ESPEN Guidelines on Enteral Nutrition: Geriatricsespen.info/documents/ENGeriatrics.pdf · ESPEN...

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Clinical Nutrition (2006) 25, 330360 ESPEN GUIDELINES ESPEN Guidelines on Enteral Nutrition: Geriatrics $ D. Volkert a, ,1 , Y.N. Berner b , E. Berry c , T. Cederholm d , P. Coti Bertrand e , A. Milne f , J. Palmblad g , St. Schneider h , L. Sobotka i , Z. Stanga j , DGEM: $$ R. Lenzen-Grossimlinghaus, U. Krys, M. Pirlich, B. Herbst, T. Schu ¨tz, W. Schro¨er, W. Weinrebe, J. Ockenga, H. Lochs a Head Medical Science Division, Pfrimmer-Nutricia, Erlangen, Germany b Head Geriatric Department, Meir Hospital, Kfar Saba, Israel c Department of Human Nutrition & Metabolism, Hebrew University, Hadassah Med School, Jerusalem, Israel d Department of Public Health and Caring Science, Uppsala University, Uppsala, Sweden e Unite´ de Nutrition Clinique, CHUV, Lausanne, Switzerland f Health Services Research Unit, University of Aberdeen, Aberdeen, UK g Department of Medicine, Karolinska Institute, Huddinge University Hospital, Huddinge, Sweden h Gastroente´rologie et Nutrition Clinique, Hopital de l’Archet, Nice, France i Metabolic Care Unit, Department of Gerontology and Metabolic Care, Charles University, Faculty of Medicine, Hradec Kralove, Czech Republic j Internal Medicine and Clinical Nutrition, Inselspital/University Hospital, Bern, Switzerland Received 18 January 2006; accepted 19 January 2006 KEYWORDS Guideline; Clinical practice; Evidence-based; Recommendations; Summary Nutritional intake is often compromised in elderly, multimorbid patients. Enteral nutrition (EN) by means of oral nutritional supplements (ONS) and tube feeding (TF) offers the possibility to increase or to insure nutrient intake in case of insufficient oral food intake. The present guideline is intended to give evidence-based recommendations for the use of ONS and TF in geriatric patients. It was developed by an interdisciplinary expert group in accordance with officially accepted standards and is based on all ARTICLE IN PRESS http://intl.elsevierhealth.com/journals/clnu 0261-5614/$ - see front matter & 2006 European Society for Clinical Nutrition and Metabolism. All rights reserved. doi:10.1016/j.clnu.2006.01.012 Abbreviations: ADL, activities of daily living; BCM, body cell mass; BMI, body-mass index; CI, confidence interval; EN, enteral nutrition; FFM, fat-free mass; IADL, instrumental activities of daily living; MAC, mid-arm circumference; MAMC, mid-arm muscle circumference; NGT, nasogastric tube; ONS, oral nutritional supplement; OR, odds ratio; PEG, percutaneous endoscopic gastrostomy; RR, relative risk; SD, standard deviation; TF, tube feeding; TSF, triceps skin fold $ For further information on methodology see Schu ¨tz et al. 173 For further information on definition of terms see Lochs et al. 174 Corresponding author. Tel.: +49 9131 7782 31; fax: +49 9131 7782 86. E-mail address: [email protected] (D. Volkert). 1 Dorothee Volkert had been employed at the Department of Nutrition Science, University of Bonn, until May 31, 2005; she was not industry employed during the development of the guidelines. $$ The authors of the DGEM (German Society for Nutritional Medicine) guidelines on enteral nutrition in geriatrics are acknowledged for their contribution to this article.

Transcript of ESPEN Guidelines on Enteral Nutrition: Geriatricsespen.info/documents/ENGeriatrics.pdf · ESPEN...

ARTICLE IN PRESS

Clinical Nutrition (2006) 25, 330–360

0261-5614/$ - sdoi:10.1016/j.c

Abbreviationnutrition; FFM,circumference;RR, relative ris

$For further�CorrespondE-mail addr

1Dorothee Voindustry emplo

$$The autacknowledged

http://intl.elsevierhealth.com/journals/clnu

ESPEN GUIDELINES

ESPEN Guidelines on Enteral Nutrition: Geriatrics$

D. Volkerta,�,1, Y.N. Bernerb, E. Berryc, T. Cederholmd, P. Coti Bertrande,A. Milnef, J. Palmbladg, St. Schneiderh, L. Sobotkai, Z. Stangaj,DGEM:$$ R. Lenzen-Grossimlinghaus, U. Krys, M. Pirlich, B. Herbst,T. Schutz, W. Schroer, W. Weinrebe, J. Ockenga, H. Lochs

aHead Medical Science Division, Pfrimmer-Nutricia, Erlangen, GermanybHead Geriatric Department, Meir Hospital, Kfar Saba, IsraelcDepartment of Human Nutrition & Metabolism, Hebrew University, Hadassah Med School,Jerusalem, IsraeldDepartment of Public Health and Caring Science, Uppsala University, Uppsala, SwedeneUnite de Nutrition Clinique, CHUV, Lausanne, SwitzerlandfHealth Services Research Unit, University of Aberdeen, Aberdeen, UKgDepartment of Medicine, Karolinska Institute, Huddinge University Hospital, Huddinge, SwedenhGastroenterologie et Nutrition Clinique, Hopital de l’Archet, Nice, FranceiMetabolic Care Unit, Department of Gerontology and Metabolic Care, Charles University,Faculty of Medicine, Hradec Kralove, Czech RepublicjInternal Medicine and Clinical Nutrition, Inselspital/University Hospital, Bern, Switzerland

Received 18 January 2006; accepted 19 January 2006

KEYWORDSGuideline;Clinical practice;Evidence-based;Recommendations;

ee front matter & 2006lnu.2006.01.012

s: ADL, activities of dafat-free mass; IADL, inNGT, nasogastric tube;k; SD, standard deviatioinformation on method

ing author. Tel.: +49 913ess: d.volkert@nutricialkert had been employeyed during the develophors of the DGEM (Gefor their contribution to

Summary Nutritional intake is often compromised in elderly, multimorbidpatients. Enteral nutrition (EN) by means of oral nutritional supplements (ONS)and tube feeding (TF) offers the possibility to increase or to insure nutrient intake incase of insufficient oral food intake.

The present guideline is intended to give evidence-based recommendations forthe use of ONS and TF in geriatric patients. It was developed by an interdisciplinaryexpert group in accordance with officially accepted standards and is based on all

European Society for Clinical Nutrition and Metabolism. All rights reserved.

ily living; BCM, body cell mass; BMI, body-mass index; CI, confidence interval; EN, enteralstrumental activities of daily living; MAC, mid-arm circumference; MAMC, mid-arm muscleONS, oral nutritional supplement; OR, odds ratio; PEG, percutaneous endoscopic gastrostomy;n; TF, tube feeding; TSF, triceps skin foldology see Schutz et al.173 For further information on definition of terms see Lochs et al.174

1 7782 31; fax: +49 9131 7782 86..com (D. Volkert).d at the Department of Nutrition Science, University of Bonn, until May 31, 2005; she was notment of the guidelines.rman Society for Nutritional Medicine) guidelines on enteral nutrition in geriatrics arethis article.

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Enteral nutrition;Oral nutritionalsupplements;Tube feeding;Geriatric patients;Undernutrition;Malnutrition;Elderly;Aged-80-and-over

relevant publications since 1985. The guideline was discussed and accepted in aconsensus conference.

EN by means of ONS is recommended for geriatric patients at nutritional risk, incase of multimorbidity and frailty, and following orthopaedic-surgical procedures. Inelderly people at risk of undernutrition ONS improve nutritional status and reducemortality. After orthopaedic-surgery ONS reduce unfavourable outcome. TF is clearlyindicated in patients with neurologic dysphagia. In contrast, TF is not indicated infinal disease states, including final dementia, and in order to facilitate patient care.Altogether, it is strongly recommended not to wait until severe undernutrition hasdeveloped, but to start EN therapy early, as soon as a nutritional risk becomesapparent.

The full version of this article is available at www.espen.org.& 2006 European Society for Clinical Nutrition and Metabolism. All rights reserved.

Summary of statements: Geriatrics

Subject

Recommendations Grade173 N umber

Indications

In patients who are undernourished or at risk ofundernutrition use oral nutritional supplementation toincrease energy, protein and micronutrient intake,maintain or improve nutritional status, and improvesurvival.

A 2

.1

In frail elderly use oral nutritional supplements (ONS) toimprove or maintain nutritional status.

A 2

.2

Frail elderly may benefit from TF as long as their generalcondition is stable (not in terminal phases of illness).

B 2

.2

In geriatric patients with severe neurological dysphagiause enteral nutrition (EN) to ensure energy and nutrientsupply and, thus, to maintain or improve nutritionalstatus.

A 2

.3

In geriatric patients after hip fracture and orthopaedicsurgery use ONS to reduce complications.

A 2

.4

In depression use EN to overcome the phase of severeanorexia and loss of motivation.

C 2

.6

In demented patients ONS or tube feeding (TF) may leadto an improvement of nutritional status.

2

.7

In early and moderate dementia consider ONS—andoccasionally TF—to ensure adequate energy and nutrientsupply and to prevent undernutrition.

C 2

.7

In patients with terminal dementia, tube feeding is notrecommended.

C 2

.7

In patients with dysphagia the prevention of aspirationpneumonia with TF is not proven.

2

.9

ONS, particularly with high protein content, can reducethe risk of developing pressure ulcers.

A 2

.10

Based on positive clinical experience, EN is alsorecommended in order to improve healing of pressureulcers.

C 2

.10

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Application

In case of nutritional risk (e.g. insufficient nutritionalintake, unintended weight loss 45% in 3 months or 410%in 6 months, body-mass index (BMI) o20 kg/m2) initiateoral nutritional supplementation and/or TF early.

B 2

.1

In geriatric patients with severe neurological dysphagiaEN has to be initiated as soon as possible.

C 2

.3

In geriatric patients with neurological dysphagiaaccompany EN by intensive swallowing therapy until safeand sufficient oral intake is possible.

C 2

.3

Initiate enteral nutrition 3 hours after PEG placement.

A 3 .2

Route

In geriatric patients with neurological dysphagia preferpercutaneous endoscopic gastrostomy (PEG) tonasogastric tubes (NGT) for long-term nutritional support,since it is associated with less treatment failures andbetter nutritional status.

A 2

.3

Use a PEG tube if EN is anticipated for longer than 4weeks.

A 3

.1

Type offormula

Dietary fibre can contribute to the normalisation of bowelfunctions in tube-fed elderly subjects.

A 3

.4

Grade: Grade of recommendation; Number: refers to statement number within the text.

Terminology

Geriatric patient—a biologically elderly patient who is at acute risk of loss of independence due to acuteand/or chronic diseases (multiple pathology) with related limitations in physical, psychological, mentaland/or social functions. The abilities to perform the basic activities of independent daily living arejeopardised, diminished or lost. The person is in increased need of rehabilitative, physical, psychologicaland/or social care to avoid partial or complete loss of independence.

Elderly—a term used to describe a particular age group, i.e. over 65 years.Very old or very elderly—a term to describe those over 85 years of age.Frail elderly—Frail elderly are limited in their activities of daily living due to physical, mental,

psychological and/or social impairments as well as recurrent disease. They suffer from multiple pathologieswhich seriously impair their independence. They are therefore in particular need of help and/or care and arevulnerable to complications.

Reduced capacity for rehabilitation—This means that the older the patient, the more difficult it is torehabilitate that patient back to normal or to his/her previous state. Specifically, the restoration ofmuscle mass after illness requires much greater effort in terms of exercise and nutrition in the elderlycompared with the younger patient. It is also implicit that other functions, including mental, are similarlymore resistant to rehabilitation.

Functional status—This term is being used in a general sense to describe global function, e.g. the abilityto perform activities of daily living (ADL), or specific function, e.g. muscle strength or immune function.

