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The Journal of the Academy of Nutrition and Dietetics, Journal of Parenteral and Enteral Nutrition, and MEDSURG Nursing Journal have arranged to publish this article simultaneously in their publica- tions. Minor differences in style may appear in each publication, but the article is substantially the same in each journal.

Copyright ª 2013 by the Academy of Nutrition and Dietetics, American Society for Parenteral and Enteral Nutrition, and Academy of Medical-Surgical Nurses.

2212-2672/$36.00 doi:10.1016/j.jand.2013.05.015 Available online 17 July 2013

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FROM THE ACADEMY

Critical Role of Nutrition in Improving Quality of Care: An Interdisciplinary Call to Action to Address Adult Hospital Malnutrition Kelly A. Tappenden, PhD, RD, FASPEN; Beth Quatrara, DNP, RN, CMSRN; Melissa L. Parkhurst, MD; Ainsley M. Malone, MS, RD; Gary Fanjiang, MD; Thomas R. Ziegler, MD

ABSTRACT The current era of health care delivery, with its focus on providing high-quality, affordable care, presents many challenges to hospital- based health professionals. The prevention and treatment of hospital malnutrition offers a tremendous opportunity to optimize the overall quality of patient care, improve clinical outcomes, and reduce costs. Unfortunately, malnutrition continues to go unrecognized and untreated in many hospitalized patients. This article represents a call to action from the interdisciplinary Alliance to Advance Patient Nutrition to highlight the critical role of nutrition intervention in clinical care and to suggest practical ways to promptly diagnose and treat malnourished patients and those at risk for malnutrition. We underscore the importance of an interdisciplinary approach to addressing malnutrition both in the hospital and in the acute post-hospital phase. It is well recognized that malnutrition is associated with adverse clinical outcomes. Although data vary across studies, available evidence shows that early nutrition intervention can reduce complication rates, length of hospital stay, readmission rates, mortality, and cost of care. The key is to systematically identify patients who are malnourished or at risk and to promptly intervene. We present a novel care model to drive improvement, emphasizing the following six principles: (1) create an institutional culture where all stakeholders value nutrition; (2) redefine clinicians’ roles to include nutrition care; (3) recognize and diagnose all malnourished patients and those at risk; (4) rapidly implement comprehensive nutrition interventions and continued monitoring; (5) communicate nutrition care plans; and (6) develop a comprehensive discharge nutrition care and education plan. J Acad Nutr Diet. 2013;113:1219-1237.

T HE UNITED STATES IS entering a new era of health care delivery in which changes in health care policy are driving

an increased focus on costs, quality, and transparency of care. This new focus on improving the quality and ef- ficiency of hospital care highlights an urgent need to revisit the long-standing challenge of hospital malnutrition and

elevate the role of nutrition care as a critical component of patient recovery. Malnutrition is common in the hospital setting and can adversely affect clinical outcomes and costs, but it is often overlooked. Although results of inter- vention studies vary, addressing hospi- tal malnutrition has the potential to improve quality of patient care and clinical outcomes and reduce costs.1

Today it is estimated that at least one third of patients arrive at the hos- pital malnourished1-5 and, if left un- treated, many of those patients will continue to decline nutritionally,5

which may adversely impact their re- covery and increase their risk of com- plications and readmission. Hospital malnutrition is not a new problem, but “the skeleton in the hospital closet,” was brought to light in Butter- worth’s call for practices aimed at proper diagnosis and treatment of malnourished patients.6 As we enter a new era of health care delivery, the time is now to implement a novel, comprehensive nutrition care model

URNAL OF THE ACADE

as part of improved quality standards and to leverage proven examples for success.

