18
Nutrition in Clinical Practice Volume 30 Number 5 October 2015 634–651 © 2015 American Society for Parenteral and Enteral Nutrition DOI: 10.1177/0884533615594012 ncp.sagepub.com hosted at online.sagepub.com Invited Review Introduction Enteral nutrition (EN) is defined as nutrition provided through the gastrointestinal (GI) tract via a tube, catheter, or stoma that delivers nutrients distal to the oral cavity. 1 Enteral access allows the short- and long-term delivery of nutrients to the digestive tract of patients who cannot maintain their require- ments with oral intake. Administration of EN has long been considered the standard of care among patients unable to meet energy and protein requirements orally. As such, many hospi- talized patients in the United States receive EN. According to the latest available statistics from the National Center for Health Statistics, patients received EN during approximately 251,000 hospital stays in 2012, 78% of which were adults. 2 The provision of EN not only provides micronutrients and macronutrients but also supports the functional and structural integrity of the largest immune organ in the body—the gut. Some of the physiologic changes induced by the delivery of EN include stimulating blood flow to maintain adequate perfusion, stimulating intestinal motility/contractility, maintaining villous height, promoting insulin sensitivity, supporting commensal bac- teria, and attenuating oxidative stress and the systemic inflamma- tory response to illness, among other things 3-7 (Figure 1). These physiologic changes help maintain intestinal barrier function and therefore prevent increases in gut permeability and decrease the virulence of pathogenic organisms (eg, bacterial transloca- tion) often seen in patients with host immune deficiencies, immunosuppression, stress, hypoperfusion, and disturbances in normal gut flora due to lack of enteral stimulation. 8 The prevalence of malnutrition in hospitalized patients has been estimated at 30%–60%, with up to 69% of patients experi- encing a decline in their nutrition status during hospitalization, 9 and published reports consistently describe incomplete delivery of EN. 10-12 To prevent the downstream complications that can result from inadequate nutrient intake in the hospital setting, including increased morbidity and mortality related to iatrogenic malnutrition, longer lengths of hospital stay, and increased hos- pital costs, healthcare providers must pay close attention to the adequacy of EN intake and adjust therapies on a frequent basis. The purpose of this article is to provide a basic review of EN in the adult hospitalized patient to guide clinicians in the manage- ment of EN. An interdisciplinary team approach is required for the successful navigation of nutrition assessment, patient and enteral access device selection, enteral formula selection and method of administration, monitoring for and troubleshooting EN-related complications, and transitioning to oral feeding. Nutrition Assessment A complete nutrition assessment includes a review of the patient’s medical, surgical, social, and diet history, anthropometric mea- surements, and laboratory data, as well as a verbal discussion with the patient and/or caregiver and completion of a nutrition-focused physical assessment. The intent of the nutrition assessment is to document baseline nutrition parameters, identify risk factors for malnutrition and specific nutrient deficits, establish individual nutrition needs, and identify any factors that may influence the provision of nutrition support therapy. 13 594012NCP XX X 10.1177/0884533615594012Nutrition in Clinical PracticeKozeniecki and Fritzshall research-article 2015 From 1 Department of Nutrition Services, Froedtert Hospital, Milwaukee, Wisconsin. Financial disclosure: None declared. This article originally appeared online on July 22, 2015. Corresponding Author: Michelle Kozeniecki, MS, RD, CNSC, Froedtert Hospital, 9200 W. Wisconsin Ave, Milwaukee, WI, 53226, USA. Email: [email protected] Enteral Nutrition for Adults in the Hospital Setting Michelle Kozeniecki, MS, RD, CNSC 1 ; and Rebecca Fritzshall, MS, RD, CNSC 1 Abstract In patients unable to tolerate oral intake, multiple options of nutrient delivery are available to the clinician. Administration of enteral nutrition (EN) has long been considered the standard of care for nutrition support among patients unable to meet energy and protein requirements orally. Healthcare practitioners must make careful decisions related to ordering, administering, and monitoring EN therapy. In the hospital setting, the registered dietitian is a key resource in enteral formula selection and method of administration, monitoring for and troubleshooting EN-related complications, and transitioning to oral feeding. The hospital setting also presents many unique challenges in providing optimal nutrition to the enterally fed patient. (Nutr Clin Pract. 2015;30:634-651) Keywords enteral nutrition; adults; nutrition therapy; nutritional support; hospitalization; nutrition assessment; malnutrition by Beth Higgins on May 19, 2016 ncp.sagepub.com Downloaded from

Nutrition in Clinical Practice Enteral Nutrition for ...criticalcarelearningpod.weebly.com/uploads/1/3/0/3/...the lungs and skin. Metabolic changes, such as fever and hyperthyroidism,

  • Upload
    others

  • View
    3

  • Download
    0

Embed Size (px)

Citation preview

Page 1: Nutrition in Clinical Practice Enteral Nutrition for ...criticalcarelearningpod.weebly.com/uploads/1/3/0/3/...the lungs and skin. Metabolic changes, such as fever and hyperthyroidism,

Nutrition in Clinical PracticeVolume 30 Number 5 October 2015 634 –651© 2015 American Societyfor Parenteral and Enteral NutritionDOI: 10.1177/0884533615594012ncp.sagepub.comhosted at online.sagepub.com

Invited Review

Introduction

Enteral nutrition (EN) is defined as nutrition provided through the gastrointestinal (GI) tract via a tube, catheter, or stoma that delivers nutrients distal to the oral cavity.1 Enteral access allows the short- and long-term delivery of nutrients to the digestive tract of patients who cannot maintain their require-ments with oral intake. Administration of EN has long been considered the standard of care among patients unable to meet energy and protein requirements orally. As such, many hospi-talized patients in the United States receive EN. According to the latest available statistics from the National Center for Health Statistics, patients received EN during approximately 251,000 hospital stays in 2012, 78% of which were adults.2

The provision of EN not only provides micronutrients and macronutrients but also supports the functional and structural integrity of the largest immune organ in the body—the gut. Some of the physiologic changes induced by the delivery of EN include stimulating blood flow to maintain adequate perfusion, stimulating intestinal motility/contractility, maintaining villous height, promoting insulin sensitivity, supporting commensal bac-teria, and attenuating oxidative stress and the systemic inflamma-tory response to illness, among other things3-7 (Figure 1). These physiologic changes help maintain intestinal barrier function and therefore prevent increases in gut permeability and decrease the virulence of pathogenic organisms (eg, bacterial transloca-tion) often seen in patients with host immune deficiencies, immunosuppression, stress, hypoperfusion, and disturbances in normal gut flora due to lack of enteral stimulation.8

The prevalence of malnutrition in hospitalized patients has been estimated at 30%–60%, with up to 69% of patients experi-encing a decline in their nutrition status during hospitalization,9 and published reports consistently describe incomplete delivery of EN.10-12 To prevent the downstream complications that can

result from inadequate nutrient intake in the hospital setting, including increased morbidity and mortality related to iatrogenic malnutrition, longer lengths of hospital stay, and increased hos-pital costs, healthcare providers must pay close attention to the adequacy of EN intake and adjust therapies on a frequent basis. The purpose of this article is to provide a basic review of EN in the adult hospitalized patient to guide clinicians in the manage-ment of EN. An interdisciplinary team approach is required for the successful navigation of nutrition assessment, patient and enteral access device selection, enteral formula selection and method of administration, monitoring for and troubleshooting EN-related complications, and transitioning to oral feeding.

Nutrition Assessment

A complete nutrition assessment includes a review of the patient’s medical, surgical, social, and diet history, anthropometric mea-surements, and laboratory data, as well as a verbal discussion with the patient and/or caregiver and completion of a nutrition-focused physical assessment. The intent of the nutrition assessment is to document baseline nutrition parameters, identify risk factors for malnutrition and specific nutrient deficits, establish individual nutrition needs, and identify any factors that may influence the provision of nutrition support therapy.13

594012 NCPXXX10.1177/0884533615594012Nutrition in Clinical PracticeKozeniecki and Fritzshallresearch-article2015

From 1Department of Nutrition Services, Froedtert Hospital, Milwaukee, Wisconsin.

Financial disclosure: None declared.

This article originally appeared online on July 22, 2015.

Corresponding Author:Michelle Kozeniecki, MS, RD, CNSC, Froedtert Hospital, 9200 W. Wisconsin Ave, Milwaukee, WI, 53226, USA.Email: [email protected]

Enteral Nutrition for Adults in the Hospital Setting

Michelle Kozeniecki, MS, RD, CNSC1; and Rebecca Fritzshall, MS, RD, CNSC1

AbstractIn patients unable to tolerate oral intake, multiple options of nutrient delivery are available to the clinician. Administration of enteral nutrition (EN) has long been considered the standard of care for nutrition support among patients unable to meet energy and protein requirements orally. Healthcare practitioners must make careful decisions related to ordering, administering, and monitoring EN therapy. In the hospital setting, the registered dietitian is a key resource in enteral formula selection and method of administration, monitoring for and troubleshooting EN-related complications, and transitioning to oral feeding. The hospital setting also presents many unique challenges in providing optimal nutrition to the enterally fed patient. (Nutr Clin Pract. 2015;30:634-651)

Keywordsenteral nutrition; adults; nutrition therapy; nutritional support; hospitalization; nutrition assessment; malnutrition

by Beth Higgins on May 19, 2016ncp.sagepub.comDownloaded from

Page 2: Nutrition in Clinical Practice Enteral Nutrition for ...criticalcarelearningpod.weebly.com/uploads/1/3/0/3/...the lungs and skin. Metabolic changes, such as fever and hyperthyroidism,

Kozeniecki and Fritzshall 635

Identifying and Diagnosing Malnutrition

Currently, there is no single laboratory test or panel that can accurately or consistently diagnose malnutrition. Despite their widespread use as nutrition markers, serum proteins such as albumin, prealbumin, and transferrin are now well established as negative acute phase reactants that are sensi-tive to acute and chronic inflammation.14,15 Severe, sustained, or repeated bouts of inflammation correlate with adverse out-comes. Since serum proteins correlate with the patient’s over-all severity of illness and level of inflammation, they can be useful predictors of morbidity and mortality in hospitalized patients.15,16

In 2012, a standardized, etiology-based approach to diag-nosing malnutrition in the adult hospitalized patient was devel-oped.17 This approach recognizes the effects of acute and chronic disease-related inflammation and includes the assess-ment of 6 characteristics, and their respective thresholds, for both moderate and severe malnutrition. Identification of 2 of 6 malnu-trition characteristics (weight loss, insufficient energy intake, depletion of subcutaneous fat, depletion of muscle mass, decline in handgrip strength, and fluid accumulation) is needed to

diagnosis protein-energy malnutrition. It is important to note that malnutrition can occur at any body mass index (BMI) and that hepatic proteins can be within normal ranges in patients with pure starvation-associated (noninflammatory) malnutrition.

Energy NeedsEnergy needs in the hospitalized adult patient are generally based on age, sex, BMI, body composition, and clinical status. A.S.P.E.N. consensus guidelines suggest that most adults require a range of 20–35 kilocalories per kilogram (kcal/kg).18 Indirect calorimetry (IC), which measures whole body oxygen consumption and carbon dioxide gas exchange to yield resting metabolic rate, is considered the gold standard for determining energy needs in the acute care setting.19 However, IC is often unavailable due to its high cost and the specialized training required. Therefore, a number of predictive equations have been developed to estimate energy needs in various patient pop-ulations, although results do not always correlate with IC across all patient populations and can vary with obesity, age, and severity of illness. If used, equations must be applied in patients similar to the reference population from which the equation was

Figure 1. Nutrition and nonnutrition benefits of early enteral nutrition. AGEs, advanced glycolytic endproducts; GI, gastrointestinal; IgA, immunoglobulin A; MALT, mucosal-associated lymphoid tissue. Reprinted with permission from McClave SA, Martindale RG, Rice TW, Heyland DK. Feeding the critically ill patient. Crit Care Med. 2014;42:2600-2610.

by Beth Higgins on May 19, 2016ncp.sagepub.comDownloaded from

Page 3: Nutrition in Clinical Practice Enteral Nutrition for ...criticalcarelearningpod.weebly.com/uploads/1/3/0/3/...the lungs and skin. Metabolic changes, such as fever and hyperthyroidism,

636 Nutrition in Clinical Practice 30(5)

derived, with the understanding that clinical judgment is still required. Regardless of the method used to determine energy needs, it is essential to adjust energy provision based on the patient’s clinical status and response to nutrition therapy.

