key: cord-0870601-pz4n7gqu
authors: Suliman,, Sally; McClave, Stephen A.; Taylor, Beth E.; Patel,, Jayshil; Omer,, Endashaw; Martindale,, Robert G.
title: Barriers to nutrition therapy in the critically ill patient with COVID‐19
date: 2021-10-26
journal: JPEN J Parenter Enteral Nutr
DOI: 10.1002/jpen.2263
sha: b79f1b66dbc81ddf5420e842a2fbf5598837b4c5
doc_id: 870601
cord_uid: pz4n7gqu

BACKGROUND: Coronavirus disease 2019 (COVID‐19) has created challenges for intensivists, as high ventilatory demands and prolonged hypermetabolism make it difficult to sustain nutrition status. The purpose of this survey was to determine current practices in nutrition therapy and identify barriers to its delivery. METHODS: A survey about delivering nutrition therapy to critically ill patients with COVID‐19 was sent to clinicians at academic and community hospitals from September to December 2020. RESULTS: Of 440 who viewed the survey, 199 (45%) completed the questionnaire. Respondents were composed of 30%, physicians and 70% registered dietitians, with 51% representing community programs, 43% academic institutions, and 6% Veterans Affairs centers. Half (49%) had protocols for managing critically ill patients with COVID‐19, and 21% had a protocol for nutrition therapy. Although most respondents (83%) attempted to feed by the intragastric route, only 9% indicated that energy/protein needs were met. The biggest barriers to delivery of enteral nutrition (EN) involved the patients unpredictable clinical course and fear of aspiration given the lack of respiratory reserve. Intensivists were reluctant to add supplemental parenteral nutrition (PN) because of perceived lack of benefit. CONCLUSION: The survey results would suggest that strategies for nutrition therapy based on the intragastric infusion of EN are unsuccessful in meeting the energy/protein needs of critically ill patients with COVID‐19. It is likely these barriers exist in providing nutrition to non‐Covid‐19 critically ill patients. Intensivists need protocols that optimally deliver intragastric EN, consider early postpyloric infusion, and address adding supplemental PN in a deteriorating nutrition status.

The emergence of the SARS-CoV-2 virus and subsequent global pandemic of coronavirus disease 2019 (COVID-19) has imposed considerable challenges for patient care and strained healthcare systems worldwide. The disease primarily affects the respiratory system to variable degrees and can lead to catastrophic clinical deterioration often requiring intensive care and mechanical ventilation to support the patient through an overwhelming inflammatory cascade. 1 Unlike other acute respiratory viral illnesses, those with severe or critical COVID-19 often experience extended stays in the intensive care unit (ICU), prolonged mechanical ventilation and may need extracorporeal oxygenation strategies, which may result in an increased risk of morbidity and mortality. 2, 3 Given the significant complications associated with COVID- 19 , there has been a focus on better understanding and protocolizing the management of these critically ill patients. However, little attention has been paid to nutrition therapy as part of this holistic supportive care. Guidelines developed by the Society of Critical Care Medicine (SCCM) in 2020, 4 in response to the pandemic, failed to adequately address the complex needs of patients and the hesitancy on the part of clinicians surrounding nutrition therapy in this population, necessitating a need to revise the paradigm. We, therefore, designed a survey to better understand the barriers incurred by these healthcare providers and to provide insights into a more effective approach to nutrition therapy in critically ill patients with COVID-19.

This is an observational, survey-based study approved by the Institutional Review Board at the University of Louisville School of Medicine.

Over a 4-month period, from September to December 2020, a survey was sent to participants across the US. The survey was sent out via three separate resources: direct email link, social media website (Facebook), and the monthly newsletter to members of the American Society for Parenteral and Enteral Nutrition (ASPEN).

The survey link was posted on a Facebook page and in the monthly ASPEN newsletter. A total of 330 people engaged the link (ie, read the survey), with 174 participating (a response rate of ∼53%). We also sent the survey link directly, via email, to 110 people, of which 25 reponded (a reponse rate of ∼23%).

Intended recipients of the survey included registered dietitians (RDs), nurses, and intensive care physicians. Although not directly a target, pharmacist members of ASPEN would have had the opportunity to respond via the link in the newsletter. All data responses regarding meeting nutrition goals were self-reported, and all data responses were anonymous and collected through the secure Research Electronic Data Capture database at the University of Louisville School of Medicine.

