Introduction
Anorexia and undernutrition have numerous negative enteric and systemic impacts. Lack of enteral nutrition induces intestinal mucosal atrophy,1 alters gastrointestinal (GI) mucosal immunity,2 decreases nutrient transport,3 and decreases enterocyte survival.4 Added metabolic consequences of undernutrition include lean body mass loss, vitamin and mineral deficiencies, and glucose intolerance, which in humans lead to longer durations of hospitalization and increased mortality.5,6
Risks of undernutrition in hospitalized dogs and cats have also been documented. In dogs with severe illness and nutritional status evaluations at the time of hospital presentation, indicators of undernutrition were associated with worse outcomes.7 Hospitalized dogs with evidence of undernutrition demonstrated hematologic abnormalities, such as decreased Hct and evidence of altered iron metabolism.8,9 Additionally, dogs hospitalized for longer than 3 days were more likely to lose weight than those hospitalized for shorter periods of time.10 Yet hospitalized dogs that met energy requirements had a lower risk of death.10,11 Additionally, it is well-known that cats have increased risk of hepatic lipidosis and decreased ability to downregulate proteolysis in states of protein undernutrition.12
Provision of early enteral nutrition has been associated with improved outcomes in specific diseases. In acute pancreatitis models, enteral nutrition improves the GI barrier, decreasing bacterial translocation.13,14 In dogs hospitalized for acute pancreatitis, early enteral nutrition decreased time to any voluntary food intake, as well as maximum intake, and improved GI food tolerance.15,16 In dogs with septic peritonitis, dogs that received any enteral nutrition were more likely to survive than dogs that only received parenteral nutrition.17,18 Early enteral nutrition decreased GI permeability, improved weight gain, and resulted in earlier clinical improvement (normalized appetite, resolution of vomiting) in puppies with enteric parvovirus.19
Despite the known risks of undernutrition and prognostic benefits of nutritional intervention, nutritional intervention is frequently delayed and adequate nutrition is not achieved in many patients.10 While the International Society of Feline Medicine guidelines for cats recommend enteral nutrition intervention after 3 days of inappetence, literature evidence for institution of this recommendation is lacking.20 Therefore, the primary objective of this study was to evaluate the factors associated with the timing of nutritional intervention through placement of feeding tubes in hospitalized dogs and cats with inadequate food intake in the ICU.
Methods
Electronic medical records were searched from an academic veterinary hospital (Kansas State University Veterinary Health Center) from January 1, 2014, through December 31, 2023, for dogs and cats that underwent nasogastric/nasoesophageal (NG) or esophagostomy feeding tube (e-tube) placement. Search terms included charge codes for feeding tube placement procedures or imaging modalities to verify correct placement (eg, radiographs, endoscopy). Duplicate results for the same feeding tube placement were omitted. Unique records identified through the above search were reviewed for study inclusion. Exclusion criteria included incomplete medical records (eg, patient care sheet for feeding information or purpose for enteral feeding tube placement not available), nutrition not administered through tube (eg, use for gastric residual management, water, or medication administration only), and outpatient feeding tube placement. Patients that had prophylactic feeding tube placement at the time of admission for a surgical procedure or physical inability to intake oral nutrition (eg, mandibular fractures, oropharyngeal dysphagia) were also excluded; these were considered unique from the goal study population, as there was not an opportunity to evaluate in-hospital voluntary intake or clearly determine whether a lack of intake was due to voluntary inappetence or physical inability, respectively (Figure 1).
Medical record screening and sequential exclusions for inclusion of hospitalized dogs and cats in a retrospective study evaluating time to feeding tube placement in ICU patients.
Citation: Journal of the American Veterinary Medical Association 263, 3; 10.2460/javma.24.07.0494
For included cases, information extracted from the medical record included date of tube placement, species, age, breed, weight, body condition score, muscle condition score (MCS), initial feeding tube type, whether a secondary tube was placed, duration of dysorexia prior to hospital administration, days to feeding tube placement following admission, days to secondary feeding tube placement, whether the patient survived to discharge (yes or no) and days to discharge following feeding tube placement, hospital service responsible for primary case management and/or primary decision to place feeding tube, underlying reason for hospitalization, concurrent clinically relevant comorbidities or additional anesthetic procedures, whether feeding instructions were adequate to calculate goal caloric intake, whether exact caloric intake could be calculated based on treatment sheet appetite recordings, and day of hospitalization (ie, weekday [Monday through Thursday] vs weekend [Friday through Sunday]). Primary reason for hospitalization and comorbidities were based on clinician documentation in the medical record; it was not attempted to independently confirm the listed diagnoses. For patients with more than 1 type of feeding tube placed during a single hospitalization event, the time to provision of enteral nutrition and time to discharge was based off the first tube placed. Individual animals could be included more than once if they experienced independent hospitalization events during the study period.