Effective management of malnutri- tion requires collaboration among multiple clinical disciplines. In many hospitals, malnutrition continues to be managed in silos, with knowledge and responsibility provided predominantly by the dietitian. However, the new era of quality care will require a deliber- ately more holistic and interdisci- plinary process to address this critical issue. All members of the clinical team must be involved, including nurses who perform initial nutrition screening and develop innovative strategies to facilitate patient compliance; dietitians who complete nutrition assessment/ diagnosis and develop evidence-based intervention(s); pharmacists who eval- uate drug�nutrient interactions; and physicians, including hospitalists, over- seeing the overall care plan and docu- mentation to support reimbursement for services. Recognition of this prob- lem and the opportunity to improve

MY OF NUTRITION AND DIETETICS 1219

FROM THE ACADEMY

patient care were the impetus behind creating the Alliance to Advance Patient Nutrition (Alliance). The Alli- ance brings together the Academy of Nutrition and Dietetics (AND), the Academy of Medical-Surgical Nurses (AMSN), the Society of Hospital Medi- cine (SHM), the American Society for Parenteral and Enteral Nutrition (A.S.P.E.N.), and Abbott Nutrition. The Alliance is made possible with support from Abbott Nutrition. These health organizations are dedicated to the ad- vancement of effective hospital nutri- tion practices to help improve patients’ medical outcomes and support all clinicians in collaborating on hospital- wide nutrition procedures. The estab- lished charter of the Alliance is to champion improved hospital nutrition practices through identification of malnourished patients and patients at risk for malnutrition, early nutrition intervention and treatment, and in- clusion of nutrition as a standard component of all care processes. Nutrition intervention for malnour-

ished patients is a low-risk, cost-effec- tive strategy to improve quality of hospital care, but it requires interdisci- plinary collaboration. As representa- tives of the Alliance, we announce a call to action. We aspire to facilitate the institution of universal nutrition screening, rapid and appropriate nu- trition interventions utilizing effective interdisciplinary nutrition partner- ships, and integration of comprehen- sive strategies to prevent or treat hospital malnutrition. This paper is not intended to provide practice-based guidelines, but rather highlights avail- able data on the critical role nutrition plays in improving patient outcomes, outlines an innovative nutrition care model, underscores the importance of an interdisciplinary approach to address hospital malnutrition, and identifies challenges believed to impair optimal nutrition care. In addition, specific solutions that can be employed by dietitians, nurses, physicians, and other health care professionals, such as nurse practitioners, physician assis- tants, pharmacists, and dietetic techni- cians, registered, are provided.

BURDEN OF HOSPITAL MALNUTRITION Although estimates of the prevalence of malnutrition vary by setting,

1220 JOURNAL OF THE ACADEMY OF NUTRI

subgroup, and method of assessment, the prevalence of malnutrition in hos- pitals is particularly startling. It is estimated that at least one third of patients in developed countries have some degree of malnutrition upon admission to the hospital1-3,5 and, if left untreated, approximately two thirds of those patients will experience a further decline in their nutrition status during inpatient stay.5 Unfortu- nately, despite the availability of vali- dated screening tools, malnutrition continues to be under-recognized in many hospitals.7,8 Moreover, among patients who are not malnourished upon admission, approximately one third may become malnourished while in the hospital.9

Historically, a variety of tools and definitions have been used throughout the nutrition literature. For the pur- poses of this paper mild through severe malnutrition will be the focus and is the intent when the term malnutrition is used. Malnutrition is most simply defined as any nutrition imbalance10

that affects both overweight and underweight patients alike and is generally described as either “under- nutrition” or “overnutrition.”11 Hospi- talized patients, regardless of their body mass index (BMI), typically suffer from undernutrition because of their propensity for reduced food intake due to illness-induced poor appetite, gastrointestinal symptoms, reduced ability to chew or swallow, or nil per os (NPO) status for diagnostic and thera- peutic procedures. In addition, they may have increased energy, protein, and essential micronutrient needs because of inflammation, infection, or other catabolic conditions. A consensus statement by AND and A.S.P.E.N. pub- lished in May 2012 defines malnutri- tion as the presence of two or more of the following characteristics: insuffi- cient energy intake, weight loss, loss of muscle mass, loss of subcutaneous fat, localized or generalized fluid accumu- lation, or decreased functional status.11

The importance of identifying at-risk patients is highlighted by data showing that malnutrition is associated with many adverse outcomes, including an increased risk of pressure ulcers and impaired wound healing, immune sup- pression and increased infection rate, muscle wasting and functional loss increasing the risk of falls, longer length of hospital stay, higher readmission

TION AND DIETETICS

rates, higher treatment costs, and increased mortality.1 Therefore, malnu- trition places a heavy burden on the patient, clinician, and health care system.