Introduction

The risk of undernutrition is increased in elderlypatients due to their decreased lean body mass andto many other factors that may compromisenutrient and fluid intake. Consequently, an ade-quate intake of energy, protein and micronutrients

has to be ensured in each patient independently ofhis/her previous nutritional status. Since restorationof body cell mass (BCM) is more difficult than inyounger persons, preventive nutritional support hasto be considered.Nutritional care should be integrated appropri-

ately into the overall care plan, which takes into

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account all aspects of the patient, personal, social,physical and psychological. A complete assessment ofthe patient should include that of nutritional status orrisk, followed by a nutritional programme reflectingethical as well as clinical considerations. In designingthe programme, it should be remembered that themajority of sick elderly patients require at least 1 gprotein/kg/day and around 30kcal/kg/day of energy,depending on their activity. Many elderly people alsosuffer from specific micronutrient deficiencies, whichshould be corrected by supplementation.

Oral nutritional therapy via assisted feeding anddietary supplements is often difficult, time-con-suming and demanding in elderly patients (due tomultimorbidity and slow responses). However,assisted oral feeding and supplements are able tosupport the physical and psychological rehabilita-tion of most elderly patients. Therefore, even intimes of declining financial and human resources, itis unacceptable to initiate tube feeding (TF) merelyin order to facilitate care or save time.

Decision making concerning TF in the elderly isoften difficult, and in many cases ethical questionsarise (see Guidelines ‘‘Ethical and legal aspectsin enteral nutrition’’). In each case, the followingquestions should be asked:

Does the patient suffer from a condition that islikely to benefit from enteral nutrition (EN)? � Will nutritional support improve outcome and/or

accelerate recovery?

� Does the patient suffer from an incurable

disease, but one in which quality of life andwellbeing can be maintained or improved by EN?

� Does the anticipated benefit outweigh the

potential risks?

� Does EN accord with the expressed or presumed

will of the patient, or in the case of incompetentpatients, of his/her legal representative?

� Are there sufficient resources available to manage

EN properly? If long-term EN implies a differentliving situation (e.g. institution vs. home), will thechange benefit the patient overall?

Sedation of the patient for acceptance of thenutritional treatment is not justified.

The present guidelines are based on studies inelderly subjects or in those in whom the averageage of the study participants is 65 years or more.

1. What are the aims of EN therapy ingeriatrics?

Provision of sufficient amounts of energy,protein and micronutrients.

Maintenance or improvement of nutritionalstatus. � Maintenance or improvement of function,

activity and capacity for rehabilitation.

� Maintenance or improvement of quality of

life.

� Reduction in morbidity and mortality.

Therapeutic aims for geriatric patients do notgenerally differ from those in younger patientsexcept in emphasis. While reducing morbidity andmortality is a priority in younger patients, ingeriatric patients maintenance of function andquality of life is often the most important aim.Considering the reduced adaptive and regenerativecapacity of the elderly, EN may be indicated earlierand for longer periods than in younger patients.

1.1. Can EN improve energy and nutrient intakein geriatric patients?

EN (oral nutritional supplement (ONS) and/or TF)increases energy and nutrient intake in geriatricpatients (Ia). Percutaneous endoscopic gastro-stomy (PEG) feeding is superior to nasogastricfeeding in this respect (Ia).

Comment: In a recent Cochrane analysis, ONS ledto an increase in energy and nutrient intake in 29out of the 33 analysed trials which had reportedintake. In three studies no difference in total intakewas found, since patients reduced their voluntaryfood consumption1 (Ia). The success of ONS issometimes limited by poor compliance due to lowpalatability, side effects such as nausea anddiarrhoea, and by cost.2–10 Variety and alterationin taste (different flavours, temperature andconsistency), encouragement and support by staff,as well as administration between the meals (andnot at meal times) are all important in order toachieve increased energy and nutrient intake.

Randomised controlled trials of TF in patientswith neurological dysphagia that compared naso-gastric (NG) with PEG feeding have shown that93–100% of the prescription was administered viathe PEG, versus 55–70% via a NG tube.11,12 In threestudies with supplemental overnight NG TF, be-tween 1000 and 1500 kcal were administered pernight in addition to daily food intake. Total energyand nutrient intake was, therefore, markedlyimproved.13–15

1.2. Can EN maintain or improve the nutritionalstatus of elderly patients?

ONS can maintain or improve nutritional status(Ia). Several studies have shown that TF also

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maintains or improves nutritional paramentersirrespective of the underlying diagnosis. Themetabolic consequences of ageing which can leadto sarcopenia and a severely reduced nutritionalstatus at the time of tube placement can impair oreven prevent successful nutritional therapy (III).

Comment: The administration of ONS has beenreported to have positive effects on nutritionalstatus irrespective of the main diagnosis. Weightloss, during acute illness and hospitalisation, can beprevented by the provision of food of high energyand protein density, combined with between mealsnacks, and by the use of ONS, when normal intakeis insufficient. Sometimes weight gain can even beachieved. Milne et al.1 analysed the percentageweight change in 34 randomised controlled trialswith 2484 elderly patients and showed a meanweight increase of 2.3% (pooled weighted meandifference; 95% confidence interval (CI) 1.9–2.7%)1

(Ia). Changes to anthropometric parameters areless consistent, but may reflect improvement ofnutritional status in general1 (Ia). Effects on bodycomposition have only occasionally been investi-gated. Increases in fat-free mass (FFM) (Ib)16,17

(IIa)18 and BCM (Ib)19 in supplemented patientshave been reported by some investigators whereasothers could not detect any change (Ib)20–22 (IIa)23.

Several observational studies exploring the ef-fect of TF in multimorbid geriatric patients haveshown improvements in nutritional status, e.g.maintenance of body weight24–27 (III) and eithermaintenance25,27 (III) or increase in albuminlevels24,26,28 (III). It should be emphasised, how-ever, that changes in albumin more usually reflectchanges in disease rather than nutritional sta-tus.29,30 In two studies of frail, mainly dementednursing home residents, weight gain has beenreported.31,32 Improvements in nutritional statushave also been described in patients with neurolo-gical dysphagia, in whom PEG feeding provedsuperior to nasogastric feeding (NGT)11,12 (Ib).The effects of nocturnal TF supplementary to dailyfood intake in elderly patients with hip fracture orfractured neck of femur, are inconsistent.13–15

Bastow et al.13 have reported the greatest benefitin undernourished patients (Compare 2.4).

The effectiveness of TF on nutritional status maybe limited by compliance with the tubes, and byside effects. The nutritional status of the frailelderly is often very reduced at the time of tubeplacement,24–26,33–38 and is accompanied by sarco-penia which is more difficult to reverse in the oldcompared with the young.39–41 Resistance training,if tolerated, may add to the effectiveness ofnutritional support.9,42 Many tube fed patients are

bedridden, and consequent immobility furtherenhances muscle wasting and prevents gain in leanmass. Weighing is also problematic in thesepatients.

1.3. Does EN maintain or improve functionalstatus or rehabilitative capacity?

Adequate nutrition is a prerequisite for anyfunctional improvement, although studies aretoo few and diverse to allow a general state-ment. Some studies have been positive and somenegative in this respect.

Comment: Available data concerning the effect ofONS on the functional capacity of elderly patientsare inconsistent, although several studies reportfunctional improvements. Thus, Gray-Donald et al.7

(Ib), observed a significantly lower frequency offalls in supplemented free-living frail elderlycompared with non-supplemented and Unossonet al.43 (Ib) describe a higher activity level inlong-term care residents after 8 weeks of ONS.Improvements in the ability to perform basicactivities of daily living (ADL) are reported in agroup of female patients after hip fracture byTidermark et al.44 (Ib), in a subgroup of severelyundernourished geriatric patients by Potter45 (Ib)and in a subgroup of patients with good acceptanceof a 6 months supplementation by Volkert et al.2

(Ib). Woo et al.46 (Ib) describe a significantlyimproved ADL status in patients during recoveryfrom chest infection after 3-months interventioncompared with the control group. Several studies,however, detected no difference between inter-vention and control groups with respect to inde-pendence in ADL (Ib)19,20,47–49 (IIa)6,50. Mobility wasalso unchanged in several studies (Ib)3,43,47 (IIa)6.Similarly, hand grip strength was unaltered in moststudies (Ib)3,6,7,17,21,51–53 (IIa)18 but this may be oflimited relevance as it only tests muscle function ofthe upper body. One randomised trial54 (IIa) as wellas two non-randomised23,55 and one uncontrolledtrial56 (IIb) report an improved hand grip strength insupplemented patients. In four trials, the effectson mental capacity were assessed and again nochanges were observed (Ib)20,43,52 (IIa)50.

At the time of tube placement, geriatric patientsare often in a significantly compromised generalcondition as well as severely functionally im-paired.24,27,36,57–59 Trials in nursing homes alsodescribe a high degree of frailty and dependencein PEG-fed residents32,36,60–63 (III).

Apart from the fractured femur studies withsupplementary overnight TF (Compare 2.4) onlya few, uncontrolled trials have reported theeffects of TF on either functional status or

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rehabilitative capacity in other groups of elderlypatients.24,33,36,64,65 Callahan et al.24 evaluated 72PEG-fed patients with severe physical and mentalimpairments before and after PEG placement usingseveral ADL scales. Improvements in functionalstatus were only rarely observed (improvement ofinstrumental activities of daily living (IADL) in 6%,ADL 10%, upper body functions 18%, lower bodyfunctions 29%) (IIb). Kaw and Sekas,36 using theFunctional Independence Measure Scale (FIM), alsofailed to show significant improvements after 18months in functional status in tube-fed nursinghome residents who were in reduced generalcondition (52% demented, 48% completely ADLdependent) (III). Weaver et al.65 used a Quality ofLife Scale adapted from Spitzer, in which orienta-tion, communicative capacity, ability to self-care,and continence were assessed. In a mixed popula-tion of PEG-fed patients (median age 76 years), nosignificant change was detected after long-termEN. Relatives of the patients with the lowest valueon the scale tended to answer ‘‘no’’ to the questionwhether they would wish TF in a similar situationfor themselves (IIb). Nair et al.33 observed nochanges in function measured by the KarnovskyPerformance Scale after 6 months of PEG feeding in31 surviving patients aged 8478 years (IIa). OnlySanders et al.64 describe an improvement in ADL in25 stroke patients (mean age 80 years) with EN viaPEG. At the time of PEG placement 84% of thepatients had a Barthel index (0–100 points) of 0points (completely dependent; mean 0.5 points).After 6 months of EN a mean increase of 4.8 pointswas observed. Six patients (24%) showed a clearimprovement (Barthel index increase from 0.5 to 9points), in 10 patients (40%), however, no or only aminimal improvement was observed (IIa).

1.4. Does EN reduce length of hospital stay?

In geriatric patients, length of hospital stay isdetermined not only by nutritional status butalso by other factors. Available results concern-ing the effect of EN on length of hospital stay areconflicting.

Comment: Undernutrition increases the risk ofcomplications thereby increasing the length ofhospital stay in geriatric patients.66–69 Consequently,improvement in nutritional status using EN shouldresult in a reduced length of hospital stay. In geriatricpatients, however, length of hospital stay is not onlydetermined by nutritional status but also by otherfactors, e.g. the assurance of adequate care afterdischarge. In addition, in times of declining financialresources, length of hospital stay is only a poorreflection of the effects of EN.

Available study results about the impact of EN onlength of stay are conflicting. In 2002 Milne et al.70

analysed seven studies with 658 participants andreported a statistically significant benefit of ONSwith respect to hospital stay. Mean length of staywas 3.4 days shorter in the supplemented com-pared with the unsupplemented group (95% CI6.1–0.7 days) (Ia). The addition of three new trialsto the meta-analysis, however, shifted the resultsto non-significant effects.1 If patients with hip orfemoral neck fracture are regarded separately,several studies report significantly shorter length ofstay in supplemented patients71–74; this could nothowever be confirmed by others75 (Compare 2.4)

The effects of TF on length of hospital stay haveonly occasionally been measured11,13,15 and requirefurther study.

1.5. Does EN improve quality of life?

The effect of ONS and TF on quality of life isuncertain.

Comment: Although quality of life is crucial in theevaluation of therapeutic benefit in geriatrics, onlya few studies have examined the effect of EN uponit. Studies investigating the effect of ONS haveemployed different parameters, e.g: general well-being, subjective health, SF 36, EQ-5D, HospitalAnxiety and Depression Scale (HADS). Some reportimprovements (IIa)3,54,76, whereas others observeno changes7,22,51 (IIa). These few available data donot allow any firm conclusion about the effects ofONS on quality of life.

