Next Article in Journal
Pilot Testing of an Intensive Cooking Course for New Zealand Adolescents: The Create-Our-Own Kai Study
Previous Article in Journal
The Vitamin D–Folate Hypothesis as an Evolutionary Model for Skin Pigmentation: An Update and Integration of Current Ideas
Previous Article in Special Issue
Protein Intake and Distribution in Relation to Physical Functioning and Quality of Life in Community-Dwelling Elderly People: Acknowledging the Role of Physical Activity
 
 
Review

Nutritional Status and Nutritional Treatment Are Related to Outcomes and Mortality in Older Adults with Hip Fracture

1
Department of Nutrition, Food Science and Physiology, Faculty of Pharmacy and Nutrition, University of Navarra, 31008 Pamplona, Spain
2
Geriatric Department, Complejo Hospitalario de Navarra, 31008 Pamplona, Spain
3
Department of Public Health, Epidemiology and Health Economics, University of Liège, CHUB23, 4000, Liège, Belgium
4
WHO Collaborating Center for Public Health Aspects of Musculoskeletal Health and Aging, Liège, Belgium
5
King Saud University, 11692 Riyadh, Kingdom of Saudi Arabia
6
Dietician Researcher; 08025 Barcelona, Spain, [email protected]
7
Centre for Metabolic Bone Diseases, University of Sheffield Medical School, University of Sheffield, Beech Hill Road, Sheffield S10 2RX, UK
8
Institute for Health and Aging, Catholic University of Australia, Fitzroy VIC 3065 Melbourne, Australia
9
Navarra Institute for Health Research (IdiSNA), 31008, Pamplona, Spain
10
CIBERobn, Physiopathology of Obesity and Nutrition, Instituto de Salud Carlos III, 28029 Madrid, Spain
11
Centre for Nutrition Research, Faculty of Pharmacy and Nutrition, University of Navarra, 31008 Pamplona, Spain
12
IMDEA Food, Research Institute on Food & Health Sciences, 28049 Madrid, Spain.
*
Author to whom correspondence should be addressed.
Nutrients 2018, 10(5), 555; https://doi.org/10.3390/nu10050555
Received: 31 January 2018 / Revised: 9 April 2018 / Accepted: 25 April 2018 / Published: 30 April 2018
(This article belongs to the Special Issue Nutrition and Ageing)

Abstract

Malnutrition is very prevalent in geriatric patients with hip fracture. Nevertheless, its importance is not fully recognized. The objective of this paper is to review the impact of malnutrition and of nutritional treatment upon outcomes and mortality in older people with hip fracture. We searched the PubMed database for studies evaluating nutritional aspects in people aged 70 years and over with hip fracture. The total number of studies included in the review was 44, which analyzed 26,281 subjects (73.5% women, 83.6 ± 7.2 years old). Older people with hip fracture presented an inadequate nutrient intake for their requirements, which caused deterioration in their already compromised nutritional status. The prevalence of malnutrition was approximately 18.7% using the Mini-Nutritional Assessment (MNA) (large or short form) as a diagnostic tool, but the prevalence was greater (45.7%) if different criteria were used (such as Body Mass Index (BMI), weight loss, or albumin concentration). Low scores in anthropometric indices were associated with a higher prevalence of complications during hospitalization and with a worse functional recovery. Despite improvements in the treatment of geriatric patients with hip fracture, mortality was still unacceptably high (30% within 1 year and up to 40% within 3 years). Malnutrition was associated with an increase in mortality. Nutritional intervention was cost effective and was associated with an improvement in nutritional status and a greater functional recovery. To conclude, in older people, the prevention of malnutrition and an early nutritional intervention can improve recovery following a hip fracture.
Keywords: older adults; hip fracture; malnutrition; body mass index; nutritional biomarkers older adults; hip fracture; malnutrition; body mass index; nutritional biomarkers

1. Introduction

Hip fractures represent a significant health risk for older populations because the incidence of fractures increases notably with age [1].
Hip fractures in geriatric patients have a negative impact on functional status and quality of life, and are associated with high mortality [2,3]. Despite the reduction in pre-surgery hospital stay (surgery performed in the first 24 h, or 48 h after admission, is associated with fewer post-operative complications) [4], and improvements in the management of complications, many patients with hip fracture presented functional deterioration [5]. Identifying the risk factors that predict functional loss after a hip fracture could reduce the costs associated with the need for help resulting from loss of autonomy [6] and institutionalization [7], and could also improve the treatment of post-operative complications. The need for help in order to be able to walk within a patient’s home, Parkinson’s disease, smoking, having suffered delirium in the previous month, having a Body Mass Index (BMI) < 22 kg/m2, and age are among the independent risk factors for hip fractures [8]. Poor nutritional status, defined by the Mini Nutritional Assessment (MNA), was associated with a higher risk of fracture at any site [9]. Among risk factors for hip fracture as well as functional loss after the fracture, malnutrition represents an area of great interest, principally because it is a modifiable risk factor. The identification of malnutrition is widely accepted as an appropriate procedure, which may help to give patients better care [10]. This review represents an actualization of the evidence previously published on this topic. The novelty of this review is that we included not only studies with nutritional interventions, but also studies that have assessed the nutritional status in older patients with hip fracture.
The principal objective of this review is to describe how both nutritional status, as revealed by malnutrition biomarkers, influences the clinical evolution and mortality of older people with hip fracture, as well as the impact of nutritional intervention. We therefore structured this paper into four chapters concerning subjects with hip fracture: (1) prevalence of malnutrition and nutritional status aspects (including anthropometry, blood biomarkers, and energy intake), (2) influence upon outcomes and complications, (3) mortality, and (4) effects of nutritional intervention.

2. Material and Methods

2.1. Data Sources and Search Strategy

A search was carried out on the electronic database MEDLINE for papers published from January 1990 until December 2017. The search strategy is detailed in Supplementary data. The search was restricted to articles in English, Spanish, or Italian. The references of the selected articles were manually revised in the search for eligible articles. Whenever there were studies with multiple publications about the same population, the study with the largest sample was selected, as long as it respected our inclusion criteria.

2.2. Inclusion and Exclusion Criteria

We included observational and cohort studies that evaluated the presence of malnutrition (defined by MNA, BMI, albumin concentration, or weight loss), and the influence of malnutrition, as revealed by nutritional biomarkers, on functional recovery, post-operative complications, and mortality in hip fracture patients. We considered as nutritional biomarkers: (1) anthropometric parameters, such as BMI, mid-arm circumference, and triceps skinfold; (2) blood concentrations of total proteins, albumin, and micronutrients such as vitamin D and calcium. We also included controlled clinical trials with nutritional intervention. We defined an intervention as cases where patients received supplements (either orally, by tube, or intravenously) or advice on the characteristics of the diet (by a specialized nurse or dietician). We consider studies (which included only males, only females, or both sexes) carried out in populations with an average age of 70 years or above. Reviews and protocols that did not provide results were excluded.

2.3. Data Extraction

The title and abstract of papers compiled from the search were evaluated by two researchers who carried out data extraction. Doubts and queries were discussed and whenever these could not be solved, the opinion of a third reviewer was requested. Studies were grouped according to their main objective. When necessary we contacted the corresponding author to request data that did not appear in the paper.

2.4. Quality Assessment

The quality of the selected studies was determined with both the National Institutes of Health (NIH) Quality Assessment tool for Observational Cohort and Cross-Sectional Studies and the Quality Assessment of Controlled Intervention Studies [11]. These tools have been designed to evaluate internal validity and bias risk for both types of observational and intervention studies, and each consists of 14 evaluation criteria. The criteria for observational studies are: aims of the study, sources of bias, sampling, participation rate, study power, data collection methods, and confounding. The criteria for intervention studies are: objective of the study, population characteristics, sampling, selection criteria, sample size justification, exposure measured, timeframe, categories of exposure, independent variables, exposure over the time, dependent variables, blinded, drop-out, and confounding. The criteria were rated as either yes, no, or “other” (i.e., CD, cannot determine; NA, not applicable; NR, not reported). The overall assessment of the studies were classified as “good”, “fair”, or “poor”.

3. Results

This review included 44 papers, which totaled 26,281 subjects with a mean age 83.6 ± 7.2 years. The population was mostly female (73.5%). The overall quality of the included studies was rated as fair (Supplementary Tables S1 and S2).

3.1. Prevalence of Malnutrition and Nutritional Status Aspects in Hip Fracture Patients

In all of the studies included, malnutrition was identified by a validated nutritional assessment tool. Nevertheless, the prevalence of malnutrition changed according to diagnostic tool used. The prevalence of malnutrition was 18.7% using the MNA (long or short form), but it was greater if other diagnostic criteria were used (BMI, albumin, or weight loss) (45.7%). The prevalence of malnutrition, of risk of malnutrition, and the diagnostic tool used in each study are presented in Table 1.
In this section we included 10 studies that assessed the nutritional status of older people with hip fracture, with a total of 1575 subjects (88.3% female, mean age 79.6 ± 4 years). The design of the studies, the general characteristics of the populations studied, and the main results are presented in Table 2.
Patients with hip fracture present malnutrition, as demonstrated by the presence of low values of the anthropometric indices. Several studies showed that energy intake in older people is smaller than that required and recommended [12,13,14,15]. They also showed that calorie and protein intake are significantly lower in geriatric patients with hip fracture compared to patients without fracture. Both the reduced intake observed in hip fracture patients and the increase of the energy requirement secondary to the inflammatory state lead to weight loss and a reduction in muscle mass and fat tissue indicators, and this hypercatabolism situation may continue up to 4 months after the fracture [16,17,18].
The importance of a good nutritional status was backed up by studies that observed how higher BMI scores were associated with a lower incidence of hip fractures [19]. An interesting and original study showed that patients with intracapsular fractures presented lower BMI scores than patients with intertrochanteric fractures. Almost half of the subjects with intracapsular fractures presented BMI scores lower than 18 kg/m2, versus only one-fifth of patients with intertrochanteric fractures [20].

3.2. Influence upon Outcomes and Complications

The general characteristics of the studies included in this section can be found in Table 3.
Espaulella et al. showed how after 6 months’ follow-up only slightly over half of the patients subject to follow-up had recovered the functional status they had before the fracture [36]. The MNA was an independent predictor of functional status upon discharge [30], at four and at 12 months [31]. Malnourished patients are more likely to suffer postoperative delirium [32], as well as other post-operative complications such as sepsis [21] and pressure ulcers [37].
Malnutrition is of double importance as it is a risk factor for hip fracture, and in patients with hip fracture it reduces the ability to recover pre-fracture functional capacity. Indeed, malnutrition is a risk factor for fracture, and malnourished older people generally present a worse functional status before the fracture and frequently recover only partially their pre-fracture level of independency in activities of daily living (ADL) following a hip fracture [27]. Conversely, well-nourished older people tend to improve their functional status at discharge after a hip fracture, as revealed by the motor-Functional Independence Measure (FIM) scale [30].
Malnutrition and risk of malnutrition are more prevalent in geriatric patients with a higher comorbidity [38], in addition to being risk factors for complications following hip fracture surgery, such as pressure ulcers [39].
Albumin could be a good blood marker of malnutrition [40]. In this context, Bohl et al. studied a large database (17,651 patients with hip fracture, mean age 84.4 ± 7.2 years) and observed a prevalence of malnutrition of 45.9%, defined as albumin values below 3.5 g/dL prior to surgery [21]. These authors reported that patients with hypoalbuminemia presented a higher prevalence of sepsis (p < 0.001), longer hospital stay (p < 0.001), and higher prevalence of readmission (p = 0.054). The benefits of a good nutritional status were also observed in other studies [18].

