Advertisement

Nutrition-Focused Care for Community-Living Adults: Healthcare Utilization and Economic Benefits

Open AccessPublished:September 10, 2022DOI:https://doi.org/10.1016/j.vhri.2022.08.005

      Highlights

      • Among hospitalized adults, especially those of older age, nutrition-focused care can improve health outcomes while lowering costs, yet few studies have evaluated the impact of nutritional care for community-living older adults from the perspective of healthcare cost savings.
      • This is a first-of-its-kind study to assess the impact of nutrition-focused care for older community-living adults who were identified as at risk/malnourished in Colombia. Using real-world findings from a study of patients receiving outpatient care, we used economic modeling to do budget impact and cost-effectiveness analyses. Our results provided robust evidence supporting both health and economic benefits of improving nutritional care for older adults living in the community.
      • Our results showed that nutrition-focused care significantly reduced overall use of healthcare resources (hospitalizations, emergency department visits, and outpatient clinic visits) by more than 40%. Modeling revealed that a $210 per-patient net cost savings could be attributed to nutrition-focused outpatient care over the 90-day study period. Our evidence of value in nutritional care can help guide health policy and decision makers aiming to reduce the burden of healthcare costs in the aging Colombian population.

      Abstract

      Objectives

      We assessed the impact of a recently reported nutritional quality improvement program (QIP) on healthcare resource utilization and costs for older, community-living adults in Bogotá, Colombia.

      Methods

      The study included 618 community-dwelling, older adults (> 60 years) who were at risk or malnourished and receiving outpatient clinical care. The intervention was a QIP that emphasized nutritional screening, dietary education, lifestyle counseling, 60-day consumption of oral nutritional supplements, and 90-day follow-up. For economic modeling, we performed 90-day budget impact and cost-effectiveness analyses from a Colombian third-party payer perspective. The base-case analysis quantified mean healthcare resource use in the QIP study population. Analysis was based on mean input values (deterministic) and distributions of input parameters (probabilistic). As the deterministic analysis provided a simple point estimate, the cost-effectiveness analysis focused on the probabilistic results informed by 1000 iterations of a Monte-Carlo simulation.

      Results

      Results showed that the total use of healthcare resources over 90 days was significantly reduced by > 40% (hospitalizations were reduced by approximately 80%, emergency department visits by > 60%, and outpatient clinical visits by nearly 40%; P < .001). Based on economic modeling, total cost savings of $129 740 or per-patient cost savings of $210 over 90 days could be attributed to the use of nutritional QIP strategies. Total cost savings equated to nearly twice the initial investment for QIP intervention; that is, the per-dollar return on investment was $1.82.

      Conclusions

      For older adults living in the community in Colombia, the use of our nutritional QIP improved health outcomes while lowering costs of healthcare and was thus cost-effective.