Protein Needs

Protein is essential for the structure, maintenance, and growth of cells, tissues, enzymes, hormones, antibodies, and transport carries. Daily protein requirements are based on a patient’s age, weight, nutrition status, and the degree of stress imposed by disease or injury. The Dietary Reference Intake (DRI) for protein for healthy adults is 0.8 g/kg.20 Hospitalized patients often experience accelerated muscle catabolism and net nega-tive nitrogen balance due to acute or chronic illness(es). Metabolically stressed adult patients generally require 1.2–2.0 g/kg of protein.21,22 The goal of protein provision in metaboli-cally stressed patients is to achieve positive nitrogen balance, or a state in which protein synthesis exceeds protein break-down. Nitrogen balance studies can be useful in assessing the adequacy of protein intake, although these studies may be dif-ficult to conduct in the hospital setting due to the need for com-plete and accurate measurements of intake (via oral, enteral, and/or parenteral routes) as well as output (including urine, stool, fistula, wound, and ostomy losses).

Fluid Needs

Water is the most abundant substance in the body, accounting for 50%–60% of body weight. Total body water does vary with age, weight, sex, and adiposity. The goal of fluid management is to maintain adequate hydration, tissue perfusion, and elec-trolyte balance. Healthy adults usually require 30–40 mL/kg daily to achieve fluid balance.21 Assessing fluid status in hospi-talized patients requires physical examination and the assess-ment of intakes and outputs, weights, laboratory values, and vital signs. Most fluid is lost from the GI tract and kidneys, although a significant amount of fluid can also be lost through the lungs and skin. Metabolic changes, such as fever and hyperthyroidism, and medical therapy, such as diuretics or dialysis, can contribute to fluid losses as well.

Micronutrient Needs

Micronutrients are required for effective metabolism and bio-chemical processes. A patient’s specific vitamin and mineral requirements vary depending on the patient’s nutrition and clinical status. A multivitamin/mineral supplement is war-ranted when the nutrition support regimen does not provide sufficient amounts and no other form of nutrition is provided.

Patient Selection

Hospitalized patients with a functional GI tract, who are unable to meet energy and protein requirements orally, are generally

candidates for EN therapy. When oral intake is deemed unsafe, insufficient, or impossible, the clinician must consider the risks and benefits of EN therapy in the context of the patient’s diag-nosis, clinical status, and prognosis and determine whether EN is consistent with the patient and/or family’s wishes.13 Some examples of conditions that merit consideration for EN therapy include endotracheal intubation, swallowing difficulty due to dysphagia, altered mental status or delirium, luminal obstruc-tion in the head and neck area, the esophagus, or the stomach from malignancy, or poor oral intake resulting in weight loss and/or malnutrition. Patients with hypermetabolic and hyper-catabolic states such as trauma, burns, and malignancy may also benefit from EN therapy, as it may be difficult for them to meet the needs with oral intake alone.

Contraindications to enteral feeding may include patients with intractable vomiting or diarrhea, severe GI malabsorp-tion, paralytic ileus, GI ischemia, severe short bowel syn-drome, or high-output enterocutaneous fistula. Relative contraindications include intestinal obstruction, diffuse perito-nitis, or when nutrition intervention is not warranted or desired by the patient or proxy.

Timing of Enteral Nutrition

Initiation of EN should always follow a complete evaluation of the patient’s disease state, medical condition, and the rela-tive risks and benefits. The timing, however, may depend on the indication for EN as well as the patient’s nutrition state. For most hospitalized patients, initiation of EN is recom-mended when oral intake is absent or likely to be absent for a period of 5–7 days.23 However, earlier initiation may be war-ranted in the moderately or severely malnourished patient to support metabolic demands and prevent functional decline. This concept is also reflected in recommendations for the postsurgical patient population, which state that EN should be considered within 7 days of surgery in the normally or overnourished, within 3–5 days of surgery in the moderately malnourished, and within 1–2 days of surgery in the severely malnourished.23 In the critically ill population, it is recom-mended that EN should be started early within the first 24–48 hours following admission to the intensive care unit (ICU)22 due to the beneficial effects on intestinal physiology and immunity discussed previously.

Enteral Access

The selection of an enteral access device should depend on the patient’s disease state, GI anatomy, function and accessibility, and expected duration of therapy.13 Short-term access options include placement through the nose or mouth with the tip of the feeding tube terminating within the stomach, past the pylorus, or distal to the ligament of Trietz. For EN therapy lasting > 4 weeks, more permanent access options include gastrostomy, jejunostomy, and gastrojejunostomy tubes. For all patients who require an enteral access device, close monitoring is required

by Beth Higgins on May 19, 2016ncp.sagepub.comDownloaded from

Page 4: Nutrition in Clinical Practice Enteral Nutrition for ...criticalcarelearningpod.weebly.com/uploads/1/3/0/3/...the lungs and skin. Metabolic changes, such as fever and hyperthyroidism,

Kozeniecki and Fritzshall 637

to maintain patient safety and prevent events such as inadver-tent tube displacement.

Enteral access devices vary with respect to tubing material and size, which is measured using the French (Fr) scale. The French size is a measure of the external diameter of a catheter. One French unit is equal to 0.33 millimeters, so the larger the French size, the larger the catheter. The most common tube sizes used in the adult population range from 8–24 Fr24,25 (Figure 2). Large-bore (≥ 14 Fr) short-term access tubes are made of a stiff polyvinyl material, are less likely to clog, and are easier and more reliable when aspirating gastric contents. Small-bore (8–12 Fr) tubes are made of silicone, polyurethane, or a mixture and are softer and more comfortable for the patient but are more prone to clogging and more difficult to use for aspiration of gastric contents.26

Oro/Nasoenteric

Oroenteric and nasoenteric feeding tubes may be used as short-term access (< 4 weeks’ duration) until more definitive mea-sures are implemented. They can also provide opportunities to assess patient tolerance of EN prior to placement of permanent feeding tubes. Oroenteric (ie, orogastric) tubes are limited by patient discomfort and are better tolerated in intubated and sedated or chemically paralyzed patients. Large-bore nasoen-teric tubes, when used, should be replaced with a more pliable tube of smaller diameter within 5–7 days to potentially reduce morbidity and improve patient discomfort.25

Oroenteric and nasoenteric feeding tubes can be placed at the bedside or using endoscopic or fluoroscopic techniques. Complications that may arise from oroenteric or nasoenteric tube placement include epistaxis, sinusitis, esophageal perfora-tion, and unintentional placement into the bronchopulmonary tree. Bedside placement of nasoenteric (gastric or small bowel) feeding tubes can be achieved without the use of technology, however, use of an electromagnetic tube placement device has demonstrated success rates as high as 90%.27-29 Achieving placement within the jejunum is most reliably achieved with endoscopic or fluoroscopic techniques. As a rule, confirmation of the feeding tube tip position should be obtained prior to the initiation of enteral support.18,25

Contraindications to short-term enteral access include cer-tain patterns of facial fracture, obstruction of the GI tract distal

to the site of access, esophageal varices or diverticula for risk of bleeding, head and neck cancers, and upper GI tract stric-tures so narrow that a tube cannot be passed through it. Disease-related or medication-induced coagulopathies should trigger heightened awareness for complication but generally do not preclude placement.25,26

Enterostomy

For long-term enteral access (> 4 weeks’ duration), percutane-ous feeding tubes can be placed using surgical, endoscopic, fluoroscopic, and radiologic techniques. These tubes are typi-cally made of silicone or polyurethane with a diameter of 14–28 Fr, with the exception of percutaneous endoscopic jejunosto-mies, which are 8–12 Fr.24 Anatomic alterations, presence of ostomy sites or drain tubes, or surgical scars may alter the loca-tion for tube insertion. Once placed, percutaneous endoscopic gastrostomy tubes may be used for feedings within 2 hours in the adult population.30 Contraindications to placement include presence of ascites, neutropenia, peritonitis, and neoplastic, inflammatory, or infiltrative disease of the gastric/abdominal wall.31

Complications from surgically placed tubes may include bleeding, peristomal leakage, skin and soft tissue infection, incisional hernia, injury to intra-abdominal viscera, and com-plications associated with general anesthesia. Delayed compli-cations may include buried bumper syndrome, gastric ulcers, fistulas, and tumor tract seeding.32 Most bumper-type tubes will need to be replaced every 1–2 years, or earlier if breakage, occlusion, or dislodgement occurs. Balloon-type tubes, which are filled with 5–10 mL of sterile water, are often used after the removal of a bumper-type tube. To prevent balloon deflation due to water leakage, the balloon water volume should be checked every week. Due to degradation of the balloons, this type of tube requires replacement every 3–4 months.32

Gastric vs Small Bowel Access

Gastric access is appropriate in most cases, as it allows for more normal nutrient digestion and absorption and more versa-tility in feeding regimen. Feeding into the stomach stimulates the gastric phase of digestion and does not bypass any potential sites for nutrient absorption. Small bowel feeding access may

Figure 2. Common French sizes of adult enteral access devices.

by Beth Higgins on May 19, 2016ncp.sagepub.comDownloaded from

Page 5: Nutrition in Clinical Practice Enteral Nutrition for ...criticalcarelearningpod.weebly.com/uploads/1/3/0/3/...the lungs and skin. Metabolic changes, such as fever and hyperthyroidism,

638 Nutrition in Clinical Practice 30(5)

be achieved by passing a feeding tube past the pylorus (duode-nal placement) or past the Ligament of Treitz (jejunal place-ment) and is most appropriate for patients with gastric outlet obstruction, gastroparesis, gastric fistula, pancreatitis, and known reflux and aspiration of gastric contents.30 Although several studies have demonstrated no difference in aspiration risk between intragastric and small bowel feeding,33,34 small bowel feeding has been promoted as a means to avoid aspiration.

Maintaining Patient Safety

Patient safety should always be considered when providing medical therapies, including the provision of EN. Two unique issues that clinicians encounter in the hospital setting are patient-initiated device removal and the high potential for enteral misconnections. It is important for all members of the healthcare team to be aware of the risk factors for both and to employ prevention strategies to avoid patient harm.

The frequency of nasogastric tube removal has been reported to be 28.9%, the highest rate among all removed devices.35 Patient characteristics found to be closely associated with tube removal include disorientation, restlessness, agita-tion, and anxiety.36 Premature discontinuation of therapeutic devices, including nasoenteric and percutaneous enterostomy devices, may result in patient harm or injury. Of particular con-cern is if inadvertent removal occurs before stoma tract matu-ration, which usually occurs within 7–10 days. If the stoma tract is not mature, the replacement tube cannot be reintro-duced through the same tract but, rather, near the original site to maintain apposition of the stomach to the abdominal wall.31 In addition to the harm that can be caused by tube displacement itself, lack of enteral access can contribute significantly to feeding delays, preventing the patient from receiving adequate nutrition delivery.37 Several strategies have been proposed to prevent self-initiated device removal including taping nasoen-teric tubes to the patient’s face, inserting nasal bridles to secure nasoenteric tubes, and using hand mittens or restraints.38,39 For combative patients with enterostomies, abdominal binders can be useful adjuncts following placement to prevent them access to their tube.25 Some institutions employ constant observers to watch patients to maintain patient safety.

