Coronavirus disease 2019 (COVID-19) is charac-terized by a severe inflammatory and highly catabolic status influencing deep changes in skeletal muscle mass and structure that can lead to sarcopenia¹. Pro-inflammatory cytokines are released due to COVID-19 infection, and physical inactivity and malnutrition during COVID-19 hospitalization could increase the risk of sarcopenia. Venovenous extracorporeal mem-brane oxygenation (vv-ECMO) is increasingly being used in COVID-19 patients as a rescue therapy for severe acute respiratory failure refractory to conven-tional therapy². More than 1,100 COVID-19 patients worldwide have undergone vv-ECMO³. Most were se-verely ill with increased muscle catabolism, weakness, and atrophy, which can result in sarcopenia and increase morbidity and mortality.

Oropharyngeal dysphagia is common in COVID-19 patients, especially those on mechanical ventilation⁴. Dysphagia is a concern in COVID-19 patients during the viral response, pulmonary, and hyperinflammation phases⁵. COVID-19 is associated with a high risk of malnutrition and many other complications, including polyneuropathy, myopathy, and various dysphagia- associated neurological complications related to dys-phagia⁶. Sarcopenia in COVID-19 patients also affects the muscles related to swallowing, causing so-called sarcopenic dysphagia⁷. Sarcopenic dysphagia is a swallowing disorder due to sarcopenia involving the whole-body skeletal muscles and swallowing muscles⁸. And severe acute respiratory distress syndrome inc-reases the risk of dysphagia. One-third of patients with severe acute respiratory distress syndrome who require ECMO reportedly have symptoms of dysphagia at the time of hospital discharge⁹.

That is, COVID-19 patients are at risk of sarco-penia and dysphagia, which can additively affect sarcopenic dysphagia and worsen their prognosis. Sarcopenic dysphagia, which is characterized by a loss of swallowing function and generalized muscle mass, can reportedly be improved by rehabilitation¹⁰. However, there is little evidence of active rehabili-tation for sarcopenic dysphagia in vv-ECMO following COVID-19 infection. This case report describes the early active rehabilitation course and progression of sarcopenic dysphagia in a 65-year-old man with severe COVID-19 who underwent awake vv-ECMO. This unique case demonstrates the importance and specific considerations of dysphagia rehabilitation during subacute critical COVID-19 infection.

The study was approved by the local institutional ethics committee (no. 2022-11-016). A 65-year-old man without underlying disease was diagnosed with COVID-19. Before hospitalization, he was fully inde-pendent in all activities of daily living (ADL) and had no swallowing problems (functional oral intake scale [FOIS] level 7). He has received the second dose of the Astra-Zeneca vaccine. As he complained of dyspnea and his oxygen saturation was low, he was admitted to a tertiary university hospital 1 d after being diag-nosed with COVID-19 (hospitalization day [HD] 0; Fig. 1). However, the respiratory failure progressed and he underwent endotracheal intubation with invasive mechanical ventilation and vv-ECMO on HD1. The patient was extubated 7 days after ECMO and under-went awake ECMO on HD7. Unfortunately, he develo-ped generalized weakness and dysphagia, could not maintain a seated posture, and required Levin tube feeding (FOIS 1).

Figure 1. Hospital course of the patient.

To improve the weakness and prevent sarcopenia progression, he began a bedside mobilization program on HD13. The mobilization team consisted of a PM&R doctor, a thoracic surgeon as an intensive care phy-sician and an ECMO intensivist, two critical care registered nurses, and a perfusionist depending on his functional needs and clinical stability. The patient was evaluated daily to assess hemodynamic and respi-ratory stability, and suitability for bed side mobilization program by comprehensive mobilization team. Dis-cussions were conducted with thoracic surgeon rega-rding the position and location of ECMO cannulation before initiating treatment. During mobilization program, real-time adjustments to the ECMO were made while monitoring O2 saturation levels. The thoracic surgeon modulated flow rate of ECMO during mobilization program. The physical therapy level was set accor-ding to his activity level¹¹. When he started rehabili-tation, his orientation showed degradation (Richmond Agitation Sedation Scale, −2; Glasgow Coma Scale, 12; Table 1). The patient received 30 min of bedside physiotherapy five times a week in the ICU. On HD19, chest radiography showed improved multifocal opacities in both lungs, and the ECMO support was withdrawn. On HD27, he was transferred from the ICU to the general ward.