      Keywords

      Introduction

      Among older adults living in communities worldwide, poor nutritional status is distressingly common, and malnutrition risk is increasingly recognized for its high toll on the health and well-being of older people.
      • Rodriguez-Sanchez B.
      • Sulo S.
      • Carnicero J.A.
      • Rueda R.
      • Rodriguez-Manas L.
      Malnutrition prevalence and burden on healthcare resource use among Spanish community-living older adults: results of a longitudinal analysis.
      • Sharman Moser S.
      • Doyev R.
      • Cohen B.
      • et al.
      Prevalence and characteristics of malnutrition among community-dwelling older adults in Israel.
      • Ahmed T.
      • Haboubi N.
      Assessment and management of nutrition in older people and its importance to health.
      • Agarwal E.
      • Miller M.
      • Yaxley A.
      • Isenring E.
      Malnutrition in the elderly: a narrative review.
      In the older population, the prevalence of malnutrition or its risk varies widely by location, age, and chronic health conditions—a range reported as 1.3% to 47.8%.
      Evidence profile: malnutrition. World Health Organization.
      Overall, up to 1 in 3 community-dwelling older people may have poor nutritional status, such as dietary protein-energy shortfall or nutrient deficiencies.
      • Rodriguez-Sanchez B.
      • Sulo S.
      • Carnicero J.A.
      • Rueda R.
      • Rodriguez-Manas L.
      Malnutrition prevalence and burden on healthcare resource use among Spanish community-living older adults: results of a longitudinal analysis.
      ,
      • Kaiser M.J.
      • Bauer J.M.
      • Ramsch C.
      • et al.
      Frequency of malnutrition in older adults: a multinational perspective using the mini nutritional assessment.
      • Ramage-Morin P.L.
      • Gilmour H.
      • Rotermann M.
      Nutritional risk, hospitalization and mortality among community-dwelling Canadians aged 65 or older.
      • Wolters M.
      • Volkert D.
      • Streicher M.
      • et al.
      Prevalence of malnutrition using harmonized definitions in older adults from different settings - a MaNuEL study.
      • Sulo S.
      • Schiffer L.
      • Sheean P.
      • Farrar I.
      • Partridge J.
      • Fitzgibbon M.
      Community-dwelling adults at nutrition risk: characteristics in relation to the consumption of oral nutritional supplements.
      • Wei J.M.
      • Li S.
      • Claytor L.
      • Partridge J.
      • Goates S.
      Prevalence and predictors of malnutrition in elderly Chinese adults: results from the China Health and Retirement Longitudinal Study.
      Malnutrition risk leads to loss of muscle and bone mass; accordingly, poorly nourished older people are at increased risk of falls and fractures, have mobility limitations, and experience disabilities that lower their capacity for independent living and even threaten survival.
      • Rodriguez M.G.
      • Sichaca E.G.
      Mortality due to malnutrition in older adults, Colombia, 2014-2016. [Mortalidad por desnutricion en el adulto mayor, Colombia, 2014-2016].
      • Jyvakorpi S.K.
      • Ramel A.
      • Strandberg T.E.
      • et al.
      The sarcopenia and physical frailty in older people: multi-component treatment strategies (SPRINTT) project: description and feasibility of a nutrition intervention in community-dwelling older Europeans.
      • Wanaratna K.
      • Muangpaisan W.
      • Kuptniratsaikul V.
      • Chalermsri C.
      • Nuttamonwarakul A.
      Prevalence and factors associated with frailty and cognitive frailty among community-dwelling elderly with knee osteoarthritis.
      Among seniors with poor nutritional status, growing evidence also shows high use of healthcare resources (eg, outpatient clinic care, hospitalizations, and emergency department [ED] visits) and correspondingly high costs for such care.
      • Rodriguez-Sanchez B.
      • Sulo S.
      • Carnicero J.A.
      • Rueda R.
      • Rodriguez-Manas L.
      Malnutrition prevalence and burden on healthcare resource use among Spanish community-living older adults: results of a longitudinal analysis.
      ,
      • Guest J.F.
      • Panca M.
      • Baeyens J.P.
      • et al.
      Health economic impact of managing patients following a community-based diagnosis of malnutrition in the UK.
      ,
      • Snider J.T.
      • Linthicum M.T.
      • Wu Y.
      • et al.
      Economic burden of community-based disease-associated malnutrition in the United States.
      Numerous studies have shown health and cost benefits of nutritional care for poorly nourished patients who were hospitalized,
      • Schuetz P.
      • Sulo S.
      • Walzer S.
      • et al.
      Cost savings associated with nutritional support in medical inpatients: an economic model based on data from a systematic review of randomised trials.
      • Sriram K.
      • Sulo S.
      • VanDerBosch G.
      Malnutrition intervention implementation.
      • Buitrago G.
      • Vargas J.
      • Sulo S.
      • et al.
      Targeting malnutrition: nutrition programs yield cost savings for hospitalized patients.
      • Elia M.
      • Normand C.
      • Norman K.
      • Laviano A.
      A systematic review of the cost and cost effectiveness of using standard oral nutritional supplements in the hospital setting.
      • Thornton Snider J.
      • Jena A.B.
      • Linthicum M.T.
      • et al.
      Effect of hospital use of oral nutritional supplementation on length of stay, hospital cost, and 30-day readmissions among Medicare patients with COPD.
      • Sulo S.
      • Feldstein J.
      • Partridge J.
      • Schwander B.
      • Sriram K.
      • Summerfelt W.T.
      Budget impact of a comprehensive nutrition-focused quality improvement program for malnourished hospitalized patients.
      • Stratton R.J.
      • Hebuterne X.
      • Elia M.
      A systematic review and meta-analysis of the impact of oral nutritional supplements on hospital readmissions.
      but relatively few have tested nutritional care strategies for older people living in the community.
      • Riley K.
      • Sulo S.
      • Dabbous F.
      • et al.
      Reducing hospitalizations and costs: a home health nutrition-focused quality improvement program.
      • Smith T.R.
      • Cawood A.L.
      • Walters E.R.
      • Guildford N.
      • Stratton R.J.
      Ready-made oral nutritional supplements improve nutritional outcomes and reduce health care use-a randomised trial in older malnourished people in primary care.
      • Zhu L.Y.
      • Chan R.
      • Kwok T.
      • Cheng K.C.
      • Ha A.
      • Woo J.
      Effects of exercise and nutrition supplementation in community-dwelling older Chinese people with sarcopenia: a randomized controlled trial.
      If health and cost benefits of nutrition care are confirmed and extended, healthcare providers have an enormous opportunity to lessen the burden of care for older community-living adults.
      • Jyvakorpi S.K.
      • Ramel A.
      • Strandberg T.E.
      • et al.
      The sarcopenia and physical frailty in older people: multi-component treatment strategies (SPRINTT) project: description and feasibility of a nutrition intervention in community-dwelling older Europeans.
      ,
      • Nikolova S.
      • Heaven A.
      • Hulme C.
      • et al.
      Social care costs for community-dwelling older people living with frailty.
      ,
      • Sulo S.
      • Lanctin D.
      • Feldstein J.
      • et al.
      Budget impact analysis of a home-based nutrition program for adults at risk for malnutrition.
      Beyond cost, healthy aging with sustained functionality and independence is important to older people.
      • Melzer T.M.
      • Manosso L.M.
      • Yau S.Y.
      • Gil-Mohapel J.
      • Brocardo P.S.
      In pursuit of healthy aging: effects of nutrition on brain function.
      • Roberts S.B.
      • Silver R.E.
      • Das S.K.
      • et al.
      Healthy aging-nutrition matters: start early and screen often [published correction appears in Adv Nutr. 2021;12(4):1597-1598].
      • Robinson S.M.
      Improving nutrition to support healthy ageing: what are the opportunities for intervention?.
      • Wiles J.L.
      • Leibing A.
      • Guberman N.
      • Reeve J.
      • Allen R.E.
      The meaning of “aging in place” to older people.
      Despite the negative health concerns and excessive costs of poor nutritional status among older people in the community, public health strategies are not yet widely used to identify and lessen such risk. Today’s health systems are designed to provide episodic acute healthcare rather than to meet the more challenging needs of community-living older people with chronic conditions.
      Integrated care for older people (ICOPE): guidelines on community-level interventions to manage declines in intrinsic capacity. World Health Organization.
      Moving forward, experts suggest that community-based health professionals can better support healthy aging by increasing the awareness and use of nutrition screening tools, prioritizing high-risk populations for screening, and following screening with specific nutritional diagnoses and appropriate interventions.
      • Roberts S.B.
      • Silver R.E.
      • Das S.K.
      • et al.
      Healthy aging-nutrition matters: start early and screen often [published correction appears in Adv Nutr. 2021;12(4):1597-1598].
      ,
      • Dwyer J.T.
      • Gahche J.J.
      • Weiler M.
      • Arensberg M.B.
      Screening community-living older adults for protein energy malnutrition and frailty: update and next steps.
      ,
      • Roberts H.C.
      • Lim S.E.R.
      • Cox N.J.
      • Ibrahim K.
      The challenge of managing undernutrition in older people with frailty.
      To facilitate nutritional practice changes for improved care, quality improvement programs (QIPs) can be followed.
      Planning for quality improvement. Agency for Healthcare Research and Quality.
      Previous study results have shown that QIP-based changes can be effectively applied to nutritional care in US hospitals to show benefits such as reduced length of stay and lower likelihood of 30-day readmissions.
      • Meehan A.
      • Loose C.
      • Bell J.
      • Partridge J.
      • Nelson J.
      • Goates S.
      Health System Quality improvement: impact of prompt nutrition care on patient outcomes and health care costs.
      • Sriram K.
      • Sulo S.
      • VanDerBosch G.
      • et al.
      Nutrition-focused quality improvement program results in significant readmission and length of stay reductions for malnourished surgical patients.
      • Sriram K.
      • Sulo S.
      • VanDerBosch G.
      • et al.
      A comprehensive nutrition-focused quality improvement program reduces 30-day readmissions and length of stay in hospitalized patients.
      For older adults using home health services or attending outpatient clinics in the United States, nutritional QIP use decreased risk of hospitalization, ED visits and outpatient clinic visits, thus yielding corresponding cost savings.
      • Riley K.
      • Sulo S.
      • Dabbous F.
      • et al.
      Reducing hospitalizations and costs: a home health nutrition-focused quality improvement program.
      ,
      • Hong K.
      • Sulo S.
      • Wang W.
      • et al.
      Nutrition care for poorly nourished outpatients reduces resource use and lowers costs.
      In this article, we report health economic impact of using a QIP that guided nutritional care for older adults who were receiving outpatient care in Bogotá, Colombia, and were identified to be malnourished or at risk. This study aimed to assess effects of the QIP on healthcare resource use (hospitalizations, ED visits, and outpatient clinic visits), and we also performed an economic analysis to demonstrate the nutritional QIP’s ability to generate economic benefits reflected as cost savings and cost-effectiveness. Although previous QIPs have demonstrated cost savings,
      • Sriram K.
      • Sulo S.
      • VanDerBosch G.
      • et al.
      Nutrition-focused quality improvement program results in significant readmission and length of stay reductions for malnourished surgical patients.
      • Sriram K.
      • Sulo S.
      • VanDerBosch G.
      • et al.
      A comprehensive nutrition-focused quality improvement program reduces 30-day readmissions and length of stay in hospitalized patients.
      • Hong K.
      • Sulo S.
      • Wang W.
      • et al.
      Nutrition care for poorly nourished outpatients reduces resource use and lowers costs.
      no other studies to date have investigated the cost-effectiveness of nutrition-focused QIPs in a population of older, community-dwelling adults.