Duration of dysorexia at presentation was based on owner-provided histories that were recorded in the medical record. Any degree of reported decreased intake was defined as dysorexia, rather than anorexia, as medical records were generally insufficient to conclude actual caloric intake prior to presentation. When a range of dysorexia duration was noted in the medical record, the shorter duration was used for statistical calculation.
In-hospital appetite was determined based on review of ICU treatment sheets throughout a patient’s hospitalization. There was considered to be a clinician-directed feeding plan when sufficient information was provided to calculate a goal caloric intake, including amounts of a specific food(s) and defined frequency. Where possible, calculation of patient intake relative to resting energy requirement (RER) or clinician’s goal caloric intake was performed. Resting energy requirement was calculated based on the predictive RER equation for current body weight:
In-hospital hyporexia was defined as intake lower than these values. In patients where these values were unable to be determined from the medical record, hyporexia was presumed based on subsequent feeding tube placement. Calculations were based on treatment sheet notation of volume of food intake. As many treatment sheets did not contain sufficient information to perform these calculations, it was not attempted to distinguish severities of hyporexia.
Statistical analysis
Statistical analyses were performed with commercial software (Prism, version 10.2.1; GraphPad Software Inc). As most data were not normally distributed based on the Shapiro-Wilk test, nonparametric analyses were used. Descriptive statistics were used to describe the study population, with continuous variables reported as median (range) and categorical variables reported as frequency. Fisher exact tests were used to compare outcomes of tube type based on species, admission day (weekend vs weekday), and whether the patient was undergoing an unrelated anesthetic procedure (yes or no), as well as association between feeding orders and recording of caloric intake (yes or no). Survival to discharge was also compared between initial feeding tube types. Likelihood of placement between years (2014 to 2018 vs 2019 to 2023) and species was also compared based on the total caseload hospitalized in the ICU for at least 2 days. Mann-Whitney tests were used to compare days to feeding tube placement between species, feeding tube types, admission days, whether an additional anesthetic procedure was performed, and provision of feeding orders, as well as to compare days to discharge between feeding tube types. The Kruskal-Wallis test, followed by post hoc analysis and Dunn multiple comparison pairwise analyses on significant models, was performed to determine whether disease category impacted time to feeding tube placement. Spearman correlation (rs) was used to compare duration of dysorexia prior to admission to time of initial feeding tube placement. Strength of correlation was defined as previously described (0 to 0.09, negligible; 0.1 to 0.39, weak; 0.4 to 0.69, moderate; 0.7 to 0.89, strong; 0.9 to 1.0, very strong).21 A P value < .05 was considered significant.
Results
Following medical record review, 295 total cases were included, 90 cases from 2014 to 2018 and 205 cases from 2019 to 2023. Feeding tubes of either type were placed sooner between 2019 and 2023 (median, 2 days; range, 0 to 16 days) versus 2014 and 2018 (median, 3 days; range, 0 to 17 days; P < .0001). Accounting for total number of patients hospitalized in the ICU for at least 2 days, feeding tubes were also less likely to be placed between 2014 and 2018 than 2019 and 2023 (OR, 0.59; P < .0001; 95% CI, 0.46 to 0.77). This was true for both cats (OR, 0.53; P < .01; 95% CI, 0.33 to 0.86) and dogs (OR, 0.64; P = .003; 95% CI, 0.48 to 0.86) when evaluated independently. Individual animal signalment characteristics and disease descriptions are included in Supplementary Table S1.