Many of the adverse outcomes influ- enced by malnutrition are potentially preventable. Nosocomial infections are a prime example. Approximately 2 million nosocomial infections occur annually in the United States,12 and those patients are more likely to spend time in the intensive care unit, be readmitted, and die as a result.13 A retrospective study by Fry and col- leagues examined nearly 1 million sur- gical patients (N¼887,189) treated at 1,368 hospitals to determine the risk of nosocomial infections and better un- derstand the underlying patient char- acteristics influencing that risk.14 The analysis showed that patients with pre- existing malnutrition and/or weight loss had a two- to threefold increased risk of developing Clostridium difficile enterocolitis, surgical-site infection, or postoperative pneumonia, and a greater than fivefold higher risk ofmediastinitis after coronary artery bypass graft sur- gery or catheter-associated urinary tract infection. Malnutrition and/or weight loss also correlated with an approximate fourfold higher risk of developing a pressure ulcer. These data are further supported by a prospective multivariate analysis demonstrating that malnutrition is an independent risk factor for nosocomial infections.15

Impaired wound healing can signifi- cantly influence length of hospital stay, and the literature supports a strong correlation between nutrition and wound healing, wherein protein syn- thesis is necessary.16 Hospitalized pa- tients are at increased risk because loss of significant lean body mass (LBM) accelerates during bed rest.17,18 A 10% loss of LBM results in immune sup- pression and increases the risk of infection, and a loss of >15% to 20% of total LBM will impair wound heal- ing.16,19 A loss of �30% leads to the development of spontaneous wounds, such as pressure ulcers, an increased risk of pneumonia, and a complete lack of wound healing.16,19 These complica- tions are also associated with a sub- stantial mortality risk, particularly in older patients. A study evaluating the care processes for hospitalized Medi- care patients (N¼2,425; aged 65 years and older) at risk for pressure ulcer

September 2013 Volume 113 Number 9

FROM THE ACADEMY

development showed that 76% of pa- tients were malnourished, and esti- mated compliance with nutrition consultation was low (34%).20

Data from several recent studies show that malnutrition can also influ- ence hospital readmission rates.21-23

These studies evaluated multiple fac- tors to identify individuals at increased risk of readmission. The largest of these studies, a retrospective observational analysis of >10,000 consecutive ad- missions (N¼6,805), reported a 30-day readmission rate of 17%.21 Comorbid- ities that significantly increased the risk of readmission included congestive heart failure, renal disease, cancer, weight loss (not defined), and iron- deficiency anemia. Weight loss corre- lated with a 26% increased risk of readmission (adjusted odds ratio¼ 1.26).21 In a large single-center study of 1,442 general surgery patients, the 30-day readmission rate was 11%.22 The most common reasons for readmission were gastrointestinal problems/com- plications (28% of readmissions), sur- gical infections (22%), and failure to thrive/malnutrition (10%). These find- ings are consistent with the hypothesis that poor nutrition contributes to post- hospital syndrome, which, together with a variety of other factors, such as sleep disturbance, pain, and discom- fort, can dramatically increase the risk of 30-day readmission, often for reasons other than the original diagnosis.24

Finally, poor clinical outcomes asso- ciated with malnutrition contribute to higher hospitalization costs. As out- lined above, malnourished patients have higher rates of infections, pres- sure ulcers, impaired wound healing, and other adverse outcomes requiring greater nursing care and more medi- cations. In turn, these complications can contribute to longer lengths of hospital stay and higher rates of read- mission, all of which indirectly con- tribute to higher hospital costs.1

Indeed, a study conducted in the United Kingdom estimated the annual expenditure for managing patients at medium or high risk of disease-related malnutrition to be EURV10.5 billion (US$11.3 billion, based on 2003 ex- change rates), more than half of which was directly related to hospital care.25

These studies strongly suggest that the consequences of unrecognized and untreated malnutrition are substantial,

September 2013 Volume 113 Number 9

not only for patients’ quality of care but also from a cost perspective. Malnutri- tion negatively affects clinical out- comes and results in higher costs and, with the changing health care land- scape, reimbursement for costs associ- ated with preventable events will be reduced. All clinicians must take action to address these concerns, improve patient quality of life, and increase the health care system value.

