irritable bowel sydrome
Cgregory30
IrritableBowelSyndrome1.pdf
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CLINICAL FEATURE
Irritable Bowel Syndrome An evidence-based review of new diagnostic criteria and treatment recommendations.
ABSTRACT: Irritable bowel syndrome (IBS) is a common, chronic gastrointestinal (GI) condition characterized by disturbances in bowel habits and abdominal pain in the absence of known organic pathology. IBS reduces quality of life and is costly to treat. It is diagnosed using the symptom-based Rome criteria for functional GI disorders, which was recently updated and released as Rome IV. Both physiologic and psychological variables play a role in the etiology of IBS and perpetuate symptoms. Although research has shed light on IBS patho- physiology, therapeutic interventions remain symptom driven, employing both pharmacologic and nonphar- macologic approaches. Here, the authors review the epidemiology and pathophysiology of IBS, summarize diagnostic and treatment strategies, and discuss implications for nursing practice.
Keywords: irritable bowel syndrome, Rome criteria, treatment approaches
Irritable bowel syndrome (IBS) is one of the most commonly diagnosed gastrointestinal (GI) dis- orders. Occurring most often in patients under
age 50,1 this chronic condition is characterized by abdominal pain and bowel dysfunction, presenting as constipation, diarrhea, or alternating periods of both.2 In addition to its physiologic manifestations, IBS is recognized as having a psychological compo- nent. In 40% to 60% of cases, IBS is accompanied by such psychological disorders as depression or anx- iety,3 and patients with IBS have been found to have a greater frequency of somatic symptoms than pa- tients who have GI symptoms in the absence of IBS.4
The development and persistence of IBS symp- toms are understood to be multifactorial. Conse- quently, diagnosis and treatment are complicated clinical endeavors. Diagnosis is made according to the symptom-based Rome criteria for functional GI disor- ders, most recently updated and released as Rome IV.5
Because curative medical interventions have yet to be discovered, treatment focuses on reducing patient symptoms. Current pharmacologic approaches, how- ever, often provide suboptimal relief.
Evidence of biologic dysregulation has been re- ported in patients with IBS and efforts to understand
the neurohormonal underpinnings of the disorder are ongoing, but the exact mechanisms leading to IBS symptoms are not completely understood.6, 7 This ar- ticle discusses recent developments in the field of IBS research and the updated diagnostic criteria. It sum- marizes the epidemiology, pathophysiology, and treat- ment of IBS, with a focus on nursing practice.
EPIDEMIOLOGY AND BURDEN OF IBS Incidence rates of IBS are seldom calculated, and prev- alence estimates fluctuate both between and within countries.2 A recent literature review by Sperber and colleagues attributed discrepancies to such factors as differences in the use of instruments, methods, and di- agnostic criteria, as well as variations in populations and cultures assessed.8 This review evaluated 83 community-based studies of IBS prevalence con- ducted in a total of 41 countries, and confirmed the global predominance of IBS among women, but could not estimate a global prevalence rate owing to the heterogeneity of the studies. The pooled prevalence rate that the investigators cited for North America, Europe, Australia, and New Zealand was 8.1%.
While IBS is not associated with increased mortal- ity rates, it represents a significant burden on affected
By Kristen Ronn Weaver, MS, ACNP, ANP, Gail D’Eramo Melkus, EdD, C-NP, FAAN, and Wendy A. Henderson, PhD, MSN, CRNP
patients and society as a result of direct medical costs, lost productivity, and reduced health-related quality of life.9 In 2010, IBS accounted for more than 2 million diagnoses in U.S. ambulatory care settings, including office, ED, and hospital outpa- tient visits.10 In the United States, estimates of IBS costs, both direct (medical management) and indi- rect (lost productivity and leisure time), exceeded $1 billion in 2004.11
A disproportionate amount of health care resources is expended treating patients with IBS and addressing the negative effects it has on patients’ quality of life.12
Despite receiving increased medical attention, how- ever, patients with IBS frequently report problematic visits with health care providers that leave them feel- ing unsupported, humiliated, insignificant, and aban- doned.13, 14 An additional burden of IBS falls on those
Figure 1. The Brain–Gut Axis
who live with and care for patients with the disorder. Studies report adverse effects on the quality of life of domestic partners of patients with IBS.15
IBS ETIOLOGY AND PATHOPHYSIOLOGY The following physiologic and psychological variables have been proposed as potential factors in the etiology and pathophysiology of IBS16: • GI dysmotility • inflammation • visceral hypersensitivity • altered intestinal microbiota • diet • genetic predisposition • stress exposure (including early life events)
IBS and stress. Stress has been identified as a mechanism in the development of IBS, and the major
STRESS
Lumen
Mucosa
Submucosa
Muscularis
Serosa
Microbiota
Intestinal crypts
Nerve innervation
The mechanisms that disrupt “cross talk” between the brain and the gut along endocrine, neural, and neuroimmune pathways are not fully understood, but this disruption appears to play a role in producing the symptoms of irritable bowel syndrome. Shown here are layers of the colon wall along with some of the structures that may be affected. Illustration by Sara Jarret.