      Methods

      Study Population and Design

      The current study design was a real-world, observational QIP conducted in Bogotá, Colombia; the population has been described previously.
      • Chavarro-Carvajal D.A.
      • Ayala A.M.
      • Venegas-Sanabria L.C.
      • et al.
      Use of a nutrition-focused quality improvement program for community-living older adults at malnutrition risk is associated with better nutritional outcomes.
      The full Colombian study was comprehensive, including evaluation of the nutrition-related outcomes,
      • Chavarro-Carvajal D.A.
      • Ayala A.M.
      • Venegas-Sanabria L.C.
      • et al.
      Use of a nutrition-focused quality improvement program for community-living older adults at malnutrition risk is associated with better nutritional outcomes.
      along with measures of physical and cognitive function, affective disorder status or psychological wellness, and quality of life.
      • Gomez G.
      • Botero-Rodríguez F.
      • Diego Misas J.
      • et al.
      A nutritionally focused program for community-living older adults resulted in improved health and well-being.
      This study population included many individuals considered to be “transitional,” that is, people with long-term conditions who are recovering from acute disease or hospital stays; many require additional homecare or assistance from caregivers.
      • Gomez G.
      • Botero-Rodríguez F.
      • Diego Misas J.
      • et al.
      A nutritionally focused program for community-living older adults resulted in improved health and well-being.
      In this population, nutritional status becomes an important risk factor for hospital readmissions, greater use of healthcare resources, disease relapses, longer recovery times or incomplete recovery, and even death.
      Older patients (> 60 years) with malnutrition or its risk according to the Mini Nutritional Assessment Short Form (MNA-SF) tool (a score of 0-7 indicates malnourished and 8-11 indicates at risk of malnutrition) were recruited at the outpatient clinical setting of the Hospital Universitario San Ignacio, in Bogotá, Colombia, between September 2019 and March 2020. A total of 618 patients completed the nutritional QIP, and full anthropometric outcome data (calf circumference, weight, and body mass index) were available for 565 patients (91.4%). Recruited individuals participated in a 60-day nutrition-focused QIP that included follow-up through 90 days; the study was completed in July 2020. Patients were excluded from participation if they had advanced dementia (Global Deterioration Scale ≥ 6), delirium, intolerance or allergy to oral nutritional supplements (ONS), or life expectancy of < 90 days.

      Study Ethics and Clinical Trials Registration

      The study protocol was approved by the Ethics and Research Committee of the Hospital Universitario San Ignacio, in Bogotá, Colombia. Each participant (or the caregiver) signed the informed consent form.
      This study is registered in ClinicalTrials.gov under identifier NCT04042987.

      QIP Intervention

      The multidimensional, nutrition-focused QIP consisted of (1) nutritional screening at baseline study visit; (2) education of patients and caregivers about the importance of good nutrition and physical exercise; (3) nutritional intervention, including dietary counseling promoting optimization of food intake and provision of ONS as standard formula (Ensure®, Abbott, USA) or diabetes-specific formula (Glucerna®, Abbott, USA) (1 bottle per day for 60 days) according to patient’s dietary needs; and (4) follow-up to reinforce education and compliance with the recommended nutrition regimen throughout the QIP. Patients were followed up to 90 days after QIP enrollment.

      Statistical Analyses

      We used descriptive analyses for sociodemographic and clinical characteristics at baseline. We determined proportions for categorical variables and calculated means ± standard deviations for quantitative variables. To assess statistical differences in health outcomes and healthcare resource use comparing results before and after QIP intervention, we used paired-sample t tests. Participants with missing data in the variables of interest were excluded from the analysis. The significance level was defined as a P value of < .05. Statistical analyses were performed using STATA 14® (StataCorp LLC, College Station, TX, USA).

      Economic Analysis: General Modeling Methodology

      The economic model was developed to perform a budget impact analysis (BIA) and a cost-effectiveness analysis (CEA) from a Colombian third-party payer perspective. The model was based on healthcare resource use and health outcomes informed by previously reported clinical study findings.
      • Chavarro-Carvajal D.A.
      • Ayala A.M.
      • Venegas-Sanabria L.C.
      • et al.
      Use of a nutrition-focused quality improvement program for community-living older adults at malnutrition risk is associated with better nutritional outcomes.
      The model enabled simulations for a 90-day base-case time horizon, according to the observation period of the underlying study; therefore, no cost discounting was applied.
      The BIA enabled the simulation of the cost consequences of the nutritional QIP intervention (after QIP) compared with baseline (before QIP). The base-case analysis was performed with the mean healthcare resource use observed in the study, and the potential variation of the results was reflected by analysis based on the upper and lower 95% confidence intervals. The CEA enabled the simulation of cost-effectiveness using the health outcomes described below. Analysis was based on the mean input values (deterministic) and input parameter distributions (probabilistic). As the deterministic analysis provided a simple point estimate, the visual presentation of CEA results in this article focuses on the probabilistic results informed by 1000 iterations of a Monte-Carlo simulation. The incremental cost-effectiveness outcomes are presented in the incremental cost-effectiveness plane on a per-patient basis.

      Health Outcomes Variables

      According to a recently published systematic review of cost-effectiveness studies on nutrition intervention in adults, most studies used quality-adjusted life-years (QALYs) as the central outcome.
      • Galekop M.M.J.
      • Uyl-de Groot C.A.
      • Ken Redekop W.
      A systematic review of cost-effectiveness studies of interventions with a personalized nutrition component in adults.
      Therefore, we used QALYs as the primary cost-effectiveness indicator. Furthermore, the model enabled CEA determinations based on health outcome variables (adverse events avoided as hospitalization, ED visits, and outpatient clinic visits) and previously reported clinical changes (body weight, MNA-SF scores, and calf circumference).
      • Chavarro-Carvajal D.A.
      • Ayala A.M.
      • Venegas-Sanabria L.C.
      • et al.
      Use of a nutrition-focused quality improvement program for community-living older adults at malnutrition risk is associated with better nutritional outcomes.