An enteral misconnection is “an inadvertent connection between an enteral feeding system and a non-enteral system such as an intravascular line, peritoneal dialysis catheter, tra-cheostomy, medical gas tubing, etc.”40 More than 116 cases of enteral misconnections were reported between 1972 and 2010,41 and they continue to occur. Inadvertently delivering EN through an intravenous system is a very serious event that can result in patient death from embolus or sepsis. Both human factors and physical and design factors have been identified as contributors to enteral misconnections. Human factors include time con-straints, fatigue, inadequate training, less than optimal room lighting, and patient transfers. Physical and design factors

include the use of universal connectors (ie, Luer connectors), which allow connection between many types of therapeutic devices, as well as inadvertent disconnection.40,42,43 In 2006, the Joint Commission issued a sentinel event alert regarding tubing misconnections44 and urged product manufacturers to imple-ment “incompatibility by design” features for small-bore con-nectors. Since then, a new standard for small-bore connectors has been developed,45 and changes to the EN delivery system have already been set in motion. On the nutrition end, a cross-spike unique to EN (“nutrition source connector”) has been developed and in use since 2012. On the patient end, a new ENFit connector (“patient access connector”) has been devel-oped for enteral administration sets, enteral syringes, and enteral feeding tubes. To improve patient safety, the ENFit con-nector will not allow connectivity with any other therapeutic devices, will provide a locking feature to prevent disconnec-tions, and will have a female connector that will fit only into a new male patient-access feeding tube port.46

Enteral Formula Selection

Commercially prepared enteral formula emerged in the late 1960s and has undergone many changes in formulation since its inception. Today, more than 100 enteral formulas are available for use in the United States and vary greatly with respect to concentration, macronutrient and micronutrient composition, fiber content, and the addition of pharmacologically active sub-stances intended to modulate the immune response. A detailed review of enteral formula components and considerations for use was recently published47; a summary is provided in Table 1. Efficacy studies are not required before enteral products can be manufactured and used in patient care because they cannot be promoted as medications to treat specific diseases. To maintain patient safety and prevent complications of bacterial contami-nation, proper use of administration sets and formula storage should also be taken into consideration when selecting an enteral formula.

Nutrient Composition of Enteral Formulas

The concentrations of enteral formulas range from 1–2 kcal/mL. Formulas with the lowest concentration are approximately 85% water and have an osmolality closer to that of the body’s intracellular and extracellular fluids (285–290 mOsm/kg). These formulas may be useful in patients with diarrhea to pre-vent osmotic-induced dumping. Formulas with the highest concentrations are approximately 70% water and may be used in patients requiring a fluid restriction secondary to conditions such as congestive heart failure, renal failure, liver failure, syn-drome of inappropriate antidiuretic hormone, or hypervolemic hyponatremia.

Carbohydrates represent the primary macronutrient in most enteral formulas and are usually provided in the form of corn syrup solids, hydrolyzed corn starch, and maltodextrin. Some

by Beth Higgins on May 19, 2016ncp.sagepub.comDownloaded from

Page 6: Nutrition in Clinical Practice Enteral Nutrition for ...criticalcarelearningpod.weebly.com/uploads/1/3/0/3/...the lungs and skin. Metabolic changes, such as fever and hyperthyroidism,

Kozeniecki and Fritzshall 639

formulas may contain sucrose or fructose as well. Most enteral formulas do not contain lactose and are gluten free.

Protein can be provided in various forms including intact or hydrolyzed proteins from soy, casein, and whey, or as crystal-line amino acids. Formulas containing hydrolyzed proteins and amino acids are often termed semi-elemental and elemental, respectively. Although they are marketed as being more easily digested and better tolerated, the superiority of elemental vs polymeric formulas has not been clearly demonstrated as there is limited research in this area. However, hydrolyzed protein formulas may be considered in patients with persistent diarrhea, pancreatic disease, or other malabsorptive conditions.22

Fat is provided in enteral formulations as long-chain fatty acids (LCFAs) obtained from corn, soybean, sunflower, and safflower oils, as medium-chain triglycerides (MCTs) from palm kernel and coconut oil, or as structured lipids that combine LCFAs and MCTs on the same molecule. Some formulas also contain eicosapentaenoic acid and docosa-hexaenoic acid from fish oil. It is important to note that although MCTs do not require bile salts or pancreatic enzymes

for digestion and are metabolized at the cellular level without the assistance of carnitine, they do not provide a source of essential fatty acids and must be used in combination with LCFAs.

Most enteral formulas have been designed to meet the DRI for vitamins and minerals in a volume of 1–1.5 liters per day. If the minimum volume required to meet the DRI is not consis-tently being provided, supplemental vitamins and minerals may be required. On the other hand, some formulas contain increased amounts of certain vitamins or minerals. It is impor-tant that the clinician pays particular attention to the amount of vitamins and minerals being provided by all sources to avoid the consequences of inadequate or excess intake.

Whereas some enteral formulas are fiber free, many contain fiber in differing types and amounts to promote the health of the GI tract and maintain regular bowel function. Insoluble fiber acts as a bulking agent, increasing the speed at which stool moves through the intestines, whereas soluble fiber keeps the stool soft by absorbing water.48 Common sources of fiber include soy fiber and guar gum. Many also contain prebiotics

Table 1. Categories of Commercially Prepared Enteral Formulas and Modular Products.

Formula Type Characteristics and Variations Considerations

Polymeric Contains whole protein as the nitrogen source. Content can vary greatly in terms of caloric density, macronutrient distribution, amount and type of fiber added, and vitamin, mineral, and electrolyte composition.

Suitable for patients with normal or near normal functioning bowel (ie, no significant malabsorptive disorders).

Hydrolyzed or “predigested”

Proteins are hydrolyzed to peptides (peptide based), amino acids (elemental), or a combination of both (semi-elemental).

Suitable for patients with extensive impairment of gastrointestinal function (ie, significant malabsorptive disorders such as persistent diarrhea, pancreatic disease, or significant gastrointestinal resection). Not intended for routine use.

Disease specific Content can vary greatly in terms of caloric density, macronutrient distribution, amount and type of fiber added, and vitamin, mineral, and electrolyte composition.

Use of some disease-specific formulas (pulmonary, diabetic, and hepatic) is not currently supported by strong research. Efforts should be made to avoid overfeeding.

•• Renal•• Diabetic•• Hepatic•• Pulmonary

Immune modulating Contain any combination of pharmacologically active substances such as arginine, glutamine, ω-3 fatty acids, γ-linolenic acid, nucleotides, or antioxidants. Can be polymeric or hydrolyzed. Content can vary greatly in terms of caloric density, macronutrient distribution, amount and type of fiber added, and vitamin, mineral, and electrolyte composition.

Intended to modulate immune function. Designed with appropriate physiologic rationale for specific patient populations, but due to conflicting outcomes data, use should be determined on a case-by-case basis.

Modular products Contain predominantly 1 nutrient. Consider the size of the enteral access device as some modular products may increase risk of tube occlusion. Ensure adequate flushing before and after administration of modular products.

•• Protein•• Carbohydrate•• Lipid•• Fiber

by Beth Higgins on May 19, 2016ncp.sagepub.comDownloaded from

Page 7: Nutrition in Clinical Practice Enteral Nutrition for ...criticalcarelearningpod.weebly.com/uploads/1/3/0/3/...the lungs and skin. Metabolic changes, such as fever and hyperthyroidism,

640 Nutrition in Clinical Practice 30(5)

in the form of fructooligosaccharides, oligofructose, or inulin. Manufacturers have also developed unique blends of fiber with the theoretical intention of improving gut flora. The overall fiber content of most enteral formulas is well below the recom-mended 14 g/1000 kcal to achieve daily intakes of 25–38 g/day. It has been recommended to avoid the use of fiber-con-taining products in hypotensive patients at high risk for devel-oping ischemic bowel and patients with severe dysmotility.22

Enteral Additives and Modular Products

Enteral formula can only be provided “as is.” Although there are many different products on the market, it is not possible for institutions to maintain a supply of them all. Therefore, a clini-cian’s ability to meet the needs of all patients using the institu-tion’s formulary may be limited. For some patients, their “ideal” formula may not even exist. In these situations, the use of modular products, which are administered separately from the enteral formula, can be helpful. More than 20 modular products are available in the United States. The largest compo-nent of each modular product is usually a single nutrient. Protein modulars are used most frequently, compared with fat or carbohydrate modulars, to help meet the protein needs of hypermetabolic or hypercatabolic patients or those with exces-sive losses through wound exudate, fistula effluent, or thera-pies such as continuous renal replacement therapy. Fiber additives are also commonly used to help manage stool fre-quency and consistency in the hospital setting.

Regulatory Standards

It is important to note that enteral formulas are considered medical foods by the U.S. Food and Drug Administration (FDA), defined as “a food which is formulated to be consumed or administered enterally under the supervision of a physician and which is intended for the specific dietary management of a disease or condition for which distinctive nutritional require-ments, based on recognized scientific principles, are estab-lished by medical evaluation.”49 Although medical foods must comply with all applicable FDA requirements for foods, they are exempt from the labeling requirements for health claims and nutrient content claims. Because the research of disease-specific formulas with regard to improved clinical outcomes is limited, it is important for the clinician to avoid using the patient’s medical condition alone to guide enteral formula selection.

Food Allergies, Sensitivities, and Strict Dietary Practices

It is important for the clinician to keep in mind each patient’s food allergies, sensitivities, and dietary practices when choos-ing an enteral formula. As mentioned previously, most enteral formulas do not contain gluten or lactose due to the

commonality of gluten and lactose intolerance in the adult population. For patients with food allergies such as egg, corn, casein, whey, and soy, the clinician should refer to the most recent product label, as ingredient lists may change due to product reformulation and/or different suppliers providing ingredients for the products. Most manufacturers will include on the product label whether it is suitable for halal or kosher practices. For vegan patients, attention should be paid to the list of ingredients to ensure that the source of protein is derived from soy rather than whey or casein.

Administration Sets and Hang Time

According to manufacturer guidelines, the hang time for sterile formula in a closed system (eg, ready-to-hang bottles or bags of formula) is 24–48 hours, whereas the hang time for a sterile formula in an open system (eg, formula poured into an admin-istration set) is 8 hours for hospitalized patients and 12 hours for patients in the home setting.30 Any nonsterile formula (eg, powder formula) that needs to be reconstituted by mixing with sterile water should hang for no more than 4 hours; if not used immediately, reconstituted formula can be refrigerated for up to 24 hours after preparation.30 Open-system enteral adminis-tration sets should be changed every 24 hours in the hospital setting to prevent unacceptably high levels of bacteria from accumulating in the tubing.50,51 Due to the increased nursing time required to change enteral formula systems more fre-quently and the reduced risk of contamination, many institu-tions prefer to use closed-system enteral formulas as much as possible. Additions to closed-system containers are to be avoided.22

Initiation and Advancement

EN may be administered in a variety of ways, and the method of administration can strongly affect the success of EN therapy. To determine the most appropriate method of administration, the clinician should consider the patient’s age, preexisting and current medical condition(s), nutrition status and requirements, the location of the feeding tube tip, and the patient’s expected tolerance.

A study by Desachy et al52 compared the initial efficacy and tolerability of early EN with immediate vs gradual introduction of optimal flow rate among 100 shock-free intubated and mechanically ventilated patients. In the immediate optimal flow group, EN was initiated at the rate corresponding to 25 kcal/kg/day (average 75 mL/hour). In the gradual introduction group, EN was initiated at a flow rate of 25 mL/hour and increased in increments of 25 mL/hour every 24 hours until the rate corresponding to 25 kcal/kg/day was reached (average of 76.5 mL/hour). Patients in the immediate group received a sig-nificantly higher amount of calories compared with those in the gradual group, with no differences in the rates of diarrhea or suspected aspiration pneumonia. The authors concluded that

by Beth Higgins on May 19, 2016ncp.sagepub.comDownloaded from

Page 8: Nutrition in Clinical Practice Enteral Nutrition for ...criticalcarelearningpod.weebly.com/uploads/1/3/0/3/...the lungs and skin. Metabolic changes, such as fever and hyperthyroidism,

Kozeniecki and Fritzshall 641

EN can be introduced at the optimal dose regimen in select patients. Patients who may benefit from more conservative ini-tiation and advancement of EN include patients who have not been fed for an extended period of time; have not received enteral nutrients in a long time; are hemodynamically unstable, requiring vasopressors or inotropic agents; are chemically par-alyzed; have recently undergone a significant bowel resection, temporary abdominal closure, or multiple abdominal re-explo-rations; or who have bowel wall edema.26

Delivery Methods

Continuous feeding is commonly used for the adult hospital-ized patient requiring EN therapy and is achieved via pump assist. The goal infusion rate is determined by dividing the desired formula volume by the number of hours of administra-tion. Because of the frequency with which enteral feeds are interrupted in the hospital setting, resulting in delivery of only 50%-60% of prescribed EN volume on a daily basis, some institutions have implemented a volume-based feeding proto-col to ensure that the volume of EN prescribed to their patients is actually provided.53,54 To allow for time away from feeding, intermittent or bolus feedings may be used. Bolus feedings are defined as formula delivered by gravity-assist or syringe over approximately 15 minutes, whereas intermittent feedings are usually delivered over 30–45 minutes via gravity assist or pump assist.55 These feeding methods are usually reserved for medically stable patients with feeding tubes terminating in the stomach. Volumes typically range from 240–720 mL per feed-ing, depending on individual tolerance, with a frequency from 2–6 times daily. Hospitalized patients may transition from 1 delivery method to another as their clinical status changes. Sample calculations are provided in Figure 3.