3.3. Malnutrition and Mortality in Older People with Hip Fractures

In this section we included those studies whose main objective was to assess the impact of malnutrition, as revealed by nutritional biomarkers, on mortality. In addition, we considered studies where a multivariable analysis was carried out and which included malnutrition biomarkers. A summary of the design, characteristics, and main results of the included studies can be found in Table 4. We included five studies, with a total of 2518 patients (71.8% females), mean age 84.3 ± 7.2 years.
Mortality was inversely associated with pre-surgery albumin levels, and patients with hypoalbuminemia had a relative risk of dying of 1.52 (95% Confidence Interval (CI) 1.37–1.70, p < 0.001) [21]. Regardless of the tool used to diagnose malnutrition, low values of albumin or BMI or low MNA were associated with an increase in mortality. Albumin concentrations of less than 36 g/L were associated with a 4-year mortality nearly six times greater (Odd-Ratio (OR) 5.85, 95% CI 2.3–16.5) [43]. Furthermore, BMI values of less than 22 kg/m2 were associated with an increase of almost seven times the mortality at 1 year, as compared to values higher than 25 kg/m2 (Hazard Ratio (HR) 7.25, 95% CI 1.6–33.7) [22]. Studies such as that of Flodin and collaborators confirm the anterior outcome, observing that subjects with a BMI greater than 26 kg/m2 had a risk almost three times less of dying after 1 year from the fracture (OR 2.6, 95%CI 1.4–5.0) [44].
Cenzer et al. showed that difficulty preparing meals after hip fracture predicts 1-year mortality (and this predictor factor has the same points as congestive heart failure) [45]. Others factors such as age, male sex, congestive heart failure, and not being able to drive complete the risk stratification scale [45].
Mortality increases progressively after a hip fracture, from an in-hospital mortality of 7%, to 11% in the first 6 months after the fracture, up to 30% in the first year and 40% at 3 years. To highlight the importance of this health problem, we summarized total mortality and the follow-up periods of the included studies in Table 5.

3.4. Effects of Nutritional Intervention

In this section we included the studies in which nutritional interventions were carried out. The general characteristics of the populations included, the design, and the main results of the studies included are presented in Table 6.
We included 18 studies, 14 of which were carried out in Europe, one in the USA, one in Australia, and two in Asia, totaling 2248 patients (each study including between 23 and 420 subjects), with an mean age of 81.6 ± 5.4. Five studies were carried out only on women, whereas the rest had mixed samples (66.8% women).
A majority of the studies (n 14) used oral nutritional supplements. One was preceded by supplementation with parenteral nutrition. In one study the supplement was administered via naso-gastric tube, and in one other study only dietary advice was used. One study did not specify the type of intervention. The characteristics of the interventions, calories used, protein content, and duration of the treatment are summarized in Table 7.
Regarding duration, in seven studies intervention was maintained during hospital stay, in four studies the duration was ≤3 months, and in two it was up to 6 months. Two of the studies did not specify the duration of treatment.
The results demonstrated that a good compliance in the use of oral supplements was associated with an increase in total energy, protein, and liquid intake during hospital stay [16,17,23,24,48]. This is important because higher nutritional intake was associated with less postoperative complications. This improvement in intake brought on an increase of IGF-1, a decrease of bone loss 1 year after the fracture [50], lesser prevalence and intensity of delirium, and lower production of oxidative stress-derived products [23]. Nutritional supplementation could also lead to a decrease in the incidence and duration of pressure ulcers, as well as delay their onset. Weight loss was found among subjects who received no supplementation (the control group) [25,51,52], probably due to a loss of muscle mass [53,54]. Two recent studies used supplements enriched with Calcium β-Hydroxy-β-Methylbutyrate (CaHMB); these studies observed an improvement in muscle indices in the intervention groups but no improvement in the control groups [54,55].
A multidisciplinary approach is required in order to reduce malnourishment in subjects admitted to hospital [25]. Having a dietician on the team [49] as well as nurses trained in nutrition [25] was associated with an increase in energy, protein, and supplement intake. In addition, a multidisciplinary approach was shown to counteract increases in the incidence of malnutrition after discharge [25]. Furthermore, nutritional intervention was associated with lower short- and long-term mortality rate as well as with an increase in quality of life (as revealed by the EuroQol-5D scale) [25,49]. Nutritional advice for well-nourished patients was associated with better performance in the ADL, and with a better recovery of the ability to walk [28].

4. Discussion

Malnutrition is a subject under intense discussion in geriatric research [57,58,59], as it is very prevalent in older people with hip fracture, it negatively influences functional recovery after fracture, it increases healthcare spending, and it is associated with high mortality. It appears that nutritional intervention aids the prevention of complications in geriatric patients with hip fracture. This review is an attempt to summarize existing evidence of these aspects. To our knowledge, this is the first review to assess the nutritional status of older people with hip fracture and how it influences complications and mortality.
Despite the variability in the main objective of the included studies, the results are homogeneous in the evidence that subjects with hip fracture have anthropometric indices indicative of malnutrition (Table 2). In addition, there is evidence that subjects with worse nutritional status have more complications (Table 3) and increased mortality (Table 4). There is a lot of variability in the main objective, as well as in the type of nutritional intervention (dietary advice, use of nutritional supplements) and in the amount of calories used in the included studies (Table 7). Despite this variability in the methods used in the studies, overall nutritional intervention has been shown to reduce complications and avoid weight loss in elderly subjects with hip fracture (Table 6).
The prevalence of malnutrition in older patients with hip fracture is higher than in community-dwelling older adults [60,61]. A further problem was associated with an increase in calorie expenditure, secondary to systemic inflammatory response, without a corresponding intake increase, whereby nutritional intake remained smaller than requirements due to factors such as pain, being bedridden, and reduced mobility [25,49].
A reduction in intake is often observed in older people, causing it to be lower than requirements [57]. These changes in intake have a multi-factor origin, among which the most frequent factors are alterations in sensory organs, loss of teeth, lack of a principal caregiver, and, in some cases, the adverse effects of certain drugs [62]. These intake alterations constitute a well-known geriatric syndrome defined as anorexia of ageing [63]. Calorie and/or protein deficits can contribute to the pathophysiology of fractures, especially through two mechanisms: (1) loss of strength and muscle mass (sarcopenia), which increases the risk of falls; and (2) low bone mineral density (osteoporosis), which reduces the resistance of bones to trauma, increasing the risk of fracture [1].
The observed variability in the parameters of nutritional status in hip fracture patients could be due to the lack of a universal consensus as to the best measure to diagnose protein-energy malnutrition. This lack of universality limits our comparison of the various studies, also making it difficult to carry out a consistent malnutrition diagnosis, which, in certain cases, can delay the clinical decision to prescribe nutritional treatment for these patients.
Despite this, the observed trend is uniform and shows that malnourished older people are at a greater risk of fracture and that the prevalence of malnutrition is high in geriatric patients admitted with hip fracture. Patients with intracapsular fracture usually have low BMI, while patients with trochanteric fracture tend to have high BMI [20,64]. Low BMI is associated with protein deficit (type II nutrients, important for maintaining weight) and type I nutrients are important for bone metabolism. In relation to this, “BMI paradox” is valid in the elderly, in which an increase in fat mass and a decrease of muscle mass are observed, and for this reason falsely high values of BMI can mask the presence of sarcopenia [65]. Despite the important limitations of the prognostic meaning of BMI in the elderly, this remains a fundamental index to assess the nutritional status for its simplicity and repeatability, and most validated nutrition assessment tools include BMI. Recent articles have proposed that the normal cut-off considered by the World Health Organization (WHO) (18.5–20.0 kg/m2) should be modified with the values that have been shown to be associated with lower mortality in the elderly (23–29 kg/m2) [66]. It would be advisable to complete the nutritional assessment by evaluating the body composition (with dual-energy absorptiometry (DXA) or with bioimpedance analysis) [67,68]. The problem is different if we consider the concentration of albumin for the diagnosis of malnutrition. The blood concentration of albumin may be a good nutritional index if the inflammatory state is taken into account, considering that its concentration does not depend only on nutritional status [40]. On the other hand, albumin has been shown to be a good prognostic index in hospitalized patients [69].
Screening tools such as the Mini-Nutritional Assessment Short-Form (MNA-SF) were able to diagnose a nutritional problem before it manifested through changes in the biochemical markers of malnutrition (such as albumin or total protein) [70]. Factors such as cognitive impairment and disability in the basic activities of daily living (ADL) were associated with lower scores in the MNA-SF [71]. This tool was also shown to be a predictive factor of destination upon discharge following the fracture [72]. Selective deficiencies such as lack of vitamin D are very prevalent in older people [73].
As well as the known effects of this deficiency on bone metabolism, there is a high concentration of vitamin D receptors in muscle tissue [7]. This situation could explain why the lack of this vitamin (scant diet input, little exposure to the sun, and the ability to make vitamin D within the skin declines with age) is so obviously associated with reduced muscle strength and a worse functional status, involving factors that increase the risk of fall and fracture [42].
The high prevalence of malnutrition in people with dementia could be one of the pathophysiological mechanisms for the high risk of falls and fractures, as well as for their poor functional recovery after a fracture [27,37,42,74]. People with dementia suffered an increase in incidence of hip fracture, as dementia is a risk factor for hip fracture [75]. Strategies for the prevention of hip fractures are very important in people with dementia because they present a higher prevalence of complications, higher risk of institutionalization, and worse functional recovery [3]. Moreover, dementia is an independent predictor for mortality [76].
Malnutrition, which is very prevalent in geriatric patients with hip fracture, is associated with the incidence of complications, with length of hospital stay (and thus increase in cost), and with mortality. Hip fracture continues to be a pathology with high mortality. In spite of the achievement of a reduction in the incidence of hip fractures, mortality has not decreased [77]. Intra-hospital mortality of elderly patients with hip fracture (7.4%) is comparable with mortality of elderly patients with heart failure (8%) [78]. The problem is that hip fracture represents an acute potentially preventable disease, for example by implanting exercise programs that have been shown to reduce the risk of falling [79]. It will be necessary to improve the post-surgical treatment to reduce complications and mortality, which at 3 years is almost twice that of patients with heart failure [80,81].
Patients with hip fracture show a state of hypercatabolism secondary to reduced intake, loss of blood, and inflammation, which leads to a reduction in plasma proteins, which are important mechanisms for the defense of oxidative stress. Cell regeneration determines an increase in the production of free radicals at the site of the fracture. Plasma oxidant markers malondialdehyde (MDA) and advanced oxidation protein products (AOPP) were significantly positively, while albumin and total antioxidant capacity (TAC) are significantly negatively associated with the duration of hospitalization.
Several studies observed lower scores in nutritional indices, such as BMI, in geriatric patients who died following a hip fracture, as compared to those who lived [82]. It may be possible to reduce mortality with adequate nutritional intervention [49]. A difficult question to answer is whether nutritional supplementation is indicated for all patients with hip fracture or only for malnourished patients. Supplementation prevented weight loss in both malnourished and well-nourished patients. This association was directly related to the dose administered [51]. A higher protein intake was associated with a lower risk of post-surgery complications [24], and an adequate energy intake reduced the development of complications and was associated with a shorter duration of hospital stay [17].
Therefore, the results of this review support the indications of the European Society of Parenteral and Enteral Nutrition (ESPEN) guidelines, according to which all older adult patients with hip fracture should receive nutritional supplements during hospitalization [83].