      Cost Calculations

      All costs were calculated from the perspective of a third-party payer, corresponding to costs generated for care in the Colombian health system and reported in year 2019 US dollars. Categories of costs included in the model were QIP implementation costs and healthcare resource utilization costs.
      QIP implementation costs (fixed and variables costs) were estimated based on records of professional staff time for completing QIP training and other QIP related tasks including patient nutrition screening/assessment, patient education provision, delivery of ONS, follow-up calls, and follow-up data collection. The cost categories reported are similar to those reported for other QIP studies.
      • Sriram K.
      • Sulo S.
      • VanDerBosch G.
      • et al.
      Nutrition-focused quality improvement program results in significant readmission and length of stay reductions for malnourished surgical patients.
      • Sriram K.
      • Sulo S.
      • VanDerBosch G.
      • et al.
      A comprehensive nutrition-focused quality improvement program reduces 30-day readmissions and length of stay in hospitalized patients.
      • Hong K.
      • Sulo S.
      • Wang W.
      • et al.
      Nutrition care for poorly nourished outpatients reduces resource use and lowers costs.
      Hourly wage rates for staff positions (eg, clinicians and administrative and research staff) were taken from publicly available, Colombian wage statistics.
      Salario en Colombia 2022. Talent.com.
      Healthcare resource utilization costs were estimated based on the costs incurred from hospitalizations, ED visits, and outpatient visits using multiple data sources outlined in Appendix Table 1 in Supplemental Materials found at https://doi.org/10.1016/j.vhri.2022.08.005.

      Results

      Patients who participated in the real-world study were older (> 60 years), living in Bogotá communities, and attending Hospital Universitario San Ignacio (Bogotá, Colombia) outpatient clinics for care. Participants were at a particular risk of poor nutrition because of their older age. In addition, many were attending the clinic for follow-up after hospitalization for an acute illness or condition. Study participants were recruited after being identified as malnourished or at risk of malnutrition when they underwent nutritional screening via the MNA-SF. Such patients were enrolled in the nutrition-focused QIP intervention, and a total of 618 completed the 90-day study. As reported previously, the participant population had a mean age of 74.1 ± 8.7 years, an average of 2.6 comorbidities, and a high proportion of females (69.4%) and were of medium socioeconomic status (76%).
      • Chavarro-Carvajal D.A.
      • Ayala A.M.
      • Venegas-Sanabria L.C.
      • et al.
      Use of a nutrition-focused quality improvement program for community-living older adults at malnutrition risk is associated with better nutritional outcomes.

      Healthcare Resource Use

      Overall healthcare resource use was significantly reduced; changes correspond to relative risk reductions of 59%, 40%, and 43%, respectively, at the timepoints of 30, 60, and 90 days (each at P < .001) (Table 1). By specific healthcare resource (hospitalizations, ED visits, and outpatient visits), utilization was significantly lowered across the 90-day study interval, that is, hospitalizations by 82%, ED visits by 64%, and outpatient visits by 38% (P < .001 for each) (Table 1).
      Table 1Healthcare resource utilization before and after QIP.
      Variable30 days
      P < .001.
      60 days
      P < .001.
      90 days
      P < .001.
      Pre-QIP

      Mean (SD)
      Post-QIP

      Mean (SD) RRR
      Pre-QIP

      Mean (SD)
      Post-QIP

      Mean (SD) RRR
      Pre-QIP

      Mean (SD)
      Post-QIP

      Mean (SD) RRR
      Overall healthcare resource use1.39 (1.24)0.57 (0.84)

      59%
      2.11 (1.82)1.26 (1.36)

      40.3%
      2.6 (2.15)1.48 (1.55)

      43.1%
      Hospitalizations0.07 (0.27)0.01 (0.15)

      85.7%
      0.14 (0.39)0.03 (0.21)

      78.6%
      0.17 (0.45)0.03 (0.22)

      82.4%
      ED visits0.10 (0.32)0.03 (0.20)

      70%
      0.22 (0.52)0.09 (0.32)

      59.1%
      0.28 (0.6)0.1 (0.33)

      64.3%
      Outpatient visits1.25 (1.13)0.56 (0.8)

      55.2%
      1.73 (1.51)1.18 (1.25)

      31.8%
      2.16 (1.85)1.35 (1.41)

      37.5%
      ED indicates emergency department; QIP, quality improvement program; SD, standard deviation; RRR, relative risk reduction.
      P < .001.

      BIA Results

      QIP intervention resulted in cost savings for each category of healthcare resource use, and the total savings related to the 618 patients included in the study were higher than the costs of the QIP intervention (pre-QIP healthcare resource costs of $301 980 vs post-QIP costs of $100 808). Consequently, the budget impact was reflected by total cost savings of $129 740 or $210 per patient over the 90-day study period (Table 2). Total cost savings equated to nearly twice the initial investment for QIP intervention; that is, the per-dollar return on investment was $1.82.
      Table 2Budget impact analysis results: cost savings based on reduced healthcare resource utilization (at 90 days).
      VariablePre-QIP

      Amount, USD
      Post-QIP

      Amount, USD
      Hospitalization costs$222 282$55 571
      Outpatient visit costs$53 359$35 844
      ED visit costs$26 302$9394
      Total healthcare resource costs$301 980$100 808
      Total QIP intervention cost$0$71 431
      Savings for QIP population (N = 618)$129 740
      Savings per patient$210
      ED indicates emergency department; QIP, quality improvement program; USD, US dollar.

      CEA Results

      After the 90-day intervention program (Table 3), the scenario post-QIP intervention dominated the scenario pre-QIP intervention, which is shown by cost savings combined with a higher efficacy, for all effectiveness outcomes studied. Based on cost savings in combination with improved health outcomes, the nutritional QIP was notably a cost-effective treatment strategy. The improvements in nutritional health measures, as described in a companion Colombian QIP study report,
      • Chavarro-Carvajal D.A.
      • Ayala A.M.
      • Venegas-Sanabria L.C.
      • et al.
      Use of a nutrition-focused quality improvement program for community-living older adults at malnutrition risk is associated with better nutritional outcomes.
      are summarized in Appendix Table 2 in Supplemental Materials found at https://doi.org/10.1016/j.vhri.2022.08.005. These include significant improvements in MNA-SF score (nutritional status in an older person), calf circumference (a proxy for leg muscle mass), body weight, and body mass index, with postintervention improvements at the level of P < .001.
      Table 3CEA results: mean per-patient QIP CEA outcomes.
      CE outcomeVariablesPre-QIPPost-QIPIncremental
      Cost per QALY gainedTotal costs$489$279−$210
      Total effectiveness0.17850.18650.008
      Cost-effectiveness$2.739$1.496Dominated
      Cost per adverse event avoidedTotal costs$489$279−$210
      Total effectiveness2.61.591.01
      Cost-effectiveness$188$175Dominated
      Cost per unit calf circumference (cm) gainedTotal costs$489$279−$210
      Total effectiveness30.2932.011.72
      Cost-effectiveness$16$9Dominated
      Cost per unit body weight (kg) gainedTotal costs$489$279−$210
      Total effectiveness59.9460.740.8
      Cost-effectiveness$8$5Dominated
      Cost per point improvement in nutritional status (MNA-SF score)Total costs$489$279−$210
      Total effectiveness9.311.422.12
      Cost-effectiveness$53$24Dominated
      CEA indicates cost-effectiveness analysis; CE, cost-effectiveness; MNA-SF, Mini Nutritional Assessment Short Form; QALY, quality-adjusted life-year; QIP, quality improvement program.
      To evaluate variability of results, probabilistic sensitivity analyses were performed and plotted in the incremental cost-effectiveness coordinate plane (Fig. 1). Such scatterplots provide density visualization; that is, darker areas represent a higher concentration of outcomes in this range. Irrespective of the cost-effective outcome, most cost-per-outcome results plotted in the lower-right corner of the incremental cost-effectiveness plane, indicating an incremental effectiveness gain accompanied by cost savings. In case that not all results are located in the lower-right corner, the probability of the QIP intervention being the dominant option could be assessed by the number of results located in the specific area of the coordinate plane. This is the case for the cost-effectiveness outcomes QALYs gained, adverse events avoided, and calf circumference gained, with a related probability of being the dominant option of 92.7%, 87.7% and 96.5%, respectively. In case that all results are located in the lower-right corner, there is a 100% probability that the QIP intervention is the dominant option, as it is seen for the cost-effectiveness body weight gain and nutritional status improvement.
      Figure thumbnail gr1
      Figure 1CEA results: probabilistic QIP cost-effectiveness outcomes per patient.
      CEA indicates cost-effectiveness analysis; MNA-SF, Mini Nutritional Assessment Short Form; QALY, quality-adjusted life-year; QIP, quality improvement program; USD, US dollar.