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components of the stress response system—the autonomic nervous system and the hypothalamic– pituitary–adrenal axis—have been the subject of numerous IBS studies. An analysis of medical data collected from active-duty U.S. service members be- tween 2001 and 2009 found the risk of developing IBS was significantly increased in those with a greater number of life stressors, a positive screen for panic syndrome or other anxiety syndromes on the Patient Health Questionnaire, and previous infectious gastro- enteritis.17 Posttraumatic stress disorder (PTSD) and depression were also associated with elevated risk, though in this study the increased risk was not found to be significant. Since both depression and PTSD have been significantly associated with IBS in previ- ous studies of military veterans, the investigators at- tribute their finding to study design. These findings illustrate the interdependence or “cross talk” between the brain and the gut in IBS, a connection commonly known as the brain–gut axis.
The brain–gut axis refers to endocrine, neural, and neuroimmune pathways that facilitate bidirectional communication between the gut, the central nervous system, the enteric nervous system, the autonomic nervous system, and the hypothalamic–pituitary– adrenal axis.18, 19 Disturbances in the brain–gut axis, including disruption of central and autonomic func- tions, peripheral hormones, amines, and peptides, have been documented in patients with IBS.6 Clinical reviews of neuroimaging studies have also shown that, compared with healthy control participants, pa- tients with IBS demonstrate differences in the central processing mechanisms of the brain–gut axis, such
as changes in connectivity and functional responsive- ness.20 Although disruptions in the brain–gut axis may play a significant role in producing many clinical manifestations of IBS, the underlying mechanisms are not fully understood.21 For the most part, patient diag- nosis remains one of exclusion, with treatment being symptom driven.
DIAGNOSING IBS The Rome III criteria for functional GI disorders served as the symptom-based diagnostic criteria for IBS since its release in 2006 until early 2016, when the Rome Foundation updated the criteria with the release of Rome IV (see Table 122, 23).5 Like Rome III, the Rome IV criteria maintains that an IBS diagnosis requires symptoms to be chronic (having persisted for at least six months), active (having occurred within the previous three months), and like all functional bowel disorders, to occur in the absence of an ana- tomic or physiologic abnormality.23 Requisite symp- tom frequency, however, has been increased from at least three days per month in Rome III to at least one day per week in Rome IV. Furthermore, in contrast to Rome III, Rome IV specifically calls for abdominal pain (rather than pain or discomfort) to be related to (versus improved with) defecation, and clarifies that it is the abdominal pain (rather than the pain’s onset) that must be associated with changes in stool fre- quency or form.22, 23 In Rome IV, subtyping by pre- dominant stool pattern—as IBS-C (with constipation), IBS-D (with diarrhea), IBS-M (with a mixed stool pat- tern), and IBS-U (unclassified because of an insufficient consistency of stool abnormality)—is now based on
Table 1. Comparison of Rome III and Rome IV Criteria22, 23
Characteristic Rome III Rome IV
Diagnostic time frame
Symptom description
Symptom association (2 or more)
Predominant stool pattern of IBS subtype (IBS-C, IBS-D, IBS-M, IBS-U)
Tool to categorize bowel habit
• Symptom onset at least six months prior
• Symptom activity during the last three months
• Symptom frequency at least three days per month
Abdominal discomfort or pain
• Improvement with defecation • Onset associated with change
in the form of stool • Onset associated with a change
in the frequency of stool
Stool type based on bowel move- ments on all days
Bristol Stool Form Scale
• Symptom onset at least six months prior
• Symptom activity during the last three months
• Symptom frequency at least one day per week
Abdominal pain
• Related to defecation • Associated with a change in
the form of stool • Associated with a change in
the frequency of stool
Stool type based on days with abnormal bowel movements
Bristol Stool Form Scale
IBS = irritable bowel syndrome; IBS-C = IBS with constipation; IBS-D = IBS with diarrhea; IBS-M = IBS with a mixed stool pattern; IBS-U = IBS unclassified.