5. Conclusions

The prevalence of malnutrition is very high in older people and increases further in older people with high comorbidities as well as in geriatric patients. Malnutrition is associated to functional alterations and this can be a cause as well as a consequence of fractures.
Malnutrition prevention could be associated with a reduction in the incidence of fractures, and with a better functional recovery following hip fracture. Fall prevention campaigns as well as advice on healthy and active ageing have contributed to the reduction in the incidence of hip fractures. The inclusion in care plans for geriatric patients with hip fracture of both nutritional assessments and the treatment of malnutrition could contribute to a better functional recovery and a reduction of mortality.

Supplementary Materials

The following are available online at https://www.mdpi.com/2072-6643/10/5/555/s1, Table S1: Results of quality assessment of the observational included studies, Table S2: Results of quality assessment of included intervention studies.

Author Contributions

V.M. is the principal investigator, he conceived the study, and he wrote this paper. This research is part of V.M.’s PhD project. S.C. contributed to the paper search, data abstraction, and the redaction of the paper. J.Y.R., J.A.K., O.B., and J.A.M. helped in the critical analysis of the findings, and in both the correction and editing of this manuscript. M.A.Z. is the supervisor of the PhD project; she contributed to the critical analysis of findings and the writing and editing of this paper.

Conflicts of Interest

V.M., S.C., O.B., J.A.K., J.A.M., M.A.Z. declare no conflicts of interest with this article. J.-Y.R.: Consulting fees or paid advisory boards: IBSA-GENEVRIER, MYLAN, RADIUS HEALTH, PIERRE FABRE. Lecture fees when speaking at the invitation of sponsor: IBSA-GENEVRIER, MYLAN, CNIEL, DAIRY RESEARCH COUNCIL (DRC). Grant Support from Industry (all through Institution): IBSA-GENEVRIER, MYLAN, CNIEL, RADIUS HEALTH.