Study population
The study population included 89 cats and 206 dogs. Accounting for all years and the total caseload hospitalized in the ICU during the study timeframe, cats were more likely to have feeding tubes placed than dogs (OR, 2.64; P < .0001; 95% CI, 2.0 to 3.4). Patients receiving feeding tubes were primarily treated by the small animal internal medicine (n = 227) and small animal surgery (63) services; 2 patients were treated exclusively by the emergency service and 1 each by the cardiology, ophthalmology, and oncology services. Cat median age was 9.0 years (range, 1.0 to 17.3 years). Median cat weight was 4.6 kg (range, 1.8 to 8.6 kg). Body condition score (median, 5.0 of 9; range, 1.0 to 9.0) and MCS (median, moderate diffuse muscle atrophy; range, normal to severe) were recorded in 62 (70%) and 39 (44%) cats, respectively. Dog median age was 7.1 years (range, 0.1 to 16.6 years). Median dog weight was 11.3 kg (range, 0.7 to 69.0 kg). Body condition score (median, 5.0; range, 1.0 to 9.0) and MCS (median, normal; range, normal to severe muscle atrophy) were recorded in 115 (56%) and 53 (26%) dogs, respectively.
Duration of inappetence and species-associated factors on feeding tube placement
Duration of dysorexia prior to hospitalization was recorded in 287 animals (97%), with a median of 4 days (range, 0 to 90 days), including a median of 3 days (range, 0 to 60 days) in cats and 4 days (range, 0 to 90 days) in dogs (P = .299). Median duration of hospitalization prior to initial feeding tube placement was 2 days (range, 0 to 17 days) and was shorter in cats versus dogs (P < .001; Table 1). However, combined duration of decreased caloric intake was not different between cats (median, 6 days; range, 0 to 62 days) and dogs (median, 6 days; range, 0 to 96 days; P = .444). Overall, days to placement of the initial feeding tube following admission was weakly negatively correlated with duration of dysorexia prior to hospitalization (rs = –0.13; P = .026; 95% CI, –0.25 to –0.01). However, when evaluating feeding tube placement in dogs and cats independently, time to placement was only correlated with preadmission dysorexia duration in cats (cats [rs = –0.29; 95% CI, –0.48 to –0.08; P = .007]; dogs [rs = –0.04; 95% CI, –0.18 to 0.10; P = .558]). A total of 19 cats (21%) and 22 dogs (11%) had a second feeding tube type placed (ie, not the replacement of an inadvertently removed feeding tube) a median of 3 (range, 1 to 6) and 4 (range, 1 to 9) days after initial tube placement, respectively. Cats were more likely to have a second tube placed than dogs (OR, 2.3; P = .018; 95% CI, 1.2 to 4.3). Median days to discharge following initial tube placement was 4 days (range, 0 to 24 days), 3 days (range, 0 to 17 days) in cats and 4 days (range, 0 to 24 days) in dogs (P = .04).
Comparison of factors associated with time (days) to placement of an initially placed nasogastric/nasoesophageal (NG) tube or esophagostomy tube (e-tube) in hospitalized dogs and cats.
Median (range) days | P value | |
---|---|---|
NG tube | ||
Duration of dysorexia prior to admission | 3 (0–90) | .056 |
Days following admission | 2 (0–16) | < .001 |
Days prior to placement | 2 (0–15) | < .001 |
E-tube | ||
Duration of dysorexia prior to admission | 4 (0–60) | .056 |
Days following admission | 3 (1–17) | < .001 |
Days prior to placement | 3 (0–17) | < .001 |
Species | < .001 | |
Cat | 2 (0–6) | |
Dog | 3 (0–17) | |
Day of admission to hospital | .030 | |
Monday–Thursday | 2 (0–16) | |
Friday–Sunday | 3 (0–17) | |
Specialty service facilitating feeding tube placement | < .001 | |
Small animal surgery | 4 (1–17) | |
Small animal internal medicine | 2 (0–15) |
Comparison of feeding tube types
Nasogastric or nasoesophageal tubes were the initial feeding tubes placed in 208 animals (71%; 47 cats [53%]; 161 dogs [78%]), while e-tubes were initially placed in 87 animals (29%; 42 cats [47%]; 45 dogs [22%]). Cats were more likely than dogs to have e-tubes placed first (OR, 3.2; P < .001; 95% CI, 1.9 to 5.4). Day of hospital admission (ie, weekend vs weekday) was not associated with the type of tube initially placed (P = .362) but was associated with time to feeding tube placement (P = .03). Forty-seven of 102 patients (46%) undergoing an ancillary anesthetized procedure had an e-tube initially placed and were more likely to have an e-tube placed initially than patients not undergoing anesthesia for reasons other than feeding tube placement (40 of 193 [21%]; OR, 3.3; P < .001; 95% CI, 1.9 to 5.4). Sixty-seven animals (23%) out of the overall study population died prior to discharge, including 50 (24.0%) that had initial NG tube placement and 17 (19.5%) that had an e-tube initially placed (P = .449). Days to discharge following feeding tube placement was shorter in patients that received an initial e-tube (median, 2 days; range, 0 to 24 days) versus initial NG tube (median, 4 days; range, 1 to 19 days; P < .001). Factors associated with time to feeding tube placement are highlighted in Table 1.