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stool form on the days in which at least one bowel movement is abnormal, as opposed to stool form on all days since onset.23 Rome IV retains the Bristol Stool Form Scale24 as a means of categorizing abnormal stool form, using 25% of stools as the threshold for subtyping the stool pattern.23
use of invasive medical procedures and spurred efforts to develop biomarkers to aid in IBS diagnosis.
Biomarkers. Over the years, it’s been suggested that various biomarkers could aid in diagnosing IBS. In 2009, Lembo and colleagues proposed a se- rum panel consisting of 10 biomarkers that included
Pharmacologic management of IBS focuses on the predominant
bowel symptom (diarrhea or constipation) and abdominal pain.
Patient education, suggestions for lifestyle modifications, and
reassurance should be provided with all IBS treatments.
The differential diagnosis of IBS should include ce- liac disease, microscopic colitis, inflammatory bowel disease, bile acid malabsorption, colorectal cancer, and dyssynergic defecation.25 However, using the Rome IV criteria, clinicians can diagnose IBS based on the following data23: • patient history, including diet as well as symptoms • physical examination, including an anorectal ex-
amination • complete blood count • C-reactive protein or fecal calprotectin level • celiac serology, if clinical suspicion is high • a colonoscopy or upper endoscopy, if recom-
mended by guidelines because of patient age, alarm signs, or family history
Symptom overlap. In clinical practice, GI diagno- ses commonly share symptoms. For instance, a sys- tematic review and meta-analysis of IBS symptoms in patients with inflammatory bowel disease (IBD) found that IBS symptoms were significantly higher in both patients with active IBD and patients whose IBD was in remission than in control participants without IBD.26 The pooled prevalence of IBS symp- toms in the two IBD groups was 39%, 35% among patients believed to be in remission and 44% among those with active IBD. Clinical trials are needed to de- velop evidence-based approaches for treating patients with IBD who have IBS-type symptoms.27 It’s been suggested that fecal calprotectin, which is a very sen- sitive measure of disease activity in IBD, should be measured in the initial evaluation of such patients.27
A recent systematic review and meta-analysis dem- onstrated that IBS symptoms also overlap with those of microscopic colitis, though therapeutic interventions are very different.28 This review reported the pooled prevalence of IBS symptoms in patients with micro- scopic colitis to be 33.4%, similar to that seen in pa- tients with other diarrhea etiologies. Symptom overlap between IBS and other GI disorders has prompted the
two cytokines, two antibodies, a chemokine, a nerve growth factor, a tissue-repair enzyme, an autoantibody, a metalloproteinase inhibitor, and a lipocalin protein.29
A few years later, Jones and colleagues extended the panel, incorporating an additional 24 biomarkers, in- cluding serologic markers for gene expression, and in- corporating four psychological measures.30
Biomarker initiatives have included studies of • colonic transit and fecal bile acids to distinguish
patients with IBS from healthy participants or to discriminate among IBS subgroups.31
• anticytolethal distending toxin B and antivincu- lin antibodies to distinguish IBS-D from other di- agnostic possibilities.32
• intestinal microbiota to identify and characterize fecal dysbiosis in patients with IBS or IBD.33
Although the diagnostic value of these tests is en- couraging, biomarkers have yet to become the gold standard for diagnosing IBS in clinical practice.
PHARMACOLOGIC INTERVENTIONS IBS is a multifactorial disorder. For this reason, phar- macologic management focuses on the predominant bowel symptom (diarrhea or constipation) and ab- dominal pain (see Table 223). Patients with IBS-M may require treatments for both diarrhea and constipa- tion.34 Patient education, suggestions for lifestyle mod- ifications, and reassurance should be provided with all IBS treatments.
