During Hospitalization, Older Patients at Risk for Malnutrition Consume <0.65 Grams of Protein per Kilogram Body Weight per Day

Abstract Background Malnutrition is prevalent in hospitalized patients. To support muscle maintenance in older and chronically ill patients, a protein intake of 1.2–1.5 g/kg/d has been recommended during hospitalization. We assessed daily protein intake levels and distribution in older patients at risk for malnutrition during hospitalization. Methods In this prospective, observational study, we measured actual food and food supplement consumption in patients (n = 102; age, 68 ± 14 years; hospital stay, 14 [8–28] days) at risk of malnutrition during hospitalization. Food provided by hospital meals, ONS, and snacks and the actual amount of food (not) consumed were weighed and recorded for all patients. Results Hospital meals provided 1.03 [0.77–1.26] protein, whereas actual protein consumption was only 0.65 [0.37–0.93] g/kg/d. Protein intake at breakfast, lunch, and dinner was 10 [6–15], 9 [5–14], and 13 [9–18] g, respectively. The use of ONS (n = 62) resulted in greater energy (1.26 [0.40–1.79] MJ/d, 300 [100–430] kcal/d) and protein intake levels (11 [4–16] g/d), without changing the macronutrient composition of the diet. Conclusion Despite protein provision of ∼1.0 g/kg/d, protein intake remains well below these values (∼0.65 g/kg/d), as 30%–40% of the provided food and supplements is not consumed. Provision of ONS may increase energy and protein intake but does not change the macronutrient composition of the diet. Current nutrition strategies to achieve the recommended daily protein intake in older patients during their hospitalization are not as effective as generally assumed.


Introduction
Hospitalization is accompanied by substantial changes in habitual food intake. Food intake during hospitalization is typically reduced because of restricted timing of food provision, adverse effects of medication, a reduced appetite, and prescribed periods of fasting. [1][2][3] Malnutrition during hospitalization is a critical and highly prevalent problem, as up to 40% of the patients have been reported to be malnourished during their hospital stay. 4,5 Malnutrition is defined as a deficiency in energy, protein, and/or micronutrients 6,7 and is generally accompanied by a more adverse clinical outcome during hospital stay. During hospitalization, malnutrition in patients has been shown to prolong the length of stay (LOS), 4,8,9 accelerate the loss of muscle mass, 10 impair functional outcome, 11 and increase the risk of morbidity and mortality. 8,9,12 Accelerated loss of skeletal muscle mass and strength is, at least partly, attributed to the negative health consequences of malnutrition. Muscle mass loss during hospitalization results in functional decline and the loss of independence in older patients. 13 Muscle atrophy, already observed during a few days of hospitalization, [14][15][16] is accelerated by the associated physical inactivity and/or an insufficient protein intake as a direct consequence of the lower energy intake. The current recommended dietary intake for protein is set at 0.8 g/kg/d for healthy adults of all ages according to the World Health Organization (WHO). 17 Recent European Society for Clinical Nutrition and Metabolism (ESPEN) nutrition guidelines recommend a higher protein intake level of 1.2-1.5 g/kg/d for malnourished patients or patients at risk for malnutrition due to acute or chronic illness, as a means to support muscle mass and strength maintenance. 18,19 Previously, we showed that during short-term hospitalization, protein intake falls well below 0.8 g/kg/d in patients undergoing elective orthopedic surgery. 20 In line with this finding, several other studies have reported that hospitalized patients do not meet these recommended protein intake levels. [21][22][23] So far, most studies have assessed food intake by using estimated dietary intake records or food frequency questionnaires in hospitalized patients, [23][24][25] whereas only a few studies have actually measured the amount of food that was consumed. [20][21][22] A difference of 30%-40% between food provision and food consumption has been reported during hospital stay, resulting in low energy and protein intake levels in older patients. 20,[26][27][28] In current practice, patients at risk for malnutrition are referred to a dietitian during hospitalization. Consequently, various nutrition strategies are applied to increase protein intake. The use of more protein-rich foods in the diet, 29 protein fortification of meals, 21,30 and/or the provision of oral nutritional supplements (ONS) [31][32][33] are being applied to increase protein intake during hospitalization. However, there are currently limited data on actual protein consumption in older patients at risk of malnutrition, their protein intake distribution pattern, and the actual consumption of the prescribed ONS during hospitalization. In the present study, we therefore assessed both food provision and food consumption from self-selected hospital meals and the actual intake of ONS and snacks in 102 older patients at risk of malnutrition during several days of hospital admission. We hypothesized that despite the existing nutrition strategies to increase protein intake, older patients at risk for malnutrition do not achieve current protein intake guidelines during hospitalization.