Table 1 . Clinical course, dysphagia and sarcopenia..

Status of dysphagia and sarcopenia		HD13	HD17	HD36	HD50	HD62	HD115	HD206
FOIS		1	1	4	5	5	7	7
VFSS	PAS (semisolid)			7	1	1
	PAS (fluid)			n/c	6	1
	VDS-O			31.5	0	0
	VDS-P			53.5	4	0
	ALFM (mm)			7	9	11
	ALUM (mm)			28	41	39
	Pharyngeal constriction ratio			0.11	0.10	0
Cognition	RASS	−2	−2	−2	−1	0	0	0
	GCS	12	12	12	14	15	15	15
	MMSE	n/c	n/c	15	14	27	28	30
Dyspnea	CAT	37	35	35		16	16	13
	mMRC Dyspnea Scale	4	4	4		3	3	1
Functional outcome	MBI	0	2	8	9	23	94	100
Sarcopenia	Hand grip strength (kg)	n/c	n/c	n/c	n/c	16		18.95
	MRC sum score	34	34	36	42	48	60	60
	BMI (kg/m2)			18.4			19.7	22.7
	SMI (kg/m2)			5.4			6.3	8.1
	Body fat percentage			27.5			23.1	16.8
	Alb (g/dL)			3.0	3.5	3.5	4.2
	Hb (g/dL)			8.5	9.7	10	12.8

HD: hospital day, FOIS: functional oral intake scale, VFSS: videofluoroscopic swallow study, PAS: Penetration-Aspiration Scale, VDS-O: Videofluoroscopic Dysphagia Scale-Oral phase, VDS-P: Videofluoroscopic Dysphagia Scale-Pharyngeal phase, ALFM: amount of lary-ngeal forward movement, ALUM: amount of laryngeal upward movement, RASS: Richmond Agitation-Sedation Scale, GCS: Glasgow Coma Scale, MMSE: Mini-Mental State Examination, CAT: COPD Assessment Test, mMRC: Modified Medical Research Council, MBI: modified Barthel index, BMI: body mass index, SMI: skeletal muscle mass index, Alb: albumin, Hb: hemoglobin..

His vitals stabilized; however, his functional status and muscle mass deteriorated, the severe dysphagia persisted and he required continued Levin tube feeding, and he could not maintain a seated position. He underwent a videofluoroscopic swallow study (VFSS) on HD36. For the evaluation of sarcopenic dysphagia, the Penetration-Aspiration Scale (PAS), Videofluoro-scopic Dysphagia Scale-Oral score, Videofluoroscopic Dysphagia Scale-Pharyngeal score, the amount of laryngeal forward movement (ALFM), the amount of laryngeal upward movement (ALUM), and the phary-ngeal constriction ratio were measured using Image J (National Institutes of Health, Bethesda, MD, USA). His VFSS result showed tracheal aspiration (PAS, 7) and incomplete pharyngeal constriction (pharyngeal constriction ratio, 0.11)¹².(Fig. 2A) The ALFM was 7 mm, the ALUM was 28 mm, and there was residue in the valleculae and pyriformis sinuses, indicating that sarcopenic dysphagia could be diagnosed on the VFSS¹³. At that time, his Medical Research Council (MRC) sum score was 36¹⁴, and skeletal muscle mass index using an Inbody S10 was 5.4 kg/m², which was below the cutoff value (<7.0 kg/m² in men) of sarco-penia according to Asian Working Group for Sarcopenia guideline. Brain magnetic resonance imaging was performed to determine the cause of the dysphagia, but no culpable lesion such as periventricular white matter hyperintensity was identified. There were no specific findings on brain imaging, and considering the findings of the MRC sum score and skeletal muscle mass index using an Inbody S10, the patient was diagnosed with sarcopenic dysphagia excluding dys-phagia caused by other causes. On HD40, he was transferred to the department of rehabilitation to improve the dysphagia, sarcopenia, and ADL.(Fig. 1) He received 30 min of dysphagia therapy, 30 min of physiotherapy, 15 min of training into ADL, 15 min of occupational therapy, and 30 min of respiratory therapy five times per week.

