1. Introduction
raumatic Brain Injury (TBI) caused by road traffic accidents is prevalent in Guilan, a province in northern Iran [1]. Injuries with a varying severity in TBI patients admitted to Poursina Hospital, the biggest trauma center in Guilan, have been reported. Surgical intervention may be required in some cases [2]. However, the majority of TBI victims with moderate injury and all severe TBI patients, having a low level of consciousness, are currently managed in the intensive care unit (ICU) [3, 4]. Enteral Nutrition (EN) and parenteral nutrition (PN) are pivotal in the management of TBI in ICU because patients with such damages are unable to eat sufficiently [5]. 
Under these conditions, the Resting Energy Expenditure (REE) increases up to 40% [6]. Failure to provide adequate amounts of energy during the first 4 days after ICU admission may lead to malnutrition [7]. Significant weight loss was reported in 68% of TBI patients 6 months after the damage, most likely because of reduced energy intake [8]. An imbalanced nutritional status leading to malnutrition was described in majority of critically ill patients during their stay in ICU [9]. Increased morbidity and mortality can be attributed to the malnutrition in these patients that makes nutritional support a vital element of their care [10].
The multidisciplinary team approach in ICU has been demonstrated to improve cost-effectiveness and patients’ outcomes. As a member of a multidisciplinary team, dietitians are educators, researchers, and translators of evidence-based guidelines into clinical practice. Dietitians in ICUs are qualified to assess patients’ nutritional needs, tailor the nutritional care plan to the disease condition and patients’ state, and recommend the best specialized enteral products to be used to achieve optimal blood glucose control. They also can provide an essential resource related to the route and timing of nutritional support and the prevention of possible complications leading to reduced energy intake, including imbalanced fluid and electrolyte, aspiration and diarrhea. 
Dietitians can help to train students in a teaching hospital setting and finally conduct research design and analyze the data to improve the quality of care of ICU patients [10]. Although the role of ICU dietitians has evolved in past years, many ICUs in Iran still lack the dietitians with expertise and practice. Moreover, physicians often do not follow dietitians’ recommendations, unless they directly contact physicians to implement the suggested treatment plan [11]. Findings in more than 150 ICUs around the world demonstrate that healthcare centers with the presence of dietitians have the best performance and higher ranking in critical care nutrition practice [12]. Incorporating the dietitians specialized in nutritional support in ICU improved energy and protein intake leading to better outcomes [13] and reduced costs [14].
The objective of this study was to investigate the impact of dietitians’ involvement in nutritional outcomes, including the timing of initial enteral nutrition, the average and the percentage of target energy and protein intake on day 4 among TBI patients admitted to Neuro-ICU. Moreover, the clinical outcomes, including the duration of mechanical ventilation and ICU length of stay (ILOS), were evaluated in cases as secondary endpoints.
2. Methods and Materials/Patients
The patients with TBI admitted to Neuro-ICU of Poursina Hospital for three years, were reviewed retrospectively in this study. Forty-eight patients were selected into the study if they were eligible. Inclusion criteria were defined as follows: Glasgow Coma Scale (GCS) score between 6 and 12, Acute Physiology And Chronic Health Evaluation II (APACHE II) score higher than 11 [15], and hospitalization in the Neuro-ICU for more than 48 h. Exclusion criteria included being female, ages younger than 18 and older than 60, having spinal cord injury, having metabolic disorders such as diabetes, thyroid and chronic kidney diseases, and absolute contraindications for enteral feeding, e.g. paralytic ileus, intestinal obstruction, short bowel syndrome, and active gastrointestinal (GI) bleeding. 
Subjects intravenously nourished with amino acids, albumin or fat emulsion during the 4 days after initiation of enteral feeding were also excluded from the study. All patients admitted to the ICU are routinely subject to ICU team collaboration. The ICU team consisted of nurses, pharmacists, and physicians. A research dietitian who conducted some research assessing the nutritional status of patients and microbial quality of the formula [16] joined the ICU team as a dietitian-nutritionist, and dietitian recommendations were received by those patients admitted to the hospital. Patients admitted to ICU before this time were classified as the control group. The study protocol was performed following the guidelines of the Medical Ethics Committee of Guilan University of Medical Sciences, Rasht, Iran, after obtaining written consent from a family member when the patient was not conscious.
Dietitian assessment and interventions
The assessment of nutritional status and the evaluation of the nutritional and microbial quality of enteral nutrition solutions were conducted before starting some interventions [16]. The interventions were designed by expert dietitians in the ICU team for advanced nutritional assessment and counseling, while there were no guidelines or written goals for formula intake in patients receiving enteral tube feeding in the Neuro-ICU. The patients’ nutrition information was collected both on and after admission on a daily basis and identified in shift change time every morning by the dietitian to give some information from nutrition’s point of view, such as the nutritional status, nutritional requirement, and recommendation for taking proper fluid, nutrients, and regulating proper timing to initiate or continue enteral feeding. Moreover, the dietitian altered the enteral solution components to increase energy density. 