The American Gastroenterological Association (AGA) guidelines on the pharmacologic manage- ment of IBS characterizes the strength of its recom- mendations as conditional (weak) or strong and grades the quality of the supporting evidence as very low, low, moderate, or high.35 Although these guide- lines discuss nine pharmaceutical agents or classes used in the treatment of IBS—linaclotide, lubipros- tone, polyethylene glycol laxatives, rifaximin, alose- tron, loperamide, tricyclic antidepressants, selective
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Table 2. Pharmacologic Interventions for IBS23
Abdominal Pain Bowel Subtype: IBS-C Bowel Subtype: IBS-D
Antispasmodics
Peppermint oil
Selective serotonin reuptake inhibitors
Tricyclic antidepressants
Chloride channel activators
Polyethylene glycol
Psyllium
Guanylate cyclase-C agonists
Opioid agonists
Antibiotics
Bile acid sequestrants
Probiotics
Mixed opioid receptor modulators
Serotonin-3 antagonists
IBS = irritable bowel syndrome; IBS-C = IBS with constipation; IBS-D = IBS with diarrhea.
serotonin reuptake inhibitors, and antispasmodics— only the use of linaclotide for IBS-C was given a strong recommendation, based on high-quality evi- dence.35 Linaclotide (Linzess), a guanylate cyclase-C agonist, stimulates the secretion of chloride and bi- carbonate into the intestine, thereby increasing intes- tinal fluid and accelerating GI transit.36
The American College of Gastroenterology (ACG) performed a systematic review to determine the effi- cacy of 11 IBS therapies, both pharmacologic and nonpharmacologic, compared with placebo or no treatment.37 The nonpharmacologic interventions included dietary manipulation, fiber, probiotics, pre- biotics, peppermint oil, and psychological therapies, including hypnotherapy. As with the AGA guide- lines, the ACG graded the quality of the evidence on which its recommendations were based (very low, low, moderate, or high) and characterized the strength of its recommendations as strong or weak. Only two therapies overall received strong recommendations for use and were supported, respectively, by evidence of high and moderate quality: linaclotide and lubipros- tone for the treatment of IBS-C. Lubiprostone (Ami- tiza), a chloride channel activator, increases intestinal fluid secretion, thereby increasing intestinal motility and stool passage.38
NONPHARMACOLOGIC INTERVENTIONS Nonpharmacologic interventions, such as diet modifi- cation, exercise, mind–body therapies, and other com- plementary approaches, are often used to provide relief of IBS symptoms. A Cochrane review of the efficacy of psychological interventions found that cognitive behavioral therapy and interpersonal psychotherapy may benefit patients with IBS, though issues regard- ing study heterogeneity, validity, and sample size were noted.39 A systematic review and meta-analysis by Ford and colleagues, which included 30 studies on the effect of psychological therapies on patients with IBS, found some beneficial effects of cognitive behavioral therapy, multicomponent psychological therapy, dy- namic psychotherapy, and hypnotherapy.40
Dietary modifications to alleviate IBS symp- toms have garnered increasing interest in recent years.41 Food ingestion can stimulate chemorecep- tors, mechanoreceptors, osmotic actions, altered se- cretion, activation of motor reflexes, and colonic fermentation, which may contribute to IBS symp- toms.42 Patients with IBS are more likely than the general population to report adverse reactions to food, with dietary intolerance often attributed to gluten (wheat and related grain species); lactose; fer- mentable oligosaccharides, disaccharides, monosac- charides, and polyols (FODMAPs); and fructose malabsorption.43 Patients with IBS have used diets excluding suspected IBS triggers with conflicting re- sults.44
In a recent prospective study of 41 patients with IBS-D, a six-week gluten-free diet significantly im- proved symptom severity scores in 29 (71%), and there was significant overall improvement in anxiety, depression, fatigue, and quality of life.45 The low- FODMAP diet has also been found to improve ab- dominal and bowel symptoms in some patients with IBS, although guidance from a nutritionist is generally recommended.34 A systematic review and meta-analysis of 14 randomized controlled trials, which included 96 patients with various IBS subtypes, found that soluble fiber supplementation had beneficial effects on global IBS symptoms.46
Intestinal microbiota play a major role in GI pro- cesses and overall health.47 Numerous studies have in- vestigated the value of probiotics in manipulating the intestinal microbiota and improving IBS symptoms. A meta-analysis of 10 randomized controlled trials that compared the efficacy of probiotics with pla- cebo in treating IBS symptoms found that probiotics containing Bifidobacterium breve, Bifidobacterium longum, or Lactobacillus acidophilus significantly reduced IBS pain.48 Abdominal distension was signif- icantly reduced by probiotics containing B. breve, Bifidobacterium infantis, Lactobacillus casei, or Lactobacillus plantarum. The researchers noted, however, that further research into such variables as
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probiotic dose, species, combinations, treatment dura- tion, IBS subtypes, and specific symptoms was needed, and emphasized that clinicians should always consider comorbid conditions when prescribing probiotics to patients.48 A systematic review and meta-analysis of 43 randomized controlled trials similarly concluded that probiotics can be effective in treating global IBS symptoms, flatulence, abdominal pain, and bloating, though investigators could draw no conclusions about individual strains or species.49
Fecal microbiota transplantation (FMT). Whereas probiotics aim to alter the native gut microbiota, FMT introduces a community of gut microorganisms to re- place or repair the native gut microbiota.50 Although it has been suggested that FMT may improve IBS symp- toms, the procedure has been performed on a limited number of patients.51 Randomized controlled trials are needed to confirm the safety and efficacy of FMT, and the U.S. Food and Drug Administration requires an in- vestigational drug application to perform FMT for any condition other than Clostridium difficile infection that is not responsive to standard therapy.51
use of needles or pressure.54 Whereas acupuncture is the insertion of needles into these acupoints, moxibustion is the application of heat (by ignited moxa).