Figure 2. VFSS findings (A) on HD36 (B) on HD62.

On HD50, VFSS was performed again, and the semisolid fluid showed improvement with a PAS of 1; only the fluid showed aspiration with a PAS of 6. (Table 1) The ALFM was 9 mm, the ALUM was 41 mm, and there was no residue in the valleculae and pyri-formis sinuses, indicating that the sarcopenic dysphagia had improved. In addition, the MRC sum score im-proved from 34 to 42 and the systemic sarcopenia improved. He started oral feeding with an International Dysphagia Diet Standardisation Initiative (IDDSI) level 2 dysphagia diet and a fluid thickener (FOIS 4)^15,16. On HD62, VFSS follow-up showed normal findings on the fluid swallowing test.(Table 1, Fig. 2B) The diet form was changed from IDDSI level 2 to IDDSI level 4^15,16. Handgrip strength (HGS) is a commonly used metric to assess overall physical performance. On HD62, the HGS was measured and recorded as 16 kg. A jamar hand dynamometer was used for measuring HGS. Three consecutive measurements with 30 s of rest after each measurements were taken from the domi-nant hand¹⁷. On HD92, the IDDSI level 7 diet was started without a fluid thickener (FOIS, 7). The MRC sum score measured on HD62 improved to 48, and he became functionally capable of walking. The albu-min level improved from 3.0 g/dL to 3.5 g/dL.(Table 1) On HD115, he was discharged home ambulating independently without sarcopenic dysphagia, sarcopenia, or ADL restrictions (FOIS, 7; MRC sum score, 60; modified Barthel index, 100).

This case report describes a patient with awake ECMO due to severe COVID-19 who underwent early rehabilitation to improve sarcopenic dysphagia and physical impairment. Severe illness caused by COVID-19 induces sarcopenic dysphagia due to the virus itself and severe illness, causing malnutrition and creating a vicious cycle. In comparison to previous study, this case report has a difference in implemen-tation of early rehabilitation therapy during ECMO treatment, with real-time adjustments to the ECMO being made. This case report shows that early com-prehensive rehabilitation, including dysphagia rehabi-litation, is necessary to break the vicious cycle of sarcopenic dysphagia.

Owing to the infectivity of COVID-19, face-to-face rehabilitative treatment is difficult¹⁸. In particular, patients undergoing ECMO have been excluded from active rehabilitation programs due to the risk of ECMO line disconnection or vital instability. Therefore, COVID-19 patients who undergo vv-ECMO are at high risk of sarcopenia progression. Sarcopenia can cause dys-phagia, leading to malnutrition and other functional declines. Exclusion from rehabilitation programs for these reasons could exacerbate dysphagia.

While the World Health Organization still considers the pandemic active, some countries are transitioning their public health approach toward regarding severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) as an endemic virus. The coronavirus, previously known only as one cause of the common cold, caused SARS in 2002, followed by Middle East respiratory syndrome and COVID-19. It is possible that a new variant will cause a new infectious disease such as serious contagious pneumonia in humans in the future. Although the risk of COVID-19 is not as emphasized as before, the importance of early comprehensive rehabilitation for preventing sarcopenic dysphagia should be considered when it recurs in the future.

In conclusion, it is important to establish an accu-rate rehabilitation protocol and implement early reha-bilitation for the prevention and improvement of sarcopenic dysphagia in patients on awake ECMO with highly infectious respiratory diseases such as COVID-19.

This work was supported by grant from Ewha Womans University Medical Center.

None of the authors has any conflict of interest to disclose. The named authors have no conflict of interest, financial benefits or otherwise.