Thoracic ultrasonographic and clinical findings at 12-month follow-up of patients admitted with COVID-19

Figures & data

Figure 1. TUS findings and corresponding score. a) The pleural line (PL) appears normal. No B-lines or consolidations are present corresponding to a score of 1. b) Multiple B-lines (B) originating from the pleural line. The B-lines involve less than 50% of the pleural line, corresponding to a score of 2. c) Multiple confluent B-lines (CB) are present. More than 50% of the pleural line is involved corresponding to a score of 3. d) A small subpleural consolidation (C) is present just below the pleural line, corresponding to a score of 4. Image courtesy of Falster et al. [11].

Table 1. Baseline characteristics of patients stratified by follow-up attendance.

	N	Patients attending follow-up (n=40)	N	Patients not attending follow-up (n=52)	P-value
Baseline characteristics
Age, years ± SD	40	6.4 ± 13.6	52	64.5 ± 17.2	0.11
Male sex, n (%)	40	26 (65)	52	32 (62)	0.73
BMI (kg/m^2) (IQR)	40	27.9 (25.1–31.3)	49	26.4 (23.3–29.9)	0.16
Excessive alcohol consumption, n (%)*	40	2 (5)	51	3 (6)	0.84
Current use of tobacco, (%)	40	0 (0)	52	6 (12)	0.019
Previous use of tobacco, (%)	40	17 (43)	44	21 (48)	0.63
Performance status (IQR)	40	0 (0–0)	52	0 (0–1.5)	0.033
Comorbidities
Hypercholesterolemia	40	8 (20)	52	10 (19)	0.93
Hypertension	40	20 (50)	52	16 (31)	0.002
Ischemic heart disease, n (%)	40	2 (5)	52	7 (13)	0.18
Supraventricular arrhythmia, n (%)	40	3 (8)	52	10 (20)	0.11
Heart valve disease, n (%)	40	1 (3)	52	6 (12)	0.11
Heart failure	40	2 (5)	52	4 (8)	0.60
Asthma	40	3 (8)	52	7 (13)	0.36
COPD	40	2 (5)	52	6 (12)	0.27
Other pulmonary disorders^€	40	4 (10)	52	3 (6)	0.45
Type I diabetes	40	1 (3)	52	1 (2)	0.85
Type II diabetes	40	2 (5)	52	10 (20)	0.046
Other endocrinological disorders^¥	40	6 (15)	52	11 (21)	0.45
Malignancy	40	7 (18)	52	7 (13)	0.56
Vital parameters at admission
Respiratory rate, breaths/min ± SD	40	21 ± 4	52	22 ± 6	0.16
Heart rate, beats/min ± SD	40	88 ± 19	52	92 ± 23	0.18
Systolic blood pressure, mmHg ± SD	40	134 ± 20	52	132 ± 22	0.40
Diastolic blood pressure, mmHg ± SD	40	79 ± 12	52	77 ± 12	0.20
Temperature, C^o ± SD	40	38.5 ± 1.1	52	38.2 ± .8	0.07
Oxygen saturation, % ± SD	40	95.8 ± 2.4	52	94.9 ± 4.1	0.14
Oxygen therapy, n (%)	40	11 (28)	52	16 (31)	0.73
Level of oxygen therapy, L/min (IQR)	11	3 (1.5–3)	16	1 (1–2)	NA
Hospitalization
Length of hospital stay, days (IQR)	40	7 (3–13)	47	7 (4–14)	0.43
Transfer to ICU, n (%)	40	7 (18)	52	7 (13)	0.59
Pulmonary embolism, n (%)	40	1 (3)	52	2 (4)	0.72

*>14 weekly units of alcohol for men and 7 for women. ^€Other pulmonary disorders encompass lung fibrosis and lung sarcoidosis. ^¥Other endocrinological disorders encompass osteoporosis, myxedema and Addison’s disease.

Table 2. Baseline characteristics of included patients stratified by ARDS during admission.