IMPACT OF NUTRITION INTERVENTION ON KEY OUTCOMES The benefits of nutrition intervention in terms of improving key clinical out- comes are well documented. Numerous studies, predominantly in patients 65 years of age and older with or at risk for malnutrition, have shown the potential of specific nutrition interventions to substantially reduce complication rates, length of hospital stay, readmission rates, cost of care, and, in some studies, mortality.5,26-36

Nutrition intervention strategies rep- resent a broad spectrum of options that can be organized into four categories: (1) food and/or nutrient delivery; (2) nutrition education; (3) nutrition counseling, and (4) coordination of nutrition care. Food and/or nutrient delivery requires an individualized approach that includes energy- and nutrient-dense food, complete oral nutrition supplements (ONS) that pro- vide macronutrients (from carbohy- drate, fat, and protein sources) combined with micronutrients (mix- tures of complete vitamins, minerals, and trace elements); enteral nutrition (EN), which in the context of this report refers to nutrients provided into the gastrointestinal tract via a tube; and/or parenteral nutrition (PN). Although the nutrition support litera- ture has generally featured smaller trials and observational studies rather than large, multicenter, randomized controlled trials, evidence strongly supports the importance of nutrition intervention. The value of EN and PN is well established in select patient pop- ulations but remains unclear in others. In addition, numerous studies have shown improved body weight, LBM, and grip strength with dietary coun- seling, with or without ONS.37 A growing number of studies have exam- ined the impact of ONS inmalnourished

JOURNAL OF THE ACADE

patients, providing the framework for our call to action. Evidence sup- porting intervention with EN and PN is beyond the scope of the current paper and will be addressed in subsequent reviews.

Clinical Complications Studies evaluating the efficacy of ONS delivery have generally shown a variety of metabolic improvements and, in many studies, a reduction in several clinical complications. One meta- analysis including seven studies (N¼284) indicates that patients re- ceiving ONS had reduced complication rates (eg, infections, gastrointestinal perforations, pressure ulcers, anemia and cardiac complications) compared with control patients.28More recently, a large Cochrane systematic review of 24 studies involving 6,225 patients 65 years of age and older at risk for malnutrition demonstrated fewer complications (eg, pressure sores, deep vein thrombosis, and respiratory and urinary infections) among patients re- ceiving ONS compared with routine care (relative risk [RR]¼0.86; 95% CI 0.75 to 0.99).27 Available evidence in- dicates high-protein ONS to be partic- ularly effective at reducing the risk of complications. A systematic review of elderly patients (older than 65 years of age) with hip fractures demonstrated a more effective reduction in the number of long-term medical complications with high-protein ONS (>20% total en- ergy from protein) than low-protein or nonprotein-containing supplements (RR¼0.78; 95% CI 0.65 to 0.95).26 A meta-analysis of four randomized trials (N¼1,224) also showed that, in patients with no pressure ulcers at baseline, high-protein ONS resulted in a signifi- cant 25% lower incidence of ulcers compared with routine care.38 In addi- tion, evidence indicates that nutrition intervention can reduce the risk of falls in frail and malnourished elderly pa- tients. In 210malnourished older adults newly admitted to an acute-care hos- pital, intervention with a protein- and energy-rich diet, ONS, calcium/vitamin D supplements, and counseling reduced the incidence of falls by approximately 60% comparedwith routine care (10% vs 23%).35 Avoidance of these preventable events can shorten length of hospital stay, decrease morbidity and mortality, and reduce liability for the hospital.

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FROM THE ACADEMY

Length of Stay Consistent with evidence that nutrition intervention can reduce clinical com- plications, strong nutrition care can also reduce the length of hospital stay. In a prospective study conducted at The Johns Hopkins Hospital, nutrition screening involving a team approach to address malnutrition and earlier inter- vention reduced the length of hospital stay byan average of 3.2 days in severely malnourished patients,5 and this trans- lated into substantial cost savings of $1,514 per patient. Two meta-analyses have shown significantly reduced length of hospital stay in patients re- ceiving ONS compared with control patients. One analysis demonstrated a reduced average length of hospital stay ranging from2days for surgical patients to 33 days for orthopedic patients (P<0.004).28 In addition, patientswith a lower BMI (<20) received the greatest benefit from optimized food and/or nutrient delivery. Likewise, in a recent meta-analysis of nine randomized trials (N¼1,227), high-protein ONS signifi- cantly reduced length of stay by an average of 3.8 days (P¼0.040) compared with routine care.31 A recent retrospec- tive analysis utilized information from >1 million adult inpatient cases found in the 2000-2010 Premier Perspectives Database maintained by the Premier Healthcare Alliance—representing a to- tal of 44 million hospital episodes from across the United States or approxi- mately20%of all inpatient admissions in the United States. Within this sample, ONS reduced length of hospital stay by an average of 2.3 days or 21%, and the average cost savingswas $4,734 or 21.6% compared with routine care.36