      Discussion

      Taken together, the findings of our economic model showcased how nutrition-focused care in community healthcare settings in Colombia could yield health improvements at the patient level along with considerable cost savings at the healthcare-system level. Our model accounted for QIP costs incurred to train healthcare professionals for nutrition-focused care for older adults and to sustain such a program. Across the 90-day study timeline, we found that the use of healthcare resources (hospitalizations, ED visits, and outpatient clinic visits) was significantly reduced by > 40%. In particular, hospitalizations were significantly reduced by approximately 80%, ED visits by more than 60%, and outpatient clinical visits by nearly 40%. Our model estimated a per-patient cost savings of $210 attributable to the nutritional QIP. In terms of cost-effectiveness, we found that irrespective of the cost-effectiveness outcome, the QIP intervention resulted in cost savings accompanied by a higher efficacy. Probabilistic sensitivity analyses have shown that these results are robust for modeling parameter-related uncertainties.
      As seen in our current study in Colombia, previous studies have also shown that QIP-based changes can be effectively applied to nutrition care in clinical settings, including outpatient clinics,
      • Hong K.
      • Sulo S.
      • Wang W.
      • et al.
      Nutrition care for poorly nourished outpatients reduces resource use and lowers costs.
      ,
      • Chavarro-Carvajal D.A.
      • Ayala A.M.
      • Venegas-Sanabria L.C.
      • et al.
      Use of a nutrition-focused quality improvement program for community-living older adults at malnutrition risk is associated with better nutritional outcomes.
      home health service programs,
      • Riley K.
      • Sulo S.
      • Dabbous F.
      • et al.
      Reducing hospitalizations and costs: a home health nutrition-focused quality improvement program.
      and hospital inpatients.
      • Meehan A.
      • Loose C.
      • Bell J.
      • Partridge J.
      • Nelson J.
      • Goates S.
      Health System Quality improvement: impact of prompt nutrition care on patient outcomes and health care costs.
      ,
      • Sriram K.
      • Sulo S.
      • VanDerBosch G.
      • et al.
      A comprehensive nutrition-focused quality improvement program reduces 30-day readmissions and length of stay in hospitalized patients.
      Notably, such nutrition-focused QIP programs yielded marked cost savings and were consistent with other studies that showed nutrition interventions to be cost-effective.
      • Zhong Y.
      • Cohen J.T.
      • Goates S.
      • Luo M.
      • Nelson J.
      • Neumann P.J.
      The cost-effectiveness of oral nutrition supplementation for malnourished older hospital patients.
      • Neelemaat F.
      • Bosmans J.E.
      • Thijs A.
      • Seidell J.C.
      • van Bokhorst-de van der Schueren M.A.
      Oral nutritional support in malnourished elderly decreases functional limitations with no extra costs.
      • Norman K.
      • Pirlich M.
      • Smoliner C.
      • et al.
      Cost-effectiveness of a 3-month intervention with oral nutritional supplements in disease-related malnutrition: a randomised controlled pilot study.
      Evidence supporting economic benefits of improving the quality of nutritional care is abundant and growing based on studies across the continuum of care. A study in 3 US healthcare outpatient clinics found that patients who participated in a nutrition-focused QIP program (N = 600) had lower healthcare resource utilization (hospitalizations, ED visits, and outpatient clinic visits), which was associated with per-patient cost savings of $485 (compared with non-QIP controls).
      • Hong K.
      • Sulo S.
      • Wang W.
      • et al.
      Nutrition care for poorly nourished outpatients reduces resource use and lowers costs.
      In a nutrition-focused QIP conducted for older patients receiving home-healthcare, hospitalization rates were reduced by approximately 20%, and total cost savings from reduced 90-day healthcare resource utilization were $1500 per patient treated.
      • Riley K.
      • Sulo S.
      • Dabbous F.
      • et al.
      Reducing hospitalizations and costs: a home health nutrition-focused quality improvement program.
      In a US multi-hospital study by Sriram et al,
      • Sriram K.
      • Sulo S.
      • VanDerBosch G.
      • et al.
      A comprehensive nutrition-focused quality improvement program reduces 30-day readmissions and length of stay in hospitalized patients.
      30-day readmissions and lengths of hospital stays were significantly lowered for at-risk and malnourished inpatients by the use of medical record-cued nutrition screening, prompt provision of ONS when needed, patient/caregiver education on the importance of nutrition, and sustained nutrition support; such reductions in the use of hospital resources were associated with savings of almost $4000 per patient.
      • Sulo S.
      • Feldstein J.
      • Partridge J.
      • Schwander B.
      • Sriram K.
      • Summerfelt W.T.
      Budget impact of a comprehensive nutrition-focused quality improvement program for malnourished hospitalized patients.
      In a randomized trial involving older patients in UK nursing homes, the use of ONS for patients with malnutrition or its risk was cost-effective compared with dietary advice alone.
      • Elia M.
      • Parsons E.L.
      • Cawood A.L.
      • Smith T.R.
      • Stratton R.J.
      Cost-effectiveness of oral nutritional supplements in older malnourished care home residents.
      Another study of 168 community-dwelling older adults used a 12-week intensive support program that included consultations with dietitians along with resistance exercise guided by physiotherapists.
      • Dorhout B.G.
      • Haveman-Nies A.
      • van Dongen E.J.I.
      • et al.
      Cost-effectiveness of a diet and resistance exercise intervention in community-dwelling older adults: ProMuscle in practice.
      Results showed improvements in Short Physical Performance Battery scores, and the intervention met the criteria for being cost-effective.
      • Dorhout B.G.
      • Haveman-Nies A.
      • van Dongen E.J.I.
      • et al.
      Cost-effectiveness of a diet and resistance exercise intervention in community-dwelling older adults: ProMuscle in practice.
      Altogether, these findings indicate that nutrition-focused QIPs are feasible across the continuum of care and provide a rationale for merging patient care and financial modeling to make the delivery of value-based medicine possible in malnourished or at-risk patient populations.
      Older people who are not well nourished are at increased risk of infections, falls and fractures, mobility limitations, and other physical and mental disabilities that lower their capacity for independent living—in turn increasing the risk of frailty, lowering quality of life, and negatively affecting survival.
      • Rodriguez M.G.
      • Sichaca E.G.
      Mortality due to malnutrition in older adults, Colombia, 2014-2016. [Mortalidad por desnutricion en el adulto mayor, Colombia, 2014-2016].
      • Jyvakorpi S.K.
      • Ramel A.
      • Strandberg T.E.
      • et al.
      The sarcopenia and physical frailty in older people: multi-component treatment strategies (SPRINTT) project: description and feasibility of a nutrition intervention in community-dwelling older Europeans.
      • Wanaratna K.
      • Muangpaisan W.
      • Kuptniratsaikul V.
      • Chalermsri C.
      • Nuttamonwarakul A.
      Prevalence and factors associated with frailty and cognitive frailty among community-dwelling elderly with knee osteoarthritis.
      ,
      • Sanders C.
      • Behrens S.
      • Schwartz S.
      • et al.
      Nutritional status is associated with faster cognitive decline and worse functional impairment in the progression of dementia: the Cache County Dementia Progression Study.
      • O’Keeffe M.
      • Kelly M.
      • O’Herlihy E.
      • et al.
      Potentially modifiable determinants of malnutrition in older adults: a systematic review.
      • Chen C.Y.
      • Gan P.
      • How C.H.
      Approach to frailty in the elderly in primary care and the community.
      Maintaining quality of life with functional independence is important to older adults,
      • Wiles J.L.
      • Leibing A.
      • Guberman N.
      • Reeve J.
      • Allen R.E.
      The meaning of “aging in place” to older people.
      so health policy and decision makers, along with healthcare professionals, are now called upon to harness the potential of maintaining nutritional health and preventing or delaying the onset of archetypal age-related diseases and the frailty condition.
      • Roberts S.B.
      • Silver R.E.
      • Das S.K.
      • et al.
      Healthy aging-nutrition matters: start early and screen often [published correction appears in Adv Nutr. 2021;12(4):1597-1598].
      Such strategies are also a way to achieve affordable healthcare for older people in Colombia. Working together, public health and healthcare professionals can help extend the years people live in good health,
      World report on ageing and health. WHO.
      as highlighted in the World Health Organization’s Decade of Healthy Aging 2020 to 2030 proposal.
      Decade of healthy ageing: baseline report. WHO.
      In terms of health and the overall population, Colombia and other Latin American countries are experiencing growth in the proportion of older people. In Colombia, the proportion of people older than 60 years old is expected to increase from 10% to 20% by 2050. Therefore, it is important for health policy makers in Colombia to build a healthcare system that promotes healthy aging.
      • Robledo L.M.G.
      • Cano-Gutiérrez C.
      • Garcia E.V.
      Healthcare for older people in Central and South America.
      A strength of Colombian healthcare is that it covers more than 95% of the population. For 2022, Colombia was 35th of nearly 100 ranked systems around the world.
      Best healthcare in the world 2022. CEOWORLD Health Care Index.
      In perspective, Australia ranked 6th, Germany 17th, Canada 23rd, the United States 30th, Uruguay 39th, and Brazil 63rd.
      Best healthcare in the world 2022. CEOWORLD Health Care Index.
      For such rankings, healthcare quality was determined by many factors—the care process (preventative care, safe care, coordinated care, and patient engagement), access (affordability and timeliness), administrative efficiency, equity, and healthcare outcomes (population health, mortality responsive to healthcare, and disease-specific health outcomes).
      Best healthcare in the world 2022. CEOWORLD Health Care Index.