References

  1. Huang, Z.; Himes, J.H.; McGovem, P.G. Nutrition and subsequent fracture risk among a national cohort of white women. Am. J. Epidemiol. 1996, 144, 124–134. [Google Scholar] [CrossRef] [PubMed]
  2. Peeters, C.M.M.; Visser, E.; Van De Ree, C.L.P.; Gosens, T.; Den Oudsten, B.L.; De Vries, J. Quality of life after hip fracture in the elderly: A systematic literature review. Injury 2016, 47, 1369–1382. [Google Scholar] [CrossRef] [PubMed]
  3. Uriz-Otano, F.; Uriz-Otano, J.I.; Malafarina, V. Factors associated with short-term functional recovery in elderly people with a hip fracture. Influence of cognitive impairment. J. Am. Med. Dir. Assoc. 2015, 16, 215–220. [Google Scholar] [CrossRef] [PubMed]
  4. NICE. The National Institute for Health. Hip Fracture in Adults. Available online: https://www.nice.org.uk/guidance/qs16 (accessed on 10 December 2017).
  5. Bellelli, G.; Mazzola, P.; Corsi, M.; Zambon, A.; Corrao, G.; Castoldi, G.; Zatti, G.; Annoni, G. The combined effect of ADL impairment and delay in time from fracture to surgery on 12-month mortality: An observational study in orthogeriatric patients. J. Am. Med. Dir. Assoc. 2012, 13, 664.e9–664.e14. [Google Scholar] [CrossRef] [PubMed]
  6. Leal, J.; Gray, A.M.; Prieto-Alhambra, D.; Arden, N.K.; Cooper, C.; Javaid, M.K.; Judge, A. Impact of hip fracture on hospital care costs: A population-based study. Osteoporos. Int. 2016, 27, 549–558. [Google Scholar] [CrossRef] [PubMed]
  7. Pioli, G.; Lauretani, F.; Pellicciotti, F.; Pignedoli, P.; Bendini, C.; Davoli, M.L.; Martini, E.; Zagatti, A.; Giordano, A.; Nardelli, A.; et al. Modifiable and non-modifiable risk factors affecting walking recovery after hip fracture. Osteoporos. Int. 2016, 27, 2009–2016. [Google Scholar] [CrossRef] [PubMed]
  8. Wiklund, R.; Toots, A.; Conradsson, M.; Olofsson, B.; Holmberg, H.; Rosendahl, E.; Gustafson, Y.; Littbrand, H. Risk factors for hip fracture in very old people: A population-based study. Osteoporos. Int. 2016, 27, 923–931. [Google Scholar] [CrossRef] [PubMed]
  9. Torres, M.J.; Féart, C.; Samieri, C.; Dorigny, B.; Luiking, Y.; Berr, C.; Barberger-Gateau, P.; Letenneur, L. Poor nutritional status is associated with a higher risk of falling and fracture in elderly people living at home in France: The Three-City cohort study. Osteoporos. Int. 2015, 26, 2157–2164. [Google Scholar] [CrossRef] [PubMed]
  10. Hedstrom, M.; Ljungqvist, O.; Cederholm, T. Metabolism and catabolism in hip fracture patients: Nutritional and anabolic intervention—A review. Acta Orthop. 2006, 77, 741–747. [Google Scholar] [CrossRef] [PubMed]
  11. National Heart Lung and Blood Institute. Study Quality Assessment Tools. Available online: https://www.nhlbi.nih.gov/health-topics/study-quality-assessment-tools (accessed on 10 December 2017).
  12. Lumbers, M.; New, S.A.; Gibson, S.; Murphy, M.C. Nutritional status in elderly female hip fracture patients: Comparison with an age-matched home living group attending day centres. Br. J. Nutr. 2001, 85, 733–740. [Google Scholar] [CrossRef] [PubMed]
  13. Durillo, F.T.P.; Durántez, J.T.; Villar, A.B.V.; Vico, A.B.S.; Camarero, M.D.M.C.; Durillo, J.P. Estudio comparativo de la ingesta alimentaria y el estado nutricional en ancianas con y sin fractura de cadera. Atención Primaria 2011, 43, 362–368. [Google Scholar] [CrossRef] [PubMed]
  14. Nematy, M.; Hickson, M.; Brynes, A.E.; Ruxton, C.H.S.; Frost, G.S. Vulnerable patients with a fractured neck of femur: Nutritional status and support in hospital. J. Hum. Nutr. Diet. 2006, 19, 209–218. [Google Scholar] [CrossRef] [PubMed]
  15. Murphy, M.C.; Brooks, C.N.; New, S.A.; Lumbers, M.L. The use of the Mini-Nutritional Assessment (MNA) tool in elderly orthopaedic patients. Eur. J. Clin. Nutr. 2000. [Google Scholar] [CrossRef]
  16. Eneroth, M.; Olsson, U.B.; Thorngren, K.G. Insufficient fluid and energy intake in hospitalised patients with hip fracture. A prospective randomised study of 80 patients. Clin. Nutr. 2005, 24, 297–303. [Google Scholar] [CrossRef] [PubMed]
  17. Anbar, R.; Beloosesky, Y.; Cohen, J.; Madar, Z.; Weiss, A.; Theilla, M.; Koren Hakim, T.; Frishman, S.; Singer, P. Tight Calorie Control in geriatric patients following hip fracture decreases complications: A randomized, controlled study. Clin. Nutr. 2014, 33, 23–28. [Google Scholar] [CrossRef] [PubMed]
  18. Koren-Hakim, T.; Weiss, A.; Hershkovitz, A.; Otzrateni, I.; Grosman, B.; Frishman, S.; Salai, M.; Beloosesky, Y. The relationship between nutritional status of hip fracture operated elderly patients and their functioning, comorbidity and outcome. Clin. Nutr. 2012, 31, 917–921. [Google Scholar] [CrossRef] [PubMed]
  19. Pérez Durillo, F.T.; Ruiz López, M.D.; Bouzas, P.R.; Martín-Lagos, Y.A. Estado nutricional en ancianos con fractura de cadera. Nutr. Hosp. 2010, 25, 676–681. [Google Scholar] [CrossRef] [PubMed]
  20. Maffulli, N.; Dougall, T.W.; Brown, M.T.; Golden, M.H. Nutritional differences in patients with proximal femoral fractures. Age Ageing 1999, 28, 458–462. [Google Scholar] [CrossRef] [PubMed]
  21. Bohl, D.D.; Shen, M.R.; Hannon, C.P.; Fillingham, Y.A.; Darrith, B.; Della Valle, C.J. Serum Albumin Predicts Survival and Postoperative Course Following Surgery for Geriatric Hip Fracture. J. Bone Joint Surg. Am. 2017, 99, 2110–2118. [Google Scholar] [CrossRef] [PubMed]
  22. Schaller, F.; Sidelnikov, E.; Theiler, R.; Egli, A.; Staehelin, H.B.; Dick, W.; Dawson-Hughes, B.; Grob, D.; Platz, A.; Can, U.; et al. Mild to moderate cognitive impairment is a major risk factor for mortality and nursing home admission in the first year after hip fracture. Bone 2012, 51, 347–352. [Google Scholar] [CrossRef] [PubMed]
  23. Fabian, E.; Gerstorfer, I.; Thaler, H.W.; Stundner, H.; Biswas, P.; Elmadfa, I. Nutritional supplementation affects postoperative oxidative stress and duration of hospitalization in patients with hip fracture. Wien. Klin. Wochenschr. 2011, 123, 88–93. [Google Scholar] [CrossRef] [PubMed]
  24. Botella-Carretero, J.I.; Iglesias, B.; Balsa, J.A.; Arrieta, F.; Zamarrón, I.; Vázquez, C. Perioperative oral nutritional supplements in normally or mildly undernourished geriatric patients submitted to surgery for hip fracture: A randomized clinical trial. Clin. Nutr. 2010, 29, 574–579. [Google Scholar] [CrossRef] [PubMed]
  25. Hoekstra, J.C.; Goosen, J.H.; de Wolf, G.S.; Verheyen, C.C. Effectiveness of multidisciplinary nutritional care on nutritional intake, nutritional status and quality of life in patients with hip fractures: A controlled prospective cohort study. Clin. Nutr. 2011, 30, 455–461. [Google Scholar] [CrossRef] [PubMed]
  26. Drevet, S.; Bioteau, C.; Mazière, S.; Couturier, P.; Merloz, P.; Tonetti, J.; Gavazzi, G. Prevalence of protein-energy malnutrition in hospital patients over 75 years of age admitted for hip fracture. Orthop. Traumatol. Surg. Res. 2014, 100, 669–674. [Google Scholar] [CrossRef] [PubMed]
  27. Goisser, S.; Schrader, E.; Singler, K.; Bertsch, T.; Gefeller, O.; Biber, R.; Bail, H.J.; Sieber, C.C.; Volkert, D. Malnutrition According to Mini Nutritional Assessment Is Associated With Severe Functional Impairment in Geriatric Patients Before and up to 6 Months After Hip Fracture. J. Am. Med. Dir. Assoc. 2015, 16, 661–667. [Google Scholar] [CrossRef] [PubMed]
  28. Li, H.J.; Cheng, H.S.; Liang, J.; Wu, C.C.; Shyu, Y.I.L. Functional recovery of older people with hip fracture: Does malnutrition make a difference? J. Adv. Nurs. 2013, 69, 1691–1703. [Google Scholar] [CrossRef] [PubMed]
  29. Wyers, C.E.; Reijven, P.L.M.; Evers, S.M.A.A.; Willems, P.C.; Heyligers, I.C.; Verburg, A.D.; Van Helden, S.; Dagnelie, P.C. Cost-effectiveness of nutritional intervention in elderly subjects after hip fracture. A randomized controlled trial. Osteoporos. Int. 2013, 24, 151–162. [Google Scholar] [CrossRef] [PubMed]
  30. Inoue, T.; Misu, S.; Tanaka, T.; Sakamoto, H.; Iwata, K.; Chuman, Y.; Ono, R. Pre-fracture nutritional status is predictive of functional status at discharge during the acute phase with hip fracture patients: A multicenter prospective cohort study. Clin. Nutr. 2017, 36, 1320–1325. [Google Scholar] [CrossRef] [PubMed]
  31. Helminen, H.; Luukkaala, T.; Saarnio, J.; Nuotio, M. Comparison of the Mini-Nutritional Assessment short and long form and serum albumin as prognostic indicators of hip fracture outcomes. Injury 2017, 48, 903–908. [Google Scholar] [CrossRef] [PubMed]
  32. Mazzola, P.; Ward, L.; Zazzetta, S.; Broggini, V.; Anzuini, A.; Valcarcel, B.; Brathwaite, J.S.; Pasinetti, G.M.; Bellelli, G.; Annoni, G. Association Between Preoperative Malnutrition and Postoperative Delirium After Hip Fracture Surgery in Older Adults. J. Am. Geriatr. Soc. 2017, 65, 1222–1228. [Google Scholar] [CrossRef] [PubMed]
  33. Mansell, P.I.; Rawlings, J.; Allison, S.P.; Bendall, M.J.; Pearson, M.; Bassey, E.J.; Bastow, M. Low anthropometric indices in elderly females with fractured neck of femur. Clin. Nutr. 1990, 9, 190–194. [Google Scholar] [CrossRef]
  34. Villani, A.M.; Miller, M.D.; Cameron, I.D.; Kurrle, S.; Whitehead, C.; Crotty, M. Development and relative validity of a new field instrument for detection of geriatric cachexia: Preliminary analysis in hip fracture patients. J. Cachexia. Sarcopenia Muscle 2013, 4, 209–216. [Google Scholar] [CrossRef] [PubMed]
  35. Bell, J.J.; Bauer, J.D.; Capra, S.; Pulle, R.C. Concurrent and predictive evaluation of malnutrition diagnostic measures in hip fracture inpatients: A diagnostic accuracy study. Eur. J. Clin. Nutr. 2014, 68, 358–362. [Google Scholar] [CrossRef] [PubMed]
  36. Espaulella, J.; Guyer, H.; Diaz-Escriu, F.; Mellado-Navas, J.A.; Castells, M.; Pladevall, M. Nutritional supplementation of elderly hip fracture patients. A randomized, double-blind, placebo-controlled trial. Age Ageing 2000, 29, 425–431. [Google Scholar] [CrossRef] [PubMed]
  37. Baumgarten, M.; Margolis, D.J.; Orwig, D.L.; Shardell, M.D.; Hawkes, W.G.; Langenberg, P.; Palmer, M.H.; Jones, P.S.; McArdle, P.F.; Sterling, R.; et al. Pressure Ulcers in Elderly Patients with Hip Fracture Across the Continuum of Care. J. Am. Geriatr. Soc. 2009, 57, 863–870. [Google Scholar] [CrossRef] [PubMed]
  38. Penrod, J.D.; Litke, A.; Hawkes, W.G.; Magaziner, J.; Koval, K.J.; Doucette, J.T.; Silberzweig, S.B.; Siu, A.L. Heterogeneity in hip fracture patients: Age, functional status, and comorbidity. J. Am. Geriatr. Soc. 2007, 55, 407–413. [Google Scholar] [CrossRef] [PubMed]