A systematic review and meta-analysis evaluating the efficacy of acupuncture in treating IBS found no differences between actual and sham acupuncture on either IBS symptoms or quality of life.55 Other investi- gations have used functional magnetic resonance im- aging (fMRI) to evaluate the effects of acupuncture on brain activation in patients with IBS-D during rec- tal distension. Chu and colleagues reported significant fMRI differences between actual and sham acupunc- ture groups: true electroacupuncture significantly heightened activation at the right insula, the pulvinar, and the medial nucleus of the thalamus, compared with sham treatment.56 Another fMRI study of pa- tients with IBS-D and rectal distension found that pa- tients who received actual moxibustion treatment experienced a significant reduction in IBS symptoms compared with those who received sham moxibustion treatment.57
A nurse-delivered intervention of cognitive-behavioral strategies,
diet, relaxation, and education resulted in significantly improved
GI symptoms and quality of life and greater reductions in daily
depression and anxiety scores in patients with IBS.
Increased physical activity. In a randomized controlled trial of 102 patients, Johannesson and colleagues found that a 12-week intervention of moderately increased physical activity significantly reduced IBS symptom severity and improved qual- ity of life.52 In addition, this study found that the pro- portion of worsening IBS symptoms was significantly greater in the physically inactive control group than in the physically active intervention group.
Yoga. A recent systematic review of six random- ized controlled trials found that yoga may have sig- nificant beneficial effects on IBS severity, anxiety, and quality of life.53 Investigators, however, could not make recommendations regarding yoga practice for IBS because of methodologic flaws in the studies re- viewed.
Traditional Chinese medicine modalities, such as acupuncture and moxibustion, have been explored as potential IBS treatments. In traditional Chinese medi- cine, the natural life force, or qi, flows through con- duits or meridians, with disease resulting when there is circulatory interference. Stimulating acupoints restores the flow of qi, and may be accomplished through the
Comprehensive self-management. Jarrett and colleagues evaluated the effect on patients with IBS of a nine-session, nurse-delivered, comprehensive self- management intervention that incorporated cognitive– behavioral strategies, diet, relaxation, and education. These investigators found that patients who under- went the intervention experienced significantly im- proved GI symptoms and quality of life compared with patients who received usual care.58 A secondary data analysis of that study revealed long-term, bene- ficial effects of the intervention, reflected by signifi- cantly lower daily levels of patient-reported stress at three-, six-, and 12-month follow-up.59 Patients with IBS who received the comprehensive self-management intervention were also found to have significantly greater reductions in daily depression and anxiety scores across three-, six-, and 12-month follow-up, compared with patients who received usual care.60 A recent follow-up evaluation of this program found that 94% of the participants who received the interven- tion still incorporate comprehensive self-management strategies into their lives, one year after their last ses- sion.61 These investigations highlight the potential for
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nurse-led initiatives to impart long-lasting, positive health effects to patients with IBS.