In patients requiring TF, impairments of cogni-tion, vigilance and speech can make assessingquality of life difficult. About 60% of the patientsin the trial of Callahan et al.24 were unable tocommunicate at the time of PEG placement, andthe majority of patients with preserved ability tocommunicate were cognitively impaired (IIb). Inthe cohort of 215 patients investigated by Banner-man et al.77 data on quality of life could only begathered in 30 patients (IIb). Verhoef and vanRosendaal78 used semi-structured interviews (witheither patients or their relatives), the KarnovskyPerformance Scale as well as the Quality of LifeIndex, in order to measure subjective quality of lifein patients after PEG placement (mean age 66718years). About 85% of the patients who were stillalive after one year and still fed via PEG (n ¼ 23)were not able to run a household, 67% weredependent in personal care and 19% were feelingvery ill. However, the majority of patients andcaregivers felt that it had been the right decision toagree to the PEG. All 10 patients who were aliveafter one year and could be asked, stated that they

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would decide in favour of PEG again. The Karnovskyindex deteriorated in three of these 10 survivingpatients and improved in six (IIb). According to theauthors, these results do not necessarily imply aclear improvement in quality of life.78 Weaver etal.65 evaluated subjective quality of life by inter-view and observed a correlation between subjec-tive and objective quality of life (Compare 1.3).Significant changes in subjective quality of lifewere not detected (IIb). Abitbol et al.26 used both abehaviour scale and a depression scale in order toassess quality of life in 59 institutionalised patients(mean age 85 years) who received EN via a PEG.The patients were bedridden, their health statuswas reduced, and infections were present in 25%.After 3 months of EN via a PEG, quality of lifescores were unchanged, although the depressionscale tended to improve. However, 16 of thesurviving patients (27%) resumed full oral nutritionand six patients (10%), returned to their own homewith a functioning PEG tube (IIb). In a cohort of 38long-term home EN patients, quality of life waspoorer in elderly than in younger patients.79

All in all, these studies do not allow for anygeneral conclusions about effects of EN on qualityof life. TF may also have side effects that mayadversely affect quality of life, e.g. gastrointest-inal symptoms, aspiration, the discomfort of thetube, or the need to use restraints.

1.6. Does EN improve survival in geriatricpatients?

ONS improve average survival (Ia). In patientswho need TF due to the severity of disease, anincrease in survival is not proven.

Comment: Meta-analysis of the data from 32randomised controlled trials with 3017 partici-pants revealed a lower mortality risk in supple-mented elderly subjects than in controls (relativerisk (RR) 0.74; 95% CI 0.59–0.92)1 (Ia). Participantswere supplemented for at least 1 week andobserved for at least 2 weeks. A further meta-analysis from 12 randomised controlled trials(n ¼ 1146) and five non-randomised studies on theeffect of ONS in hospitalised geriatric patients withmixed diagnoses reached similar conclusions (RR0.58; 95% CI 0.4–0.83)80 (Ia). In contrast, a meta-analysis from five studies on the effect of proteinand energy supplementation, mainly in hip fracturepatients, showed no effect on mortality risk.75

Studies on supplementary overnight TF in hipfracture patients have produced similar results(Compare 2.4).

The effect of TF on the survival of elderlypatients without a hip fracture was investigated

in nine non-randomised controlled studies (non-randomised for ethical reasons) (Table 1) and sev-eral uncontrolled observational studies (Table 2).

Four of the controlled studies were carried out inhospitals,33,81,82,84 five in nursing homes.60–63,83

Two of the studies were prospective,33,81 and theothers were retrospective comparisons of EN vs. noEN. In five studies, participants with advanceddementia were investigated.33,61,62,81,84 The mostrecent of these studies was retrospective anddescribes a mean survival of 59 and 60 days in 23severely demented dysphagic patients with PEGand in 18 patients without PEG.84 A databaseanalysis from Mitchell et al.62 in 1386 nursing homeresidents with severe cognitive impairment—where 135 were enterally fed—showed no increasein survival (III). Mortality rate after one year wassurprisingly low (15%). Meier et al.81 prospectivelystudied 99 acutely ill patients with advanceddementia, seventeen of whom were already beingfed by PEG at the time of hospital admission, 51had a PEG inserted in hospital, and the remaining31 consumed regular food orally. Half of all patientsdied during the following 6 months irrespective ofthe nutritional regimen. Nair et al.33 observed ahigher mortality rate in 55 severely dementedpatients with PEG after 6 months compared with acontrol group without a PEG (44% vs. 26%).According to the authors, the groups were com-parable regarding age, gender and comorbidity.PEG patients, however, suffered more often fromsevere hypoalbuminaemia (mean albumin con-centration 28.675 vs. 33.274 g/l in the controlgroup) suggesting more severe underlying inflam-matory disease. The only trial that detecteda significantly reduced mortality in nursing homeresidents with severe cognitive impairment isthe data base analysis from Rudberg et al.61

After 30 days, 15% had died in the group ofenterally fed patients compared with 30% in thecontrol group. After 1 year, the difference wasless distinct, but still statistically significant (50%vs. 61%). The control group was comparableregarding dementia, comorbidity, functional statusand BMI (III).

Two further non-randomised controlled studies innursing home patients with various diagnoses and alow percentage of demented patients also failed toshow prolonged survival in the enterally fedpatients.60,63 In the databank analysis from Mitchellet al.63 mortality in 551 tube-fed nursing homeresidents with chewing and swallowing difficultieswas even higher than in 4715 residents withoutnutritional therapy (III). Approximately half of theparticipants showed severe cognitive impairments(66% of tube-fed patients vs. 46% of the control

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Table

1Mortality

intube-fedelderly

subjects(con

trolled,no

n-rand

omised

stud

ies).

Article

Study

Typeof

EN

Patients

Diagn

osis

Mortality(%

)

Firstau

thor

Type

Place

nAge

(yea

rs)

Dem

entia

(%)

CVE

(%)

CA

(%)

Dyspha

gia

(%)

Other

charac

teristics

306

1

M7SD

Ran

geday

mon

year

Mitch

ell62

R(datab

ase)

NH

TF

135

87(M

d)(65–

107)

100seve

re47

6—

63%instab

leco

ndition,

30%dec

ubitus,

33%seve

reADL-de

pen

den

t,84

%ch

ewingor

swallowingproblems

o5

ca.15

No

1251

87(M

d)(65–

107)

100seve

re27

7—

52%instab

leco

ndition,

15%dec

ubitus,

45%seve

reADL-

dep

ende

nt,

61%ch

ewingor

swallowingproblems

o5

ca.15

Meier

81

PH

68PEG

,31

no99

84.8

(63–

100)

100ad

vanc

ed0

0—

Allac

utelyill,

56%dec

ubitus,

62%infections

ca.20

5065

Nair3

3P

HPEG

5583

710

100ad

vanc

ed0

0—

NoCA,CVE,

seve

redisea

se,EN

due

tolow

oral

intake

44

No

3380

78

100ad

vanc

ed0

0—

NoCA,CVE,

seve

redisea

se26

Rud

berg6

1R(datab

ase)

NH

NG

353

8577

X65

93co

g.im

p.

(63seve

re)

——

100

100%

dyspha

gia&

eating

dep

ende

nce,

96%dep

ende

ntin

6ADL

1550

No

1192

8677

X65

93co

g.im

p.

(64seve

re)

——

100

100%

dyspha

gia&

eating

dep

ende

nce,

96%dep

ende

ntin

6ADL

3061

ESPEN Guidelines on Enteral Nutrition 337

ARTICLE IN PRESS

Table

1(con

tinu

ed)

Article

Study

Typeof

EN

Patients

Diagn

osis

Mortality(%

)

Firstau

thor

Type

Place

nAge

(yea

rs)

Dem

entia

(%)

CVE

(%)

CA

(%)

Dysph

agia

(%)

Other

charac

teristics

306

1

M7SD

Ran

geday

mon

year

Mitch

ell63

R(datab

ase)

NH

TF

551

87(M

d)

X65

31(66seve

reco

g.im

p.)

597

—10

0%ch

ewingor

swallowingdifficu

lties,

47%instab

leco

ndition,

12%dec

ubitus,

83%seve

rely

ADL-dep

ende

nt

22

No

4715

87(M

d)

X65

50(46seve

reco

g.im

p.)

306

100%

chew

ingor

swallowingdifficu

lties,

40%instab

leco

ndition,

9%dec

ubitus,

46%seve

rely

ADL-dep

ende

nt

12

Bou

rdel-

March

asson6

0R

NH

PEG

5874

79

n.a.

(NH55

%)

n.a.

(NH

19%)

n.a.

5336

%an

orex

ia,

10%un

consciou

s,allseve

rely

dep

enden

t,66

%dec

ubitus

14

No

5082

78

n.a.

(NH55

%)

n.a.

(NH

19%)

n.a.

4456

%an

orex

ia,

0%un

consciou

s,allseve

rely

dep

enden

t,14

%dec

ubitus

10

Cow

en82

RH

All

149

76712

2056

010

0Se

riou

sco

morbidity,

42%he

miplegia,

32%CHF,

20%dec

ubitus,

70%alert,

85%urine-inco

ntinen

t

2762

PEG

8060

Spon

tane

ousim

prove

men

t10

No

1878

No/

NG

51

Crogh

an83

RNH

All

4069

(31–

96)

2590

583

55%aspiration,

20%mob

ile

Tube

1553

No

743

ADL¼

Activitiesof

daily

living

,CA¼

canc

er,CHF¼

cong

estive

heartfailure,

cog.im

p.¼

cogn

itiveim

pairm

ent,

CVE¼

cerebrova

scular

even

t,EN¼

enteralnu

trition,

Hospital,

ONS:

oral

nutritiona

lsupplem

ents,TF¼

tubefeed

ing,

EN¼

enteralnu

trition(¼

ONS&

TF)

Md¼

Med

ian,

M7SD¼

Mea

n7stan

darddev

iation

,mon¼

mon

ths,

n.a.¼

notav

ailable,

NG¼

nasoga

strictube,

NH¼

nursingho

me,

PEG¼

percu

tane

ousen

dosco

pic

gastrostom

y,P¼

prospec

tive

,R¼

retrospe

ctive.

D. Volkert et al.338

ARTICLE IN PRESS

Table

2Mortality

intube-fedelderly

subjects(observationa

lstud

ieswitho

utco

ntrolgrou

p).

Article

Study

type

Typeof

EN

Patients

Diagn

osis

Mortality

Firstau

thor

nAge

(yr)

(Ran

ge)

Dem

entia

CVE

CA

Dyspha

gia

Other

charac

teristics

30day

3mon

6mon

1ye

arM7SD

(%)

(%)

(%)

(%)

(%)

(%)

(%)

(%)

Nursing

homeresiden

tsGolden

32

RPEG

102

8976

(71–

104)

89seve

re20

010

0Pe

rsistent

dyspha

gia,

low

intake

,75

%co

mpl.