      Strengths and Limitations of This Study

      This is a first-of-its-kind study assessing the impact of a nutrition-focused QIP on cost-effectiveness for at-risk and malnourished patients receiving care in Colombian outpatient clinics. By using a real-world study design, we were able to assess endpoints that supported the development of a BIA and CEA. As such, our study findings provided evidence supporting both health and economic benefits of improving nutritional care via QIP for older adults living in the community.
      The study has several limitations. It used an observational QIP methodology, so the study had limitations inherent to trials that are not randomized controlled trial designs. Second, the results of this study may not be generalizable to all outpatient populations in Colombia or other. Third, administrative institution-level and patient survey data were mainly used to confirm healthcare resource utilization, so it is possible that healthcare visits outside of the institution or its network were not fully captured. Finally, we used a time horizon of 90 days. A recent study conducted among community-dwelling adults in Singapore demonstrated that the positive impact of a nutritional intervention could be sustained over 180 days.
      • Chew S.T.H.
      • Tan N.C.
      • Cheong M.
      • et al.
      Impact of specialized oral nutritional supplement on clinical, nutritional, and functional outcomes: a randomized, placebo-controlled trial in community-dwelling older adults at risk of malnutrition.
      It is unclear how long the positive effects of a nutritional QIP could be sustained in our population, so we invite longer-term nutritional QIP investigations on health outcomes and healthcare resource use.
      To confirm and extend our findings on health and cost benefits of nutrition-focused care for older, community-living adults in Colombia, we propose the use of prospective randomized study designs among patients who are attending outpatient clinics or are receiving care in home health-assistance programs. With randomized assignment to treatments, such studies could be used to assess designated health and cost benefits of (1) dietary food counseling, (2) physical exercise, and (3) provision of ONS, with study treatments used singly or in combination.

      Conclusions

      For older, community-living adults, nutritional care—screening for malnutrition risk, provision of nutrition education and intervention when needed, and follow-up—can improve nutritional outcomes while lowering costs of healthcare. Results showed overall use of healthcare resources (hospitalizations, ED visits, and outpatient clinic visits) was significantly reduced by more than 40% equating to a total savings of $210 per patient over 90-day period. Total cost savings equated to nearly twice the initial investment for QIP intervention; that is, the per-dollar return on investment was $1.82.
      For cost-effectiveness, the post-QIP nutritional intervention was favored over pre-QIP care, with differences expressed as cost savings combined with a higher efficacy. Such findings underscore the opportunities for implementing nutritional care programs to lessen the increasing burden of costs for healthcare in the aging population of Colombia and worldwide.

