific RMR equations11,12 developed recently in the present study as we did not have access to dual energy x-ray absorptiometry routinely for our patients nor access to additional anthropometric measurement such as transverse abdominal diameter.
Conclusions
This case-series reports a reduced m-RMR in SCI patients requiring mechanical ventilatory support compared to the estimated need using the predictive equations. To avoid over- and under-feeding, nutritional support should be individualized and based on accurate measurements, preferably by using indirect calorimetry. The development of a validated RMR equation for the ventilator-dependent SCI population is warranted.
Disclaimer statements
Contributors SW – data measurement, data analysis, manuscript preparation; PS – data measurement, manuscript revision; AG – data analysis, manuscript revision; AW – data analysis, manuscript revision; FD – data analysis, manuscript revision; MB – data analysis, manuscript revision; MS – data analysis, manuscript revision.
Funding None.
Conflicts of interest Part of the study data was submitted to the American Spinal Injury Association annual conference in May 2018.
Acknowledgements
All authors contributed to the report. The authors are grateful to all medical and nursing-staff facilitating the RMR measurements and Janine Turner for proof-reading the manuscript. Patient consent was obtained for this information to be published.
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