Study Design
In the current prospective observational study, the nutrition content of hospital meals, snacks, and ONS was assessed, and actual food, snack, and ONS consumption was measured in n = 102 patients during their hospitalization. Three different nursing wards (respiratory n = 36, geriatric n = 32, and general surgery n = 34) were selected to include patients between February 2017 and June 2017. The Malnutrition Universal Screening Tool (MUST) was used to screen patients for malnutrition 34 upon arrival in the nursing ward as a part of standard admission procedures. Patients gave consent to collect their food trays after meal consumption after information concerning the project was given orally. Patients were included if they were screened as malnourished (MUST score 2) or at risk for malnutrition (MUST score 1) or if they were indicated as at risk for malnutrition by a dietitian for various reasons (ie, recent weight loss, having nutrition support at home, or reporting low food intake during hospitalization). Age, gender, body mass index, reason for admission, and LOS were recorded. Patients were excluded if they received exclusive or supplemental parenteral or enteral nutrition or if their hospital stay was expected to be <3 days. There was no additional burden on the patients during hospitalization. Retrospective, blinded patient data and observational food intake data were collected under the Agreement on Medical Treatment Act and the Personal Data Protection Act, according to medical ethical standards. The study was registered at www.trialregister.nl (no. NTR6178).

Provision of Hospital Meals
There were 3 strict time slots every day during which hospital meals were provided: breakfast (∼8:00 AM), lunch (∼12:00 PM), and dinner (∼5:30 PM). Patients were provided with voluntary hot and/or cold drinks, snacks, and ONS 3 times a day in between the main meals (at set time points at 10:00 AM, 2:00 PM, and 7:00 PM). During the provision of all meals, there was mealtime assistance. Patients chose their main meal and portion size (0.5, 1, or 2) the day before. Data were collected for a minimum of 3 days and data collection was stopped after a maximum 7 days (Supplementary Figure 1).

Consumption of Hospital Meals
Researchers collected a description of the patients' ordered meal, which was available on the serving tray. This was done for breakfast, lunch, and dinner. The researchers collected the serving tray, and all leftovers were weighed using a scale (Soehnle, Backnang, Germany) when patients were finished eating. To assess snack and ONS consumption, snack and supplement leftovers were weighed, and the researcher collected wrappers and nursing notes and communicated with food assistants, patients, and family. A researcher was present at the ward during the entire assessment period.

Oral Nutritional Supplements
Of the total group of 102 patients, n = 62 were prescribed with ONS. Energy and/or protein ONS were provided as a cold beverage in between the main meals. To allow assessment of the data based on ONS use, data are presented for the non-ONS group and ONS group. ONS provision varied from 1 supplement per week to 3 supplements per day, which was a result of the prescription by the dietitian and provision by the food assistant. A variety of different flavors and energy and/or protein ONS were available during the assessment period (for a full description of the prescribed ONS, see Supplementary Table 1).

Nutrition Content of Hospital Meals
For all provided and consumed food, total energy (MJ and kcal), protein (g and percentage of energy provided by macronutrient [En%]), carbohydrate (g and En%), and fat (g and En%) were calculated, based upon product specifications provided by the food suppliers and the Dutch Food    content in hospital meals and snacks was not consumed and was discarded (P < .001). Total macronutrient composition of the consumed hospital meals (g and En%) is presented in Table 2.

Protein Provision and Consumption
Protein provision and consumption (g/kg/d) from selfselected hospital meals, snacks, and ONS during hospitalization are presented in Figure 1. Protein provision was

Energy Provision and Consumption Between Groups
Energy provision and consumption from self-selected hospital meals, snacks, and ONS during hospitalization are presented in Figure 2A Figure 2A) and ONS ( Figure 2B)  On average, 37% of the provided energy content was not consumed and was discarded (P < .001). After correction for ONS consumption in the ONS group, there were no differences in total energy intake consumed from meals and snacks between the non-ONS and ONS groups.

Protein Provision and Consumption Between Groups
Protein provision and consumption (g/kg/d) from selfselected hospital meals, snacks, and ONS during hospitalization are presented in Figure 2C and 2D. Main meals
Dietary protein intake strongly correlated with daily energy intake in both the non-ONS group (r = 0.894; P < .001) and ONS group (r = 0.860; P < .001) ( Figure 5). Relative contribution of protein to total energy intake (En% protein) did not differ between groups (P = .422).