Readmissions Hospital readmission rate is another important outcome that can be improved through nutrition interven- tion. Thirty-day readmission rates de- creased from 16.5% to 7.1% in a community hospital that implemented a comprehensive malnutrition clinical pathway program focused on identifi- cation of at-risk patients, nutrition care decisions, inpatient care, and discharge planning.30 A prospective randomized trial in acutely ill patients 65 to 92 years of age (N¼445) demonstrated a signifi- cantly lower 6-month readmission rate among those who received a normal hospital diet plus high-protein ONS

1222 JOURNAL OF THE ACADEMY OF NUTRI

compared with those patients who received only the normal hospital diet (29% vs 40%, respectively; hazard ratio¼0.68; 95% CI 0.49 to 0.94).32

Finally, analysis of the Premier Per- spectives Database showed that use of ONS reduced 30-day readmission rates by6.7%,36 indicating the significant real- world benefit of nutrition intervention on a key patient outcome.

Mortality Several meta-analyses have also demonstrated reduced mortality in patients receiving optimized nutri- ent care. An analysis of 11 studies (N¼1,965) found significantly lower mortality rates among hospitalized pa- tients receiving ONS (19%) compared with control patients (25%; P<0.001).28

This represented a 24% overall reduc- tion in mortality, and patients with lower average BMI (<20) receiving ONS had a greater reduction in mortality. Among elderly patients hospitalized for hip fracture, significantly fewer patients had an unfavorable combined outcome (mortality or medical complication) if they received ONS vs routine care (RR¼0.52; 95% CI 0.32 to 0.84).29

Another systematic review of 32 studies (N¼3,021) found that, in elderly patients, ONS significantly reduced mortality compared with routine care (RR¼0.74; 95% CI 0.59 to 0.92).33 Sub- group analyses from the original Cochrane review and two updates have consistently shown reduced mortality in undernourished patients receiving ONS compared with routine care.27,33,34

Collectively, these data provide solid evidence that nutrition intervention significantly contributes to improved clinical outcomes and reduced cost of care, primarily in patients 65 years of age and older and those with, or at risk for, malnutrition. However, it is important to note that isolated studies and meta-analyses have not demon- strated such significantly improved clinical outcomes with nutrition inter- vention.37,39-42 Additional research studies, particularly well-powered, randomized controlled clinical trials, are always beneficial to further explore the effects of nutrition intervention on clinical outcomes and to assess how those benefits can translate into cost savings. Nevertheless, given the impor- tance of adequate nutrition to cell and organ function, coupled with promising

TION AND DIETETICS

clinical data reported to date, the time is now to act on the evidence at hand and implement nutrition intervention strategies shown to be safe and efficacious.

ALLIANCE NUTRITION CARE RECOMMENDATIONS If we are to make progress toward improving nutrition care practices that guarantee every malnourished or at- risk patient is identified and treated effectively, we must proactively iden- tify barriers impacting the provision of nutrition care. Toward this end, at least six key challenges must be overcome. First, despite at least one third of hos- pitalized patients being admitted malnourished, a majority of these pa- tients continue to go unrecognized or are inadequately screened.43 Second, while the responsibility of patients’ nutrition care is often placed on the dietitian many institutions lack ade- quate dietitian staffing to properly address all patients. Third, nutrition care is often delayed due to the pa- tient’s medical status, lack of diet order, and time to nutrition consult. In fact, a study at Johns Hopkins found that time to consultation from admission is nearly 5 days,5 which is similar to the average length of hospital stay.44