Glutamine powder, as the source of nutrient for enterocytes [17], was added to the enteral solutions. Before dietitian’s involvement in the ICU team, feeding formula consisted of a mixture of natural foods with vitamins and Ensure® Nutrition Powder (Abbott Nutrition, Columbus, Ohio, USA) containing 645 kcal/L (35 g protein/L). By adding more proportion of Ensure® Nutrition Powder and glutamine (10 g/L), the dietitian increased the energy and protein density of the enteral formulato 990 kcal/L (60 g protein/L). The alterations were designed to achieve the ultimate goals of daily protein and energy requirements estimated from 1.5-2 g/kg [5] and from 25-30 kcal/Kg [18], respectively, according to the recommendations. During the study, all patients received intravenous dextrose water, if it was required to calculate and include their energy contents.
Data collection
Basic patient characteristics, including age and weight, as well as GCS and APACHE II scores within 24 h after admission and timing of initial enteral feeding, were recorded. The volume of formula delivered to the cases during 4 days was determined to calculate the daily energy and protein intake. Administration of high-dose tube feeding was defined as ≥60% of target energy needs [19]. Additionally, clinical parameters including ILOS and the duration of mechanical ventilation were registered for all patients.
Statistical analysis
All statistical analyses were performed using Statistical Package for the Social Sciences (SPSS) software v. 22. Independent t-test and Chi-Square test were used to compare quantitative and nominal qualitative variables, respectively. A P-value less than 0.05 was considered statistically significant. Data were expressed as Mean±SD.

3. Results
Basic characteristics
The baseline and clinical characteristics of the 48 patients enrolled in the study are summarised in Table 1. There were no significant differences in age, weight and APACHEII and GCS scores among the study participants. 
Nutritional outcomes
The patients’ nutritional outcomes of enteral nutrition provided for both groups are shown in Table 2. Patients under the dietitian recommendations had significantly lower timing of initial enteral nutrition compared to the other cases (67 vs. 93 h, P=0.02). There was a statistically significant difference in average energy intake on day 4 between the control and dietitian intervention groups (880 vs. 1280 kcal, P≤0.001). In agreement with our findings, the percentage of target energy intake on day 4 was found to be significantly higher among patients under the dietitian interventions, compared with the controls (53.61 vs. 31.60%, P≤0.001). 

As shown in Table 2, the difference between the two groups in protein intake on day 4 was considered to be statistically significant (37.10 vs. 69.50g, P≤0.001). Furthermore, the percentage of target protein intake on day 4 appeared to be significantly lower in patients in the control group than in those receiving interventions (34.57 vs. 64.99%, P≤0.001). The average volume of formula delivered to patients on day 4 was not statistically different between the two groups of cases (1368 vs. 1294 mL, P=0.33). In this study, 8% and 37% of subjects in the control groups and interventional groups received more than 60% of their energy requirements, respectively (κ2=5.77, P=0.01). No death was observed between the groups of patients during the present study.
Clinical outcomes
The clinical outcomes of both groups are shown in Table 2. There was no statistically significant difference in the duration of mechanical ventilation between the groups (12.50 vs. 11.16 days, P=0.59). Although patients under the dietitian recommendations had lower ILOS compared to the controls (14.20 vs. 16.16 days), this difference was not significant. Additionally, after removing the effects of age, gender, GCS, and APACHE II scores, there was no statistically significant difference in duration of mechanical ventilation and ILOS between the two groups of cases. 
4. Discussion
This study investigated the influences of dietitian’s involvement in the ICU team in the nutritional and clinical outcomes among head injury cases in the Neuro-ICU. Dietitian involvement in the ICU setting increased energy and protein intake on day 4, reduced the timing of initial feeding and potentially improved clinical outcomes in TBI patients. Overall, results indicated the importance of a dietitian as a member of the ICU team.
Nutritional outcomes
In this study, it has been shown that patients in the dietitian group had significantly lower timing of initial enteral nutrition compared to the other subjects in the control group. Nutrition is the fundamental of critical care support among TBI patients. Brain Trauma Foundation (BTF) recommends initiation of tube feeding no later than 72 h after trauma in TBI cases [20]. This provides sufficient time to assess risks including hemodynamic instability, large-volume fluid resuscitation or bowel distension [21]. Previous studies have demonstrated the beneficial effects of the presence of clinical nutritionists in the ICU teams in terms of the average time to start enteral nutrition [22]. Therefore, dietitian recommendations in ICU lead to decrease in the feeding time, following the BTF.