Discussion
Despite a protein provision of 1.0 g/kg/d, protein intake was merely 0.65 kg/kg/d in older patients who were deemed at risk for malnutrition during their hospitalization. In total, 37% of the provided food was discarded and 32% of the provided ONS were not consumed. Total energy and protein intake per day were greater in those patients receiving ONS, which did not affect the macronutrient composition of the diet. Median protein intake per main meal ranged from 8 to 13 g protein in all patients.
In the present study, we assessed the consumption of self-selected hospital meals, snacks, and ONS in patients who were classified as at risk for malnutrition during their hospitalization. Daily energy intake was merely 5.0 MJ/d (1200 kcal/d), which is well below patients' calculated resting metabolic rate (5.6 MJ/d/1340 kcal/d). Consequently, patients seemed to remain in a negative energy balance during their entire hospital stay. An energy deficit during hospitalization accelerates the loss of skeletal muscle mass and strength. 37 Muscle atrophy typically observed during hospitalization 14,15 has been attributed to the lack of sufficient protein consumed as a direct consequence of a decline in food intake. Current guidelines suggest a protein intake of 1.2-1.5 g/kg/d to support muscle mass maintenance in malnourished patients or patients at risk for malnutrition due to acute or chronic illness. 18,19 In the present study, we show that protein consumption during long-term hospitalization does not even nearly reach the suggested protein intake guidelines. In fact, <4% of the patients consumed ≥1.2 g/kg/d protein. Merely 35% of the patients consumed an amount of protein that was equal to or more than the required 0.8 g/kg/d that is prescribed by WHO for healthy adults (Figure 1).
The amount of protein that was provided via the hospital diet was 1.0 g/kg/d. Even if patients would have fully consumed all meals and ONS that were provided, the ESPEN guidelines on daily protein intake would not have been reached in 72% of the patients. With 30%-40% of the provided food and supplements being discarded, daily protein intake did not even reach WHO guidelines on recommended protein intake. In our hospital, current practices to increase protein intake in these patients include the provision of energy and/or protein-rich snacks in between main meals, counseling to motivate patients to choose protein-rich products, and/or the prescription of ONS. Clearly though, these existing strategies are not effective enough to reach a protein intake at the level of WHO, let alone the ESPEN guidelines on protein intake for patients. Moreover, during hospitalization, patients are less physically active and food intake is typically reduced. To maintain protein intake at habitual intake levels under conditions of a reduced energy intake likely requires the installment of a more protein-dense diet.
One of the often applied strategies to increase protein intake is to provide ONS. The current study was an observational study. We assessed how many ONS a patient received and/or consumed during their hospital stay. We noticed that even when the dietitian prescribed multiple supplements per week, supplements were often not provided or not consumed by the patients. This resulted with some patients consuming only 1 supplement per week, which would not likely have any impact. Previous work showed higher energy and protein intake in patients being prescribed with ONS, providing up to 8-30 g protein extra per day. 31,38,39 Our data extend these findings by showing that even though ∼30% of the ONS were discarded, they still seemed effective in increasing energy and protein intake when compared with those patients not receiving ONS. However, providing patients with ONS did not change the protein density of the hospital diet ( Figure 5). Though ONS provision did increase absolute daily energy and protein intake, the increase in protein intake would be greater if products with greater protein content were used. Using more proteindense ONS may represent an effective strategy to allow the diet to become more protein dense, with relatively more protein being consumed at the same or even a lower energy intake level ( Figure 5). This is especially required to allow patients to maintain their habitual protein intake level, which is necessary to attenuate muscle mass loss during hospitalization. As there are numerous types of ONS with varying protein contents for different patient populations, dietitians should make an informed decision on the optimal prescription of the right product(s) and matching diet for each individual patient.
Previous research has shown that to increase postprandial muscle protein synthesis rates, ingestion of at least 20 g of a high-quality protein is needed. [40][41][42][43][44] Our data clearly show that the amount of protein consumed at breakfast (10 [6-15] g), lunch (9 [5][6][7][8][9][10][11][12][13][14] g), and dinner (13 [9][10][11][12][13][14][15][16][17][18] g) remains well below the proposed 20 g (Figure 3). As this is in line with previous work showing inadequate protein intake with breakfast and lunch, it is essential to increase the protein content of each meal. 20,[45][46][47] Apart from using protein-dense ONS as described above, providing more protein-dense products or fortifying main meals would allow patients to consume more protein per meal. Previous studies have shown that providing protein-fortified foods (such as bread, yogurt, cake, fruit juice, and soup) or using more proteindense foods (such as dairy, eggs, fish, meat) can be effective in increasing both absolute as well as relative protein intake during hospitalization. 21,29,30 Another potential strategy to increase total daily protein intake could be by creating an additional meal moment to consume a protein-rich snack or supplement. The ingestion of a protein-rich snack before sleep could serve as such an additional meal moment to increase protein intake. Our laboratory has recently shown that protein ingestion prior to sleep increases overnight muscle protein synthesis rates in older individuals. 48,49 Whether these nutrition intervention strategies are effective to increase daily protein and/or energy intake during hospitalization remains to be assessed.
In conclusion, energy and protein intake levels are well below suggested guidelines in hospitalized patients at risk for malnutrition. As 30%-40% of the provided food and supplements are not consumed, actual protein consumption remains well below the minimal requirements of 0.8 g/kg/d and far below recommended intake levels of 1.2-1.5 g/kg/d. Although the provision of ONS increases habitual energy and protein intake, it does not affect the macronutrient composition of the diet. Current nutrition strategies to achieve the recommended daily protein intake in older patients during their hospitalization are not as effective as generally assumed and should be redesigned.