ADL-dep

enden

t,stab

leco

ndition,

noterm

inal

stag

e,LE

atleast1mon

1224

38

Abuk

sis5

7R

PEG

4784

711

(44–

100)

8749

0—

94%desoriented

,96

%bed

ridden

4Kaw

36

RPEG

4674

(19–

96)

5224

7—

48%co

mpletely

ADL-

dep

enden

t,on

ly4%

could

dec

idein

favo

urof

PEG

them

selves,poo

rge

neral

cond

ition

2050

70%470

Geriatric

patien

ts(all465yr

ormea

nage

465yr)

Lind

eman

n85

PPEG

3683

(X65

)10

00

011

84%low

intake

(53%

chron,

31%ac

ute),

6%beh

avioural

disorder

2542

Sand

ers5

9R

PEG

103

77—

100

00

100

allseve

rely

ADL-dep

enden

t(BI0-5P)

5478

8190

Dwolatzky8

6P

PEG

3285

76

(X65

)84

533

2872

%refusalto

eat

545

NG

9082

79

(X65

)68

432

3763

%refusalto

eat

2080

Abuk

sis5

7R

PEG

6780

716

(26–

103)

5230

1031

79%bed

ridden

,11

%un

consciou

s29

Paillaud

35

RPEG

7383

79

(X65

)45

—4

4549

%an

orex

ia,30

%infection

44%reduc

edmob

ility,

44%dec

ubitus

3252

63

Fay2

7R

PEG

8070

.2—

3252

2379

31%dec

ubitus,

91%in

need

ofassistan

cein

ADL,

76%faec

al-,

90%urine-inco

ntinen

t

1755

70

NG

2969

.8—

1341

2841

21%dec

ubitus,

86%in

need

ofassistan

cein

ADL,

66%faec

al-,

82%urine-inco

ntinen

t

2845

70

Callaha

n24

PPEG

9979

79

(60–

98)

3541

13—

35%ne

uro-deg

enerative

disorder,seve

rephy

sica

lan

dmen

talim

pairm

ent

2250

Cioco

n25

PNG

7082

(65–

95)

34—

—47

50%refusalto

eat,

3%oe

sopha

gus-ob

struction,

multiple

&ad

vanc

eddisea

se

541

Quill87

RNG/G

554

70(X

70)

3149

27—

69%inco

mpeten

tAbitbol

26

PPEG

5983

77

50%485

30—

242

31%MNwitho

utdys,

25%refusalto

eat

54%dec

ubitus,49

%pulmon

ary

infection

25

Bussone

88

RPEG

155

84(70–

98)

24—

3—

35%ne

urol,

38%dep

ression

16

Bussone

89

PPEG

101

83.6

(70–

98)

2236

4—

38%dep

ression

14Markgraf9

0R/P

PEG

5487

(65–

94)

——

24—

72%ne

urol,multimorbid

33Rah

a91

?PEG

161

79(53–

99)

—81

—88

12%MN

2039

Finu

cane

92

PPEG

2882

(68–

99)

—93

—10

07%

Parkinson;

NG-intoleran

t8

ESPEN Guidelines on Enteral Nutrition 339

ARTICLE IN PRESS

Table

2(con

tinu

ed)

Article

Study

type

Typeof

EN

Patients

Diagn

osis

Mortality

Firstau

thor

nAge

(yr)

(Ran

ge)

Dem

entia

CVE

CA

Dyspha

gia

Other

charac

teristics

30day

3mon

6mon

1ye

arM7SD

(%)

(%)

(%)

(%)

(%)

(%)

(%)

(%)

James

93

RPEG

126

80(M

d)

(53–

94)

—10

0—

100

aspirationrisk

2338

4653

Wan

klyn

94

RPEG

3774

(48–

89)

—10

0—

—92

%he

miplegia

68Wijdicks

95

RPEG

6374

(Md)

(41–

98)

0 adva

nced

100

0—

noterm

inal

stag

es;

63%he

miplegia,

21%ap

hasia,

35%reduc

edco

nsciou

sness

14 (2wks)

Mixed

coho

rtswithhigh

perce

ntage

ofelderly

Clarkston

96

RPEG

4271

.4(33–

99)

——

24—

67%ne

urol,9%

MN

2648

Frieden

berg9

7P

PEG

6476

(39–

97)

——

20—

80%seve

rene

urol.dysfunc

tion

,38

%respiratoryproblems,

seve

reco

gnitiveim

pairm

ent

33

Horton98

RPEG

224

75(20–

103)

670

15—

—8

Kohli99

RPEG

100

82(47–

102)

4—

238

48%MN

16La

rson

100

RPEG

314

n.a.

(3–92

)—

—1

—75

%ne

urol,

13%orop

haryng

eal

1666

%460

Ligh

t101

RPEG

416

75(18–

103)

1130

9—

19%MN;-

23Llan

eza1

02

RPEG

7367

(30–

96)

——

19—

34%ne

urol,18

%AP

26Markgraf1

03

RPEG

8469

714

(35–

98)

——

39—

59%ne

urol,polym

orbid

3165

%X65

Nicho

lson

104

RPEG

168

70(16–

96)

—58

—18

15%ne

urol,9%

obstruction

9.5

Rab

enec

k105

RPEG

7368

68.1

(18–

102)

—19

30—

29%ne

urol

5926

%475

Rim

on106

PPEG

339

71.3

(14–

96)

——

11—

82%ne

urol

19.5

Sali107

RPEG

3275

(38–

88)

—53

1310

016

%pseud

obulbar

paralysis

16Sand

ers5

9R

PEG

361

68.5

—29

3318

100

20%misce

llan

eous

diagn

oses

2844

5263

Skelly

58

PPEG

7469

(Md)

(28–

90)

—42

2623

%ch

ron.

neurol;

seve

refunc

tion

ally

impaired

(38%

BI0,

Md1point)

1935

42

Stua

rt108

RPEG

4870

(Md)

——

—17

—66

%ne

urol,13

%COPD

31Stua

rt108

Rop

.G.

5565

(Md)

——

—29

—64

%ne

urol,7%

COPD

24Tan1

09

RPEG

4465

(14–

94)

—39

3610

059

%ne

urol,7%

Parkinson

Taylor

110

RPEG

9776

.5(o

1–97

)—

555

25%othe

rCNS-disea

ses,

55%im

pairedvigilanc

e,87

%assistan

cein

toilet

&tran

sfer

2253

Wolfsen

111

R/P

PEG

/PEJ

201

66716

(X18

)—

—36

—64

%ben

igndisea

se,

esp.ne

urol

50

Hom

een

tera

lnu

tritionpatien

tsElia

112

BANS

HEN

1230

—(65–

75)

—10

0—

41%bed

ridden

,31

%ho

use-bou

nd25

2970

—(X

75)

—10

0—

47%bed

ridden

,30

%ho

use-bou

nd36

How

ard113

RHEN

787

7978

(X65

)10

0ne

urom

uscu

lardyspha

gia

53Sand

ers1

14

PPEG

8774

(35–

88)

——

—PEG

-com

plica

tion

sat

home

17Schn

eider

115

PHEN

5486

(Md)

(60–

101)

100

00

010

0%low

intake

4680

148

75(M

d)

(1–97

)0

57

097

3%low

intake

(asindication),

20%ALS

1759

6465

(Md)

(40–

92)

00

100

100

0%low

intake

(asindication)

1263

3275

(Md)

(1–94

)0

00

010

0%low

intake

due

todep

ressionor

disea

serelated

stress

1944

ADL¼

activities

ofdaily

living

,ALS¼

amyo

trop

hic

lateral

sclerosis,

AP¼

aspiration

pne

umon

ia,

BANS¼

British

Artificial

Nutrition

Survey,

BI¼

Barthel

Index

,CA¼

canc

er,

chron¼

chronic,

compl.¼

completely,COPD¼

chronicob

structive

pulmon

arydisea

se,CVE¼

cerebrova

scular

even

t,Dys¼

Dyspha

gia,

EN¼

enteralnu

trition,

Gastrostomy,

HEN¼

home

enteralnu

trition,

LE¼

life

expec

tanc

y,Md¼

med

ian,

MN¼

malnu

trition,

M7SD¼

mea

n7stan

dard

dev

iation

,mon¼

mon

ths,

n.a.¼

notav

ailable,NG¼

nasoga

stric

tube,

neurol¼

neurolog

ical,op

.G.¼

operative

gastrostom

y,P¼

prospec

tive

,PEG¼

percu

tane

ousen

dosco

pic

gastrostom

y,PEJ¼

percu

tane

ousen

dosco

pic

jejuno

stom

y,R¼

retrospec

tive

.

D. Volkert et al.340

ARTICLE IN PRESS

ESPEN Guidelines on Enteral Nutrition 341

group) and 83% and 46%, respectively, wereseverely dependent in basic ADLs. The mortalityrate after one year was comparably low in bothgroups (22% and 12%, respectively). Bourdel-March-asson et al.60 (III) reported in a mixed population of108 severely dependent nursing home residents amortality rate of 14% in the PEG group vs. 10% inthe group without nutritional support. Gastroin-testinal and pulmonary complications were also notsignificantly different. The prevalence of dementiain the nursing home was reported to be 55% and ofstroke 19%. Specific prevalence data for the studygroup, however, are not given.

Two trials in dysphagic patients reach differentconclusions. Croghan et al.83 report no differencein mortality between 15 tube-fed and seven orallyfed nursing home residents suffering from aspira-tion, who underwent videofluoroscopic swallowingevaluation mainly because of stroke. Cowen et al.82

(III) recruited 149 severely ill hospital patients withdysphagia and compared the mortality of threesubgroups after one year: Death had occurred in60% of 80 patients who had received a PEG, in 10%of 18 patients who did not receive a PEG becausetheir clinical situation had improved in hospital,and in 78% of 51 patients who did not receive a PEGfor other reasons (28 had refused EN, 12 had diedbefore PEG placement, one patient was transferredto another hospital and 10 patients were fed via aNGT).

The study by Cowen et al.82 is an example of thedifficulty of all non-randomised controlled studies,i.e. there is a lack of comparability between theintervention and control group. The enterally fedpatients from almost all studies described aboveare probably not comparable with the patients inthe control group. The only exception is the studyfrom Rudberg et al.61 In the studies from Meieret al.81 and Murphy and Lipman84 the groups are notproperly described. In the non-randomised studies,the enterally fed patients obviously differed fromthose patients who did not receive EN—for avariety of reasons. The decision not to use EN isprobably linked to the status of the patients insome respects. Moreover, the heterogeneity ofgeriatric patient populations provides a multitudeof factors which may influence outcome, e.g. maindiagnosis, comorbidity, nutritional status and gen-eral condition, mood, various functional para-meters including cognition, vigilance, self-careability, mobility and continence which are presentat the same time in different combinations and to avarying extent.

Observational studies reporting mortality ofenterally fed elderly subjects focus on mortalityafter 30 days or after 1 year (Table 2). However,

comparisons between studies are generally difficultdue to the heterogeneous populations involved thatare often not properly characterised. In most of thestudies, between 10% and 30% of the participantsdied after 30 days. Lower mortality rates arereported by Abuksis et al.57 and Dwolatzkyet al.86 mainly in the demented elderly, byFinucane et al.92 and Horton et al.98 in geriatricpatients with predominantly cerebrovascularevents, and by Ciocon et al.25 in a mixed populationof elderly patients. Extremely high 30 day mortalityrates of 46% and 54% are described by Schneideret al.115 and Sanders et al.59 in the dementedelderly. One year after initiation of EN, mortalityrates between 15% and 90% are reported (Table 2).The highest as well as the lowest mortality rate isreported in demented patients59,62 (Compare 2.7).

Mitchell et al. who performed a meta-analysis ofseven controlled studies on mortality with orwithout PEG, draw the conclusion that the impactof TF on survival ‘‘is not known because the level ofevidence is limited’’.116 Further studies are neededin groups in whom nutrition may further reasonablybe expected to influence mortality.

2. EN in specific diagnostic groups

2.1. Is EN indicated in patients with under-nutrition?

Undernutrition and risk of undernutrition repre-sent essential and independent indications forEN in geriatric patients. ONS is recommended inorder to increase energy, protein and micronu-trient intake, maintain or improve nutritionalstatus, and improve survival in patients who areundernourished or at risk of undernutrition (A).ONS and/or TF are recommended early inpatients at nutritional risk (e.g. insufficientnutritional intake, unintended weight loss 45%in 3 months or 410% in 6 months, BMIo20 kg/m2) (B).

Comment: Undernutrition in geriatric patients isassociated with poor outcome. Essential signs ofundernutrition in the elderly are unintended weightloss 45% in 3 months or 410% in 6 months as wellas a BMI below 20 kg/m2. Risk of undernutrition isindicated by loss of appetite, reduced oral intakeand stress (physical as well as psychological).

In a Cochrane analysis of 49 studies including4790 randomised elderly patients with manifestundernutrition or risk of undernutrition, positiveeffects of ONS have been shown: there is increasein energy and nutrient intake, maintenance orimprovement of nutritional status and reduction of

ARTICLE IN PRESS

D. Volkert et al.342

mortality risk1 (Ia) (Compare 1.1, 1.2 and 1.6).ONS are, therefore, clearly recommended (A).Effects on functionality and quality of life are,however, uncertain (Compare 1.3 and 1.5).

