To the Editor:
We have read with great interest the article by Brugliera et al.  reporting the prevalence of dysphagia and malnutrition in COVID-19 patients admitted to the San Raffaele Hospital in Milan (Italy). In their work, authors present a three-step nutritional protocol specifically developed for patients infected by SARS-Cov-2. The study is meritorious especially for its potential implications for healthcare policies as targeting a condition (i.e., malnutrition) that has been severely neglected during this time of pandemic. In particular, Brugliera et al.  reported an extremely high prevalence of dysphagia (i.e., >90%) in their COVID-19 patients. Moreover, the vast majority of them (i.e., >70%) presented a moderate-to-marked risk of malnutrition. The protocol the authors implemented at the San Raffaele Hospital has showed very good results, with 43.7% and 46.8% of participants showing an increase and stability of the BMI after discharge, respectively.
However, it is important to consider that the assessment of nutritional status via BMI presents some limitations, especially in older people. In fact, the BMI is not a direct measure of adiposity since its numerator (i.e., body weight) includes both fat and fat free mass. With aging, the organism undergoes through the inversion of the ratio between muscle mass and fat mass, the so-called condition of sarcopenic obesity, which is characterized by (1) a qualitative worsening of the muscle (due to intra- and inter-infiltrates of fat), and (2) the association with negative health-related outcomes . Furthermore, body weight and BMI can be confounded by the presence of ascites and edema in some individuals. Besides of weakening the reliability of these measures (especially in older and complex patients), the excess of fluids also impacts on the results of the bioelectrical impedance analysis.
The impact of COVID-19 on nutritional status cannot be entirely explained by older age and pathologies, as suggested in the article. Functions, age-related physiological modifications, and psycho-social factors also need to be considered as major contributors of malnutrition (Fig. 1) .
In particular, advancing age is associated with an increase of circulating levels of pro-inflammatory cytokines, the so-called “inflamm-aging” phenomenon. Interestingly, adipose tissue is today recognized as an endocrine organ producing a variety of pro-inflammatory cytokines and adipokines. This explains why the excess of fat mass is able to generate a vicious cycle worsening the consequences of obesity via a parallel enhancement of the inflammatory cascade . It has been suggested that the SARS-Cov-2 infection can trigger a rapid activation of the innate immune cells. In fact, infected patients tend to present markedly elevated levels of pro-inflammatory cytokines and chemokines . It seems logical that the obesity background of the individual may exponentially increase the inflammatory reaction of the organism to the pathogen, determining the most severe cases in this population.
Another aspect to consider in addition to what presented by Brugliera et al.  is that sarcopenia is not limited to lower limbs, but should be recognized as a whole body process, also affecting respiratory, masticatory, and swallowing muscles . Recently, the construct of a “sarcopenic dysphagia”, characterized by the concomitant presence of sarcopenia and dysphagia, has been evoked . Consistently, another condition representing an early phase of dysphagia has been indicated with the concept of “presbyphagia”. This latter is not a pathological condition, but occurs with the aging process and determines subtle changes in the swallowing dynamic paving the way for future impaired swallowing . In other words, presbyphagia may predispose to overt dysphagia. The diagnosis of swallowing disorders is composed by a three step process (Table 1) .
Instrumental evaluations frequently cannot be performed because not readily available in most settings. However, screening instruments for the early identifications of swallowing impairments are available, easy to be implemented, and sometimes may be even used for diagnostic purposes. For example, the EAT-10  tool is a simple, 10-item questionnaire providing an objective evaluation of swallowing difficulties.
Beyond the swallowing function, it is also important to consider the masticatory function. Dental problems may have a critical impact on the nutritional status, especially in older persons. Poor oral health may result in increased risk of malnutrition, sarcopenia, and frailty .
The assessment of nutritional status, swallowing capacity, and masticatory function is highly recommended as part of the normal clinical practice. Here we propose a protocol for nutritional screening and interventions in COVID-19 patients (Table 2). However, these critical aspects contributing to the individual’s health are often neglected in normal times. It is not surprising that they have been frequently overlooked during the COVID-19 pandemic as soon as the clinical focus has been shifted towards the treatment of the coronavirus infection. The fact that the standard assessment of the nutritional status can be more challenging during the COVID-19 pandemic does not justify such superficial approach, especially in those patients developing the most severe forms of the disease (and thus at risk of wasting syndromes). In this scenario, clinicians may still rely on rapid screening tools able to identify people at risk of malnutrition, swallowing disorders and/or masticatory problems. Direct interviews with the patient about recent dietary patterns or weight changes might be difficult to conduct because of the severe respiratory conditions as well as for the presence of other comorbidities (e.g., cognitive decline, low level of consciousness). There might also be difficulties at retrieving information from caregivers or relatives due to the lockdown and the limited access to the hospitals. In this context, telemedicine may represent a possible solution for both monitoring the patient as well as obtaining additional information from family members.
In conclusion, the nutritional status should be assessed in all patients, especially today in those affected by COVID-19. The evaluation should be conducted at the admission and at every major change of the health status. The preliminary data coming from the San Raffaele hospital about malnutrition and dysphagia should foster reflections on the importance of early detecting malnutrition and/or swallowing impairment in order to potentially prevent the most serious consequences of COVID-19. The role of nutrition cannot be any longer overlooked (independently of the SARS-CoV-2 infection), given its relevance for the patients and the healthcare systems.
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Azzolino, D., Passarelli, P.C., D’Addona, A. et al. Nutritional strategies for the rehabilitation of COVID-19 patients. Eur J Clin Nutr 75, 728–730 (2021). https://doi.org/10.1038/s41430-020-00795-0
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