The survey was composed of 39 questions grouped into seven sections:

Demographics (questions 1-8), ICU proning and treatment schedule (question 9-14), volitional oral diet (questions 15-17), enteral tube feeding (questions [18] [19] [20] [21] [22] [23] [24] , parenteral nutrition (PN) (questions 25-28), additional ICU data (questions 29-32), and design of a nutrition regimen (questions 33-39) ( Table 1) . For each variable, participants were asked to choose from a range of responses provided. All questions had to be answered for the survey to be considered complete. More than half the questions allowed for further free-text elaboration, and the final question allowed for free-text comments.

The purpose of the survey was to ask participants specific questions regarding the nutrition support practices offered to patients with severe SARS-CoV-2 infection being treated in their ICU. In addition to demographic data, participants were asked about the use of enteral nutrition (EN) and PN, design of a COVID-19-specific nutrition regimen, and barriers to delivering adequate nutrition to these patients who were often undergoing treatment for acute respiratory distress syndrome (ARDS) with severe hypoxia.

Only descriptive analysis of the results were performed. In areas in which comparisions are made, large numerical differences are reported.

Of the 440 individuals who viewed the survey link, 199 completed the survey in its entirety (45% response rate 

Forty-six (91/199) percent of respondents reported that the average daily census of patients with COVID-19 in the ICU exceeded 20 cases at the peak of the pandemic (as determined by each individual institution). However, at the time of receipt of the survey, the average daily census of COVID-19 patients in the ICU had dropped, such that only 20% (40/199) of respondents still had >20 cases and 42% (84/199) had between 5 and 20 cases. Approximately half 49%, (98/199) of the respondents indicated that a policy was in place for managing the patient with severe COVID-19 at their institution ( Figure 1 ). Academic centers reported having a policy for managing COVID-19 patients at a higher rate than did nonacademic centers (62% vs 37%, respectively).

Twenty-one percent (42/199) indicated that a specific policy for nutrition therapy for the critically ill patients with COVID-19 was in place at their institution ( Figure 1) , a finding no different between academic and community medical centers.

In an effort to determine preexisting expertise in nutrition support of the critically ill patient, practitioners were asked about their confidence or comfort level in prescribing the nutrition regimen for such patients. Seventy-one percent, (142/199) felt capable and were com-fortable prescribing nutrition therapy to critically ill patients vs 29%

(58/199) who indicated some reluctance ( Figure 2 ). Additionally, 72% 

Respondents were asked which concerns or conditions resulted in ICU patients with SARS-CoV-2 infection being kept with no oral or enteral feeding for a prolonged duration. The most common reason (67%, 134/299, ) for withholding nutrition therapy was fear of bowel ischemia and the need for one or more vasopressor agents. Further concern for potential ischemia (as evidenced by rising lactate levels or mean arterial pressure <60 mm Hg) and potential risk of aspiration because of gastrointestinal symptoms (nausea, vomiting, bloating, and abdominal distention) were common reasons for keeping patients orally restricted as well ( Figure 3 ). Other reasons for withholding nutrition therapy included the use of neuromuscular blockade agents, planned invasive procedures, abdominal sepsis, or high gastric residual volumes of >300 ml. When asked how long patients were allowed to be kept orally restricted prior to the placement of a nasogastric tube, 23% (46/199) responded that nutrition therapy was never withheld for > 2 days, whereas 45% (90/199) indicated that patients were allowed to remain without oral intake for ≥ 5-7 days.

Prone positioning was performed in awake and sedated patients on mechanical ventilation at both academic and community medical centers. Sixty percent, (120/199) of respondents indicated that prone positioning was used in >60% (120/199) of their patients, whereas 22% (44/199) reported that use of proning was limited to <5% (9/199) of their patients. Awake voluntary proning was ordered "as tolerated by the patient" in 42% (84/199) of responses. When asked about efforts to maintain oral diet or provide EN via a feeding tube during awake voluntary proning, 18% (36/199) of respondents indicated that patients were placed on a regular diet "as tolerated" with solid food. Another 58% (116/199) reported that patients were placed on a regular diet with oral supplements, but the intake or tolerance by these patients was not clear. The remaining 24% (48/199) of respondents provided patients with tube feeding only, oral supplements only, clear liquids, or just kept patients orally restricted.