The effects of TF in undernourished elderlypatients are unclear due to limited data. Veryoften TF is not initiated until advanced under-nutrition has developed, which is a clear impedi-ment to the success of nutritional therapy(Compare 1.2). Results from several studies how-ever, indicate maintenance or improvement ofnutritional parameters in undernourished elderlypatients after TF24–26 (III). Effects on functionalstatus and quality of life are uncertain (Compare1.3 and 1.5).

It is highly recommended to initiate nutritionalsupport, not only in manifest undernutrition, but assoon as there are indications of nutritional risk, andas long as physical activity is possible, EN—

together with rehabilitative exercise—can help tomaintain muscle mass (C). Early routine nutritionalscreening is mandatory. Several tools (e.g. ESPENguidelines,117 MNA118) are available for this pur-pose.

2.2. Is EN indicated in frail elderly?

In frail elderly, ONS are recommended in order toimprove or maintain nutritional status (A).

Frail elderly may benefit from TF as long as theirgeneral condition is stable (not in terminalphases of illness). TF is therefore recommendedearly in case of nutritional risk (B), wherenormal food intake is insufficient.

Comment: Frail elderly are limited in their ADL dueto physical, mental, psychological and/or socialimpairments a well as recurrent disease. Theysuffer from multiple pathology which seriouslyimpairs their independence. Therefore they are inparticular need of help and care and are vulnerableto complications. An inadequate intake of fluidsand nutrients is a common problem in thesesubjects. Frail elderly therefore are at high risk ofundernutrition and its serious consequences. Ex-perience has shown that the ability to eat sufficientamounts orally is inversely associated with theextent of frailty. Decreasing oral intake maytherefore be an indication of the progress orseverity of disease or frailty.

ONS lead to a significant increase in energy andnutrient intake as well as to a stabilisation orimprovement of nutritional status in mixed samplesof multimorbid elderly with acute and/or chronicdiseases, at home as well as in nursing homes andhospitals (Table 3). Effects on functional status andquality of life are uncertain due to limited data.

Effects on length of hospital stay and mortalityhave been investigated only occasionally. Potter etal.127 found a reduced length of hospital stay onlyin a subgroup of patients with adequate initialnutritional status. Data on mortality are contro-versial in frail elderly.8,127

Clinical experience shows that frail elderly, atnutritional risk, may benefit from TF as long as theirgeneral condition is stable. Observational studiesindicate a relatively good prognosis in tube-fed frailelderly nursing home residents with good healthstatus32,57 (III) (Table 2). Although data are scarce,it is recommended that nutritional support beinitiated early, as soon as there are indications ofnutritional risk and as long as physical activity ispossible since EN—together with rehabilitativeexercise—can help to maintain muscle mass (C).Nutritional screening has to be implemented as amatter of routine for early detection of risk ofundernutrition. Several tools (e.g. ESPEN guide-lines,117 MNA118) are available for this purpose.

TF is not recommended in frail elderly who haveprogressed to an irreversible final stage, e.g. withextreme frailty and advanced disease (irreversiblydependent in ADL, immobile, unable to commu-nicate, as well as high risk of death) (IV).

2.3. Is EN indicated in geriatric patients withneurological dysphagia?

In geriatric patients with severe neurologicaldysphagia, EN is recommended in order toensure energy and nutrient supply and, thus, tomaintain or improve nutritional status (A). Forlong-term nutritional support PEG should bepreferred to NGT, since it is associated with lesstreatment failures, better nutritional status (A),and it may also be more convenient for thepatient. In patients with severe neurologicaldysphagia TF has to be initiated as soon aspossible (C). EN should accompany intensiveswallowing therapy until safe and sufficient oralintake from a normal diet is possible (C).

Comment: In neurological dysphagia, nutritionaltherapy depends on the type and extent of theswallowing disorder. Nutritional therapy may rangefrom normal food, to mushy meals (modifiedconsistency), thickened liquids of different consis-tencies or total EN delivered via NGT or PEG.Nutritional therapy and swallowing therapy have tobe closely coordinated. Typical complications ofneurological dysphagia are aspiration with bronch-opulmonary infections136–139 and undernutrition,causing extended length of hospital stay andrecurrent hospitalisations.139–141 Mortality due todysphagia is significantly enhanced.139 Patients

ARTICLE IN PRESS

Table

3Oralsupplemen

tation

inmixed

coho

rtsof

frailelderly.

Article

Study

type

Patients

Supplements

Resu

lts

Firstau

thor

nAge

(yr)

Nutrition

alPlace

Energy

Protein

Duration

Intake

Nutrition

alstatus

Func

tion

alstatus

Qua

lity

oflife

M7SD

(ran

ge)

status

(kca

l/d)

(g/d

)

EProt

Cha

ndra

119

RCT

30(70–

84)

MN

Atho

me

Individ.

n.a.

4wks

n.a.

n.a.

Weigh

t+TSF+

Alb,PA

+im

mun

erespon

se+

n.a.

n.a.

Gray-Don

ald7

RCT

5078

BMI19

73

Atho

me

500–

700

17–26

12wks

(+)

n.a.

Weigh

t+skinfolds¼

AMC,CC¼

Han

dgrip¼

falls+

Well-

being¼

subjective

health¼

(460

)

Paye

tte3

RCT

8380

77

BMI20

73

Atho

me

500–

700

17–26

16wks

+(+)

Weigh

t+skinfolds¼

AMC,CC¼

Han

dgrip¼

mob

ility¼

days

inbed

+

‘‘Em

otiona

lrole

func

tion

ing’’+

(465

)

Volkert2

RCT

4685

MN

Atho

me

250

15.0

6mon

n.a.

n.a.

Weigh

ADL+

(inco

mplian

tsubgrou

p)

n.a.

(75–

98)

BMI19

72

Woo

46

RCT

8173

BMI20

75

Atho

me

500

17.0

1mon

++

Weigh

t+(m

)fatmass+

FFM+(m)

ADL+

activity+

men

talfunc

tion¼

appetite¼

slee

p+

n.a.

(465

)

Wou

ters

22

RCT

6882

BMI24

72

Nursing

home

250

8.8

6mon

++

weigh

t+

FFM,FM

,CC¼

Alb,PA¼

Han

dgrip¼

ADL¼

mob

ility¼

slee

p+

¼

(X65

)

Wou

ters

120

RCT

5583

BMI24

72

Nursing

home

250

8.8

6mon

n.a.

n.a.

Vit.C,E,

Cysteine+

Antiox.

capac

ity+

n.a.

n.a.

(X65

)

Ban

erjee1

21,122

RCT

6381

n.a.

Nursing

home

265

18.6

14wks

¼+

TSF+

Alb,Trf,

PA¼

%T-Lympho

cytes¼

Com

plemen

tC3¼

Skin

problems+

n.a.

(60–

98)

Bec

k123

RCT

1685

BMI20

(M)

Nursing

home

380

5.0

2mon

¼n.a.

weigh

n.a.

n.a.

(65–

96)

MNA17

–23

,5

Ek124

RCT

482

8028

.5%MN

Nursing

home

400

16.0

26wks

n.a.

n.a.

Skin

test+

n.a.

n.a.

Fiataron

e20

RCT

5088

71

BMI

25.5

(M)

Nursing

home

360

15.0

10wks

¼n.a.

Weigh

t+FF

FM(+)

Alb,Fe

,HDL¼

Vit.D,E,

Folate¼

ADL¼

depression¼

men

talfunc

tion¼

n.a.

(470

)

Han

key1

25

RCT

1481

72

weigh

t45

kg,Alb

33g/

L

Nursing

home

680

n.a.

8wks

+n.a.

weigh

t(+)

TSF,AMC

+Album

in¼

n.a.

n.a.

(475

)

ESPEN Guidelines on Enteral Nutrition 343

ARTICLE IN PRESS

Table

3(con

tinu

ed)

Article

Study

type

Patients

Supplements

Resu

lts

Firstau

thor

nAge

(yr)

Nutrition

alPlace

Energy

Protein

Duration

Intake

Nutrition

alstatus

Func

tion

alstatus

Qua

lity

oflife

M7SD

(ran

ge)

status

(kca

l/d)

(g/d

)

EProt

Larsson8

RCT

435

8029

%MN

Nursing

home

400

16.0

26wks

n.a.

n.a.

n.a.

n.a.

Lauq

ue53

RCT

3585

BMI22

71

Nursing

home

300–

500

20–30

60day

s+

+Weigh

t+Han

dgrip¼

MNA+

n.a.

(465

)MNA

17-23.5

Uno

sson

43

RCT

430

8026

%MN

Nursing

home

400

16.0

26wks

n.a.

n.a.

n.a.

Activity+

,mob

ility¼

men

talfunc

tion¼

gene

ralwell-being¼

n.a.

Hub

sch1

9RCT

7286

MN

Hospital

500

30.0

3wks

++

Weigh

FFM¼

BCM+

Alb,Trf,

RBP¼

Vit.B1,

C+

ADL(+)

n.a.

(75–

99)

McE

voy1

26

RCT

51n.a.

MN

Hospital

644

36.4

4wks

n.a.

n.a.

Weigh

t+TSF+,

AMC¼

Alb¼

n.a.

n.a.

Potter

127

RCT

381

83(M

d)

Non

-obese

hospital

540

22.5

Hospital

(Md17

day

s)+

n.a.

Weigh

t+AMC(+)

ADL+

(MN)

n.a.

(61–

99)

Bun

ker1

28

NRT

5880

BMI

24.4

(M);

Atho

me

200(in

under-

weigh

tpatients

300)

20.0

12wks

n.a.

n.a.

Alb,PA¼

,RBP+

Fe,Zn

,Se

+lympho

cyte-pop

ulations¼

skin

test

(+)

n.a.

n.a.

(70–

85)

19%o20

Ced

erho

lm55

NRT

2374

71

MN

Atho

me

400

40.0

3mon

n.a.

n.a.

Weigh

t+TSF,

AMC+

Alb,Orosomuc

oid¼

skin

test+

Han

dgrip+

pea

kflow¼

n.a.

BMI17

(M)

Bos

18

NRT

2379

MN

Hospital

400

30.0

10day

s+

+Weigh

t+FF

M+

Alb,Trf,

PA¼

CRP,

IGF-I¼

Immun

glob

ulin¼

Com

plemen

tC3¼

Han

dgrip

(+)

n.a.

(69–

90)

BMI

2173

Bou

rdel-M

.129

NRT

672

83Alb

3275

Hospital

400

30.0

15day

s+

+n.a.

Dec

ubitus

(+)

n.a.

(465

)

D. Volkert et al.344

ARTICLE IN PRESS

Cha

ndra

130

UCT

21460

MN

Atho

me

500

17.5

8wks

n.a.

n.a.

Alb,PA

,Trf,

RBP+

Zn+,

Ferritin¼

skin

test+

lympho

cyte

pop

ulations+

n.a.

n.a.

Gray-Don

ald131

UCT

1479

76

MN

Atho

me

500

KA

12wks

++

Alb

(+),

RBP,

Hb¼

lympho

cyte

coun

t+

Han

dgrip¼

Well-

being

+(4

60)

Lipschitz

132

UCT

1275

‘‘Highrisk’’

Atho

me

1050

39.0

16wks

++

Weigh

t+Alb,TIBC,Vit.+

Hb,metals¼

lympho

cyte

coun

skin

test¼

n.a.

n.a.

Harrill133

UCT

1889

(Md)

n.a.

Nursing

home

355

13,0

30day

s(+)

(+)

Vit.A,C,B1,

B2+

Alb,Hb,Ht,

Fe¼

n.a.

n.a.

Welch

134

UCT

1581

Alb

32g/

LNursing

home

n.a.

n.a.

6mon

++

Weigh

t+Alb,Hb,Ht+

Fe,TIBC,Trf¼

Dec

ubitus+

n.a.

Bou

rdel-M

.23

UCT

1187

MN

Hospital

400

30.0

4wks

¼¼

Weigh

t+musclemass¼

Alb+

Han

dgrip+

n.a.

BMI18

73

Joosten1

35

UCT

5083

76

BMI24

.574

Hospital

600

19.0

1376day

s+

n.a.

n.a.

n.a.

n.a.

Alb

3676g/

L

Katak

ity5

6UCT

12(71–

84)

n.a.

n.a.