  39. Hommel, A.; Bjorkelund, K.B.; Thorngren, K.-G.; Ulander, K. Nutritional status among patients with hip fracture in relation to pressure ulcers. Clin. Nutr. 2007, 26, 589–596. [Google Scholar] [CrossRef] [PubMed]
  40. Cabrerizo, S.; Cuadras, D.; Gomez-Busto, F.; Artaza-Artabe, I.; Marin-Ciancas, F.; Malafarina, V. Serum albumin and health in older people: Review and meta analysis. Maturitas 2015, 81, 17–27. [Google Scholar] [CrossRef] [PubMed]
  41. Formiga, F.; Chivite, D.; Mascaró, J.; Ramón, J.M.; Pujol, R. No correlation between mini-nutritional assessment (short form) scale and clinical outcomes in 73 elderly patients admitted for hip fracture. Aging Clin. Exp. Res. 2005, 17, 343–346. [Google Scholar] [CrossRef] [PubMed]
  42. Perez-Barquero, M.M. Desnutricion como factor pronostico en ancianos con fractura de cadera. Med. Clin. 2007, 128, 721–728. [Google Scholar] [CrossRef]
  43. Miyanishi, K.; Jingushi, S.; Torisu, T. Mortality after hip fracture in Japan: The role of nutritional status. J. Orthop. Surg. 2010, 18, 265–270. [Google Scholar] [CrossRef] [PubMed]
  44. Flodin, L.; Laurin, A.; Lökk, J.; Cederholm, T.; Hedström, M. Increased 1-year survival and discharge to independent living in overweight hip fracture patients. Acta Orthop. 2016, 87, 146–151. [Google Scholar] [CrossRef] [PubMed]
  45. Cenzer, I.S.; Tang, V.; Boscardin, W.J.; Smith, A.K.; Ritchie, C.; Wallhagen, M.I.; Espaldon, R.; Covinsky, K.E. One-Year Mortality After Hip Fracture: Development and Validation of a Prognostic Index. J. Am. Geriatr. Soc. 2016, 64, 1863–1868. [Google Scholar] [CrossRef] [PubMed]
  46. Gumieiro, D.N.; Rafacho, B.P.M.; Gonçalves, A.F.; Tanni, S.E.; Azevedo, P.S.; Sakane, D.T.; Carneiro, C.A.S.; Gaspardo, D.; Zornoff, L.A.M.; Pereira, G.J.C.; et al. Mini Nutritional Assessment predicts gait status and mortality 6 months after hip fracture. Br. J. Nutr. 2013, 109, 1657–1661. [Google Scholar] [CrossRef] [PubMed]
  47. Uriz-Otano, F.; Pla-Vidal, J.; Tiberio-Lopez, G.; Malafarina, V. Factors associated to institutionalization and mortality over three years, in elderly people with a hip fracture-An observational study. Maturitas 2016, 89, 9–15. [Google Scholar] [CrossRef] [PubMed]
  48. Sullivan, D.H.; Nelson, C.L.; Klimberg, V.S.; Bopp, M.M. Nightly enteral nutrition support of elderly hip fracture patients: A pilot study. J. Am. Coll. Nutr. 2004, 23, 683–691. [Google Scholar] [CrossRef] [PubMed]
  49. Duncan, D.G.; Beck, S.J.; Hood, K.; Johansen, A. Using dietetic assistants to improve the outcome of hip fracture: A randomised controlled trial of nutritional support in an acute trauma ward. Age Ageing 2006, 35, 148–153. [Google Scholar] [CrossRef] [PubMed]
  50. Schurch, M.-A. Protein Supplements Increase Serum Insulin-Like Growth Factor-I Levels and Attenuate Proximal Femur Bone Loss in Patients with Recent Hip Fracture. Ann. Intern. Med. 1998, 128, 801. [Google Scholar] [CrossRef] [PubMed]
  51. Bruce, D.; Laurance, I.; McGuiness, M.; Ridley, M.; Goldswain, P. Nutritional supplements after hip fracture: Poor compliance limits effectiveness. Clin. Nutr. 2003, 22, 497–500. [Google Scholar] [CrossRef]
  52. Myint, M.W.; Wu, J.; Wong, E.; Chan, S.P.; To, T.S.; Chau, M.W.; Ting, K.H.; Fung, P.M.; Au, K.S. Clinical benefits of oral nutritional supplementation for elderly hip fracture patients: A single blind randomised controlled trial. Age Ageing 2013, 42, 39–45. [Google Scholar] [CrossRef] [PubMed]
  53. Tidermark, J.; Ponzer, S.; Carlsson, P.; Soderqvist, A.; Brismar, K.; Tengstrand, B.; Cederholm, T. Effects of protein-rich supplementation and nandrolone in lean elderly women with femoral neck fractures. Clin. Nutr. 2004, 23, 587–596. [Google Scholar] [CrossRef] [PubMed]
  54. Malafarina, V.; Uriz-Otano, F.; Malafarina, C.; Martinez, J.A.; Zulet, M.A. Effectiveness of nutritional supplementation on sarcopenia and recovery in hip fracture patients. A multi-centre randomized trial. Maturitas 2017, 101, 42–50. [Google Scholar] [CrossRef] [PubMed]
  55. Ekinci, O.; Yanik, S.; Terzioglu Bebitoglu, B.; Yilmaz Akyuz, E.; Dokuyucu, A.; Erdem, S. Effect of Calcium beta-Hydroxy-beta-Methylbutyrate (CaHMB), Vitamin D, and Protein Supplementation on Postoperative Immobilization in Malnourished Older Adult Patients With Hip Fracture: A Randomized Controlled Study. Nutr. Clin. Pract. 2016. [Google Scholar] [CrossRef] [PubMed]
  56. Houwing, R. A randomised, double-blind assessment of the effect of nutritional supplementation on the prevention of pressure ulcers in hip-fracture patients. Clin. Nutr. 2003, 22, 401–405. [Google Scholar] [CrossRef]
  57. Agarwal, E.; Miller, M.; Yaxley, A.; Isenring, E. Malnutrition in the elderly: A narrative review. Maturitas 2013, 76, 296–302. [Google Scholar] [CrossRef] [PubMed]
  58. Camina-Martin, M.A.; de Mateo-Silleras, B.; Malafarina, V.; Lopez-Mongil, R.; Nino-Martin, V.; Lopez-Trigo, J.A.; Redondo-del-Rio, M.P. Nutritional status assessment in geriatrics: Consensus declaration by the Spanish Society of Geriatrics and Gerontology Nutrition Work Group. Maturitas 2015, 81, 414–419. [Google Scholar] [CrossRef] [PubMed]
  59. Granic, A.; Mendonça, N.; Hill, T.; Jagger, C.; Stevenson, E.; Mathers, J.; Sayer, A. Nutrition in the Very Old. Nutrients 2018, 10, 269. [Google Scholar] [CrossRef] [PubMed]
  60. Watterson, C.; Fraser, A.; Banks, M.; Isenring, E.; Miller, M.; Silvester, C.; Hoevenaars, R.; Bauer, J.; Vivanti, A.; Ferguson, M. Evidence based practice guidelines for the nutritional management of malnutrition in adult patients across the continuum of care. Nutr. Diet. 2009, 66, S1–S34. [Google Scholar] [CrossRef]
  61. Leggo, M.; Banks, M.; Isenring, E.; Stewart, L.; Tweeddale, M. A quality improvement nutrition screening and intervention program available to Home and Community Care eligible clients. Nutr. Diet. 2008, 65, 162–167. [Google Scholar] [CrossRef]
  62. García Lázaro, M.; Montero Pérez-Barquero, M.; Carpintero Benítez, P. Importancia de la malnutrición y otros factores médicos en la evolución de los pacientes con fractura de cadera. An. Med. Interna 2004, 21, 557–563. [Google Scholar] [CrossRef] [PubMed]
  63. Malafarina, V.; Uriz-Otano, F.; Gil-Guerrero, L.; Iniesta, R. The anorexia of ageing: Physiopathology, prevalence, associated comorbidity and mortality. A systematic review. Maturitas 2013, 74, 293–302. [Google Scholar] [CrossRef] [PubMed]
  64. De Laet, C.; Kanis, J.A.; Oden, A.; Johanson, H.; Johnell, O.; Delmas, P.; Eisman, J.A.; Kroger, H.; Fujiwara, S.; Garnero, P.; et al. Body mass index as a predictor of fracture risk: A meta-analysis. Osteoporos. Int. 2005, 16, 1330–1338. [Google Scholar] [CrossRef] [PubMed]
  65. Malafarina, V.; Úriz-Otano, F.; Iniesta, R.; Gil-Guerrero, L. Sarcopenia in the elderly: Diagnosis, physiopathology and treatment. Maturitas 2012, 71. [Google Scholar] [CrossRef] [PubMed]
  66. Ben-Yacov, L.; Ainembabazi, P.; Stark, A.H. Is it time to update body mass index standards in the elderly or embrace measurements of body composition? Eur. J. Clin. Nutr. 2017, 71, 1029–1032. [Google Scholar] [CrossRef] [PubMed]
  67. Rolland, Y.; Gallini, A.; Cristini, C.; Schott, A.; Blain, H.; Beauchet, O.; Cesari, M. Body-composition predictors of mortality in women aged $ 75 y: Data from a large population-based cohort study with a 17-y follow-up 1–4. Am. J. Clin. Nutr. 2014, 1352–1361. [Google Scholar] [CrossRef] [PubMed]
  68. Graf, C.E.; Karsegard, V.L.; Spoerri, A.; Makhlouf, A.M.; Ho, S.; Herrmann, F.R.; Genton, L. Body composition and all-cause mortality in subjects older than 65 y. Am. J. Clin. Nutr. 2015, 101, 760–767. [Google Scholar] [CrossRef] [PubMed]
  69. Iwata, M.; Kuzuya, M.; Kitagawa, Y.; Iguchi, A. Prognostic value of serum albumin combined with serum C-reactive protein levels in older hospitalized patients: Continuing importance of serum albumin. Aging Clin. Exp. Res. 2006, 18, 307–311. [Google Scholar] [CrossRef] [PubMed]
  70. Drescher, T.; Singler, K.; Ulrich, A.; Koller, M.; Keller, U.; Christ-Crain, M.; Kressig, R.W. Comparison of two malnutrition risk screening methods (MNA and NRS 2002) and their association with markers of protein malnutrition in geriatric hospitalized patients. Eur. J. Clin. Nutr. 2010, 64, 887–893. [Google Scholar] [CrossRef] [PubMed]
  71. Brooke, J.; Ojo, O. Enteral nutrition in dementia: A systematic review. Nutrients 2015, 7, 2456–2468. [Google Scholar] [CrossRef] [PubMed]
  72. Portegijs, E.; Buurman, B.M.; Essink-Bot, M.L.; Zwinderman, A.H.; de Rooij, S.E. Failure to Regain Function at 3 months After Acute Hospital Admission Predicts Institutionalization Within 12 Months in Older Patients. J. Am. Med. Dir. Assoc. 2012, 13, 569.e1–569.e7. [Google Scholar] [CrossRef] [PubMed]
  73. Ethgen, O.; Hiligsmann, M.; Burlet, N.; Reginster, J.Y. Cost-effectiveness of personalized supplementation with vitamin D-rich dairy products in the prevention of osteoporotic fractures. Osteoporos. Int. 2016, 27, 301–308. [Google Scholar] [CrossRef] [PubMed]
  74. Rolland, Y.; Pillard, F.; Lauwers-Cances, V.; Busquere, F.; Vellas, B.; Lafont, C. Rehabilitation outcome of elderly patients with hip fracture and cognitive impairment. Disabil. Rehabil. 2004, 26, 425–431. [Google Scholar] [CrossRef] [PubMed]
  75. Huang, S.-W.; Lin, J.-W.; Liou, T.-H.; Lin, H.-W. Cohort study evaluating the risk of hip fracture among patients with dementia in Taiwan. Int. J. Geriatr. Psychiatry 2015, 30, 695–701. [Google Scholar] [CrossRef] [PubMed]
  76. Penrod, J.D.; Litke, A.; Hawkes, W.G.; Magaziner, J.; Doucette, J.T.; Koval, K.J.; Silberzweig, S.B.; Egol, K.A.; Siu, A.L. The association of race, gender, and comorbidity with mortality and function after hip fracture. J. Gerontol. Ser. A Biol. Sci. Med. Sci. 2008, 63, 867–872. [Google Scholar] [CrossRef]
  77. Karampampa, K.; Ahlbom, A.; Michaëlsson, K.; Andersson, T.; Drefahl, S.; Modig, K. Declining incidence trends for hip fractures have not been accompanied by improvements in lifetime risk or post-fracture survival—A nationwide study of the Swedish population 60 years and older. Bone 2015, 78, 55–61. [Google Scholar] [CrossRef] [PubMed]
  78. Rodríguez-Pascual, C.; Vilches-Moraga, A.; Paredes-Galán, E.; Ferrero-Marinez, A.I.; Torrente-Carballido, M.; Rodríguez-Artalejo, F. Comprehensive geriatric assessment and hospital mortality among older adults with decompensated heart failure. Am. Heart J. 2012, 164, 756–762. [Google Scholar] [CrossRef] [PubMed]