Eighty-three percent, (166/199) of respondents indicated that EN was infused initially into the stomach, with 30%, (60/199) switching to postpyloric if intolerant to gastric feeds. Initial postpyloric placement was utilized by only 11%, (22/199) . The most common type of enteral access device placed by 58%, (116/199) of respondents was a smallergauge nasogastric tube, followed by a large-bore plastic sump tube in 17%, (34/199) and to a lesser extent, either an electromagnetic (Cortrak) or optic vision-guided (Kangaroo with IRIS technology) feeding tube in 11% (22/199) and 2%, (4/199), respectively. For patients infected with SARS-CoV-2, placement of feeding tubes was performed most often by nurses (as indicated by 49%, 98/199 of respondents).

Others responsible for tube placement included intensivists in 15%, (30/199) dietitians in 4%, (8/199) or another healthcare provider, as suggested by the remaining 31%, (62/199) of respondents. The situation was no different for patients without COVID-19 because as nurses, similarly, were the most likely members of the healthcare team to place feeding tubes, as indicated by 47%, (94/199) of respondents.

The regimen for delivery of EN during the first week of illness prescribed advancement to goal by 72 h in less than half (47%, 94/199) of respondents. The remainder of the respondents indicated more cautious feeding, slowing the ramp up to goal out to 7 days, restricting feeds to <50%, or providing only trophic feeding over the first week 

Twenty-three percent, (46/199) of these practitioners responded that they believed the benefit, or value, of PN was equal to EN. Twenty percent (40/199) reported concern that PN might be associated with 

Respondents identified a number of significant barriers to the provision of adequate nutrition therapy in critically ill COVID-19 patients ( Figure 6 ). Unpredictability of the patient's clinical course was seen as the most common obstacle to providing good nutrition, reported by 75%, (150/199) of respondents, in which patients who seemed to be stable receiving some nutrition support suddenly underwent an abrupt and profound deterioration, leading to excessive energy and protein deficits. Reluctance to perform additional procedures for enteral access (24%, 48/199) , ventilatory demands (30%, 60/199), and concern about harmful effects of PN (23%, 46/199) ultimately contributed to difficulty delivering adequate energy for more than half (53%, 106/199) of respondents. 

The COVID-19 pandemic has now been present in the US for >20 Failure to use EN more aggressively was attributed to fear of bowel ischemia or aspiration in patients who were hypercoagulable, required vasopressor therapy, and had no respiratory reserve. Failure to use PN more readily was attributed to concerns for worse outcomes, greater hyperglycemia/hypertriglyceridemia, 9 This has remained a significant issue throughout the pandemic despite some advances in therapeutic interventions and is likely the principal barrier to providing adequate nutrition to these patients. This uncertainty has led to an unstructured atmosphere in the ICU with no standardized protocol for providing nutrition therapy. Furthermore, the unpredictability and everchanging landscape in caring for COVID-19 patients results in nutrition therapy being an afterthought, and often leads to prolonged periods of starvation, weight loss, and increases in the risk of refeeding syndrome. 14 The significant degree of hypoxia experienced by these patients is a unique characteristic of the infection, often termed "happy hypoxia" and is a major barrier to volitional oral diet and EN based on several comments from our survey. Over the course of the pandemic, the therapeutic approach to this hypoxia has evolved. Initially, physicians were quick to rely on mechanical ventilation as the sole intervention, whereas now the majority of intensivists try to use alternative therapies where possible, such as NIPPV and high-flow oxygen, to avoid mechanical ventilation. 15, 16 As a result, patients are often left on NIPPV or high-flow oxygen per nasal cannula for extended periods of time because of significant oxygen demands. With such little respiratory reserve, the idea of initiating nutrition therapy becomes an added burden of concern for physicians. Based on the results of our survey, many of these intensivists feel that the initiation of nutrition therapy is associated with its own unique set of risks and so is often intentionally withheld. Clinicians are adopting a "hope for the best, plan for the worst" mentality, which may be restricting full delivery of the nutrition support regimen and contributing to worsening complications. Among those perceived risks appears to be significant concern for aspiration pneumonia, which would be considered catastrophic in patients with such severe hypoxia. Therefore, nutrition is withheld in the hopes of avoiding mechanical ventilation and poorer outcomes.