Monitoring, Troubleshooting, and Managing Complications

As patient condition can change quickly and frequently in the hospital setting, continuous reassessment and reevaluation are

required in order for the clinician to adapt the nutrition support plan to the patient’s needs. Recommended monitoring for patients receiving EN includes adequacy of intake; weight; hydration status; electrolyte and acid-base balance; glycemic control; presence of nausea, vomiting, abdominal distention, pain, or discomfort; stool frequency and consistency; patency of the enteral access device; and the potential for vitamin/min-eral deficiencies and drug-nutrient interactions. The frequency of monitoring should depend on the patient’s severity of ill-ness, level of metabolic stress, and degree of malnutrition. This section reviews some of the common and more serious compli-cations seen in the adult hospitalized patient population, including potential causes and strategies to mitigate them (Table 2).

Refeeding Syndrome

The term refeeding syndrome is generally reserved to describe the metabolic alterations that occur during nutrition repletion of severely malnourished or starved individuals in amounts greater than a weakened cardiopulmonary system can accom-modate.87,88 Hypophosphatemia is considered the hallmark of refeeding syndrome, although other clinical manifestations include hypokalemia, hypomagnesemia, thiamin deficiency, and sodium retention/fluid overload. Clinicians should always consider the patient’s nutrition status when initiating EN, as this can help determine the patient’s risk of developing meta-bolic alterations that could potentially lead to multiorgan sys-tem dysfunction and even death.89 Patients most at risk for refeeding syndrome include those with minimal intake for > 7 days with evidence of metabolic stress; significant weight loss; undernutrition as a result of chronic disease(s); anorexia ner-vosa; persistent nausea, vomiting, or diarrhea; malabsorptive conditions; or history of excessive alcohol intake.56,87,90 Although clinicians could be inclined to believe that refeeding is unlikely among an increasing percentage of overweight and obese patients, coupled with modern practices of conservative energy provision, the prevalence of acute and chronic disease-related malnutrition renders refeeding syndrome a very real

Continuous (Set Rate- or Volume-Based)1) Determine target volume: 1440 mL/day2) Determine duration of therapy: 24 hours/day3) Determine pump rate (Set Rate): 1440 mL ÷ 24 hours = 60 mL/hr4) For volume-based feeding: Start with set rate and adjust based on the volume remaining and number of hours left in the day. Maximum infusion rate may be institution-specific.

Intermittent and Bolus1) Determine target volume: 1440 mL/day2) Determine number of feedings per day: 3 feedings/day3) Determine volume per feeding: 1440 mL ÷ 3 feedings = 480 mL per feeding4) Determine duration of each feeding: 15-45 minutes per feeding, individualized based on patient tolerance

Figure 3. Sample enteral nutrition calculations based on method of administration.

by Beth Higgins on May 19, 2016ncp.sagepub.comDownloaded from

Page 9: Nutrition in Clinical Practice Enteral Nutrition for ...criticalcarelearningpod.weebly.com/uploads/1/3/0/3/...the lungs and skin. Metabolic changes, such as fever and hyperthyroidism,

642 Nutrition in Clinical Practice 30(5)

Table 2. Complications in Enterally Fed Patients and Prevention/Treatment Strategies.

Complication Cause Prevention/Treatment

Refeeding syndrome55-57

•• Rapid reintroduction of carbohydrates during nutrition repletion in severely malnourished or starved individuals

•• Correct electrolyte abnormalities prior to initiation and during delivery of nutrition

•• Start and increase calorie provision conservatively over the course of 5–7 days

•• Minimal initial fluid and sodium provided•• Supplement with 50–100 mg intravenous/oral thiamin for 5–7

daysNausea/

vomiting58-63•• Motion sickness•• Emotional stress•• Headaches or migraines•• Indigestion•• Delayed gastric emptying

•• Provide an anti-emetic regimen•• Use prokinetic agents to increase gastric motility•• Reduce, replace, or discontinue medications that delay gastric

emptying•• Consider a lowfat, isotonic, or more calorically dense formula•• Ensure enteral formula and water flushes are delivered at room

temperature•• Temporarily reduce the enteral infusion rate by 20–25 mL/

hour or extend the infusion time of cycled or intermittent feeds•• Obtain postpyloric enteral access

Aspiration pneumonia64

•• Contaminated oropharyngeal secretions •• Adequate handwashing and hand disinfection•• Elevate head of bed 30–45 degrees, especially while providing

enteral nutrition•• Provide subglottic suctioning, drain condensate from ventilator

circuits, and provide chlorohexidine oral rinse as appropriate•• Achieve adequate glucose control•• Avoid unnecessary antibiotics

Diarrhea30,65-69 •• Medications•• Infections, illness severity, and disease

states•• Bacterial contamination•• Enteral formula

•• Discontinue or reduce dose of offending medication, or replace with alternative non–diarrhea-causing medication

•• Change from liquid solution to tablet form or dilute hypertonic medications

•• Identify and treat underlying medical/surgical issues and infections

•• Consider adjusting the type of formula depending on disease state to prevent malabsorption

•• Use a clean, aseptic technique when handling the feeding system

•• Use sterile, liquid formula formulations over powder, reconstituted formulas when possible

•• Limit formula hang time, especially when using an open system

•• Provide education and training on policies, procedures, and practices associated with preparing, storing, and administering enteral formula

•• Adjust fiber type and/or amount provided; consider decreasing insoluble fiber or increasing soluble fiber

•• Consider an isotonic formula or slower infusion rate•• Try a peptide-based formula or one with a higher percentage

of fat from medium chain triglycerides or structured lipids•• Ensure that the formula, modulators, and water flushes are

room temperatureConstipation70-75 •• Medications

•• Laxative abuse•• Inadequate fluid or fiber intake•• Neuromuscular, hypothyroid, and

gastrointestinal disorders•• Lack of physical activity

•• Adjust medications that decrease gastrointestinal motility•• Add or adjust bowel regimen•• Use fiber-containing enteral formulas if no contraindication

exists•• Increase amount of free water provided•• Promote ambulation as able

(continued)

by Beth Higgins on May 19, 2016ncp.sagepub.comDownloaded from

Page 10: Nutrition in Clinical Practice Enteral Nutrition for ...criticalcarelearningpod.weebly.com/uploads/1/3/0/3/...the lungs and skin. Metabolic changes, such as fever and hyperthyroidism,

Kozeniecki and Fritzshall 643

Complication Cause Prevention/Treatment

Ileus22,76-81 •• Electrolyte imbalances•• Major lower gastrointestinal surgeries•• Delayed enteral nutrition•• Inflammation•• Medications

•• Correct electrolyte abnormalities•• Consider initiating early enteral nutrition in setting of a mild to

moderate ileus•• Limit sedatives and paralytic agents as much as possible

Clogged feeding tube18,82-86

•• Suboptimal flushing techniques•• Improper medication administration•• Precipitation of enteral formulas by

gastric acid•• Small-bore feeding tubes•• Formula composition

•• Flush enteral devices with 20–30 mL of warm water every 4 hours during continuous feeds and before and after intermittent feedings and medications

•• Avoid flushing enteral access devices with carbonated beverages and juices

•• Minimize contact of liquid medications with enteral formula or crush tablets into a fine powder before mixing with water

•• Avoid frequent checking of gastric residual volumes•• Reference manufacturer recommendations to ensure the

enteral formula being used is compatible with the patient’s enteral access device

•• Treat clogged tubes with a warm water flush with moderate pressure, activated enzyme solutions, or an approved declogging device

•• Replace enteral access device

Table 2. (continued)

possibility. Based on case reports, refeeding syndrome can manifest itself up to 5 days after the initiation of feedings.88

A variety of strategies have been suggested to prevent the deleterious effects of refeeding syndrome. Any serum electro-lyte abnormalities should be corrected prior to initiation of nutrition. Calorie provision should be started and increased conservatively, although recommendations vary. Common rec-ommendations include starting energy intake at 15–20 kcal/kg/day, 1000 kcal/day, or 50% of estimated needs57 and gradually increasing to goal amounts over 5–7 days, keeping in mind that the minimum carbohydrate requirement to suppress gluconeo-genesis, spare proteins, and supply fuel to the central nervous system is approximately 100–150 g/day.58 The amount of fluid and sodium initially supplied should be minimized because of the expansion of the extracellular water compartments and the propensity to retain these during initial refeeding. Serum val-ues of sodium, potassium, magnesium, and calcium should be monitored daily during the first week and replaced as indi-cated. Last, because thiamin is an essential cofactor in the metabolism of carbohydrate, supplementation in the range of 50–100 mg/day intravenously or 100 mg orally for 5–7 days is recommended for patients at risk for refeeding.87

Nausea/Vomiting

There are many causes of nausea and vomiting, which are often quite similar. Common causes include motion sickness, emo-tional stress (fear), headaches or migraines, indigestion, food poisoning, various viruses, and certain smells or odors. The most common cause of nausea and vomiting, especially in criti-cally ill patients, appears to be delayed gastric emptying.59,60

Risk factors for delayed gastric emptying include hyperglyce-mia, illness severity, low Glasgow Coma Score, elevated intra-cranial pressure, traumatic brain injury, recent anesthesia or surgery, surgical vagotomy, use of certain medications (eg, opi-ates, analgesics, anticholinergics), rapid infusion of formula, and the use of a high fat formula.59-62,91

Nausea and vomiting have been reported in up to 26% of patients receiving EN therapy.63 Usually, these symptoms can be successfully managed without needing to initiate parenteral nutri-tion. Anti-emetic medications can help manage nausea quite effectively if scheduled on a regular basis. Prokinetic agents such as metoclopramide and erythromycin can increase gastric motil-ity and are especially effective when used in combination.92 If delayed gastric emptying is suspected, other interventions may include reducing, replacing, or discontinuing opiates, analgesics, and anticholinergics. Adjustments to the EN formula or regimen should also be considered, if possible. Strategies may include changing the enteral formula to one that is low in fat, isotonic, or more calorically dense, ensuring that enteral formula and water flushes are being administered at room temperature, temporarily reducing the rate of enteral infusion by 20–25 mL/hour, extend-ing the infusion time of cycled or intermittent feeds, and obtain-ing postpyloric enteral access.60,61,63,91

Gastric Residual Volume and Aspiration Pneumonia

Historically, gastric residual volumes (GRV) have been used to assess tolerance to EN and determine one’s risk for aspiration/aspiration pneumonia. This practice remains controversial as neither the practice nor the method of checking GRV itself is

by Beth Higgins on May 19, 2016ncp.sagepub.comDownloaded from

Page 11: Nutrition in Clinical Practice Enteral Nutrition for ...criticalcarelearningpod.weebly.com/uploads/1/3/0/3/...the lungs and skin. Metabolic changes, such as fever and hyperthyroidism,

644 Nutrition in Clinical Practice 30(5)

validated. Limitations to accurate measurement include the position of the patient, type and size of the syringe used, and the size, material, and position of the tip of the feeding tube.93 In addition, the quality (color, consistency) and composition of gastric volumes are rarely differentiated and may include recently administered medications and water flushes rather than undigested formula alone.