Disease associations
In cats, the most common reason for hospitalization was hepatobiliary disease (n = 28), which was documented as primary hepatic lipidosis via cytology in 18 cats, followed by renal disease (13), primary GI disease (11), and endocrine, infectious, and pancreatic disease (8 each). Clinically relevant comorbidities were recorded in 27 cats, with endocrine being most common (n = 7), followed by renal and hepatobiliary disease (4 each); hepatic lipidosis was the cause of hepatobiliary disease in all 4 of these cats. In dogs, the most common reason for hospitalization was primary GI disease (n = 63), followed by renal disease (33), hepatobiliary disease (24), and pancreatic disease (22). Clinically relevant comorbidities were documented in 61 dogs, with the most common being endocrine (n = 15) and pancreatic disease (11). While time to feeding tube placement differed between disease categories in both dogs (P < .001) and cats (P = .016), pairwise comparisons between categories were not significant (Supplementary Table S2). Further, cats with hepatobiliary disease were not more likely to have an initial e-tube placed compared to cats with other diseases (OR, 1.9; P = .18; 95% CI, 0.8 to 4.4).
Impact of feeding treatment plans
Feeding instructions on treatment sheets, including diet type and amount, were adequate to estimate goals for caloric intake in 53 patients (18%), including 21 cats (24%) and 32 dogs (16%; P = .102). There was no difference in whether adequate feeding instructions were provided between 2014 and 2018 (10.0%) versus 2019 and 2023 (19.5%; P = .061). Appetite assessment recorded in the medical record was adequate to estimate actual caloric intake based on inclusion of specific diet, amount offered, and percent of offered meal ingested in 42 patients (14%), including 12 cats (13%) and 30 dogs (15%). This included 24 animals with specific feeding instructions and 18 animals without specific feeding instructions. Patients with specific feeding instructions were more likely to have an exact caloric intake recorded (OR, 10.3; P < .001; 95% CI, 4.9 to 21.0). Feeding tubes were also placed sooner following admission in patients with specific feeding instructions (median, 2 days; range, 0 to 16 days) versus without (median, 3 days; range, 0 to 17 days; P = .034).
Discussion
The overall median time to feeding tube placement of 6 days, including prehospitalization and postadmission time, documented in this study is well outside the guidelines for feline patients as outlined by the International Society of Feline Medicine and likely detrimental for canine patients as well.20 The present study identified multiple factors at an academic veterinary hospital associated with time to feeding tube placement in hospitalized dogs and cats, which can help guide clinician awareness.
Median time to initial feeding tube placement following hospitalization was shorter in cats by 1 day (with a smaller range of up to 6 versus 17 days) compared to dogs and may reflect the higher concerns for hepatic lipidosis in feline patients. As obligate carnivores, cats have metabolic differences that increase the risk of early complications from undernutrition compared to dogs, including a decreased ability to downregulate amino acid catabolism.22 Additionally, prolonged anorexia can lead to hepatocyte lipid accumulation and secondary hepatic lipidosis.23 Widespread knowledge of this disease likely contributed to faster placement of enteral feeding tubes in cats with dysorexia. Indeed, hepatobiliary disease, including primary hepatic lipidosis, was the most common underlying condition leading to hospitalization in the cats in this study. Interestingly, the time to feeding tube placement was not shorter in cats with hepatobiliary disease compared to other diseases in pairwise comparisons, but this may reflect the recognized risk of cats developing secondary hepatic lipidosis regardless of presenting medical condition. In this study, cats were more likely than dogs to have an e-tube placed first and more likely than dogs to have an e-tube placed following NG tube placement prior to discharge. It is possible that this reflects clinicians’ experiences that cats tend to require a semipermanent method to provide enteral nutrition during their prolonged recovery time in the home environment or reflects an underappreciation for the consequences of undernutrition in dogs. Although the total number of feeding tubes placed was higher in dogs than cats in this study, cats were more likely to have a feeding tube placed when compared to the total hospitalized caseload, which could support these considerations.