204

9.0

12wks

n.a.

n.a.

Hb¼

Vit.C,D,B1

Han

dgrip+

men

talfunc

tion¼

dark

adap

tion¼

n.a.

ADL¼

activities

ofdaily

living

,Alb¼

album

in,AMC¼

arm

muscle

circum

ferenc

e,Antiox.¼

antiox

idative,

BCM¼

bod

yce

llmass,

BMI¼

bod

y-massindex

[Kg/

m2],

CC¼

calf

circum

ferenc

e,CRP¼

C-rea

ctiveprotein,E¼

energy,Fe¼

iron

,FF

fatfree

mass,FM¼

fatmass,Hb¼

hemog

lobin,

Ht¼

hematoc

rit,n.a.¼

notav

ailable,M¼

Mea

n,(m

male

participan

ts,Md¼

med

ian,

MN¼

malnu

trition,

MNA¼

MiniNutrition

alAssessm

ent,

mon¼

mon

ths,

NRT¼

non-rand

omised

trial,PA¼

prealbum

in,Prot¼

protein,RCT¼rand

omised

controlled

trial,

RBP¼

Retino

lbindingprotein,Re

f.¼

referenc

e,SD¼

stan

darddev

iation

,Se¼

Selen,

TIBC¼

totaliron

bindingca

pac

ity,

TSF¼

Tricep

sskinfold,Trf¼

Tran

sferrin,

UCT¼un

controlled

trial,Vit.¼

vitamin,wks¼

wee

ks,Zn¼

Zinc

.+improv

emen

tin

supplem

entedgrou

p(SG)co

mpared

toco

ntrolgrou

p(CG).

(+)tren

dtowardsim

prove

men

t,no

tsign

ifica

nt;¼

nodifferenc

eSG

–CG.

ESPEN Guidelines on Enteral Nutrition 345

ARTICLE IN PRESS

D. Volkert et al.346

with acute stroke and dysphagia often alreadyexhibit a poor nutritional status on hospital admis-sion, which negatively impacts on outcome andcosts: length of hospital stay is extended, rehabi-litation is delayed and survival is reduced.141–143

These results are confirmed by the current inter-national FOOD study.144

Controlled trials studying the effects of EN afterdysphagic stroke are not available, since controlgroups without nutritional support would be un-ethical. It is common sense, however, that energyand nutrient supply has to be ensured in thesepatients in order to maintain nutritional status andto avoid the development of undernutrition. Due tothe strong physiological plausibility based on thefact that patients with severe neurological dysphy-gia are not able to sustain their life withoutnutritional support, this recommendation wasrated at the highest level.

Nutritional status: In a Cochrane analysis ofinterventions for dysphagia in acute stroke ENdelivered via PEG was associated with a greaterimprovement of nutritional status when comparedto EN delivered via NGT.145 These results are basedon a randomised controlled trial conducted byNorton et al.11 (Ib) in 30 patients and on unpub-lished data from the authors of the Cochraneanalysis from 19 further patients. In anotherrandomised controlled trial in 40 patients withneurological dysphagia (mean age 60 years), thegroup receiving PEG also exhibited weight gain aswell as an increase in mean serum albumin andtransferrin. Due to a high drop out rate noevaluation was undertaken in the NGT group12 (Ib).

Functional status: Sanders et al.64 reported animprovement in ADL in 25 stroke patients (meanage 80 years) with EN via PEG (PEG placement onaverage 14 days after stroke). At the time of PEGplacement Barthel index was 0 points (completelydependent) in 84% of patients (mean 0.5 points).After 6 months of EN a mean increase of 4.8 pointswas observed. Six patients (24%) showed a clearimprovement (Barthel index increase from 0.5 to 9points). In 10 patients (40%), however, no or only aminimal improvement was observed (IIa).

Resuming oral nutrition: Dysphagia may bereversible in stroke patients.146 In various studiesbetween 4% and 29% of patients resumed full oralnutrition after 4–31 months11,92,93,95,112,115 (III)(Table 4). In the British Artificial Nutrition Survey(BANS) no difference between 65- and 75-year oldelderly people and younger adults (16–64 years)was found, although resumption of oral nutritionwas slightly reduced in the elderly above the age of75 years112 (Table 4). Schneider et al.115 report therate of resuming oral nutrition in different diag-

nostic groups of tube-fed patients at home. Among148 neurological patients with dysphagia (mean age75 years), 24% regained the ability to eat sufficientamounts orally within the study period of 2427494days.

Mortality: Clear statements about the effect ofEN on overall mortality after dysphagic stroke arenot possible since the investigated groups are tooheterogeneous, and control groups without nutri-tional support would be unethical (Compare 1.6).In the study of Norton et al.11 mortality after 6weeks was significantly lower in the PEG group thanin the group fed by NGT (12% vs. 57%), due probablyto the lower percentage of the prescribed intakereached in the latter. In the recent multicentreFOOD trial147 no difference in 6-month mortalitywas found between 162 dysphagic stroke patientswith PEG and 159 patients with NGT. However,these results are of limited value since only thosepatients were enrolled in whom the responsibleclinician was uncertain of the best feeding practice.Furthermore the duration of the intervention isunclear and there was a greater delay to first TF inthe PEG group than in the nasogastic group. Becauseof these methodological problems, results of theFOOD trial have to be interpreted with caution.

Timing of tube placement: In patients withsevere neurological dysphagia, TF has to beensured immediately unless there are compellingreasons against it. Studies investigating the role ofearly TF after acute cerebrovascular events in age-mixed samples have shown that early TF is feasiblealso in elderly patients148,149 and has a positiveimpact on survival148 and length of hospital stay144

(III). In a retrospective analysis of stroke patients(19% of patients 465 years) by Nyswonger andHelmchen,149 the group receiving TF within 72 hafter the cerebrovascular event had a reducedhospital stay compared to patients that received TFafter 72 h (III). Taylor148 found that patients, whohad spent less than 5 days without nutrient supply,had a lower mortality than patients who had morethan 5 days without nutrition. Interestingly, thisdifference was statistically significant only inpatients aged 465 years and was less distinct inyounger patients. The authors conclude that olderpatients react more sensitively to food deprivationthan younger patients and that TF should beinitiated as early as possible in this group (III).

In the recent multicentre FOOD trial147 nodifference in outcome was found between dyspha-gic stroke patients who received EN via a PEGwithin 7 days of hospital admission and anothergroup in whom TF was avoided for at least 7 days.Again, these results are of limited value because ofmethodological problems (see above).

ARTICLE IN PRESS

Table

4Re

sumingoral

nutritionafteren

teralnu

tritionin

elderly

patients.

Article

Study

Patients

TypeofEN

Proportion

resu

mingfull

oralnutrition(%

)

Tim

eperiod

Firstau

thor

Type

Place

nAge

(yr)

Prop

ortion

ofelderly

M7SD

(Ran

ge)

Neu

rologicdys

pha

gia

Finu

cane

92

PHospital

2882

(68–

99)

PEG

4%6mon

ths

Elia

112

PAtho

me

2970

—(X

75)

EN10

%12

mon

ths

Elia

112

PAtho

me

1230

—(65–

75)

EN15

%12

mon

ths

Norton1

1P

Hospital

1676

—PEG

19%

6mon

ths

Schn

eider

115

PAtho

me

148

75(M

d)

(1–97

)EN

24%

4mon

ths(M

)Wijdicks

95

RHospital

6374

(Md)

(41–

98)

PEG

28%

2–36

mon

ths

(Md4mon

ths)

James

93

RHospital

126

80(M

d)

(53–

94)

PEG

29%

4–71

mon

ths

Mixed

coho

rts

(Md31

mon

ths)

Quill87

RHospital

55470

(X70

)51

%480

yrNG

4%—

Clarkston

96

RHospital

4271

.4(33–

99)

PEG

7%2mon

ths

Dwolatzky8

6P

Hospital

122

—(X

65)

PEG

/NG

8%3mon

ths

Markg

raf1

03

RHospital

8469

714

(35–

98)

65%X65

yrPEG

12%

14–22

9day

s(M

108day

s)Markg

raf9

0R/P

Hospital

5487

(65–

94)

PEG

13%

14–22

9day

s(M

133day

s)Bussone

88

RHospital

155

84(70–

98)

PEG

14%

Larson

100

RHospital

314

—(3

–92

)66

%460

yrPEG

14%

Skelly

58

PHospital

7469

(Md)

(28–

90)

PEG

15%

6mon

ths

Tan1

09

RHospital

4465

(14–

94)

PEG

16%

1–44

mon

ths

How

ard113

RAtho

me

887

7978

(X65

)EN

17%

12mon

ths

Nicho

lson

104

RHospital

168

70(M

d)

(16–

96)

PEG

21%

4mon

ths(M

d)

Wolfsen

111

R/P

Hospital

201

66716

—PEG

/PEJ

21%

2757

353day

s(M

d14

4day

s)

Sali107

RHospital

3275

(38–

88)

PEG

22%

2–8mon

ths

Mitch

ell63

RAtho

me

551

87(M

d)

(65–

107)

TF

25%

12mon

ths

Taylor

110

PHospital

9776

.5(o

1–97

)PEG

25%

1day

–7yr

(Md32

7day

s)Abitbol

26

PHospital

5983

77

—50

%485

yrPEG

27%

12mon

ths

Verhoe

f78

PHospital

7166

718

(17–

89)

PEG

28%

12mon

ths

EN¼

enteralnu

trition,

mea

n,Md¼

Med

ian,

NG¼

nasoga

strictube,

prospec

tive

,PEG¼

percu

tane

ousen

dosco

pic

gastrostom

y,PEJ¼

percu

tane

ousen

dosco

pic

jejuno

stom

y,R¼

retrospec

tive

,SD¼

stan

darddev

iation

,TF¼

tube

feed

ing,

yr¼

years.

ESPEN Guidelines on Enteral Nutrition 347

ARTICLE IN PRESS

Table

5Su

pplemen

tary

overnigh

ttubefeed

ingin

elderly

frac

ture

patients.

Article

Patients

Supplement

Resu

lts

Firstau

thor

nAge�

(yr)

Diagn

osis

Energy

and

protein/d

ayDuration

Intake

Nutrition

alstatus

Clinica

lco

urse

Bastow13

58CG

80Fe

mur

neck

+100

0kcal

16–39

day

sTotalintake

mAnthrop

ometry

mADL¼

64SG

81frac

ture

&malnu

trition

+28gprot

Md26

day

sFo

odintake¼

Proteins

mLO

Rk

LOSk

Mortality

(k)

Hartgrink

14

67CG

8378

Hip

frac

ture

&risk

ofpressuresores

+150

0kcal

7an

d14

day

s,resp.

mDespitelow

toleranc

eIntend

edto

feed

:Alb,TP¼

Pressure

sores¼

only

40%tolerated

tube41wk

62SG

8477

+60gprot

Actua

llyfed:

Alb

m,TPm

Sullivan

15

10CG

7776

Hip

frac

ture

&go

odnu

tritiona

lstatus

+138

3kcal

1676day

sm

Alb,

tran

sferrin¼

Com

plica

tion

8SG

7572

+86gprot

ADL¼

LOS¼

In-hospital

mortality¼

6-mon

thsmortalityk

ADL¼

activities

ofdaily

living

,Alb¼

album

in,CG¼

controlgrou

p,LO

leng

thof

reha

bilitation

,LO

leng

thof

stay,Md¼

med

ian,

prot¼

protein,SG¼

Supplemen

tedgrou

p,

TP¼

totalprotein,yr¼

years.

mincrea

se,k

dec

rease(orim

prove

men

tin

thesupplmen

tedgrou

pco

mpared

totheco

ntrolgrou

p);¼

nodifferenc

ebetwee

nthegrou

ps.

�Mea

nor

mea

n7stan

dard

dev

iation

.