Pneumonia and bacterial contamination of the respira-tory tract are often caused by aspiration of contaminated oropharyngeal secretions originating from the upper airway, teeth, artificial airway, ventilator-circuit condensate, or nasal sinuses.64 Additional data suggest the relative impor-tance of oropharyngeal colonization over gastric colonization in the development of ventilator-associated pneumonia.94-96 Nonnutrition prevention strategies, therefore, include (but are not limited to) adequate handwashing and hand disinfection; head of bed elevation of 30–45 degrees especially while receiving EN; scheduled drainage of condensate from venti-lator circuits (if applicable); subglottic suctioning; chloro-hexidine oral rinse in selected patients; avoidance of unnecessary antibiotics; and insulin therapy to maintain serum glucose levels within the desired range.

Regarding GRV, the results of several studies have demon-strated that a lower GRV cutoff value of 50–150 mL compared with a higher cutoff of 250–500 mL does not decrease the risk of

regurgitation, aspiration, or pneumonia97-99 but instead increases the unnecessary withholding of EN.100 It has been recommended that interruption of EN should be avoided for GRV < 500 mL in the absence of other signs and symptoms of intolerance (nausea, vomiting, bloating, abdominal discomfort or distention) but that close monitoring is warranted in patients with gastric residuals between 200 and 500 mL, ensuring that all measures to reduce aspiration risk are initiated.22 Recently, results from a large ran-domized controlled trial suggest no beneficial effect of monitor-ing GRV at all; however, these results represent primarily a medical population with a low incidence of GI disorders.101 Although GRV may not be useful in determining aspiration risk, it remains a simple and insightful tool to help clinicians detect early signs of GI dysfunction, thereby allowing for timely inter-vention. Figure 4 provides an example of an algorithm designed to manage GRV and optimize patient tolerance to EN.

Diarrhea

Diarrhea is a serious condition and can cause electrolyte abnor-malities, dehydration, loss of nutrients, fecal incontinence leading to skin breakdown, malabsorption from increased transit time, and inadequate nutrient intake from pausing or stopping EN. The inci-dence of diarrhea in the hospital setting is difficult to determine given the lack of a standardized definition and wide range of

Yes

No

No

Yes

Yes

No

Measure gastric residual volumes every 4 hoursor

Before intermittent feedings

GRV > 500 mL?

Are there other signs of intolerance?Examples: abdominal distention, firmness, or pain; retching/vomiting

1.) Refeed residuals up to 500 mL

2.) Hold tube feeds for 1 hour and recheck GRV

Strategies to reduce aspiration risk and improve EN tolerance:

1.) Elevate HOB > 30°

2.) Good oral care

3.) Regular assessment of tube position

4.) Achieve glycemic control to prevent gastroparesis

5.) Minimize use of narcotics and sedatives

6.) Promote regular bowel movements

7.) Use prokinetic agents as indicated

8.) Place post-pyloric feeding tube

1.) Discard residual (total amount)

2.) Restart tube feeds at half of the previous rate (minimum 20 mL/hr). Give half goal volume if intermittent.

3.) Notify physician

4.) Utilize strategies to reduce aspiration risk and improve tolerance

1.) Hold tube feeds OR decrease rate by half

2.) Notify physician

3.) Utilize strategies to reduce aspiration risk and improve tolerance

4.) Restart/advance tube feeds when issue resolved

1.) Continue feeding

2.) Utilize strategies to reduce aspiration risk and improve tolerance

GRV > 500 mL?

Figure 4. Sample algorithm for managing gastric residual volumes. EN, enteral nutrition; GRV, gastric residual volume; HOB, head of bed.

by Beth Higgins on May 19, 2016ncp.sagepub.comDownloaded from

Page 12: Nutrition in Clinical Practice Enteral Nutrition for ...criticalcarelearningpod.weebly.com/uploads/1/3/0/3/...the lungs and skin. Metabolic changes, such as fever and hyperthyroidism,

Kozeniecki and Fritzshall 645

patient populations studied.22,65,102 It has been reported that diar-rhea occurs in 30% of patients on medical and surgical floors and > 80% of patients in intensive care units.13,23 In tube-fed patients alone, the incidence of diarrhea ranges from 11.3%–66.1%, depending on the definition used.103 Definitions of diarrhea often include frequency of bowel movements of 3 or more watery or loose bowel movements in a 24-hour period, or stool weight of > 200 g/day. Descriptive terms such as passage of loose, unformed stool or the presence of both abnormal stool frequency and liquid consistency are also used.65,104,105 Although diarrhea is a com-monly reported side effect of EN, it can also be caused by many

other factors in the hospitalized patient. Traditionally, diarrhea is categorized as motility-related, malabsorptive, inflammatory/exudative, secretory, or osmotic (Table 3). Therefore, managing diarrhea in the enterally fed patient requires a systematic approach prior to making changes to the enteral feeding regimen. Understanding the type of diarrhea can help establish a differential diagnosis and guide treatment strategies.

Infectious etiologies and medical conditions should always be considered, evaluated, and treated appropriately if identi-fied. Clostridium difficile infection is the most frequently iden-tified cause of nosocomial diarrhea.107 The incidence and

Table 3. Categories of Diarrhea.66,106

Type Description Characteristics Common Causes

Dysmotility Altered gastric, small bowel, or colonic motility causing rapid transit time or increased intestinal motility

•• Alternating between constipation and diarrhea

•• Diabetic neuropathy•• Hyperthyroidism•• Irritable bowel syndrome•• Postsurgical (gastrectomy, vagotomy)

•• Improvement overnight or when fasting

•• Intermittent, nonlocalizing abdominal pain

•• Sensation of incomplete evacuation after bowel movement

Inflammatory or exudative

Impaired water and electrolyte absorption due to intestinal inflammation

•• Elevated white blood count•• Presence of mucus, blood,

and/or plasma proteins in stool

•• Intestinal lumen damaged (graft-vs-host disease, radiation enteritis)

•• Small bowel disorders (Crohn’s disease, ulcerative colitis)

Malabsorptive Damage to or loss of absorptive ability causing maldigestion of nutrients

•• Bloating •• Gastric bypass surgery•• Excess gas •• Pancreatic insufficiency or disease•• Steatorrhea •• Short bowel syndrome•• Weight loss •• Small bowel bacterial overgrowth

•• Small bowel mucosal diseases (celiac sprue)Osmotic The bowel is unable to

reabsorb fluid as it passes through the intestinal lumen due to the presence of nonabsorbable, osmotically active solutes

•• Decreased stool with fasting or withholding the poorly absorbed substrate

•• Bowel resection or villi and brush border atrophy

•• Incomplete breakdown or malabsorption of nutrients in small intestine (lactose, hyperosmolar substances, sugar alcohols, fat)

•• Medication induced (osmotic laxatives and antacids [magnesium, phosphate, sulfate], sugar alcohol containing [mannitol, sorbitol, xylitol])

•• Fecal osmotic gap > 50 mOsm/kg

•• Stool volume of < 1 liter daily (usually proportionate to the offending substrate)

Secretory An increase in the amount of fluid drawn into the intestinal lumen at a rate exceeding the absorptive capacity of the bowel

•• Low or absent fecal osmotic gap (< 50 mOsm/kg)

•• Alcohol abuse•• Bile acid malabsorption•• Endocrine disorders (hypothyroidism)•• Hormones secreted by neuroendocrine

tumors•• Infectious agents (Escherichia coli,

Salmonella, Clostridium difficile)•• Medication induced (antiarrhythmics,

antibiotics, antineoplastics, biguanides, calcitonin, cardiac glycosides, colchicine, nonsteroidal anti-inflammatory drugs, prostaglandins, ticlopidine)

•• Stool volume of > 1 liter daily•• Unrelated with food intake or

no change in stool with fasting

•• Postsurgical (cholecystectomy, intestinal resection)

by Beth Higgins on May 19, 2016ncp.sagepub.comDownloaded from

Page 13: Nutrition in Clinical Practice Enteral Nutrition for ...criticalcarelearningpod.weebly.com/uploads/1/3/0/3/...the lungs and skin. Metabolic changes, such as fever and hyperthyroidism,

646 Nutrition in Clinical Practice 30(5)

duration of diarrhea has also been associated with severity of illness, hypermetabolic stress, serum albumin level, decreased immunity, glucose control, white blood cell count, and periph-eral oxygen saturation.108-110

Medication administration also has the potential to contrib-ute to diarrhea. Liquid medication solutions, for example, can contain a number of poorly absorbed sweeteners (eg, sorbitol) and stabilizers, which increase the osmolality of the medica-tion and, therefore, the potential to cause diarrhea. As little as 10–20 g/day of sorbitol has been shown to produce GI side effects (gas, cramping, bloating, and diarrhea) and doses ≥ 20 g/day can produce osmotic-induced dumping syndrome.70,111,112 A dose of 1.3–3.9 g of acetaminophen provides about 8–24 g sorbitol.67 Other medications known to cause diarrhea include antibiotics, antihypertensives, cholinergics, GI agents, glu-cose-lowering agents, anti-inflammatory drugs, laxatives, pro-kinetic agents, selective serotonin reuptake inhibitors, and chemotherapy agents.68,104,113 Discontinuing or reducing the dose of an offending medication or changing the form of the medication can help reduce medication-induced diarrhea. Addition of probiotics may attenuate diarrhea, especially if associated with antibiotic use; however, more research is needed to determine the strains and doses needed to provide benefit.22,71 Antidiarrheal medications can also be considered.

After all other causes of diarrhea have been ruled out, an assessment of the EN regimen may be warranted. EN-associated diarrhea has been attributed to microbial contamination, low fiber content, and hyperosmolarity of the EN formula.108 As mentioned previously, many hospitals now use closed systems of EN administration to reduce the risk of contamination. Use of soluble fiber-containing enteral formula can help reduce the incidence of diarrhea, as shown in a 2008 meta-analysis.114 Soluble fiber modular products can be used if such enteral for-mulas are unavailable. Slowing the formula infusion rate or changing to an iso-osmolar formula may also be beneficial,26 although the osmolarity of the EN formula is not thought to be a major contributor to diarrhea in enterally fed patients with a functioning GI tract.69 For patients with maldigestion or mal-absorption, the addition of a semi-elemental or elemental for-mula with greater percentage of fat from MCTs or structured lipids may improve tolerance.115

Constipation

Constipation is also common among enterally fed patients, especially the elderly and bedridden. In critically ill patients, the incidence of constipation has been reported in the range of 15%-83%.72 Many definitions of constipation exist, although most consistently identify infrequent and difficult defecation as defining characteristics.114 The main causes of constipation among patients receiving EN are medications (benzodiaze-pines and opioids being the most common), inadequate fluid intake or dehydration, inadequate fiber intake, and lack of

physical activity.67,73,112 Other causes of constipation include neuromuscular disorders, hypothyroid disorders, GI motility disorders, and history of laxative abuse.112 Constipation can cause abdominal distension or bloating, vomiting, fecal impac-tion, and bowel perforation, therefore increasing the need for nursing, medical, and/or pharmaceutical interventions.74 For these reasons, constipation has been associated not only with feeding intolerance and delays in EN therapy but also with dif-ficulty weaning from mechanical ventilation in critically ill patients, longer length of ICU stay, and decreased quality of life.73-75

Management of constipation in the enterally fed patient may include adjustments in fiber, fluid, and/or medications with the goal of restoring normal bowel function and decreas-ing symptoms related to constipation. Use of fiber-containing enteral formulas can help to normalize bowel function and reduce the need for laxatives.114,116 To minimize constipation associated with increased fiber intake, at least 1 mL/kcal of fluid is required.48 It is worth noting that the use of concen-trated enteral formulas will likely require large water flush volumes to meet this fluid requirement. If constipation does not improve with increased fiber intake, or if fluid restriction is warranted due to other medical conditions such as conges-tive heart failure or renal disease, stool softeners, laxatives, and/or enemas may be required to manage and prevent con-stipation. Other patients who may require a scheduled bowel regimen include those receiving medications that decrease GI motility (eg, sedatives or opioids)75 or who are unable to ambulate.