Most patients (71%) in this study had NG tubes placed initially, with 32% having a subsequent e-tube placed. This is not surprising, as e-tube placement requires general anesthesia and, therefore, greater hemodynamic and metabolic stability. Metabolic abnormalities are common in critically ill dogs and cats, including acid base disorders, electrolyte disturbances, and water imbalance.24–27 These abnormalities can result in deleterious cardiovascular effects,28 making many dogs and cats poor anesthetic candidates at the time of presentation. Placing an NG tube prior to an e-tube allows for stabilization and is thought by some clinicians to help reduce morbidity associated with e-tube placement.29 These factors may contribute to the higher percentage of patients receiving an initial NG tube. In this study, however, there was no difference in mortality between patients with NG tubes versus e-tubes placed initially. These findings could be influenced by clinician decision-making on which enteral feeding route to pursue on a case-by-case basis. It is possible that an initial NG tube was chosen to allow stabilization prior to general anesthesia or determine whether a patient would otherwise eat voluntarily before placing an e-tube. Notably, though, there was a longer duration of time to enteral feeding provision in patients that had an initial e-tube placed. While it could not be completely determined due to the retrospective nature of the study, this potentially suggested that clinicians intending to place an e-tube elected not to place an NG tube in the interim period and that increased awareness of providing nutrition prior to e-tube placement is warranted.
Independent clinician practices also influenced time to initial feeding tube placement. Dogs and cats that had specific enteral nutrition goals and specific feeding instructions on treatment sheets (ie, diet type and amount per feeding) were more likely to have enteral feeding tubes placed sooner than those patients without specific feeding instructions. This suggested that clinicians who prioritize the nutritional status of their patients place feeding tubes earlier. Further, patients that had specific feeding instructions were also over 10 times as likely to have caloric intake recorded, suggesting that objective information versus subjective appetite assessments (eg, “good,” “great”) may increase clinician awareness of hyporexia. It further supports the need to involve the full care team, ensuring that ICU veterinary nurses and assistants appreciate the importance of documenting this information. This study was not designed to evaluate patient outcomes based on these factors, and future studies are required to add to the current knowledge base of how early enteral nutrition impacts patient survival and length of hospital stay. The rising cost of veterinary care may impact a clinician’s decision to place feeding tubes in hospitalized patients in the early period of hospitalization if prognosis is uncertain.
Hospital-associated factors were also related to timing of enteral nutrition. This study showed that patients admitted over the weekend (Friday through Sunday) had a longer period to feeding tube placement versus those admitted Monday through Thursday. Though the retrospective nature of this study did not allow determination of the exact reason, it is possible that this was associated with admission through the emergency service and primary case management by interns for most of the years included in this study. Whether this was due to lack of time for feeding tube placement while managing emergency-case receiving or decreased doctor experience, it suggests that increased education in nutritional assessment of patients and feeding tube placement might be beneficial. Another possible factor may have been decreased nursing staff on the weekends to provide the experienced care needed for patients with feeding tubes or time constraints to record exact food intake. Lastly, it is possible that feeding tube placement was delayed over the weekend for initial e-tube placement, without interim NG tube placement for some patients. In human medicine, there is a similar hypothetical association called the “weekend effect,” which states that patient outcomes are worse over the weekend. In 1 study30 of risk factors affecting delayed enteral nutrition (> 48 hours after admission to the hospital), provider-level factors were associated with delayed enteral nutrition, but there was no association with weekend versus nonweekend days. In another study,31 understaffing was associated with risks of undernutrition in an ICU setting, particularly the lack of dietician coverage over the weekend. Studies are lacking in veterinary medicine that evaluate patient safety or case outcomes based on day of presentation or level of doctor education, but this study suggested that better oversight from more-experienced clinicians, active educational efforts, and active awareness of delayed weekend feeding may help patients receive earlier enteral nutrition. When considering education, the time to place a feeding tube was significantly shorter in the last 5 years compared to the first 5 years of the study. This could be due to better understanding of how early enteral nutrition impacts physiology and possible case outcomes. Most of the veterinary-specific literature recording the effects of enteral nutrition in hospitalized patients has been published within the last 10 years. Supportive of this consideration, feeding tubes were also more likely to be placed in hospitalized patients during the last 5 years of the study when accounting for the total hospitalized caseload. Continuing to highlight and study the case outcomes associated with early enteral nutrition may help clinicians prioritize nutritional management in their anorexic or hyporexic hospitalized patients. Owner factors may have also impacted this finding, with more owners willing to make substantial investments into the care of their dogs and cats in recent years.32–34