  79. Pérez-Ros, P.; Martinez-Arnau, F.M.; Malafarina, V.; Tarazona-Santabalbina, F.J. A one-year proprioceptive exercise programme reduces the incidence of falls in community-dwelling elderly people: A before–after non-randomised intervention study. Maturitas 2016, 94, 155–160. [Google Scholar] [CrossRef] [PubMed]
  80. Bajaj, N.S.; Bhatia, V.; Sanam, K.; Ather, S.; Hashim, T.; Morgan, C.; Fonarow, G.C.; Nanda, N.C.; Prabhu, S.D.; Adamopoulos, C.; et al. Impact of atrial fibrillation and heart failure, independent of each other and in combination, on mortality in community-dwelling older adults. Am. J. Cardiol. 2015, 114, 909–913. [Google Scholar] [CrossRef] [PubMed]
  81. Butrous, H.; Hummel, S.L. Heart Failure in Older Adults. Can. J. Cardiol. 2016, 32, 1140–1147. [Google Scholar] [CrossRef] [PubMed]
  82. Foss, N.B.; Kehlet, H. Mortality analysis in hip fracture patients: Implications for design of future outcome trials. Br. J. Anaesth. 2005, 94, 24–29. [Google Scholar] [CrossRef] [PubMed]
  83. Volkert, D.; Berner, Y.N.; Berry, E.; Cederholm, T.; Bertrand, P.C.; Milne, A.; Palmblad, J.; Schneider, S.; Sobotka, L.; Stanga, Z.; et al. ESPEN guidelines on enteral nutrition: Geriatrics. Clin. Nutr. 2006, 25, 330–360. [Google Scholar] [CrossRef] [PubMed]
Table 1. Prevalence of malnutrition or risk of malnutrition and nutritional screening tool used in the included studies.
Table 1. Prevalence of malnutrition or risk of malnutrition and nutritional screening tool used in the included studies.
ReferenceTotal
n
WN
n
RMN
n
MN
n
Cut-Off for Malnutrition
[21]17,6519549-8102Albumin < 3.5 g/dL
[22]17349-57BMI < 22 kg/m2
[23]23977BMI
[20]9659-37BMI < 18.5 kg/m2
[24]6034-26Weight loss ≥ 5% 1 m, or ≥ 10% 6 m, and/or albumin < 2.7 g/dL
[14]2511113Hospital’s own screening tool §
Total of subjects18,0289711188232
Percentage 53.9% 45.7%
ReferenceTotal
n
WN
n
RMN
n
MN
n
Cut-Off for Malnutrition
[15]4918238MNA
[19]8038357MNA
[25]12789362MNA
[17]5032180MNA
[26]5072914MNA
[27]97443716MNA
[28]16259-103MNA
[29]15287-65MNA
[18]215959525MNA-SF ¥
[30]204559851MNA-SF
[31]59431623642MNA-SF
[32]41515218578MNA-SF
Total of subjects2195992774411
Percentage 45.2%35.3%18.7%
§ This screening tool is based on changes in dietary intake, weight, and other risk factors (pressure ulcers, presence of infection, period of fasting, and the need for help with eating and drinking); Risk of malnutrition cut-off point: Body Mass Index (BMI) between 20 and 22 kg/m2; Mini-Nutritional Assessment (MNA) cut-off points: well-nourished ≥ 24 points, at risk for malnutrition at 17–23.5 points, and malnourished at less than 17 points; ¥ Mini-Nutritional Assessment-Short Form (MNA-SF) cut-off points: well-nourished 12–14 points, at risk of malnutrition 8–11 points, and malnourished 0–7 points; WN: well-nourished; RMN: risk of malnutrition; MN: malnourished.
Table 2. Nutritional status and biomarkers in patients with hip fracture.
Table 2. Nutritional status and biomarkers in patients with hip fracture.
Authors
Origin
Publication Year
Design
Aim
Setting
n (Male/Female)
Age, Mean ± SD (Years)
BMI (kg/m2)
Anthropometry
Measurement of Body Composition
Biomarkers
(1) Exclusion Criteria
(2) Definition of Malnutrition
Main Outcomes
Mansell
UK
1990 [33]
Observational
Comparison of anthropometric measurements of women with HF, with healthy volunteers in the community (C) and patients admitted to geriatric wards (G)
n 663 (0/663)
HF 470
Community 103
Geriatric 90
MAC (cm)
HF 22.8 ± 0.2
Community 28.6 ± 0.27
Geriatric 25.9 ± 0.41
(1) For healthy female: housebound or wheelchairs
(2) NA
Fractured group were older than healthy subjects (p < 0.001).
HF vs. Community: ↓ MAC ↓ AMA ↓↓ TSF ↓↓ AFA (p < 0.001)
Significant MAC reduction per year of age:
−0.20 ± 0.03 cm/year (HF)
−0.15 ± 0.06 cm/year (Community)
Significant TSF reduction per year of age:
−0.16 ± 0.03 mm/year (HF)
HF = 77.3 ± 0.3 years
Community 72.5 ± 0.5 years
Geriatric 79.1 ± 0.8 years
TSF (mm)
HF 13.0 ± 0.6
Community 24.7 ± 0.6
Maffulli
UK
1999 [20]
Observational
Nutritional differences in patients with intertrochanteric (IT) and intracapsular (IC) fractures
n 119 (91/28)
IT 17–54
IC 11–37
80.8 ± 9.1 years
21.5 ± 4.1 kg/m2
Intertrochanteric TSF 11.6 ± 4.5 mm
BSF 6.1 ± 4 mm
MAC 23.5 ± 3.6 cm
Intracapsular TSF 10.6 ± 4 mm
BSF 5.4 ± 2.4 mm
MAC 21.9 ± 3.1cm
(1) Pathologic fracture
(2) BMI < 18 kg/m2
Malnourished → 45% IC vs. 20% IT (p < 0.001)
19% Overweight or obese → 22% IT vs. 2% IC
Complications 15% IC vs. 3% IT (p < 0.05)
BMI: IC < IT (20.1 ± 3.3 vs. 22.5 ± 4.6 kg/m2, p < 0.01)
Murphy
UK
2000 [15]
Observational
Assess the sensitivity and specificity of MNA, and its comparability with other nutritional tools
n 49 (0/49)
79.5 ± 9 years
23.7 ± 4.3 kg/m2
Albumin 36.9 ± 4.7 g/L(1) Cognitive impairment
(2) MNA
Patients had low mean values for body weight, albumin and transferrin
Mean energy intake was below the estimated average requirementMNA < 17:
Sensitivity: 27–57%
Specificity: 66–100%
Lumbers
UK
2001 [12]
Cross-sectional
Intake and nutritional status in
HF compared to day center attendees (DC)
n 125
HF 75 (0/75)
DC 50 (0/50)
80.2 ± 7.9 years
25.5 ± 4.8 kg/m2
HF
MAC 27.1 ± 4.3 cm
TSF 17 ± 2.7 mm
MUAMC 21.4 ± 3.4 cm
Day Centers
MAC 31.3 ± 4.7 cm
TSF 18.9 ± 2.8 mm
MUAMC 23.3 ± 3.8 cm
(1) Mental function test < 7
(2) NA
HF patients vs. day center attendees have:
lower BMI (24.1 ± 4.7 vs. 27.5 ± 4.9 kg/m2, p < 0.001); lower MUAMC, albumin, proteins and energy intake and higher CRP (p < 0.01)
Albumin ↔ RCP (r = −0.45)
Nematy
UK
2006 [14]
Observational
Nutritional status and energy intake
n 25 (7/18)
85.3 ± 1.5 years
21.9 ± 1.0 kg/m2
Albumin 36 ± 2.6 g/L (1) Pathological fracture or elective surgery
(2) Changes in dietary intake, weight loss, pressure sore, infection, and need help for eating
At risk of malnutrition group (n 17) had lower BMI and lower energy intake versus well-nourished group (n 8)
BMI: ARM 19.6 ± 1.1 vs. WN 25 ± 1.5 kg/m2
Energy intake: ARM 3602 ± 320 vs. WN 5044 ± 528 kJ/day
Perez
Spain
2010 [19]
Observational
Prevalence of malnutrition
n 80 (24/56)
80.6 ± 6.3 years
27.1 ± 4.4 kg/m2
TSF 5.5 ± 2.3 mm
BSF 8.1 ± 4.8 mm
MAC 26.8 ± 3.9 mm
CC 31.9 ± 4 cm
(1) NA
(2) MNA
Length of hospital stay: men 15.3 ± 5.8 days; women 14.9 ± 12 days
MNA ↔ BMI r = 0.6
Perez
Spain
2011 [13]
Observational
Nutritional status and intake of HF vs. community dwelling study participants
n 86 (0/86)
HF = 44
Community = 42
MAC (cm)
HF 27.3 ± 3.2
Community 29.1 ± 4.1
(1) No osteoporotic fractures or major trauma
(2) NA
HF has lower BMI, arm and leg circumference than community dwelling (p < 0.05)
Energy intake (kcal): HF 1417; community dwelling 2052 (p < 0.001)
Calcium (mg/dL): HF 827; community dwelling 1265 (p < 0.001)
Vitamin D (μg/dL): HF 1.6; community dwelling: 5.2 (p < 0.001)
Age
HF = 77.9 ± 4.7 years
Community = 76.2 ± 4.6 years
Calf circumference (cm)
HF 32.5 ± 3.6
Community 35.1 ± 4.4
BMI kg/m2
HF = 27.6 ± 3.7
Community = 31.3 ± 4.6
Koren-Hakim
Israel
2012 [18]
Retrospective
Association of MNA-SF with functional status, comorbidity, and mortality (36 months)
n 215 (61/154)
83.5 ± 6.1 years
26.4 ± 4.9 kg/m2
WN28.1 ± 4.0 kg/m2
ARM 25.5 ± 5.1 kg/m2
MN 22.7 ± 3.7 kg/m2
(1) Terminal illnesses and multi-trauma
(2) MNA
MNA ↔ BMI, ADL, cognitive status, readmission, mortality 36 m, CCI and CIRS-G
Independent variables for mortality → Charlson comorbidity index and functional status (ADL)
Villani
Germany
2013 [34]
Cross-sectional
Evaluate new screening tool for detection cachexia
n 71(19/52)
82.2 ± 5.8 years
Men 23.9 ± 2.9 kg/m2
Women 25.9 ± 3.8 kg/m2
M:
MAC (cm) 26.7 ± 3.3
TSF (mm) 11.5 ± 4.8
W:
MAC (cm) 27.1 ± 3.9
TSF (mm) 16.4 ± 5.4
(1) Pathological fracture or malignancy, residing in residential care
(2) NA
Patients with cachexia:
5 new tool
4 (consensus definition)
New tool:
Sensitivity 75% and specificity 97%
Positive predictive value 60%, negative predictive value 99%
Bell
Australia
2014 [35]
Prospective
Concurrent and predictive validity of malnutrition diagnostic measures
n 142 (45/97)
83.5 years
NA(1) NA
(2) MNA-SF < 8
BMI < 18.5 kg/m2
ALB < 35 g/L
ICD10-AM
Geriatrician (subjective clinical assessment)
Malnutrition prevalence with different tools: BMI (12.7%), MNA-SF (27%), ICD10-AM (48.2%), Albumin (53.2%), subjective assessment (55.1%)
MNA-SF ↔ ICD10-AM (r = 0.3) and BMI (r = 0.2)
ICD10-AM ↔ subjective assessment (r = 0.6)
ICD10-AM independent predictor of 4-month mortality (OR 3.6, 95%CI 1.1–11.8)
ADL: activities of daily living; AFA: arm fat area; AMA: arm muscle area; ARM: at risk of malnutrition; BMI: body mass index; BSF: biceps skinfold; CIRS-G: cumulative illness rating scale for geriatrics; CRP: C-reactive protein; HF: hip fracture; ICD10-AM: international classification of disease 10th revision-Australian modification; MAC: mid-arm circumference; MN: malnourished; MNA: Mini Nutritional Assessment; MUAMC: mid-upper arm muscle circumference; TSF: triceps skinfold; WN: well-nourished. . ↓: lower; ↓↓ much lower; ↔: correlation.
Table 3. Association of nutritional status, as revealed by nutritional biomarkers, with outcomes and post-operative complications.
Table 3. Association of nutritional status, as revealed by nutritional biomarkers, with outcomes and post-operative complications.
Authors
Origin
Design
Aim
n (Male/Female)
Age, Mean ± SD (Years)
BMI (kg/m2)
Biomarkers
Exclusion Criteria
MN Definition Tool
Main Outcomes
Formiga
Spain
2005 [41]
Prospective observational
Relationship between nutritional status and complications
n 73 (12/61)
81.5 ± 7.1 years
Cholesterol 4.3 ± 1.1 mmol/L
Albumin 30.6 ± 3.6 g/L
TLC/mm3 1278 ± 463
Pathological or multiple fractures, terminally ill patients, surgery delayed
>48 h or lipid-lowering drug
MNA-SF <11
MNA-SF → 11 ± 0.5
MNA-SF not predict → nosocomial infections and pressure ulcers
Albumin predict → nosocomial infections
↓ TLC years ↓ Albumin predict → pressure ulcers
Barthel index ↔ Charlson comorbidity index r = −0.9 (p < 0.0001)
Length of hospital stay = 16.4 days
Montero
Spain
2007 [42]
Prospective cohort
Relationship
between malnutrition and recovery
n 110 (22/88)
81.4 ± 7.3 years
25(OH)vitD 10.8 ± 5.3 ng/ml
TLC/ mm3 1545 ± 592
Albumin 32.6 ± 3.8 g/L
Prealbumin 15.3 ± 4.7 mg/dL
Cholesterol 160.5 ± 40.8 mg/dL
Transferrin 195.9 ± 47.1 mg/dL
Pathologic or major trauma fractures
Anthropometric and blood biomarkers