      Article and Author Information

      Author Contributions: Concept and design: Sulo, Gomez, Schwander, Misas, Chavarro-Carvajal, Cano-Gutiérrez
      Acquisition of data: Misas, Chavarro-Carvajal, Venegas-Sanabria, Cano-Gutiérrez
      Analysis and interpretation of data: Sulo, Schwander, Brunton, Gracia, Venegas-Sanabria
      Drafting of the manuscript: Sulo, Schwander, Brunton, Gomez, Misas, Gracia
      Critical revision of the paper for important intellectual content: Sulo, Schwander, Brunton, Gomez, Misas, Gracia, Chavarro-Carvajal, Venegas-Sanabria, Cano-Gutiérrez
      Statistical analysis: Gomez, Misas, Gracia
      Provision of study materials or patients: Chavarro-Carvajal
      Obtaining funding: Cano-Gutiérrez
      Conflict of Interest Disclosures: Drs Sulo and Gomez, Mr Brunton and Misas, and Ms Gracia are employees and stockholders of Abbott Laboratories. Dr Cano reported receiving speaker honoraria from Abbott outside the present work. No other conflicts were reported.
      Funding/Support: This study was supported by a research grant (HA38) from Abbott Laboratories to the Hospital Universitario San Ignacio, Bogotá, Colombia.
      Role of the Funder/Sponsor: The funder participated in the study design and writing of the manuscript.

      Acknowledgment

      The authors thank the Aging Institute of Pontificia Universidad Javeriana in Bogotá, Colombia, for their assistance with the QIP implementation, patient enrollment, and follow-up. The authors also thank Cecilia Hofmann, PhD, of C. Hofmann & Associates for manuscript review and editing.