Fourth, nurses provide and oversee patient care 24/7, observe nutrition intake and tolerance, and interact continually with the patient and their family/caregivers, yet they are rarely included in nutrition care.45 Fifth, in many care environments, physician sign-off is required to implement a nutrition care plan. Dietitian recom- mendations are implemented in only 42% of cases.46 Finally, many patients experience difficulty consuming meals without assistance, contributing to more than half of hospitalized patients not finishing their meals.47

To address these barriers and shift the paradigm of nutrition care, the Alliance Steering Committee, whose members possess broad-ranging ex- pertise and clinical experience, devel- oped several key principles for advancing patient nutrition. Through a series of meetings conducted over the past year, the committee explored the following topics: empowerment of all clinicians; recognition and diagnosis of all patients; same-day automatic intervention for all at-risk patients;

September 2013 Volume 113 Number 9

Figure 1. The Alliance’s Key Principles for Advancing Patient Nutrition. EHR¼electronic health record.

FROM THE ACADEMY

education and involvement of patients in their nutrition care; and apprecia- tion of the value of nutrition by all hospital stakeholders. Six principles deemed essential elements of optimal patient nutrition care were derived from these topics (Figure 1). Attain- ment of these six ideals, however, will require processes and collaboration among all hospital stakeholders, in- cluding dietitians, nurses, physicians, and administrators, each of whom must fulfill their role in this effort (Figure 2). Translation of these pro- cesses into a practical interdisciplinary nutrition care algorithm is illustrated in Figure 3.

Principle 1: Create an Institutional Culture Where All Stakeholders Value Nutrition True progress requires that all hospital stakeholders, including clinicians and administrators, fully understand the

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pervasiveness of hospital malnutrition and the effect patient nutrition caremay have on overall clinical outcomes. Cli- nicians and administrators often fail to prioritize understanding the extent of malnutrition in their institutions and its potential impact on cost and/or quality of care. Nurses and physicians receive limited formal nutrition education dur- ing training and often do not prioritize nutrition among the competing prior- ities within patient care. Failing to pri- oritize nutrition within an institution may limit available nutrition interven- tion options and human resources (eg, dietitian nutrition-focused nurses and physicians) required for optimal nutrition care. To be successful, in- stitutions need motivated nutrition champions at all levels of clinical care and administration. To ensure that clinicians and hospital

leaders understand the clinical and financial implications of malnutrition and take proper steps to address it,

JOURNAL OF THE ACADE

the Alliance offers the following recommendations:

� Clinicians must be educated on the recognition of malnourished patients and evidence-based nutrition interventions. Discus- sion of nutrition care plans should be a mandated compo- nent of daily team meetings (rounds or huddles).

� Malnutrition must be appropri- ately included as part of the pa- tient’s diagnosis and nutrition interventions must be viewed as a core component of a patient’s medical therapy. Nutrition treat- ment plans should be addressed with the same consistency and rigor as other therapies.

� Hospital administrators must recognize the financial benefit of optimal nutrition care. Institu- tional financial data must be reviewed to identify challenges

MY OF NUTRITION AND DIETETICS 1223

Principle Key Hospital Stakeholders

Dietitian Nurse Physician Hospital administrator

1. Create an Institutional Culture Where All Stakeholders Value Nutrition

� Serve as primary authority on “all things nutrition”

� Educate key hospital stakeholders on improved patient outcomes and reduced costs achieved with optimal nutrition care

� Host hospital-wide learning opportunities at regular intervals

� Recognize the essential role that nurses play in achieving enhanced patient outcomes through individualized nutrition care

� Incorporate nutrition into routine care checklists and processes

� Include patient dietary intake into team huddles

� Provide leadership under- scoring nutrition care as an essential part of patient- centered care

� Know evidence regarding impact of malnutrition and effectiveness of nutrition intervention

� Include dietitian in daily team huddles/rounds

� Incorporate nutrition into routine care checklists and processes

� Become a nutrition cham- pion and provide support for the development of effective nutrition care processes

� Share quality and eco- nomic gains to be made by investing in nutrition care with hospital leadership team

2. Redefine Clinicians’ Role to Include Nutrition Care

� Actively contribute nutri- tion expertise and engage other team members with assessment data on prog- ress made with nutrition care efforts

� Regularly participate in interdisciplinary rounds

� Ensure practices are in place to support imple- mentation of nutrition intervention

� Develop proce

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