38.8% regained pre-fracture functional state
Dementia ↔ ↓ functional recovery
25(OH)vit D <10 ng/ml ↔ ↓ pre-fracture functional state, with bedridden (1 year) and with no functional recovery (p < 0.05)
Factors associated to bedridden (1 year) OR, 95%CI
-
pre-fracture functional status 10.02, 2.83–35.47 p < 0.01
-
Caloric malnutrition 9.57 (2.18–42.84) p < 0.01
-
Protein malnutrition 15.23 (1.36–1.70) p < 0.05
Baumgarten
USA
2009 [37]
Prospective cohort
Identify care settings associated with increased pressure ulcers risk
n 658 (152/506)
83.2 ± 6.6 years
23.8 ± 5.1 kg/m2Fractures occurred during hospital stay
Subjective Global Assessment (SGA)
Pressure ulcers at baseline ↔ ↑ severe illness, ↑ comorbidity, ↓ nutritional status, ↓cognitive status (p < 0.05)
Albumin < 30 g/L: 31.5%
Length of hospital stay 5.6 ± 2.8 (no pressure ulcers) vs. 6.6 ± 3.8 (pressure ulcers) (p < 0.001)
Drevet
France
2014 [26]
Prospective observational
Protein Energy Malnutrition prevalence
n 50 (15/35)
86.1 ± 4.4 years
22.6 ± 4.3 kg/m2Road accident
MNA
Prevalence of PEM was 28% (n 14)
Mean hospital stay: PEM 21.9 ± 16.7 vs. 13.4 ± 6.7 in non-PEM (p = 0.012)
Goisser
Germany
2015 [27]
Observational
Relationship between nutritional status (MNA) and functional and clinical course
n 97 (20/77)
84 ± 5 years
NATerminal state, cancer-related pathologic fractures, cancer with acute radiation or chemotherapy
MNA
Patients at risk for malnutrition and malnourished:
-
Baseline, ↑ comorbidities ↑ Charlson comorbidity index ↑ pressure ulcers ↓ cognitive status (p < 0.05)
-
All times, ↓ ADL score (p < 0.05)
-
68% did not regain pre-fracture ADL
-
18% did not regain pre-fracture mobility level (p = 0.02)
Bohl
USA
2017 [21]
Retrospective
Association between albumin with death, and postoperative complications
n 17,651 (12,595/5056)
84.4 ± 7.2 years
24.6 ± 5.6 kg/m2
Albumin 35 ± 5 g/dL
Preoperative serum albumin concentration not available
Albumin concentration
18.5% had BMI < 20 kg/m2
Patients with hypoalbuminemia had higher rates:
-
of death (RR 1.52. 95%CI 1.37–1.70. p < 0.001)
-
of sepsis (RR 1.92. 95%CI 1.36–2.72. p < 0.001)
-
of longer legnth of hospital stay, 5.7 ± 4.7 vs. 5.0 ± 3.9 days (p < 0.001)
Helminen
Finland
2017 [31]
Prospective
Prognostic significance of MNA and albumin
n 594 (169/425)
84 years
24.9 kg/m2
Albumin 33.5 g/L
Pathological or periprosthetic fractures, institutionalization, prefecture inability to walk
MNA-SF
All nutritional measures were significantly associated with mortality
Being at risk for malnutrition or being malnourished were significantly associated with impaired mobility at 4 months and 1 year
Mazzola
Italy
2017 [32]
Prospective
If nutritional status predict postoperative delirium
n 415 (104/309)
84 ± 6.6 years
NA
Albumin 33 ± 5.4 g/L
Nonoperative approach and preoperative delirium
MNA-SF
Risk to develop postoperative delirium:
-
at risk for malnutrition: OR 2.42, 95%CI 1.29–4.53
-
malnourished: OR 2.98, 95%CI 1.43–6.19
Inoue
Japan
2017 [30]
Prospective
Relationship between nutritional status and functional recovery
204 (39/165)
82.7 ± 9.2 years
20.2 ± 2.5 kg/m2
Albumin 36 ± 9 g/L
Terminal disease, chronic liver disease, pre-fracture ambulation difficulty, no weight-bearing, discontinued postoperative rehabilitation
MNA-SF
Well-nourished had higher motor-FIM score at discharge
Motor-FIM at discharge was significant associated with MNA-SF
ADL: activities of daily living; BMI: body mass index; FIM: functional Independence Measure; HF: hip fracture; MNA: Mini Nutritional Assessment; PEM: protein energy malnutrition; OR: odd-ratio; 95%CI: 95% confidence interval. ↔: correlation.
Table 4. Relationship between nutritional status and mortality.
Table 4. Relationship between nutritional status and mortality.
Authors
Origin
Year
Design
n (Male/Female)
Age, Mean ± SD (Years)
BMI kg/m2 (Mean ± SD)Exclusion CriteriaMain Outcomes
Miyanishi
Japan
2010
Retrospective [43]
n 129 (24/103)
79 years
Survivors 78 ± 11 years
Non-survivors 81 ± 10 years
21 ± 2.9 (Survivors)
18.9 ± 3.5 (Non Survivors)
NANon-survivors have:
↓* BMI, hemoglobin, albumin and ↑* dementia, complications
Mortality predictors (4-year mortality):
Albumin (<36 g/L) OR = 5.85 and BMI (<18.9 kg/m2); OR = 1.16
Schaller
Switzerland
2012
Sub-analysis of RCT [22]
n 173 (36/137)
84.2 ± 6.7 years
NASevere cognitive impairment (MMSE > 15) or deliriumRisk factor for ↑mortality (1-year mortality):
MMSE <25 (HR = 5.77, 95%CI: 1.55–21.55)
Male sex (HR = 3.55, 95%CI: 1.26–97)
BMI <22 vs. >25 (HR = 7.25, 95%CI: 1.61–33.74)
Vitamin D per 1ng/ml (HR = 0.93, 95%CI: 0.87–0.998)
Gumieiro
Brasil
2013
Prospective [46]
n 86 (20/66)
80.2 ± 7.3 years
NAPathological fractureMNA ↔ gait impairment OR = 0.77 (0.66–0.90) p = 0.001
↑ 1 point MNA → ↑* 29% chance of walking
MNA ↔ mortality HR = 0.87 (0.76–0.99) p = 0.04
↑ 1 point MNA → ↓* 15% mortality risk
Flodin
Sweden
2016
Prospective [44]
n 843 (227/616)
82 ± 7 years
22.7 ± 3.8 kg/m2Severe cognitive impairment, admitted from nursing-homes1-year mortality (p = 0.006):
BMI > 26 = 6%
BMI 22–26 = 18%
BMI < 22 = 16%
BMI > 26 indicates a higher likelihood of returning to independent living (OR 2.6, 95%CI 1.4–5.0)
Uriz-Otano
Spain
2016
Prospective [47]
n 430 (97/333)
84.2 ± 7.4 years
NATumor, high impact fracture3-year mortality:
Albumin HR 0.61, 95%CI 0.42–0.90
Predictors of 3-year mortality:
Age, HR 1.04, 95%CI 1.01–1.06
Comorbidity, HR 1.19, 95%CI 1.09–1.30
Complications, HR 1.17, 95%CI 1.05–1.31
MMSE: Mini-Mental State Examinatio; RCT: randomized clinical trial; ↓*: significantly less; ↑*: significantly more.
Table 5. Total mortality during hospital stay, and at various stages after discharge.
Table 5. Total mortality during hospital stay, and at various stages after discharge.
ReferenceIn-Hospital<6 Months1 Year36 Months>36 Monthsn
[18]6% 36.7% 215
[20]6% 119
[21]7.4% 17,651
[22] 27% 173
[27]15% 97
[29] 7.70% 152
[31] 30%26% 594
[35]4.9%14.8% 142
[36]4%21.1% 171
[39] 29.1%42.40% 420
[41]10% 73
[42]6.4%11.8%19.4% 110
[43] 48%129
[45] 27% 857
[46] 12.8% 86
[48]1.7%17.9% 57
[49]11.6%20.6% 302
23,093
Total mortality (%)7.4%20.4%29.3%39.4%48%
Table 6. Nutritional intervention in patients with hip fracture.
Table 6. Nutritional intervention in patients with hip fracture.
Author
Year
Origin
Design
Aim
n (Male/Female)
Age, Mean ± SD (years)
Follow-Up (FU)
BMI kg/m2 (Mean ± SD)
Measurement of Body Composition
Exclusion CriteriaResults
Schürch [50]
1998
Switzerland
RCT
Effects of oral protein supplements on bone metabolism
n 82 (8/74)
IG 41
CG 41
80.7 ± 7.4 years
6 months
24.3 ± 4.0 kg/m2
MAC (cm)
24.1 ± 3.1
Pathologic fracture, fracture caused by severe trauma, history of contralateral hip fracture, severe mental impairment, bone disease, renal failure, and life expectancy < 1 yearIG (at 6m):
↓ rehabilitation stay (42.2 ± 6.6 vs. 53 ± 4.6 days) p = 0.018
↑increase IGF-1 and IgM p < 0.05
50% reduction of proximal femur bone loss (1 year)
Espaulella [36]
2000
Spain
RCT
Nutritional supplement and functional recovery, complications and mortality
n 171 (36/135)
IG 85
CG 86
82.6 ± 6.6 years
Follow-up: 6 months
25.4 ± 5 kg/m2
MAC: 24.6 ± 3.8 cm
Albumin: 35 ± 5.5 g/L
Advanced dementia, intravenous nutrition, pathologic fractures, and accidental fallsPatients with ≥1 complication (6 months):
IG 44 (55%)
CG 57 (70.4%) p = 0.04
IG: ↑ increase albumin (3 months and 6 months)
Bruce [51]
2003
Australia
RCT
Nutritional supplements and prevention of weight loss and improvement of outcomes
n 109 (0/109)
IG 50
CG 59
83.9 ± 7.7 years
Follow-up: 6 months
22.8 ± 2.6 kg/m2
Albumin 38.8 ± 4.1 g/L
BMI < 20 or BMI > 30 kg/m2, residents of nursing homes, diseases that influence nutritional intake, diabetes, and fracture due to a major traumaWeight loss (all patients):
At 4 weeks
31.5% > 5% weight loss
20.7% > 7.5% weight loss
At 8 weeks
27.4% > 5% weight loss
14.6% > 5% weight loss
Fewer weight loss ↔ ↑ number of cane (p = 0.019) and ↑duration of supplementation (p < 0.05)
Houwing [56]
2003
The Netherlands
RCT
Effect of a high-protein supplement on the development of pressure ulcers
n 103 (19/84)
81.0 ± 1.1 years
23.9 ± 0.5 kg/m2Terminal care, metastatic hip fracture, insulin-dependent diabetes, renal disease, hepatic disease, BMI > 40 kg/m2. 55.3% developed pressure ulcers stage I or II.
Incidence of pressure ulcers stage II:
supplement 18%, placebo 28%
57% of patients developed pressure ulcers by the second day
Sullivan [48]
2004
USA
RCT
Efficacy of enteral nutrition to decrease complications and long-term outcomes
n 57 (39/19)
IG 27
CG 30
79 ± 7.6 years
Follow-up: 6 months
22.1 ± 4.4 kg/m2
BSF: 6.4 ± 3.3 mm
Albumin: 33.9 ± 4.5 g/L
Pathological fracture, significant trauma to other organ systems, metastatic cancer, cirrhosis of the liver, and organ failureIG:
↑ intake of total nutrients p = 0.012
At discharge:
↑ Albumin: IG 29 ± 5 vs. CG 25 ± 5 g/L p = 0.002
Tidermark [53]
2004
Sweden
RCT
Effects of nutritional treatment on nutritional and functional status
n 60 (0/60)
82.9 ± 5.4 years
Follow-up: 12 months
20.4 ± 2.3 kg/m2<70 years, BMI > 24 kg/m2, cognitive impairment and institutionalized, dependent to walk, fractures older than 24 h, pathological fractures, rheumatoid arthritis.Lean body mass decreased in the CG and protein groups, but remained the same in the protein plus nandrolone group.
ADL declined only in the CG.
Eneroth [16]
2005
Sweden
RCT
Effects of nutritional supplements on nutritional status and intake.
n 80
IG 40 (7/33)
CG 40 (10/30)
81.4 ± 7.6 years
23.9 ± 3.8 kg/m2Multiple and pathologic fractures, malignant disease, inflammatory joint disease, dementia, depression, acute psychosis, epileptic seizures, insulin-treated diabetes mellitus, heart, kidney, or liver insufficiencyPEM baseline:
CG 33%, IG 38%
Fluid intake:
IG = 1856 ml, CG = 1300ml (p < 0.0001)
Energy intake during days 1–10:
IG = 1296 kcal/day CG = 916 kcal/day (p = 0.003)
Difference between actual and needed energy intake:
IG = −228 kcal/day CG = −783 kcal/day (p = 0.0003)
Duncan [49]
2006
UK
RCT
Effectiveness of dietetic assistants (DAs) to reduce in-hospital and 4 months mortality.
n 302 (0/302)
GT 145
GC 157
83.5 years
Follow-up: 4 months
NAPathologic fractureMortality
In trauma unit IG 4%, CG 10% (p = 0.048)
At 4 months IG 13%, CG 23% (p = 0.036)
-
Energy intake = IG 1105; CG 756 kcal/day (p < 0.001)
-
Supplement intake: IG 409; CG123 kcal/day (p < 0.001)
-
MAC change: IG −0.9; CG −1.3 cm (p = 0.002)