      References

        • Rodriguez-Sanchez B.
        • Sulo S.
        • Carnicero J.A.
        • Rueda R.
        • Rodriguez-Manas L.
        Malnutrition prevalence and burden on healthcare resource use among Spanish community-living older adults: results of a longitudinal analysis.
        Clinicoecon Outcomes Res. 2020; 12: 355-367
        • Sharman Moser S.
        • Doyev R.
        • Cohen B.
        • et al.
        Prevalence and characteristics of malnutrition among community-dwelling older adults in Israel.
        Clin Nutr ESPEN. 2018; 28: 179-185
        • Ahmed T.
        • Haboubi N.
        Assessment and management of nutrition in older people and its importance to health.
        Clin Interv Aging. 2010; 5: 207-216
        • Agarwal E.
        • Miller M.
        • Yaxley A.
        • Isenring E.
        Malnutrition in the elderly: a narrative review.
        Maturitas. 2013; 76: 296-302
      1. Evidence profile: malnutrition. World Health Organization.
        • Kaiser M.J.
        • Bauer J.M.
        • Ramsch C.
        • et al.
        Frequency of malnutrition in older adults: a multinational perspective using the mini nutritional assessment.
        J Am Geriatr Soc. 2010; 58: 1734-1738
        • Ramage-Morin P.L.
        • Gilmour H.
        • Rotermann M.
        Nutritional risk, hospitalization and mortality among community-dwelling Canadians aged 65 or older.
        Health Rep. 2017; 28: 17-27
        • Wolters M.
        • Volkert D.
        • Streicher M.
        • et al.
        Prevalence of malnutrition using harmonized definitions in older adults from different settings - a MaNuEL study.
        Clin Nutr. 2019; 38: 2389-2398
        • Sulo S.
        • Schiffer L.
        • Sheean P.
        • Farrar I.
        • Partridge J.
        • Fitzgibbon M.
        Community-dwelling adults at nutrition risk: characteristics in relation to the consumption of oral nutritional supplements.
        J Prim Care Community Health. 2020; 112150132720922716
        • Wei J.M.
        • Li S.
        • Claytor L.
        • Partridge J.
        • Goates S.
        Prevalence and predictors of malnutrition in elderly Chinese adults: results from the China Health and Retirement Longitudinal Study.
        Public Health Nutr. 2018; 21: 3129-3134
        • Rodriguez M.G.
        • Sichaca E.G.
        Mortality due to malnutrition in older adults, Colombia, 2014-2016. [Mortalidad por desnutricion en el adulto mayor, Colombia, 2014-2016].
        Biomedica. 2019; 39: 663-672
        • Jyvakorpi S.K.
        • Ramel A.
        • Strandberg T.E.
        • et al.
        The sarcopenia and physical frailty in older people: multi-component treatment strategies (SPRINTT) project: description and feasibility of a nutrition intervention in community-dwelling older Europeans.
        Eur Geriatr Med. 2021; 12: 303-312
        • Wanaratna K.
        • Muangpaisan W.
        • Kuptniratsaikul V.
        • Chalermsri C.
        • Nuttamonwarakul A.
        Prevalence and factors associated with frailty and cognitive frailty among community-dwelling elderly with knee osteoarthritis.
        J Community Health. 2019; 44: 587-595
        • Guest J.F.
        • Panca M.
        • Baeyens J.P.
        • et al.
        Health economic impact of managing patients following a community-based diagnosis of malnutrition in the UK.
        Clin Nutr. 2011; 30: 422-429
        • Snider J.T.
        • Linthicum M.T.
        • Wu Y.
        • et al.
        Economic burden of community-based disease-associated malnutrition in the United States.
        JPEN J Parenter Enter Nutr. 2014; 38: 77S-85S
        • Schuetz P.
        • Sulo S.
        • Walzer S.
        • et al.
        Cost savings associated with nutritional support in medical inpatients: an economic model based on data from a systematic review of randomised trials.
        BMJ Open. 2021; 11e046402
        • Sriram K.
        • Sulo S.
        • VanDerBosch G.
        Malnutrition intervention implementation.
        J Acad Nutr Diet. 2018; 118: 813
        • Buitrago G.
        • Vargas J.
        • Sulo S.
        • et al.
        Targeting malnutrition: nutrition programs yield cost savings for hospitalized patients.
        Clin Nutr. 2020; 19: 2896-2901
        • Elia M.
        • Normand C.
        • Norman K.
        • Laviano A.
        A systematic review of the cost and cost effectiveness of using standard oral nutritional supplements in the hospital setting.
        Clin Nutr. 2016; 35: 370-380
        • Thornton Snider J.
        • Jena A.B.
        • Linthicum M.T.
        • et al.
        Effect of hospital use of oral nutritional supplementation on length of stay, hospital cost, and 30-day readmissions among Medicare patients with COPD.
        Chest. 2015; 6: 1477-1484
        • Sulo S.
        • Feldstein J.
        • Partridge J.
        • Schwander B.
        • Sriram K.
        • Summerfelt W.T.
        Budget impact of a comprehensive nutrition-focused quality improvement program for malnourished hospitalized patients.
        Am Health Drug Benefits. 2017; 10: 262-270
        • Stratton R.J.
        • Hebuterne X.
        • Elia M.
        A systematic review and meta-analysis of the impact of oral nutritional supplements on hospital readmissions.
        Ageing Res Rev. 2013; 12: 884-897
        • Riley K.
        • Sulo S.
        • Dabbous F.
        • et al.
        Reducing hospitalizations and costs: a home health nutrition-focused quality improvement program.
        JPEN J Parenter Enter Nutr. 2020; 44: 58-68
        • Smith T.R.
        • Cawood A.L.
        • Walters E.R.
        • Guildford N.
        • Stratton R.J.
        Ready-made oral nutritional supplements improve nutritional outcomes and reduce health care use-a randomised trial in older malnourished people in primary care.
        Nutrients. 2020; 12: 517
        • Zhu L.Y.
        • Chan R.
        • Kwok T.
        • Cheng K.C.
        • Ha A.
        • Woo J.
        Effects of exercise and nutrition supplementation in community-dwelling older Chinese people with sarcopenia: a randomized controlled trial.
        Age Ageing. 2019; 48: 220-228
        • Nikolova S.
        • Heaven A.
        • Hulme C.
        • et al.
        Social care costs for community-dwelling older people living with frailty.
        Health Soc Care Community. 2022; 30: e804-e811
        • Sulo S.
        • Lanctin D.
        • Feldstein J.
        • et al.
        Budget impact analysis of a home-based nutrition program for adults at risk for malnutrition.
        Am Health Drug Benefits. 2020; 13: 95-101
        • Melzer T.M.
        • Manosso L.M.
        • Yau S.Y.
        • Gil-Mohapel J.
        • Brocardo P.S.
        In pursuit of healthy aging: effects of nutrition on brain function.
        Int J Mol Sci. 2021; 22: 5026
        • Roberts S.B.
        • Silver R.E.
        • Das S.K.
        • et al.
        Healthy aging-nutrition matters: start early and screen often [published correction appears in Adv Nutr. 2021;12(4):1597-1598].
        Adv Nutr. 2021; 12: 1438-1448
        • Robinson S.M.
        Improving nutrition to support healthy ageing: what are the opportunities for intervention?.
        Proc Nutr Soc. 2018; 77: 257-264
        • Wiles J.L.
        • Leibing A.
        • Guberman N.
        • Reeve J.
        • Allen R.E.
        The meaning of “aging in place” to older people.
        Gerontologist. 2012; 52: 357-366
      2. Integrated care for older people (ICOPE): guidelines on community-level interventions to manage declines in intrinsic capacity. World Health Organization.
        • Dwyer J.T.
        • Gahche J.J.
        • Weiler M.
        • Arensberg M.B.
        Screening community-living older adults for protein energy malnutrition and frailty: update and next steps.
        J Community Health. 2020; 45: 640-660
        • Roberts H.C.
        • Lim S.E.R.
        • Cox N.J.
        • Ibrahim K.
        The challenge of managing undernutrition in older people with frailty.
        Nutrients. 2019; 11: 808
      3. Planning for quality improvement. Agency for Healthcare Research and Quality.
        • Meehan A.
        • Loose C.
        • Bell J.
        • Partridge J.
        • Nelson J.
        • Goates S.
        Health System Quality improvement: impact of prompt nutrition care on patient outcomes and health care costs.
        J Nurs Care Qual. 2016; 31: 217-223
        • Sriram K.
        • Sulo S.
        • VanDerBosch G.
        • et al.
        Nutrition-focused quality improvement program results in significant readmission and length of stay reductions for malnourished surgical patients.
        JPEN J Parenter Enter Nutr. 2018; 42: 1093-1098
        • Sriram K.
        • Sulo S.
        • VanDerBosch G.
        • et al.
        A comprehensive nutrition-focused quality improvement program reduces 30-day readmissions and length of stay in hospitalized patients.
        JPEN J Parenter Enter Nutr. 2017; 41: 384-391
        • Hong K.
        • Sulo S.
        • Wang W.
        • et al.
        Nutrition care for poorly nourished outpatients reduces resource use and lowers costs.
        J Prim Care Community Health. 2021; 1221501327211017014
        • Chavarro-Carvajal D.A.
        • Ayala A.M.
        • Venegas-Sanabria L.C.
        • et al.
        Use of a nutrition-focused quality improvement program for community-living older adults at malnutrition risk is associated with better nutritional outcomes.
        Clin Nutr ESPEN. 2022; 48: 291-297
        • Gomez G.
        • Botero-Rodríguez F.
        • Diego Misas J.
        • et al.
        A nutritionally focused program for community-living older adults resulted in improved health and well-being.
        Clin Nutr. 2022; 41: 1549-1556
        • Galekop M.M.J.
        • Uyl-de Groot C.A.
        • Ken Redekop W.
        A systematic review of cost-effectiveness studies of interventions with a personalized nutrition component in adults.
        Value Health. 2021; 24: 325-335
      4. Salario en Colombia 2022. Talent.com.
        https://co.talent.com/salary
        Date accessed: January 11, 2022
        • Zhong Y.
        • Cohen J.T.
        • Goates S.
        • Luo M.
        • Nelson J.
        • Neumann P.J.
        The cost-effectiveness of oral nutrition supplementation for malnourished older hospital patients.
        Appl Health Econ Health Policy. 2017; 15: 75-83
        • Neelemaat F.
        • Bosmans J.E.
        • Thijs A.
        • Seidell J.C.
        • van Bokhorst-de van der Schueren M.A.
        Oral nutritional support in malnourished elderly decreases functional limitations with no extra costs.
        Clin Nutr. 2012; 31: 183-190
        • Norman K.
        • Pirlich M.
        • Smoliner C.
        • et al.
        Cost-effectiveness of a 3-month intervention with oral nutritional supplements in disease-related malnutrition: a randomised controlled pilot study.
        Eur J Clin Nutr. 2011; 65: 735-742
        • Elia M.
        • Parsons E.L.
        • Cawood A.L.
        • Smith T.R.
        • Stratton R.J.
        Cost-effectiveness of oral nutritional supplements in older malnourished care home residents.
        Clin Nutr. 2018; 37: 651-658
        • Dorhout B.G.
        • Haveman-Nies A.
        • van Dongen E.J.I.
        • et al.
        Cost-effectiveness of a diet and resistance exercise intervention in community-dwelling older adults: ProMuscle in practice.
        J Am Med Dir Assoc. 2021; 22: 792-802.e2
        • Sanders C.
        • Behrens S.
        • Schwartz S.
        • et al.
        Nutritional status is associated with faster cognitive decline and worse functional impairment in the progression of dementia: the Cache County Dementia Progression Study.
        J Alzheimers Dis. 2016; 52: 33-42
        • O’Keeffe M.
        • Kelly M.
        • O’Herlihy E.
        • et al.
        Potentially modifiable determinants of malnutrition in older adults: a systematic review.
        Clin Nutr. 2019; 38: 2477-2498
        • Chen C.Y.
        • Gan P.
        • How C.H.
        Approach to frailty in the elderly in primary care and the community.
        Singapore Med J. 2018; 59: 240-245
      5. World report on ageing and health. WHO.
      6. Decade of healthy ageing: baseline report. WHO.
        • Robledo L.M.G.
        • Cano-Gutiérrez C.
        • Garcia E.V.
        Healthcare for older people in Central and South America.
        Age Ageing. 2022; 51afac017
      7. Best healthcare in the world 2022. CEOWORLD Health Care Index.
        • Chew S.T.H.
        • Tan N.C.
        • Cheong M.
        • et al.
        Impact of specialized oral nutritional supplement on clinical, nutritional, and functional outcomes: a randomized, placebo-controlled trial in community-dwelling older adults at risk of malnutrition.
        Clin Nutr. 2021; 40: 1879-1892