Ileus

The presence or absence of bowel sounds is often used to deter-mine whether the GI tract is functional and may therefore deter-mine EN initiation or delay.117 However, bowel sounds do not always correlate with normal bowel function. In the setting of ileus, for example, bowel sounds can range from hypoactive to nonexistent, but in the setting of an obstruction, bowel sounds may become louder, high-pitched, or even hyperactive.118 The lack of peristalsis, which characterizes ileus, leads to the accu-mulation of both gas and fluids within the bowel, causing abdominal distension, nausea, and/or vomiting if gastric decom-pression is not provided.76,77,119 Ileus occurs in 24%–75% of postoperative patients and 50%–80% of critical care patients.77 Major lower GI surgeries are the most common cause of an ileus, and other risk factors include infection and inflammation, electrolyte imbalances, delayed EN, and the certain use of drugs (sedatives, opioid analgesics, alpha-2 adrenergic receptor ago-nists, and catecholamine vasopressors).22,78,119,120

After surgery, small bowel, gastric, and colonic motility are regained within 24 hours, 1–2 days, and 3–5 days, respectively.79,119 Nutrition is commonly withheld in this population, or provided parenterally, until return of bowel function due to concern that

by Beth Higgins on May 19, 2016ncp.sagepub.comDownloaded from

Page 14: Nutrition in Clinical Practice Enteral Nutrition for ...criticalcarelearningpod.weebly.com/uploads/1/3/0/3/...the lungs and skin. Metabolic changes, such as fever and hyperthyroidism,

Kozeniecki and Fritzshall 647

the digestive tract will not tolerate feedings following the manip-ulation experienced during surgery and anesthesia. However, the presence of enteral nutrients initiates intestinal propulsive activ-ity and stimulates the secretion of various intestinal hormones, which have a positive effect on GI motility.119 An early study showed that EN can be safely initiated immediately postopera-tively with ileus resolving within 48 hours.80 Other studies have shown quicker return of bowel function with early enteral feed-ing.81,82,121 For these reasons, guidelines support feeding through mild to moderate ileus.22

Clogged Feeding Tubes

All feeding tubes are subject to mechanical complications such as occlusion/clogging, for a variety of reasons. Usual causes include suboptimal flushing techniques, improper medication administration, precipitation of enteral formulas by gastric acid (protein denaturation), and use of small-bore feeding tubes.83,84,122 High-fiber and calorically dense formulas have also been identified as risk factors for tube occlusion.

To prevent clogging, several strategies may be employed. Enteral access devices should be flushed with 20–30 mL of warm water every 4 hours during continuous feeding, before and after intermittent feeding, and before and after medication administration.18,85 Although liquids have long been considered the preferred medication formulation selected for administration via enteral feeding tubes,86 many are acidic. It is therefore impor-tant to minimize contact with EN formulas as these acidic fluids have a high potential to contribute to tube occlusion.123 If no other alternatives are available, tablets should be crushed to a fine powder before mixing with water to avoid accumulation of pill fragments within the tube.83 Frequent checking of GRVs should be avoided when possible to reduce the likelihood of tube occlusion from precipitation of the enteral formula.84,122 In gen-eral, most adult enteral formulas are manufactured to allow smooth flow through enteral tube diameters as small as 8–12 Fr, although it is best to reference the manufacturer’s recommenda-tions when choosing an enteral formula to ensure that it is com-patible with your patient’s enteral access device.

Once an enteral access device has become occluded, the cli-nician must either remove and replace the device or remove the clog. Several methods for restoring tube patency have been described.84 In general, a warm water flush with moderate pressure is recommended as the first-line treatment for clogged feeding tubes. If this is not successful, activated enzyme solu-tions can be used. Carbonated beverages and juices such as cola and cranberry juice, respectively, are not recommended due to their acidity and the potential to cause subsequent occlu-sions. Several declogging devices are also available, including the Intro-Reducer (Health Improvement Associates, Freeland, MI, USA), the Clog Zapper (CorPak MedSystems, Buffalo Grove, IL, USA), and the DeClogger (Bionix, Toledo, OH, USA). If all attempts to restore patency to an existing enteral access device fail, the clinician must replace the device.

Drug-Nutrient Interactions

A drug-nutrient interaction involves alteration of the kinetics (absorption, metabolism, disposition, or elimination) or dynamics (clinical/physiological) of a drug or nutrition ele-ment or a compromise in nutrition status as a result of the action or side effect of a drug.18 There is no universal approach to the management of drug-nutrient interactions in clinical practice, however, several drugs are commonly thought to require cessation of EN for up to 1–2 hours before and after administration of the drug. Among these are levothyroxine, carbidopa/levodopa, fluoroquinolones such as ciprofloxacin, warfarin, and phenytoin. The proposed mechanisms are myr-iad, including but not limited to protein binding, chelation interaction with divalent cations, specific nutrient content of the enteral formula, positioning of the enteral feeding tube, and adsorption to the enteral tubing.13 Although it is important for the clinician to be cognizant of potential drug-nutrient interac-tions, it is also important to consider the quality of evidence on this topic. The literature suffers many limitations including lack of prospective, randomized, controlled trials and therefore lacks strong evidence to support cessation of EN for medica-tion administration. Furthermore, at this time there is no estab-lished consensus in determining whether a drug-nutrient interaction is even clinically significant. Holding EN for administration of medications significantly challenges the abil-ity of the clinician to provide adequate nutrition support. Therefore, based on a risk-benefit analysis, the clinician’s approach may include changing the management approach immediately or continuing the current regimen and monitoring for therapeutic effect or signs and symptoms of complications associated with interaction.124 Future research should focus on determining the effect of different feeding methods and enteral formulations and validating the proposed mechanisms of spe-cific nutrients on drug availability and metabolism.

Transitioning to Oral Intake

Although EN is often needed during critical and acute illness, it should be discontinued when the patient can consume and tolerate adequate amounts of an oral diet. The length of time needed for this transition may vary considerably, depending on the patient’s underlying illnesses and current medical condi-tion. If the patient was mechanically ventilated for a prolonged period of time, had a tracheostomy placed, or displays cogni-tive deficits, altered mental status, or signs of difficulty with swallowing, a swallow evaluation should be done prior to ini-tiating an oral diet. Once a diet has been started, adjustments in the enteral feeding schedule can help promote appetite and oral intake while still providing adequate nutrition intake through supplemental EN. Several strategies include nocturnal feeding, intermittent feedings between meals, or stopping EN 1 hour before meals. Prior to discontinuing EN, it is important to assess the adequacy of oral energy and nutrient intake through

by Beth Higgins on May 19, 2016ncp.sagepub.comDownloaded from

Page 15: Nutrition in Clinical Practice Enteral Nutrition for ...criticalcarelearningpod.weebly.com/uploads/1/3/0/3/...the lungs and skin. Metabolic changes, such as fever and hyperthyroidism,

648 Nutrition in Clinical Practice 30(5)

food recall or a formal calorie count. When the patient is con-suming 60%-75% of estimated energy and protein needs, the clinician should consider stopping EN and removing the tem-porary enteral access device. If the patient is unable to demon-strate adequate oral intake for > 4 weeks, a permanent feeding tube should be considered.

Transitioning to Home or an Alternate Healthcare Setting With EN

For patients who are medically stable to discharge from the hospital but are unable to achieve or maintain adequate nutri-tion by the oral route, EN should be continued in the home or alternate healthcare setting. Early discharge planning and active communication with all members of the patient care team (eg, physician, dietitian, nurse, social worker, and case manager) are required for a successful transition.

The case manager can determine if the patient has appropri-ate insurance coverage for home EN formula and supplies. As many insurance companies follow Medicare guidelines, the patient will likely need to meet criteria under the prosthetic device benefit provision, which requires that the patient have “a permanently inoperative internal body organ or function thereof.”125 Specific criteria include anticipated length of ther-apy for > 3 months, documentation of pathology to or nonfunc-tion of the structures that normally permit food to reach the digestive tract, or disease of the small bowel impairing diges-tion and absorption of an oral diet.

Prior to discharge from the hospital, the clinician should be sure that the patient has an appropriate route of administration, is receiving the appropriate enteral formula and nutrient provi-sion, and is using an appropriate delivery method. The formula of choice and its administration should be well tolerated. The clinician should reassess all nutrition needs and verify the indi-cation for a specialized formula, if applicable. Intermittent feedings using gravity bags or bolus feedings with syringes are the preferred method of administration for gastric feedings. If continuous gastric feedings are needed, Medicare and other third party payers require documentation of medical necessity or the failure of intermittent or bolus feedings before covering the cost of a feeding pump.

Patient and caregiver education is important to ensure safe and adequate administration of EN at home and should begin early in the discharge planning process as well. Areas of educa-tion from home EN include a comprehensive review of the nutrition prescription (eg, name of the formula and volume required, route of administration, method of administration, feeding schedule, and volume/frequency water flushes), enteral feeding equipment and techniques, and complications associ-ated with EN therapy. The homecare agency can provide addi-tional education once the patient is in the home setting.

Last, and of utmost importance, a primary clinician who will be responsible for ordering and managing home EN should

be identified prior to patient discharge from the hospital, and the patient should follow up with this clinician soon after dis-charge. The patient should be monitored periodically for changes in his or her nutrition status and needs, fluid and elec-trolyte balance, and tube placement and maintenance.

Summary

EN support has become a routine part of the care of hospital-ized patients who have a functional GI tract but are unable to meet their nutrition needs orally. All healthcare practitioners should be familiar with patient selection, timing of EN initia-tion, enteral access, and EN-related complications. Whereas multidisciplinary management of EN is of utmost importance, the registered dietitian is a key resource in determining indi-vidual nutrition needs, selecting the appropriate enteral for-mula, monitoring the adequacy of nutrient provision, and assisting with EN-related complication management and the transition to oral intake or to the home setting with EN. Due to the prevalence of hospital malnutrition and its myriad conse-quences including increased morbidity and mortality, longer lengths of hospital stay, and increased hospital costs, it is important to routinely monitor patients at risk for malnutrition and to initiate safe, timely, and adequate EN therapy when indicated.

Statement of Authorship

M. Kozeniecki and R. Fritzshall equally contributed to the con-cepts and content presented in the manuscript; drafted and/or criti-cally revised the manuscript; and agree to be fully accountable for ensuring the integrity and accuracy of the work. All authors read and approved the final manuscript.

References

1. Teitelbaum D, Guenter P, Howell WH, Kochevar ME, Roth J, Seidner DL. Definition of terms, style, and conventions used in A.S.P.E.N. guide-lines and standards. Nutr Clin Pract. 2005;20:281–285.

2. AHRQ Healthcare Costs and Utilization Project (HCUP) Nationwide Inpatient Sample (NIS) 2012 data. http://hcup.ahrq.gov/. Accessed February 1, 2015.

3. Kudsk KA. Current aspects of mucosal immunology and its influence by nutrition. Am J Surg. 2002;183:390–398.

4. Jabbar A, Chang WK, Dryden GW, McClave SA. Gut immunology and the differential response to feeding and starvation. Nutr Clin Pract. 2003;18:461–482.

5. Kang W, Kudsk KA. Is there evidence that the gut contributes to mucosal immunity in humans? JPEN J Parenter Enteral Nutr. 2007;31:246–258.

6. McClave SA, Heyland DK. The physiologic response and associated clinical benefits from provision of early enteral nutrition. Nutr Clin Pract. 2009;24(3):305–315.

7. McClave SA, Martindale RG, Rice TW, Heyland DK. Feeding the criti-cally ill patient. Crit Care Med. 2014;42(12):2600–2610.