The average and the percentage of target energy or protein intake on day 4 have been shown to be significantly lower in controls than those of the dietitian group. These results confirm the preceding researches that the dietitian recommendations lead to higher energy intake [23], support the individual nutritional requirements and case care [12, 24-26]. Higher energy and protein intake in patients receiving dietitian recommendations on day 4 compared to those in controls seems to be mostly related to the enteral formula with high energy and protein as no significant changes were observed in the average volume of formula delivered to patients on day 4 between two groups of cases. The beneficial impacts of high-calorie and protein-dense formulas on a daily intake of tube-fed patients have been demonstrated in another research [27]. 
Generally, there are several interruptions in ICUs, including fasting for specific clinical procedures and tube feeding intolerance, which make delivery of prescribed formulas difficult [22, 28]. TBI patients have an intolerance to enteral feeding in the first 2 weeks after admission for a variety of reasons [5] including reduced GI mobility and delayed gastric emptying that can result in elevated gastric residual volume and gastro-oesophageal reflux disease [29]. To increase the delivery of enteral nutrition, barriers such as intolerance to tube feeding could be controlled using a standardized protocol, including measurement of gastric retention [30-32]. 
Although there are more than 40 clinical guidelines for TBI identified at the National Guideline Clearing house online database, they mostly concentrate on emergency department treatment. There are only few guidelines to address nutritional concerns related to TBI [33] 'publisher': National Academies Press (US. In addition, lack of sufficient nutritional medicine courses [34] might lead to the inappropriate prescription of enteral formulas by physicians, which is one of the most common reasons for underfeeding in critically ill patients [35].
Clinical outcomes
In the present study, there was no statistically significant difference in the duration of mechanical ventilation and ILOS between two groups of cases. Dietitian recommendations gave rise to a significant decrease in ILOS within the first 3 days [10, 36], but the mechanical ventilation did not reduce [37]. Likewise, concordant with our results, Minard et al., (2000) reported no significant difference in ICU stay between early and late tube-fed patients [38]. 
A number of studies have shown that enteral nutrition with an enhanced immune formula [39], or tube feeding via the jejunum [40] or both [41], significantly reduces ILOS in a timely manner (within 18-36 h after trauma). Although decreased significantly in the dietitian group, the average initial time for enteral nutrition is defined as late feeding according to the American Society for Parenteral and Enteral Nutrition (ASPEN) guidelines that evaluate the feeding launched over 48 h after ICU admission as late feeding [14]. 
In agreement with our findings, some researches have demonstrated no impact of early enteral nutrition (in the first 6–24 h) on ILOS or duration of mechanical ventilation [42, 43]. The discrepancy between these findings might be explained by differences in the populations, severity of the trauma, and routes and times of administration.
Some limitations should be regarded when interpreting the findings of the present study. First, the sample size limits the study’s power to analyze the measured outcomes. Second, we were not completely able to account for the role of confounding factors, including cerebral edema, intracranial pressure, and systemic injuries. Another limitation of our work was that we could not include female population in this study. Finally, intolerance to tube feeding in patients could not be recorded with detailed information. 
Randomized Controlled Trials (RCTs) with mixed ICU patients which include both males and females are required to investigate the role of dietitian recommendations on the nutritional and clinical outcomes among TBI patients. Enteral feeding protocols are suggested to be implemented in intensive care units of Iran. We also recommend to conduct the present study with larger sample size and longer follow-up time.
5. Conclusion
This study indicated the importance of a dietitian as a member of the ICU team. Dietitian recommendations in the ICU setting raised energy and protein intake and reduced the timing of initial feeding in TBI patients. However, these enhanced results were still not satisfactory for clinical outcomes. Based on the findings of this project, it seems that the daily attendance of dietitians during a multidisciplinary shift change in ICU may be required to assess the nutritional needs of patients, particularly in the first week of admission.
Ethical Considerations
Compliance with ethical guidelines
Written informed consent was obtained from all patients or from their family members when the patient was not conscious.
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Authors contributions
Conceptualization and methodology: Fatemeh Ramezani Kapourchali, Ali Malekshahi Moghadam, Anoush Dehnadi Moghadam, Shahrokh Yousefzadeh-Chabok, Fatemeh Toorang; Data collection: Fatemeh Ramezani Kapourchali, Ali Malekshahi Moghadam, Fatemeh Toorang; Data Analysis: Fatemeh Ramezani Kapourchali; Drafting the article: Fatemeh Ramezani Kapourchali; Critically revising the article: Sara Ramezani, Shahrokh Yousefzadeh-Chabok; Reviewing the submitted version of manuscript and Approving the final version of the manuscript: All authors.
Conflict of interest
The authors declared no conflict of interest.


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