D. Volkert et al.348

ARTICLE IN PRESS

ESPEN Guidelines on Enteral Nutrition 349

In earlier studies, long periods of 44–63 daysbetween the acute event and PEG placement arenoticeable.91,93,107 Three studies on the naturalcourse of dysphagia after stroke show that sponta-neous remission of the swallowing difficulty occurs7–14 days after the acute event in 73–86%.150–152

Based on clinical experience, prognosis of dyspha-gia seems to be better in medial cerebral infarctthan in brain stem infarct (IV). If severe dysphagiapersists longer than 14 days after the acute event,a PEG should be placed immediately. Controlledtrials on the ideal timing and length of TF inneurological dysphagia, that also consider thevarying kinds and extents of swallowing disorders,are still not available.

2.4. Is EN indicated after orthopaedic surgery ingeriatric patients?

ONS are recommended in geriatric patients afterhip fracture and orthopaedic surgery in order toreduce complications (A).

Comment: Voluntary oral intake is often insuffi-cient to meet the enhanced requirements ofenergy, protein and micronutrients after orthopae-dic surgery. Rapid deterioration in nutritionalstatus, and impaired recovery and rehabilitationare common.

The results of several randomised studies of ENafter hip fracture are summarised in a Cochraneanalysis75 that includes eight trials testing supple-mentary overnight TF, five trials with ONS and threestudies regarding the effects of supplementary oralprotein. The quality of most of the studies and theavailability of outcome data were considered poorby the authors of the Cochrane analysis.75 Inaddition, a recent randomised controlled study153

and two non-randomised trials with ONS areavailable.4,6,154

Energy and nutrient intake: Administration ofONS leads to a significant increase in energy andnutrient intake.75 However, several trials71,74,155

have shown that the daily requirements for energyand protein are still not met. This may be due topoor compliance of less than 20%,7 to intolerance ofsupplements by some patients,155 and to require-ments being markedly increased.

Supplementary overnight TF enables the admin-istration of larger amounts of enteral formu-lae,13–15 but is of limited tolerance in practice. Inthe trial of Hartgrink et al.14 only 40% tolerated thisintervention longer than 1 week and only one-quarter for the whole study period of 2 weeks.

Nutritional status: Information about the effectsof ONS on nutritional status is sparse and incon-sistent. Delmi et al.71 observed a larger increase in

albumin and transferrin levels in supplementedpatients than in the unsupplemented control group(Ib), whereas Lawson et al.154 and Williams et al.6

detected no difference with respect to serumalbumin (IIa). In the study of Lawson et al.154 BMIand mid-arm muscle circumference (MAMC) werealso unaffected, however transferrin and haemo-globin decreased less than in the unsupplementedgroup. Williams et al.6 reported a positive effect ontriceps skinfold thickness (TSF) and MAMC in thesupplemented group. In contrast Tidermark et al.44

registered weight loss, and Brown and Seabrock74

observed decreases in body weight, mid-armcircumference (MAC) and TSF in the supplementedas well as in the control group.

Positive effects of protein supplementation onbone density and parameters of bone metabolismwere described by Tkatch et al.72 and Schurchet al.73 (Ib). A 6-month administration of protein-enriched supplements led to a significant attenua-tion of loss of bone mineral density when comparedto the control group. Even short-term supplemen-tation (o40 days) was accompanied by a smallerdecrease in proximal femur bone mineral densitythan in the unsupplemented group. However, otherskeletal sites were unaffected. Moreover, proteinrepletion was shown to be associated with anincrease in serum osteocalcin72 and insulin-likegrowth factor-I,73 both of which are importantmediators of bone metabolism.

The effect of supplementary overnight TF onnutritional status of elderly patients with eitherhip or femoral neck fracture was investigated inthree randomised controlled studies13–15 (Ia)(Table 5). Initial nutritional status as well as resultswere inconsistent. Clear improvements were re-ported by Bastow et al.13 who divided theirpatients into ‘‘thin’’ and ‘‘very thin’’ according toanthropometric measurements. In both interven-tion groups (‘‘thin’’ and ‘‘very thin’’), anthropo-metric parameters (body weight, TSF, MAC)and postoperative prealbumin increased during16–39 days. ‘‘Very thin’’ patients had the greatestbenefit from the nutritional therapy. No change inserum albumin was observed in the study ofHartgrink et al.14 in 62 patients intended to receivesupplementary TF. An evaluation of the actuallytube-fed patients however (n ¼ 25 after 1 week,n ¼ 16 after 2 weeks), revealed increased serumconcentrations of albumin and total protein. Noeffects on plasma proteins were reported in thestudy of Sullivan et al.15 who examined patientswith a relatively good nutritional status (BMI24.1 kg/m2, albumin 32 and 35 g/l, respectively),with respect to albumin, transferrin and cholester-ol values.

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D. Volkert et al.350

Length of hospital stay: Data concerning thelength of hospital stay are inconsistent. Delmi etal.71 found a significantly shorter length of hospitalstay (including rehabilitation) in patients receivingONS (median 24 days) compared to control patients(median 40 days) (Ib). Protein administration in thetrials of Tkatch et al.72 and Schurch et al.73 wasalso associated with a significantly reduced lengthof stay (30 and 21 days, respectively). In five otherstudies, however, the observed differences werenot significant.44,75

A positive impact of supplementary overnight TFon the length of hospital stay of geriatric patientsafter hip or femur neck fracture cannot be firmlyconcluded from the data available.13–15

Functional status: Data regarding functionalstatus are heterogeneous and unsatisfactory. TheCochrane analysis of Avenell and Handoll75 refers tofour studies investigating this aspect. Only one ofthem showed positive effects of ONS on ADL-functions after 6 months.44 The non-randomisedtrial of Williams et al.6 showed a trend towardsimproved mobility and greater independence athospital discharge in supplemented patients. Oralsupplementation of calcium, protein and vitaminsin the study of Espaulella et al.47 showed nosignificant changes in mobilisation, ADL status anduse of walking aids when compared to the controlgroup receiving an isocaloric placebo as well.

Bastow et al.13 assessed the time between thepatient0s operation and the achievement of phy-siotherapy goals (e.g. recovering independent mobi-lity). Thin patients (according to anthropometricmeasurements; see above) receiving supplementaryovernight TF, achieved independent mobility in 10days, while thin control patients did so in 12 days.Very thin patients from the intervention groupreached this goal after 16 days whereas very thincontrol patients needed 23 days to regain indepen-dent mobility (Po0:05) (IIa). ADL status at discharge,however, was not affected by the intervention.13

Postoperative complications and mortality: ONShave a positive impact on the rate of postoperativecomplications. Thus, Lawson et al.154 in theirrecent non-randomised study found a significantlylower rate of complications in post-operativelysupplemented orthopaedic patients than in thoseunsupplemented (IIa). In the study of Tkatch etal.72 the complication rate in protein supplementedpatients was significantly lower during hospitalstay, as well as 7 months later, compared to thecontrol group with isocaloric placebo. The pooledanalysis of five randomised studies in the meta-analysis of Avenell and Handoll75 revealed aborderline reduction of the risk of complicationsin supplemented patients (RR 0.61, 95% CI

0.36–1.03). When risks for mortality and complica-tions were combined in these five studies, thechances of an unfavourable outcome were reducedin supplemented patients (RR 0.52, 95% CI0.32–0.84)72 (Ia).

If mortality was considered separately in themeta-analysis of five studies with ONS, no reductionin mortality risk was found.75 The same was true inthe study of Espaulella et al.47 Combining mortalityoutcome of all the studies with supplementaryovernight TF did not produce a significant riskreduction either (RR 0.99; 95% CI 0.5–1.97).75 Thepooled analysis of studies using ONS or overnight TFin geriatric patients with either hip or femoral neckfracture also did not show a significant reduction ofmortality risk in the enterally fed patients whencompared to controls (RR 0.94; 95% CI 0.59–1.50).75

2.5. Is EN indicated in the perioperative phase ofmajor surgery in geriatric patients?

There is no evidence that nutritional therapy inelderly patients undergoing major surgery (e.g.pancreatic surgery, head and neck surgery)should be different from that in younger pa-tients. We therefore refer to the Guidelines.‘‘Surgery and transplantation’’.

It is generally recognised, however, that elderlyare at higher risk of being undernourished thanyounger patients and restoration of BCM is moredifficult. Therefore, preventive nutritional supporthas to be considered.

2.6. Is EN indicated in elderly patients withdepression?

EN is recommended in depression in order toovercome the phase of severe anorexia and lossof motivation (C).

Comment: Depression is common in elderly pa-tients, but often not recognised due to thedifficulty of discriminating it from other symptomsof old age. Anorexia and refusal to eat are integralsymptoms of this disease, and depression is there-fore regarded as a major cause of undernutrition inthe elderly.156 Undernutrition may itself contributeto the depressive states often seen in theelderly.157 Depression can be treated by severalmethods, especially by drugs, although this maytake some time to be effective. Based on positiveclinical experience and expert opinion, EN isrecommended in the elderly suffering from depres-sion in order to support the patient during the earlyphase of severe anorexia and loss of motivation,thereby preventing the development of under-nutrition with its serious consequences (C).

ARTICLE IN PRESS

Table

6Prev

alen

ceof

aspirationpne

umon

iain

tube-fedelderly

patients.

First

author

Studytype

Patients

Aspirationpneumonia

(AP)

nAge�

(yea

rs)

Diagn

oses

Before

After

Timeperiod

Patel160

P24

72CVE,

CA,dem

entia

58%

14/2

4(58%

)(all)

UntilAPor

dea

th12

/14(86%

)(w

ithAP)

Paillaud

35

R73

8379

Mixed

15%

53%

2,6,

12mon

ths

Sali107

P32

75Mixed

9%— 3/

5(60%

)dea

thsdue

toAP

2–48

8day

s

Abitbol

26

P59

8377

Nursing

homeresiden

ts49

%51

%

30day

s

Bae

ten1

61

P90

72CA,ne

urolog

ical

disea

se—

6%

12mon

ths

Wijdicks

95

P63

74Apop

lex

—16

%

Hospital

stay

Peschl

151

P33

76Cereb

raldysfunc

tion

s—

18%

2–36

mon

ths

Kaw

36

R46

74Neu

rologica

ldisea

se,dem

entia

—22

%6mon

ths

Stua

rt108

R12

570

CA,dem

entia,

cach

exia

—28

%12

,18

mon

ths

Bou

rdel-M

arch

asson6

0R

4681

79

Mixed

—39

%30

day

s

Fay2

7R

8070

Apop

lex,

dem

entia,

PEG

—6%

/32%

14/1

92day

s

2970

Parkinson

NG

—24

%/4

6%14

/141

day

s

Golden

32

R10

289

76

dem

entia

—51

%6mon

ths

AP¼

aspirationpne

umon

ia,CA¼

carcinom

a,CVE¼

cerebrova

scular

even

t,NG¼

nasoga

strictube,

prospec

tive

,R¼

retrospe

ctive.

�Mea

nor

mea

n7stan

dard

dev

iation

.

ESPEN Guidelines on Enteral Nutrition 351

ARTICLE IN PRESS

D. Volkert et al.352

2.7. Is EN indicated in dementia?

ONS or TF may lead to an improvement innutritional status in demented patients. In earlyand moderate dementia ONS—and occasionallyTF—may contribute to ensuring an adequateenergy and nutrient supply and to preventingundernutrition from developing; they are there-fore recommended (C). In those with terminaldementia, TF is not recommended (C). Thedecision in each case must be made on anindividual basis.

Comment: An indequate intake of energy andnutrients is a common problem in dementedpatients. Undernutrition may be caused by severalfactors including anorexia (common cause: poly-pharmaco-therapy), insufficient oral intake (for-getting to eat), depression, apraxia of eating or,less often, enhanced energy requirement due tohyperactivity (constant pacing).158 In advancedstages of dementia, dysphagia may develop andmight be an indication for EN in a few cases.

Some studies with ONS have shown improve-ments in body weight (Ib)49,159 (IIa)50. In tube-feddemented elderly patients, two studies reportedweight gain31,32 (III), but two others reported nochange (III)24 (IIb)86. Available trials regarding theeffects of ONS (Ib)49 (IIa)50 or TF24,33,36 onfunctional status, report no improvement (Com-pare 1.5). In terms of survival most studies show nobenefit.33,81,84,94 On the other hand, Rudberg etal.61 described lower mortality, compared to con-trols, at 30 days and 1 year in enterally fed patientswith severe cognitive impairment (IIb). Very lowmortality rates have been reported in PEG-feddemented nursing home residents.32,57,62 On theother hand, in one retrospective study comparingmortality rates in different diagnostic groups,outcome was worst among the demented59 (III).