8. Vaishnavi C. Translocation of gut flora and its role in sepsis. Indian J Med Microbiol. 2013;31:334–342.

9. Somanchi M, Tao X, Mullin GE. The facilitated early enteral and dietary management effectiveness trial in hospitalized patients with malnutrition. JPEN J Parenter Enteral Nutr. 2011;35(2):209–216.

by Beth Higgins on May 19, 2016ncp.sagepub.comDownloaded from

Page 16: Nutrition in Clinical Practice Enteral Nutrition for ...criticalcarelearningpod.weebly.com/uploads/1/3/0/3/...the lungs and skin. Metabolic changes, such as fever and hyperthyroidism,

Kozeniecki and Fritzshall 649

10. O’Meara D, Mireles-Cabodevila E, Frame F, et al. Evaluation of delivery of enteral nutrition in critically ill patients receiving mechanical ventila-tion. Am J Crit Care. 2008;17(1):53–61.

11. Quenot JP, Plantefeve G, Baudel JL, et al. Bedside adherence to clinical practice guidelines for enteral nutrition in critically ill patients receiving mechanical ventilation: a prospective, multi-centre, observational study. Crit Care. 2010;14:R37.

12. Kemper M, Weissman C, Hyman AI. Caloric requirements and supply in critically ill surgical patients. Crit Care Med. 1992;20(3):344–348.

13. Ukleja A, Freeman KL, Gilbert K, et al. Standards for nutrition support: adult hospitalized patients. Nutr Clin Pract. 2010;25:403–414.

14. Jensen GL, Bistrian B, Roubenoff R, Heimburger DC. Malnutrition syndromes: a conundrum vs continuum. JPEN J Parenter Enteral Nutr. 2009;33(6):710–716.

15. Fuhrman MP, Charney P, Mueller CM. Hepatic proteins and nutrition assessment. J Am Diet Assoc. 2004;104(8):1258–1264.

16. Gibbs J, Cull W, Henderson W, Daley J, Hur K, Khuri SF. Perioperative serum albumin level as a predictor of operative mortality and mor-bidity: results from the National VA Surgical Risk Study. Arch Surg. 1999;134(1):36–42.

17. White JV, Guenter P, Jensen G, Malone A, Schofield M; Academy of Nutrition and Dietetics Malnutrition Work Group; A.S.P.E.N. Malnutrition Task Force; A.S.P.E.N. Board of Directors. Consensus statement of the Academy of Nutrition and Dietetics/American Society for Parenteral and Enteral Nutrition: characteristics recommended for the identification and documentation of adult malnutrition (undernutrition). J Acad Nutr Diet. 2012;112(5):730–738.

18. A.S.P.E.N. Board of Directors and the Clinical Guidelines Task Force. Guidelines for the use of parenteral and enteral nutrition in adult and pediatric patients. JPEN J Parenter Enteral Nutr. 2002;26(1 suppl):1SA–138SA.

19. Wooley JA, Sax HC. Indirect calorimetry: applications to practice. Nutr Clin Pract. 2003;18(5):434–439.

20. Institute of Medicine, Food and Nutrition Board. Dietary Reference Intakes for Macronutrients: Energy, Carbohydrate, Fiber, Fat, Fatty Acids, Cholesterol, Protein and Amino Acids. Washington, DC: National Academies Press; 2005:265–645.

21. Mirtallo J, Canada T, Johnson D, et al; Task Force for the Revision of Safe Practices for Parenteral Nutrition. Safe practices for parenteral nutrition. JPEN J Parenter Enteral Nutr. 2004;28(6):S39–S70.

22. McClave SA, Martindale RG, Vanek VW, et al; A.S.P.E.N. Board of Directors; American College of Critical Care Medicine; Society of Critical Care Medicine. Guidelines for the provision and assessment of nutrition support therapy in the adult critically ill patient: Society of Critical Care Medicine (SCCM) and American Society for Parenteral and Enteral Nutrition (A.S.P.E.N.). JPEN J Parenter Enteral Nutr. 2009;33(3): 277–316.

23. Stroud M, Duncan H, Nightingale J. Guidelines for enteral feeding in adult hospital patients. Gut. 2003;52(suppl 7):vii1–vii12.

24. Minard G. Enteral access. Nutr Clin Pract. 1994;9:172–182. 25. Miller KR, McClave SA, Kiraly LN, Martindale RG, Benns MV. A tuto-

rial on enteral access in adult patients in the hospitalized setting. JPEN J Parenter Enteral Nutr. 2014;38(3):282–295.

26. Charney P, Malone A. ADA Pocket Guide to Enteral Nutrition. Chicago, IL: D. Faulhaber; 2006.

27. Koopman M, Kudsk K, Szotkowski M, Rees SM. A team-based protocol and electromagnetic technology eliminate feeding tube placement compli-cations. Ann Surg. 2011;253(2):287–302.

28. Gray R, Tynan C, Reed L, et al. Bedside electromagnetic-guided feeding tube placement: an improvement over traditional placement technique? Nutr Clin Pract. 2007;22(4):436–444.

29. Rivera R, Campana J, Hamilton C, Lopez R, Seidner S. Small bowel feed-ing tube placement using an electromagnetic tube placement device: accu-racy of tip location. JPEN J Parenter Enteral Nutr. 2011;35(5):636–642.

30. Bankhead R, Boullata J, Brantley S, et al. Enteral nutrition practice recom-mendations. JPEN J Parenter Enteral Nutr. 2009;33(2):122–167.

31. Stayner JL, Bhatnagar A, McGinn AN, Fang JC. Feeding tube placement: errors and complications. Nutr Clin Pract. 2012;27(6):738–748.

32. Toussaint E, Van Gossum A, Ballarin A, Arvanitakis M. Enteral access in adults. Clin Nutr. 2015;34(3):350–358.

33. Kearns PJ, Chin D, Mueller L, Wallace K, Jensen WA, Kirsch CM. The incidence of ventilator- associated pneumonia and success in nutrient delivery with gastric versus small intestinal feeding: a randomized clinical trial. Crit Care Med. 2000;28:1742–1746.

34. Strong RM, Condon SC, Solinger MR, Namihas BN, Ito-Wong LA, Leuty JE. Equal aspiration rates from postpylorus and intragastric-placed small-bore nasoenteric feeding tubes: a randomized, prospective study. JPEN J Parenter Enteral Nutr. 1992;16:59–63.

35. Mion LC, Minnick AF, Leipzig RM, Catrambone CD, Johnson ME. Patient-initiated device removal in intensive care units: a national preva-lence study. Crit Care Med. 2007;35(12):2714–2720.

36. McGinnis C. The feeding tube bridle: one inexpensive, safe, and effective method to prevent inadvertent feeding tube dislodgement. Nutr Clin Pract. 2011;26(1):70–77.

37. McClave SA, Sexton LK, Spain DA, et al. Enteral tube feeding in the intensive care unit: factors impeding adequate delivery. Crit Care Med. 1999;27(7):1252–1256.

38. Kee YYK, Brooks W, Dhami R, Bhalla A. Evaluating the use of hand control mittens in post stroke patients who do not tolerate naso-gastric feeding. Cerebrovas Dis. 2007;23(suppl 2):93.

39. Popovich MJ, Lockrem JD, Zivot JB. Nasal bridle revisited: an improve-ment in the technique to prevent unintentional removal of small-bore nasoenteric feeding tubes. Crit Care Med. 1996;24(3):429–431.

40. Guenter P, Hicks RW, Simmons D, et al. Enteral feeding misconnec-tions: a consortium position statement. Jt Comm J Qual Patient Saf. 2008;34(5):285–292.

41. Simmons D, Symes L, Guenter P, Graves K. Tubing misconnections: nor-malization of deviance. Nutr Clin Pract. 2011;26(3):286–293.

42. Guenter P, Hicks RW, Simmons D. Enteral feeding misconnections: an update. Nutr Clin Pract. 2009;24(3):325–334.

43. Guenter P. New enteral connectors: raising awareness. Nutr Clin Pract. 2014;29(5):612–614.

44. The Joint Commission Sentinel Event Alert. Tubing Misconnections—A Persistent and Potentially Deadly Occurrence. http://www.jointcom-mission.org/sentinel_event_alert_issue_36_tubing_misconnections—a_ persistent_and_potentially_deadly_occurrence/default.aspx. Published 2006. Accessed May 10, 2015.

45. ISO Small Bore Connectors Working Group. ANSI/AAMI/ISO 80369-1:2010. Small Bore Connectors for Liquids and Gasses in Healthcare Applications—Part 1: General Requirements. Arlington, VA: Association for the Advancement of Medical Instrumentation; 2011.

46. Global Enteral Device Supply Association. Stay connected 2015. http://www.stayconnected.org/index.html. Published December 2014. Accessed May 10, 2015.

47. Brown B, Roehl K, Betz M. Enteral nutrition formula selection: current evi-dence and implications for practice. Nutr Clin Pract. 2015;30(1):72–85.

48. Wong K. The role of fiber in diarrhea management. Support Line. 1998;20(6):16–20.

49. U.S. Food and Drug Administration. Draft guidance for industry: fre-quently asked questions about medical foods. 2nd ed. http://www.fda.gov/Food/GuidanceRegulation/GuidanceDocumentsRegulatoryInformation/MedicalFoods/ucm054048.htm. Published 2013. Accessed February 3, 2015.

50. Kohn CL. The relationship between enteral formula contamination and length of enteral delivery set usage. JPEN J Parenter Enteral Nutr. 1991;15:567–571.

51. Perez SK, Brandt K. Enteral feeding contamination: comparison of dilu-ents and feeding bag usage. JPEN J Parenter Enteral Nutr. 1989;13: 306–308.

by Beth Higgins on May 19, 2016ncp.sagepub.comDownloaded from

Page 17: Nutrition in Clinical Practice Enteral Nutrition for ...criticalcarelearningpod.weebly.com/uploads/1/3/0/3/...the lungs and skin. Metabolic changes, such as fever and hyperthyroidism,

650 Nutrition in Clinical Practice 30(5)

52. Desachy A, Clavel M, Vuagnat A, Normand S, Gissot V, Francois B. Initial efficacy and tolerability of early enteral nutrition with immedi-ate or gradual introduction in intubated patients. Intensive Care Med. 2008;34:1054–1059.

53. Heyland DK, Murch L, Cahill N, et al. Enhanced protein-energy provision via the enteral route feeding protocol in critically ill patients: results of a cluster randomized trial. Crit Care Med. 2013;41:2743–2753.

54. Taylor B, Brody R, Denmark R, Southard R, Byham-Gray L. Improving delivery through the adoption of the “Feed Early Enteral Diet Adequately for Maximum Effect (FEED ME)” protocol in a surgical trauma ICU: a quality improvement review. Nutr Clin Pract. 2014;29:639–648.

55. Lord L, Harrington M. Enteral nutrition implementation and management. In: Merritt R, ed. The A.S.P.E.N. Nutrition Support Practice Manual. 2nd ed. Silver Spring, MD: American Society for Parenteral and Enteral Nutrition; 2005:76–89.

56. Byrnes MC, Stangenes J. Refeeding in the ICU: an adult and pediatric problem. Curr Opin Clin Nutr Metab Care. 2011;14:186–192.

57. National Institute for Health and Clinical Excellence. Nutrition support in adults. Clinical guideline CG32.

58. Cahill GF. Starvation in man. N Engl J Med. 1970;282:668–675. 59. Chapman MJ, Nguyen NQ, Deane AM. Gastrointestinal dysmotility:

evidence and clinical management. Curr Opin Clin Nutr Metab Care. 2013;16(2):209–216.

60. Taylor SJ, Manara AR, Brown J. Treating delayed gastric emptying in critical illness: metoclopramide, erythromycin, and bedside (cor-trak) nasointestinal tube placement. JPEN J Parenter Enteral Nutr. 2010;34(3):289–294.

61. Ali T, Hasan M, Hamadani M, Harty RF. Gastroparesis. South Med J. 2007;100(3):281–286.

62. Sidery MB, Macdonald IA, Blackshaw PE. Superior mesenteric artery blood flow and gastric emptying in humans and the differential effects of high fat and high carbohydrate meals. Gut. 1994;35(2):186–190.

63. Malone A, Seres D, Lord L. Complications of enteral nutrition. In: Mueller CM, ed. The A.S.P.E.N. Adult Nutrition Support Core Curriculum. Silver Spring, MD: A.S.P.E.N.; 2012.