Several comments from our survey indicate that the risk of aspiration was also a reason to restrict both volitional oral intake and EN via an enteral access device, despite most studies showing reduced risk of aspiration pneumonia with enteral feeding 17 in non-COVID-19 critically ill patients. 18 Infection with SARS-CoV-2 appears to cause a unique disease process, leading to severe ARDS in many patients, who then require placement in the ICU. Early in the pandemic, it was thought that placement on mechanical ventilation led to poorer outcomes and increased risk of death, and so practices such as awake proning were adopted to avoid intubation. 19 This again led to an increase in reluctance to feed patients because of aspiration concerns. Our survey revealed that up to 44% of responders adopted an "as tolerated" approach to feeding when it came to awake proning. Such practice highlights the lack of clear societal guidelines and results in periods of up to 7-10 days without adequate nutrition. 20 Furthermore, a frequent lack of proning beds occurred because of the sheer number of critically ill patients. In their place, most ICU teams adopt a manual proning policy with standard beds, which often leads to facial edema, neck torticollis, inadvertent dislodgement of endotracheal tubes and other lines, and an increase in oral secretions, as commented on by several responders in our survey. In a small trial of 33 prone patients with COVID-19, the most common complication was facial edema (26 of 33 of patients), with only two patients inadvertently removing their nasogastric tube. EN was generally well tolerated, except in two patients requiring increased maneuvers, which resulted in vomiting and withholding of EN. 21 In a systematic review of feeding intolerance of non-COVID-19 prone patients in six studies, the need to stop EN and vomiting episodes were primarily higher in only one study. 22 These additional problems continue to push nutrition therapy down the list of priorities when approaching critically ill patients with COVID-19.

The profound cytokine storm caused by the virus results in severe insulin resistance. This development, combined with the introduction of glucocorticoids as the mainstay of therapy later in the pandemic, has led to clinically noticeable unpredictability surrounding glycemic control, which was reported to be a significant concern for ICU providers in the survey. This appears to influence the ICU providers, having direct consequences on the initiation and continuation of nutrition therapy, as well as the route and volume of delivery, again highlighting the unstructured approach to nutrition support in critically ill patients with COVID-19.

A surprising finding was reluctance on the part of physicians to initiate PN in critically ill patients. This indicated a significant misconcep-tion or personal bias about the risks associated with use of PN. 7, 11, 23 According to the survey, respondents often felt that prolonged trophic enteral feeding was adequate, despite evidence for ongoing deterioration of nutrition status in these COVID-19 patients with prolonged hypermetabolism. 24 Other reasons for such hesitancy included the lack of dedicated intravenous access and, in particular, a fear that placing a patient in Trendelenburg position to place a dedicated central line would cause aspiration or worsening hypoxia. Interestingly, there was a higher likelihood of withholding PN in academic centers compared with community hospitals, despite a push from dietitians to be more aggressive. Such responses from the survey show a fundamental lack in adopting recent guidelines surrounding the safety of PN and demonstrate a need for the ASPEN guidelines to create a new paradigm for PN to truly address these concerns.

An overarching message from the findings of this survey, and the literature, is that gastric feeding alone is not enough. Prolonged attempts at gastric feeding may lead to dramatic underfeeding and a decline of nutrition status. As a result, each institution should perform a selfevaluation of its ICU practices and determine its access to nutrition expertise. If gastric feeding is not sufficient early, it may be more fruitful to transition to smallbowel feeding sooner or add in supplemental PN to ensure adequate nutrition support and work around the concerns of providers. 25 As with any study, limitations exist. Clearly, the questionnaire is not a validated survey instrument, but it does allow us to gauge some common clinical practices associated with providing nutrition therapy in critically ill patients with COVID-19 across various healthcare organizations throughout the US. Although we had a good response rate (45%), the data were gathered more from dietitians than physicians.

This relatively low response rate from physicians may indicate that the answers were not reflective of the entire physician population or the general practice among this group. In addition, the survey requested an opinion of the practitioner, as opposed to defined measurements of nutrition therapy received or complications experienced by the patient.

Lastly, participants were selected from groups whose members likely have a higher interest in critical care nutrition, such as ASPEN members. As such, they may be more likely to follow published guidelines compared with general ICU providers, and so again, responses may not accurately reflect common ICU practices. In contrast, this could highlight an underrepresentation of the extent of the knowledge gap in critical care nutrition.

Lastly, we have not made any recommendations based on these findings. This survey has highlighted some real gaps in the approach to nutrition therapy in critically ill patients with COVID-19. We suggest a more methodical approach to nutrition support in this patient population and revision of earlier recommendations that were made at the start of the pandemic. There is an obvious need to provide physicians with a clear and meaningful set of recommendations for prescribing nutrition therapy in critically ill COVD-19 patients. Such guidelines would allay any apprehension surrounding complications related to providing adequate nutrition therapy and may lead to improved outcomes in patients after a prolonged hospitalization. The unfortunate arrival of the COVID-19 pandemic raises new challenges for nutrition therapy and has shown a need to reacquire skills for the

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