IMPLICATIONS FOR NURSING PRACTICE Nurses can promote early consideration of IBS as a potential diagnosis and improve patient education, support, and communication in the following ways: • Become familiar with IBS prevalence rates, as
well as IBS sex and age predominance. • Learn about the disorders that can mimic IBS
signs and symptoms. • Review the Rome IV guidelines, noting which
tests and invasive procedures may be avoided. • Remain aware of the advances in research into
IBS etiology and perpetuation of symptoms. • Understand the high frequency of comorbid psy-
chological disorders and possible life stressors in patients with IBS.
• As part of patient assessment, inquire about di- etary and medication changes, life stressors, and support networks. Although IBS is a common, multifactorial, GI dis-
order that exacts a significant toll on both patients and society, significant advances have been made in the field, and therapeutic options show promise. On- going efforts to understand the many components of IBS will foster a comprehensive, personalized ap- proach to patient care that recognizes the individu- ality of each affected patient. Nursing professionals play a vital role in the collaborative process of pa- tient care and can aid in the development of diagnos- tic and therapeutic approaches, in both the clinical and the research domains. Such innovation, when attuned to the diverse needs of patients with IBS, can produce therapeutic gains and bring symptomatic relief to this deserving patient population. ▼
3. Dekel R, et al. The use of psychotropic drugs in irritable bowel syndrome. Expert Opin Investig Drugs 2013;22(3): 329-39.
4. Patel P, et al. Irritable bowel syndrome is significantly asso- ciated with somatisation in 840 patients, which may drive bloating. Aliment Pharmacol Ther 2015;41(5):449-58.
5. Drossman DA. Functional gastrointestinal disorders: history, pathophysiology, clinical features and Rome IV. Gastroen- terology 2016 Feb 19 [Epub ahead of print].
6. Camilleri M. Physiological underpinnings of irritable bowel syndrome: neurohormonal mechanisms. J Physiol 2014; 592(14):2967-80.
7. Mayer EA, Tillisch K. The brain-gut axis in abdominal pain syndromes. Annu Rev Med 2011;62:381-96.
8. Sperber AD, et al. The global prevalence of IBS in adults re- mains elusive due to the heterogeneity of studies: a Rome Foundation working team literature review. Gut 2016 Jan 27 [Epub ahead of print].
9. Inadomi JM, et al. Systematic review: the economic impact of irritable bowel syndrome. Aliment Pharmacol Ther 2003; 18(7):671-82.
10. Peery AF, et al. Burden of gastrointestinal, liver, and pancre- atic diseases in the United States. Gastroenterology 2015; 149(7):1731-41 e3.
11. Everhart JE, Ruhl CE. Burden of digestive diseases in the United States part I: overall and upper gastrointestinal dis- eases. Gastroenterology 2009;136(2):376-86.
12. Agarwal N, Spiegel BM. The effect of irritable bowel syn- drome on health-related quality of life and health care ex- penditures. Gastroenterol Clin North Am 2011;40(1):11-9.
13. Håkanson C, et al. Being in the patient position: experiences of health care among people with irritable bowel syndrome. Qual Health Res 2010;20(8):1116-27.
14. Ringstrom G, et al. The importance of a person-centered approach in diagnostic workups of patients with irritable bowel syndrome: a qualitative study. Gastroenterol Nurs 2013;36(6):443-51.
15. Canavan C, et al. Review article: the economic impact of the irritable bowel syndrome. Aliment Pharmacol Ther 2014;
Kristen Ronn Weaver is a predoctoral fellow in the Digestive Disorders Unit, National Institute of Nursing Research (NINR), National Institutes of Health (NIH), Bethesda, MD, and a doc- toral student at the New York University (NYU) Rory Meyers College of Nursing, New York City. Gail D’Eramo Melkus is as- sociate dean for research and the Florence and William Downs Professor in Nursing Research at the NYU Rory Meyers College of Nursing. Wendy A. Henderson is an investigator and chief of the Digestive Disorders Unit, NINR, NIH. Contact author: Kris- ten Ronn Weaver, [email protected]. The authors have re- ceived funding from the Division of Intramural Research, NINR, NIH, U.S. Department of Health and Human Services (KRW, an Intramural Research Training Award, Graduate Partnership Program; WAH, No. 1ZIANR000018, 01-05). Additional sup- port was provided to KRW by the NYU Rory Meyers College of Nursing, the Jonas Center for Nursing and Veterans Health- care, and the Columbia University Presbyterian Hospital School of Nursing Alumni Association. The authors have disclosed no potential conflicts of interest, financial or otherwise.
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