64. Kollef MH. The prevention of ventilator-associated pneumonia. N Engl J Med. 1999;340:627–634.

65. Majid HA, Emery PW, Whelan K. Definitions, attitudes, and manage-ment practices in relation to diarrhea during enteral nutrition: a survey of patients, nurses, and dietitians. Nutr Clin Pract. 2012;27(2):252–260.

66. Juckett G, Trivedi R. Evaluation of chronic diarrhea. Am Fam Physician. 2011;84(10):1119–1126.

67. Beckwith MC, Feddema SS, Barton RG, Graves C. A guide to drug therapy in patients with enteral feeding tubes: dosage form selection and administration methods. Hosp Pharm. 2004;39(3):225–237.

68. Chang SJ, Huang HH. Diarrhea in enterally fed patients: blame the diet? Curr Opin Clin Nutr Metab Care. 2013;16(5):588–594.

69. Thorson MA, Bliss DZ, Savik K. Re-examination of risk factors for non-Clostridium difficil-associated diarrhoea in hospitalized patients. J Adv Nurs. 2008;62(3):354–364.

70. Lefton J. Management of common gastrointestinal complications in tube-fed patients. Support Line. 2002;24(1):19–25.

71. Hempel S, Newberry SJ, Maher AR, et al. Probiotics for the prevention and treatment of antibiotic-associated diarrhea: a systematic review and meta-analysis. JAMA. 2012;307(18):1959–1969.

72. Guerra TL, Mendonca SS, Marshall NG. Incidence of constipation in an intensive care unit. Rev Bras Ter Intensiva. 2013;25(2):87–92.

73. Bittencourt AF, Martins JR, Logullo L, et al. Constipation is more fre-quent than diarrhea in patients fed exclusively by enteral nutrition: results of an observational study. Nutr Clin Pract. 2012;27(4):533–539.

74. Johanson JF. Review of the treatment options for chronic constipation. Med Gen Med. 2007;9(2):25.

75. Mostafa SM, Bhandari S, Ritchie G, Gratton N, Wenstone R. Constipation and its implications in the critically ill patient. Br J Anaesth. 2003;91(6):815–819.

76. Phipps M, Bush JA, Buhrow D, et al. Ileus development in the trauma/surgical intensive care unit: a process improvement evaluation. Dimens Crit Care Nurs. 2011;30(3):164–168.

77. Caddell KA, Martindale R, McClave SA, Miller K. Can the intestinal dys-motility of critical illness be differentiated from postoperative ileus? Curr Gastroenterol Rep. 2011;13(4):358–367.

78. Aderinto-Adike AO, Quigley EM. Gastrointestinal motility problems in critical care: a clinical perspective. J Dig Dis. 2014;15(7):335–344.

79. Wilson JP. Postoperative motility of the large intestine in man. Gut. 1975;16(9):689–692.

80. Moss G. Maintenance of gastrointestinal function after bowel surgery and immediate enteral full nutrition. II. Clinical experience, with objec-tive demonstration of intestinal absorption and motility. JPEN J Parenter Enteral Nutr. 1981;5(3):215–220.

81. Hur H, Si Y, Kang WK, Kim W, Jeon HM. Effects of early oral feeding on surgical outcomes and recovery after curative surgery for gastric cancer: pilot study results. World J Surg. 2009;33(7):1454–1458.

82. Kasparek MS, Mueller MH, Glatzle J, et al. Postoperative colonic motility increases after early food intake in patients undergoing colorectal surgery. Surgery. 2004;136(5):1019–1027.

83. Marcuard SP, Perkins AM. Clogging of feeding tubes. JPEN J Parenter Enteral Nutr. 1988;12:403–405.

84. Frankel EH, Enow NB, Jackson KC, Kloiber LL. Methods of restoring patency to occluded feeding tubes. Nutr Clin Pract. 1998;13:129–131.

85. Scanlan M, Frisch S. Nasoduodenal feeding tubes: prevention of occlu-sion. J Neurosci Nurs. 1992;24:250–259.

86. Gora ML, Tschampel MM, Visconti JA. Considerations of drug therapy in patients receiving enteral nutrition. Nutr Clin Pract. 1989;4(3):105–110.

87. Kraft MD, Btaiche IF, Sacks GS. Review of the refeeding syndrome. Nutr Clin Pract. 2005;20:625–633.

88. Skipper A. Refeeding syndrome or refeeding hypophosphatemia: a sys-tematic review of cases. Nutr Clin Pract. 2012;27(1):34–40.

89. Weinsier RL, Krumdieck CL. Death resulting from overzealous total parenteral nutrition: the refeeding syndrome revisited. Am J Clin Nutr. 1981;34:393–399.

90. Miller SJ. Death resulting from overzealous total parenteral nutrition: the refeeding syndrome revisited. Nutr Clin Pract. 2008;23(2):166–171.

91. Rhoney DH, Parker D Jr, Formea CM, Yap C, Coplin WM. Tolerability of bolus versus continuous gastric feeding in brain-injured patients. Neurol Res. 2002;24(6):613–620.

92. Nguyen NQ, Chapman M, Fraser RJ, Bryant LK, Burgstad C, Holloway RH. Prokinetic therapy for feed intolerance in critical illness: one drug or two? Crit Care Med. 2007;35(11):2561–2567.

93. Edwards SJ, Metheny NA. Measurement of gastric residual volume: state of the science. Medsurg Nurs. 2000;9:125–128.

94. Bonten MJM, Kullberg BJ, van Dalen R, et al. Selective digestive con-tamination in patients in intensive care. The Dutch Working Group on Antibiotic Policy. J Antimicrob Chemother. 2000;46:351–362.

95. Bergmans DC, Bonten MJ, Gaillard CA, et al. Prevention of ventilator-associated pneumonia by oral decontamination: a prospective, random-ized, double-blind, placebo-controlled study. Am J Respir Crit Care Med. 2001;164:382–388.

96. Bonten MJ, Gaillard CA, van Tiel FH, Smeets HG, van der Geest S, Stobberingh EE. The stomach is not a source for colonization of the upper respiratory tract and pneumonia in ICU patients. Chest. 1994;105:878–884.

97. Pinilla JC, Samphire J, Arnold C, Liu L, Thiessen B. Comparison of gastrointestinal tolerance to two enteral feeding protocols in critically ill patients: a prospective, randomized controlled trial. J Parenter Enter Nutr. 2001;25:81–86.

98. McClave SA, Lukan JK, Stefater JA, et al. Poor validity of residual vol-umes as a marker for risk of aspiration in critically ill patients. Crit Care Med. 2005;33:324–330.

99. Montejo JC, Miñambres E, Bordejé L, et al. Gastric residual volume dur-ing enteral nutrition in ICU patients: the REGANE study. Intensive Care Med. 2010;36(8):1386–1393.

by Beth Higgins on May 19, 2016ncp.sagepub.comDownloaded from

Page 18: Nutrition in Clinical Practice Enteral Nutrition for ...criticalcarelearningpod.weebly.com/uploads/1/3/0/3/...the lungs and skin. Metabolic changes, such as fever and hyperthyroidism,

Kozeniecki and Fritzshall 651

100. Mentec H, Dupont H, Bocchetti M, Cani P, Ponche F, Bleichner G. Upper digestive intolerance during enteral nutrition in critically ill patients: frequency, risk factors, and complications. Crit Care Med. 2001;29(10):1955–1961.

101. Reignier J, Mercier E, Le Gouge A, et al. Effect of not monitoring residual gastric volume on risk of ventilator-associated pneumonia in adults receiv-ing mechanical ventilation and early enteral feeding: a randomized con-trolled trial. JAMA. 2013;309:249–256.

102. Whelan K, Schneider SM. Mechanisms, prevention, and management of diarrhea in enteral nutrition. Curr Opin Gastroenterol. 2011;27(2):152–159.

103. Lebak KJ, Bliss DZ, Savik K. What’s new on defining diarrhea in tube-feeding studies? Clin Nurs Res. 2003;12(2):174–204.

104. Eisenberg P. An overview of diarrhea in the patient receiving enteral nutri-tion. Gastroenterol Nurs. 2002;25(3):95–104.

105. World Health Organization. Diarrhoeal disease. http://www.who.int/mediacentre/factsheets/fs330/en/. Published April 2013. Accessed March 15, 2015.

106. Schiller LR. Secretory diarrhea. Curr Gastroenterol Rep. 1999;1(5): 389–397.

107. Gerding DN, Johnson S, Peterson LR, Mulligan ME, Silva J. Clostridium difficile-associated diarrhea and colitis. Infect Control Hosp Epidemiol. 1995;16(8):495–477.

108. Jack L, Coyer F, Courtney M, Venkatesh B. Diarrhoea risk factors in enterally tube fed critically ill patients: a retrospective audit. Intensive Crit Care Nurs. 2010;26(6):327–334.

109. Huang HH, Hsu CW, Kang SP, et al. Association between illness severity and timing of initial enteral feeding in critically ill patients: a retrospective observational study. Nutr J. 2012;11:30.

110. Wierdsma NJ, Peters JHC, Weijs PJM, et al. Malabsorption and nutri-tional balance in the ICU: fecal weight as a biomarker: a prospective observational pilot study. Crit Care. 2011;15(6):R264.

111. Jain NK, Patel VP, Pitchumoni CS. Sorbitol intolerance in adults. Prevalence and pathogenesis on two continents. J Clin Gastroenterol. 1987;9(3):317–319.

112. Lutomski DM, Gora ML, Wright SM, Martin JE. Sorbitol content of selected oral liquids. Ann Pharmacother. 1993;27(3):269–274.

113. Ratnaike RN, Jones TE. Mechanisms of drug-induced diarrhea in the elderly. Drugs Aging. 1998;13(3):245–253.

114. Elia M, Engfer MB, Green CJ, Silk DB. Systematic review and meta-analysis: the clinical and physiological effects of fibre-containing enteral formulae. Aliment Pharmacol Ther. 2008;27(2):120–145.

115. Hegazi RA, Wischmeyer PE. Clinical review: optimizing enteral nutri-tion for critically ill patients—a simple data-driven formula. Crit Care. 2011;15(6):234.

116. Shankardass K, Chuchmach S, Chelswick K, et al. Bowel function of long-term tube-fed patients consuming formulae with and without dietary fiber. JPEN J Parenter Enteral Nutr. 1990;14(5):508–512.

117. Rothnie NG, Harper RA, Catchpole BN. Early postoperative gastrointes-tinal activity. Lancet. 1963;2:64–67.

118. Parrish CR. Enteral feeding: the art and the science. Nutr Clin Pract. 2003;18:76–85.

119. Holte K, Kehlet H. Postoperative ileus: a preventable event. Br J Surg. 2000;87(11):1480–1493.

120. Delaney CP, Senagore AJ, Gerkin TM, et al. Association of surgical care practices with length of stay and use of clinical protocols after elective bowel resection: results of a national survey. Am J Surg. 2010;199(3): 299–304.

121. Lassen K, Kjaeve J, Fetveit T, et al. Allowing normal food at will after major upper gastrointestinal surgery does not increase morbidity: a ran-domized multicenter trial. Ann Surg. 2008;247(5):721–729.

122. Powell KS, Marcuard SP, Farrior ES, Gallagher ML. Aspirating gastric residuals causes occlusion of small-bore feeding tubes. JPEN J Parenter Enteral Nutr. 1993;17(3):243–246.

123. Klang M, McLymont V, Ng N. Osmolality, pH, and compatibility of selected oral liquid medications with an enteral nutrition product. JPEN J Parenter Enteral Nutr. 2013;37(5):689–694.

124. Chan LN. Drug-nutrient interactions. JPEN J Parenter Enteral Nutr. 2013;37(4):450–459.

125. Centers for Medicare and Medicaid Services. National coverage deter-mination (NCD) for enteral and parenteral nutritional therapy (180.2). http://www.cms.gov/medicare-coverage-database/details/ncd-details.aspx?NCDId=242&ver=1. Accessed March 7, 2015.

by Beth Higgins on May 19, 2016ncp.sagepub.comDownloaded from