Weight change: IG −0.35; CG −1 kg (p = 0.16)
Hommel [39]
2007
Sweden
Quasi-experimental
Effects of an improved care intervention in relation to nutritional status and pressure ulcers
n 420
IG 210 (70/140)
CG 210 (62/148)
81 ± 10.4 years
24.3 ± 4.4 kg/m2
MAC 27.7 ± 4.4 cm
TSF 14.8 ± 6.8 mm
NALength of hospital stay: IG 11.8 ± 7.4 vs. CG 10.8 ± 5.8 days
Pressure ulcers: IG 10%; CG 20.5% (p = 0.009)
Botella-Carretero [24]
2010
Spain
RCT
Effect of perioperative supplements on nutritional status and postop complications
n 60 (16/44)
IG 30 (6/24)
CG 30 (10/20)
83.6 ± 5.8 years
24.4 ± 3.1 kg/m2
TSF 11.9 ± 4.1 mm
MAC 24.4 ± 3.2 cm
MNA 18.6 ± 3.4
Albumin 33 ± 4g/L
Weight loss > 5% in 1 month or weight loss > 10% in 6 months, albumin < 27 g/L, renal failure, hepatic insufficiency, respiratory failure, and any gastrointestinal condition, any nutritional support in the past 6 monthsCG: decrease and worse recovery of albumin and prealbumin (p = 0.002; p = 0.001)
IG: ↑ energy and protein intake (p = 0.042; p < 0.001)
↑ protein intake → ↓ post-operative complications OR = 0.925 (0.869–0.985) (p = 0.003)
Fabian [23]
2011
Austria
RCT
Effect of nutritional supplement on post-operative oxidative stress and length of hospital stay
n 23 (0/23)
IG 14
CG 9
83.8 ± 7.4 years
Follow-up: 3 weeks
21.2 ± 3.4 kg/m2
Albumin 36.6 ± 3.8 g/L
Renal disease, liver failure, severe congestive heart failure, severe pulmonary disease, and any gastrointestinal condition that might preclude the patient from adequate oral nutritional intakeIG ↑ energy and protein intake (p < 0.05)
Albumin, total protein, and total antioxidant capacity (post-operative):
↓ CG (p < 0.05) ↓ IG
Advance oxidation protein products and malondialdehyde: in CG levels still elevated during time but not in IG
Length of hospital stay: IG 17 ± 4 vs. CG 19 ± 9 days
Albumin ↔ CRP and total antioxidant capacity (p < 0.05)
Length of hospital stay ↔ AOPP and MDA (p < 0.01)
Hoekstra [25]
2011
The Netherlands
Prospective
Effectiveness of a multidisciplinary intervention on nutritional status
n 127 (31/96)
IG 61
CG 66
80.3 ± 8.3 years
26.8 ± 4.5 kg/m2Severe dementia, cancer, pathologic fracture, renal and hepatic dysfunction, pacemaker IG ↑ energy intake protein, vitamin D, zinc, calcium (p < 0.01)
IG lower reduction of EuroQol-5D (p < 0.05)
↓* BMI, BCM, and FM (3 months) (both groups)
Li [28]
2013
Taiwan
Randomized (1 year)
Effects of protein-energy malnutrition on the functional recovery
n 162 (51/111)
IG 80
CG 82
78.2 years
NACognitive impairment, terminally illMalnutrition prevalence: IG 60% vs. CG 67%
MN → ↓ performance of ADL, IADL, and recovery of walking ability (p < 0.05)
IG → ↑ performance of ADL, IADL, and recovery of walking ability (p < 0.01)
Wyers [29]
2013
The Netherlands
RCT
Cost-effectiveness of dietary intervention comprising combined dietetic counseling and ONS
n 152 (108/44)
IG 73
CG 79
78.5 years
NAPathological or periprosthetic fracture, disease of bone metabolism, life expectancy < 1 year, ONS before hospital admission, dementia. The additional cost of the nutritional intervention was only 3% of the total cost
Total cost was not significantly different between both groups
Nutritional intervention was likely to be cost effective for weight as the outcome over 3 months
Myint [52]
2013
Hong Kong
RCT
Clinical, nutritional and rehabilitation effects of an oral nutritional supplementation
n 121 (41/80)
IG 61
CG 60
81.3 ± 6.5 years
Follow-up: 6 months
20.7 ± 2.9 kg/m2
TSF 12.6 ± 5.6 mm
MAC 24.3 ± 3 cm
Albumin 29.3 ± 4.6 g/L
Tube feeding, unstable medical condition, BMI ≥ 25 kg/m2, malignancy, contraindication for high-protein diet, and mentally incapacitatedBMI decrease of 0.25 and 0.003 kg/m2 in the ONS group, and 0.72 and 0.49 kg/m2 at hospital and follow-up (p = 0.012)
Length of hospital stay was shortened by 3.8 days in the ONS group (p = 0.04)
Intake adequate: 67% in the ONS group, 9% in the control group (p < 0.001)
Anbar [17]
2014
Israel
RCT
Optimization of supplementation by measurement of resting energy requirements and the effect on outcomes
n 50 (17/33)
IG 22
CG 28
83.1 ± 6.3 years
24.9 ± 3.9 kg/m2Presented to hospital >48 h after the injury, steroids and/or immunosuppression therapy, oncologic disease, multiple fractures, dementiaONS = 19.6% of total energy
IG:
↑ Energy and protein intake (p = 0.001)
↓ complications (p = 0.012) and infections (p = 0.008)
↓ length of hospital stay (p = 0.061)
In all patients:
Energy balance ↔ complications (r = −0.417; p = 0.003) and with length of hospital stay (r = −0.282; p = 0.049)
Ekinci [55]
2016
Turkey
RCT
Effects of CaHMB on wound healing, mobilization, fat-free mass and muscle strength
n 62 (0/62)
IG 32
CG 30
82.6 ± 7.1 years
22.0 ± 2.4 kg/m2Diabetes, renal and hepatic failure, gastrointestinal intolerance, endocrine pathology, and dementia.Patients who were mobile on day 30:
- IG 81.3% vs. CG 26.7% (p = 0.001)
Muscle strength on day 30 was higher in IG vs. CG (p = 0.026)
Malafarina [54]
2017
Spain
RCT
Effects of ONS on muscle mass and nutritional biomarkers
n 107
IG 55
CG 52
85.4 ± 6.3 years
25.4 ± 4.9 kg/m2
Albumin 3.1 ± 0.4 g/dL
Diabetes, Barthel index <40 prior to the fracture, tumor, pathological or high-impact fracturesBMI and ALM was stable in IG, but decreased in CG.
ONS (p = 0.006), function ambulation categories prior to the fracture (p = 0.007) and Barthel index prior to the fracture (p = 0.007) are protective for loss of ALM
ALM = appendicular lean mass; AOPP: advanced oxidation protein products; BCM: Body Cellular Mass; BMI = body mass index; BSF = biceps skinfold thickness; CG = control group; FM: fatt mass; IADL: instrumental activities o daily living; IGF-1 = insulin-like growth factor; HS = handgrip strength; IG = intervention group; MAC = mid-arm circumference; MNA = Mini Nutritional Assessment; ONS = oral nutritional supplement; RCT = randomized controlled trial; TSF = triceps skin fold thickness; ↓* = significantly less; ↑* = significantly more; ↔ = significant association.
Table 7. Characteristics of the nutritional intervention and composition of the nutritional supplementation used in the included studies.
Table 7. Characteristics of the nutritional intervention and composition of the nutritional supplementation used in the included studies.
Author
Year
Origin
Type of Supplement
Administration Method
kcalNutritional CompositionTreatment Duration
Adherence Rate (%)
Control Group
Schürch [50]
1998
Switzerland
Oral liquid supplement; single oral dose of vit D3 200.000 UI
Ca: 550 mg/day
250 kcal/day 20 g protein, 3.1 g lipid, 35.7 g carbohydrates,
90% milk proteins
5 days a week for 6 months
AR:
IG 73%
CG 80%
Placebo: 54.5 g carbohydrates
Single oral dose of vitamin D 200.000 UI
Calcium: 550 mg/day
Espaulella [36]
2000
Spain
Oral liquid supplement
200 mL
149 kcal20 g protein, 800 mg calcium, 25 IU vitamin D360 days
AR:
IG 94.1%
CG 94.2%
Placebo 200 mL, 155 kcal; mainly carbohydrates
Bruce [51]
2003
Australia
Oral liquid supplement (235 mL/day)352 kcal17.6 g protein, 11.8 g fat, 44.2 g carbohydrate, vitamins and minerals28 days after surgeryHospital diet only
Houwing [56]
2003
The Netherlands
Oral liquid supplement (400 mL/day)500 kcal40 g proteinImmediately postoperatively during 4 weeks or until discharge
AR: 75% of patients consumed >75% of daily dose
Non-caloric placebo supplement
Sullivan [48]
2004
USA
Standard care + post-operative nightly via enteral feeding tube:
1375 mL (125 mL/h) over 11 h
1031 kcal85.8 g proteinWhen volitional intake exceeded 90% of estimated requirements for 3 consecutive days or was discharged: mean 15.8 ± 16.4 days
AR: 83.3%
Standard care
Tidermark [53]
2004
Sweden
PR: protein-rich liquid supplement (200 mL/day)
PR-N: PR + nandrolone decanoate injections (every third week)
1 g of calcium + 400 IE vitamin D3
200 kcal/day
nandrolone: 25 mg intramuscular injection
20 g protein6 monthsStandard treatment
1 g of calcium + 400 IE vitamin D3
Eneroth [16]
2005
Sweden
Hospital diet + intravenous nutrition (1 l/day) followed by
400 mL/day oral supplement
Oral supplement 400 kcal/dayIV: amino acids, fat, carbohydrate, and electrolytes 3 days → IV
7 days → oral
Hospital diet only
Duncan [49]
2006
UK
NAMean supplement: 409 kcal/dayNANAMean standard supplement: 123 kcal/day
Hommel [39]
2007
Sweden
Oral nutritional supplement twice a day 125 kcal/100 mL enriched with arginine, zinc, vitamins A, B, C, and E, selenium, and carotenoidsNAFrom post-surgery to dischargeNA
Botella-Carretero [24]
2010
Spain
Oral nutritional supplement intake (2 × 200 mL/day)400 kcal/day40 g protein/dayFrom admission until discharge
AR 52.2 ± 12.1%
Control group: no supplement
Fabian [23]
2011
Austria
Oral liquid supplementSupplements were administered when intake of energy < 20 kcal and/or protein < 1 g/kg body weight/day40% protein, 41% carbohydrate, 19% fat, vitamins and mineralsFrom post-surgery to dischargeStandard medical treatment
Hoekstra [25]
2011
The Netherlands
Nurse and doctor encouraged and motivated patients to eat and drink; if MNA < 24, dietician consulted with the patient NANANAStandard nutritional care
Wyers [29]
2013
The Netherlands
Oral liquid nutritional supplement (500 mL/day)
Dietetic counseling
500 kcal40 g proteinStarted during hospital admission and continued until 3 months after surgeryUsual care
ONS on demand: 13% received ONS and 23% received dietetic counseling
Myint [52]
2013
Hong Kong
Oral liquid nutritional supplement (240 mL twice daily)
1.2 g of calcium + 800–1000 IU vitamin D
500 kcal18–24 g proteinStarted within 3 days after admission until discharge or 28 days
AR = 77.7%
NA
1.2 g of calcium + 800–1000 IU vitamin D
Anbar [17]
2014
Israel
Standard ONS (237 mL) or
diabetic ONS (237 mL)
Patients received the difference between intake and measured energy expenditure
355 kcal
237 kcal
13.5 g protein
9.9 g protein
Started 24 h after surgery
AR = 100%
Usual hospital diet = 1800 kcal, 80 g protein
Ekinci [55]
2016Turkey
Oral liquid nutritional supplement (220 mL twice daily)NA36 g protein
3 g CaHMB
1000 IU vitamin D
30 daysUsual hospital diet: 1900 kcal, 76 g protein, 63 g fat
Malafarina [54]
2017
Spain
Oral liquid nutritional supplement (220 mL twice daily)660 kcal60 g protein
4.6 g CaHMB
1500 IU vitamin D
During hospital admission, until discharge
Mean treatment duration: 42.3 ± 20.9 days
AR = all of the subjects took more than 80%
Usual hospital diet: 1500 kcal, 87 g protein, 59 g fat
Back to TopTop