Additionally, patients managed by surgery services had longer times before placement of a feeding tube compared to those managed by the internal medicine service. This finding could be influenced by the exclusion of patients whose feeding tubes were placed prophylactically during surgery at the time of hospital admission, which could have indicated clinician foresight and anticipation of postoperative inappetence in some surgical patients. This observation also correlated with the finding that patients with planned anesthetic procedures also had longer time to feeding tube placement. Early enteral nutrition in hospitalized patients may be overlooked by clinicians expecting to place 1 feeding tube under a single anesthetic event, despite this decision delaying adequate nutrition in the preceding days. Other explanations include unanticipated postanesthetic complications, such as pancreatitis or ileus in surgical patients, in cases where it was expected that the surgery would alleviate initial problem causing anorexia, as is in the case of GI foreign body surgery.35 Early intervention in animals with postoperative anorexia via NG tube placement or e-tube placement may be warranted, especially for those with prolonged poor nutrition prior to their procedure or prolonged anesthetic times.36
The biggest limitation to this study was its retrospective nature. While we identified factors associated with time after hospitalization to provision of enteral nutrition, patient or external influences on these factors could not be determined. Therefore, these findings do not necessarily represent the complete picture of clinical decision-making. For example, it is likely that patient characteristics, such as oxygen dependency, intractable vomiting, or coagulopathies, contraindicated earlier placement of either feeding tube type in some animals. Furthermore, this study could not account for cases where feeding tube placement was declined by clients due to either preference or financial constraints. It is likely that the study’s exclusion criteria influenced both case associations with time to placement (ie, lack of association with underlying disease in cats) and overall time to placement. Many high-risk patients had feeding tubes placed prophylactically and were, therefore, not included. In this way, our study may overestimate the amount of time to provide nutrition to the entire population of patients presenting to the Kansas State University Veterinary Health Center overall or to individual services (eg, surgery services). However, the goal of our study was to specifically focus on those patients within the ICU. In contrast, this study only evaluated patients that ultimately had feeding tubes placed; as previous literature10 demonstrates undernutrition in many hospitalized small animals, this study could also underestimate the period of undernutrition for the overall ICU population. Further, the lack of differences between disease categories may reflect the relatively small number of patients in each category, with as few as 4 animals in some categories, and lack of statistical power to determine a difference. Lastly, this study only evaluated 1 academic veterinary hospital. It would be interesting to compare these findings with private specialty veterinary hospitals and hospitals with veterinary nutritionists on staff.
In conclusion, this study revealed practical information for clinicians caring for dogs and cats in an ICU setting. Results suggested that prioritizing nutritional support for patients admitted on weekends or awaiting semipermanent feeding tube placement could reduce the time spent in-hospital before caloric needs are met. Clinician- and ICU-driven practices to provide specific feeding plans and record food intake are likely keys to improved recognition of the need for nutritional support, whether through placement of feeding tubes or other means of ensuring adequate caloric intake. Future prospective studies could investigate clinician decision-making practices that influence timing of feeding tube placement and impact on patient outcomes.
Supplementary Materials
Supplementary materials are posted online at the journal website: avmajournals.avma.org.
Acknowledgments
None reported.
Disclosures
The authors have nothing to disclose. No AI-assisted technologies were used in the generation of this manuscript.
Funding
The authors have nothing to disclose.
ORCID
M. C. Jugan https://orcid.org/0000-0002-6963-7646
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