In conclusion, tube-fed demented patients varyconsiderably with respect to their prognosis. Out-come and also the success of nutritional therapy indemented patients are strongly influenced by theseverity of disease, the kind and extent ofcomorbidities and by their general condition. It istherefore recommended that adequate and highquality nutrition is ensured, especially in the earlyand middle stages of dementia, in order to preventundernutrition developing and to help maintain astable general condition (C).

TF may be useful in some demented patients.The following aspects have to be considered indecision-making:

presumed or previously expressed wishes of thepatient with respect to TF;

severity of the disease; � the individual prognosis and life expectancy of

the demented patient;

� the anticipated quality of life of the patient with

or without TF;

� the anticipated complications and impairments

due to TF;

� the mobility of the patient.

The decision for or against TF has always to bemade individually and together with relativesand care givers, legal custodian, family doctorand therapists, and in case of doubt, with legaladvice.

For patients with terminal dementia (irreversi-ble, immobile, unable to communicate, completelydependent, lack of physical resources) TF is notrecommended (C).

2.8. Is EN indicated in geriatric patients withcancer?

In principal, nutritional therapy in geriatricpatients with cancer does not differ from young-er cancer patients (see Guidelines on ‘‘Non-surgical oncology’’).

Comment: It is generally recognised, however, thatelderly are at higher risk of being undernourishedthan younger patients and restoration of BCM ismore difficult. Therefore, preventive nutritionalsupport has to be considered.

2.9. In patients with dysphagia does TF preventaspiration pneumonia by improving functionalstatus?

Due to the heterogeneity of the studies, and lackof data on prevalence before the TF, firmconclusions can not be drawn.

Comment: Dysphagia may enhance aspiration frompharyngeal contents, but, on the other hand, TFmay enhance reflux and aspiration of gastriccontents. Several studies have reported the pre-valence of aspiration pneumonia in tube-fedelderly patients (Table 6). Due to the heterogeneityof patient groups and lack of data on theprevalence of aspiration before TF, it is difficultto draw any firm conclusion whether bypassingdysphagia, using a NG tube or PEG helps to reducethe incidence of pneumonia. It certainly has thepotential to increase reflux and aspiration. Dataabout the incidence of aspiration pneumonia duringnutritional support via PEG compared to NGT arecontroversial.12,27,86,161 It is also not proven thatsurgical or endoscopic jejunostomy prevents thiscomplication.

ARTICLE IN PRESS

Table

7PEG

versus

nasoga

strictubefeed

ingin

elderly

patients.

First

author

Study

type

nAge�

(years)

Diagn

oses(place

)Duration

Treatment

failure

Intake

Nutritional

status

Aspiration

Other

complica

tions

Mortality

LOS

Bae

ten1

61

P44

PEG

72710

Mixed

(hospital)

18720

day

sk

n.a.

n.a.

¼n.a.

n.a.

n.a.

RCT

46NG

Norton1

1P

16PEG

76Apop

lexia

(hospital)

6wks

km

mn.a.

n.a.

kk

RCT

14NG

79

Park

12

P20

PEG

5675

Neu

rolog.

dyspha

gia

(hospital)

4wks

km

/m¼

/mn.a.

n.a.

RCT

20NG

6573

Dwolatzky8

6P

32PEG

85Chron

ic,

mixed

(hom

e)

4wks/1

2wks

kn.a.

¼/m

kn.a.

NRT

90NG

82

Fay2

7R

80PEG

70.2

Mixed

(hospital)

1427

192

day

sk

n.a.

¼k

¼¼

n.a.

NRT

29NG

68.8

LOS¼

leng

thof

stay,n.a.¼

notav

ailable,NG¼

nasoga

strictube,

NRT¼

non-rand

omised

trial,

PEG¼

percu

tane

ousen

dosco

pic

gastrostom

y,P¼

prospec

tive

,R¼

retrospec

tive

,RCT¼rand

omised

controlled

trial,Re

f.¼

referenc

e,wks¼

wee

ksm

increa

se,k

dec

rease(improv

emen

tin

thePEG

-group

compared

totheNG-group

);¼

nodifferenc

ebetwee

nPEG

andNG.

�Mea

nor

mea

n7stan

dard

dev

iation

.

ESPEN Guidelines on Enteral Nutrition 353

ARTICLE IN PRESS

D. Volkert et al.354

2.10. Can EN prevent or improve pressure ulcersin geriatric patients?

ONS, particular high protein ONS, can reduce therisk of developing pressure ulcers (A). Based onpositive clinical experience, EN is also recom-mended in order to improve healing of pressureulcers (C).

Comment: Adequate nutrition is a prerequisite forpreventing and healing pressure ulcers. Studiesaddressing this topic are difficult to conductbecause of the multifactorial origin of pressureulcers, various uncontrollable factors affecting thedevelopment of pressure ulcers and the necessarilylong observational periods. Only few trials areavailable examining the effects of EN on preventionor healing of decubitus ulcers. These trials varygreatly with respect to study design, patientpopulation and reported outcome variables.

A recent meta-analysis of four randomised con-trolled trials showed that oral nutritional supple-mentation was associated with a significantly lowerincidence of pressure ulcer development in at-riskpatients compared to routine care (odds ratio (OR)0.75; 95% CI 0.62–0.89)162 (Ia). Three of the fourstudies used high protein ONS (30 energy percent).Three other studies, which were not meta-analy-sable, showed a trend towards improved healing ofexisting pressure ulcers in patients receivingONS.162

Available studies on the effect of TF do not showsignificant effects, neither on healing nor onprevention of decubitus ulcers,14,26,31,60,62 how-ever, overall quality of the studies is poor.

The importance of protein in pressure sorehealing was suggested in an 8-week non-rando-mised study in 28 undernourished nursing homeresidents with decubitus ulcers.163 The administra-tion of a TF formula with 61 g protein per litre (24energy percent) was more successful in decreasingtotal pressure ulcer surface area than a TF formulawith 37 g protein per litre (14 energy percent).

Clinical experience suggests that wound healingin elderly patients may be improved by theadministration of supplements containingprotein and micronutrients that are involved inwound healing (zinc, arginine, carotenoids, vita-mins A, C and E). Crucial for the effect of thesenutrients is the local circulation in the pressureulcer area, which determines effective nutrienttransport and local metabolism as well as removalof toxic cell products. Besides the correction ofnutrient deficiencies, the correct positioning of thepatient to allow optimal blood circulation to thepressure area and to minimise further tissuedamage is crucial.

3. Special practical aspects of EN in

geriatric patients

3.1. How should EN be delivered: by PEG or byNGT?

In elderly patients in whom EN is anticipated forlonger than 4 weeks, placement of a PEG tube isrecommended (A).

Comment: Five studies (four prospective, threerandomised) comparing PEG with NGT, show thesuperiority of PEG (Table 7) in allowing the admin-istration of greater amounts of energy and nutrientsover longer periods, resulting in better nutritionalstatus (Ib)11,12 (IIa)86 The use of NGT is associatedwith more tube displacements86 (IIa) and more re-insertions (Ib)12,161 (III)27. Less treatment failureswith PEG are reported in all studies (Ib)11,12,161

(IIa)86 (III)27. Moreover, fewer fixations are necessaryin PEG patients, and the management is easier bothfor patients and nursing staff161 (Ib).

Improved survival in PEG-fed patients was ob-served in one randomised controlled trial and onenon-randomised trial (Ib)11 (IIa)86. In their retro-spective study, however, Fay et al.27 found nodifference in mortality between PEG- and NGT-fedpatients. Dwolatzky et al.86 (IIa) and Fay et al.27

(III) reported a lower incidence of aspiration inpatients fed by PEG than by NGT. However, Parket al.12 and Baeten and Hoefnagels161 found nodifference in aspiration rates in their randomisedstudies. In geriatric patients the frequent combina-tion of neurological swallowing difficulties withcognitive impairment (dementia, Parkinson’s dis-ease, recurrent cerebrovascular events) is asso-ciated with a higher risk of aspiration. In thesesituations, early PEG placement compared to NGTmight be advantageous.

An important aspect of PEG in patients withneurological dysphagia is that it allows moreeffective swallowing therapy without interferenceby NGT. As swallowing improves, TF can be reducedas oral intake increases, and in many cases it can becompletely abandoned.

3.2. When should TF be initiated after PEGplacement?

TF can be initiated 3 h after PEG placement ingeriatric patients (A).

Comment: In three randomised prospective studiesthat included elderly patients, early feeding (3–4 hafter PEG placement) vs. delayed feeding (24 hafter PEG placement) was studied164–166 (Ib).Tolerance and safety were equal whether nutritionwas initiated 3 or 24 h after PEG placement.164,165

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ESPEN Guidelines on Enteral Nutrition 355

Another study comparing initiation of nutrition 4vs. 24 h after PEG placement, also found nosignificant differences between the two groups.166

These results confirm early feeding after PEGplacement as a safe and effective procedure inelderly patients.

3.3. Is EN in geriatric patients associated withspecific complications?

Complications of EN are similar to those in otherage groups. There is no information availableabout the prevalence of specific complications indifferent age groups.

3.4. Is dietary fibre beneficial for enterally fedgeriatric patients?

Available studies suggest that dietary fibre cancontribute to the normalisation of bowel func-tions in elderly tube-fed subjects (B).

With respect to ONS no studies are available.

Comment: Elderly patients often suffer fromgastrointestinal problems, including constipationand diarrhoea. The effect of dietary fibre in ONS onbowel function has not been studied. Since dietaryfibre intake from food is usually low in geriatricpatients, fibre-containing products are generallyrecommended.

Few studies of the effects of fibre-containingenteral formulae on bowel function in elderlysubjects are available.167–172 Despite great differ-ences in study populations, gastrointestinal pro-blems and the type and amount of fibre used, thesestudies all report that fibre helps to normalisebowel functions during TF.

In a randomised cross-over study design with 10long-term tube-fed elderly patients recoveringfrom stroke without diarrhoea the administrationof 28.8 g soy/oat fibre per day (14.4 g/l) signifi-cantly increased the number of bowel movementsper day (0.970.4 vs. 0.570.2, Po0:05) and faecalweights (57731 vs. 32725 g/d, Po0:05)167 (Ib). Arandomised pilot study with seven immobile long-term care residents on long-term TF also reportedmore stools with a softer consistency168 (III).

In long-term care patients with diarrhoea ENwith 12.8 g soy fibre/1000 kcal resulted in signifi-cantly fewer reports of diarrhoea (6 vs. 26,Po0:01) and markedly improved bowel functioncompared with the control group without fibre169

(Ib). In a prospective observational study with 20elderly bedridden patients (mean age 7975 years)with diarrhoea, receiving EN due to cerebrovascu-lar events, Nakao et al.170 demonstrated thatsoluble fibre decreased the frequency of daily

bowel movements significantly and simultaneouslyimproved faecal features in the course of 4 weekswith gradually increasing fibre administration from7 to 28 g/d (III). A retrospective chart review in 50long-term care patients with mixed diagnoses (age28–83 yr, median age 71 yr) who received EN with14 g soy polysaccharides/l for at least 3 weeks alsoresulted in fewer loose stools and diarrhoea than inpatients given a fibre-free solution171 (III). Homannet al.172 investigated the effects of 20 g partiallyhydrolised guar gum/l in a prospective, randomisedcontrolled trial with 100 surgical and medicalpatients. About 30 patients (mean age 60 years,mainly gastric or oesophageal resection) receivedtotal EN and 70 patients (mean age 69 years, mainlymetastatic malignancies) received supplementaryEN. In patients receiving total EN with fibre and inthe whole group receiving fibre the incidence ofdiarrhoea was significantly lower than in patientsreceiving the standard diet without fibre.

In order to increase tolerance and avoid gastro-intestinal side-effects such as bloating and flatu-lence, the mode of administration (rate,temperature) is important. In subjects not used todietary fibre intake, fibre fortified feedings shouldbe added gradually.

Since different kinds of fibre may have dissimilareffects in different clinical situations, furtherstudies are necessary to elucidate the role ofspecific types of dietary fibre in enterally fedgeriatric patients.

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