	N	Patients with ARDS during hospitalization (n=13)	Patients without ARDS during hospitalization (n=27)	P-value
Baseline characteristics
Age, years ± SD	40	61.6 ± 14.0	59.8 ± 13.6	0.35
Male sex, n (%)	40	10 (77)	16 (59)	0.27
BMI (kg/m^2) (IQR)	40	29.9 (26.1–38.9)	27.7 (24.5–3.1)	0.047
Excessive alcohol consumption, n (%)*	40	0 (0)	2 (7)	1.0
Current use of tobacco, (%)	40	0 (0)	0 (0)	1.0
Previous use of tobacco, (%)	40	4 (31)	13 (48)	0.30
Performance status (IQR)	40	0 (0–1)	0 (0–0)	0.19
Comorbidities
Hypercholesterolemia	40	5 (38)	3 (11)	0.043
Hypertension	40	8 (62)	12 (44)	0.31
Ischemic heart disease, n (%)	40	1 (8)	1 (4)	0.59
Supraventricular arrhythmia, n (%)	40	1 (8)	2 (7)	0.97
Heart valve disease, n (%)	40	0 (0)	1 (4)	1.0
Heart failure	40	1 (8)	1 (4)	0.59
Asthma	40	0 (0)	3 (11)	0.54
COPD	40	1 (8)	1 (4)	0.59
Other pulmonary disorders^€	40	1 (8)	3 (11)	0.74
Type I diabetes	40	1 (8)	0 (0)	1.0
Type II diabetes	40	2 (15)	0 (0)	0.1
Other endocrinological disorders^¥	40	2 (15)	4 (15)	0.96
Malignancy	40	2 (15)	5 (19)	0.81
Vital parameters at admission
Respiratory rate, breaths/min ± SD	40	22 ± 4	21 ± 4	0.18
Heart rate, beats/min ± SD	40	88 ± 18	88 ± 20	0.48
Systolic blood pressure, mmHg ± SD	40	134 ± 17	134 ± 22	0.47
Diastolic blood pressure, mmHg ± SD	40	77 ± 13	81 ± 12	0.17
Temperature, C^o ± SD	40	38.8 ± 1.1	38.4 ± 1.1	0.15
Oxygen saturation, % ± SD	40	94.6 ± 2.8	96.3 ± 2.0	0.016
Oxygen therapy, n (%)	40	7 (54)	4 (15)	0.01
Level of oxygen therapy, L/min (IQR)	11	3 (2–3)	1.8 (1.3–2.5)	NA
Hospitalization
Length of hospital stay, days (IQR)	40	15 (9–31)	4 (3–8)	<0.001
Transfer to ICU, n (%)	40	7 (54)	0 (0)	<0.001
Pulmonary embolism, n (%)	40	0 (0)	1 (4)	1.0

*>14 weekly units of alcohol for men and 7 for women. ^€Other pulmonary disorders encompass lung fibrosis and lung sarcoidosis. ^¥Other endocrinological disorders encompass osteoporosis, myxedema and Addison’s disease.

Table 3. Outcomes of included patients stratified by ARDS during admission.

	N	All included patients (n=40)	Patients with ARDS during hospitalization (n=13)	Patients without ARDS during hospitalization (n=27)	P-value
Baseline characteristics at follow-up
Days between discharge and TUS ± SD	40	393 ± 18	387 ± 18	396 ± 17	0.06
Dyspnea, n (%)	40	10 (25)	3 (23)	7 (26)	0.85
Cough, n (%)	40	5 (13)	0 (0)	5 (19)	0.15
Chest pain, n (%)	40	0 (0)	0 (0)	0 (0)	1.0
Cerebral complaints, n (%)*	40	18 (45)	9 (69)	9 (33)	0.033
Gastrointestinal complaints, n (%)^€	40	3 (8)	1 (8)	2 (8)	0.97
Musculoskeletal complaints, n (%)^¥	40	5 (13)	2 (15)	3 (11)	0.70
Rash, n (%)	40	1 (3)	1 (8)	0 (0)	0.33
Weight gain, n (%)	40	15 (38)	5 (38)	10 (37)	0.93
Weight loss, n (%)	40	7 (18)	2 (15)	5 (19)	0.81
TUS findings
Total B-lines (Mongodi protocol) (IQR)	40	0 (0–1)	1 (0–6)	0 (0–0)	0.008
Total B-lines (Complete TUS) (IQR)	40	0 (0–1)	1 (0–7)	0 (0–1)	0.016
Score (Mongodi protocol) (IQR)	40	8 (8–8)	8 (8–10)	8 (8–8)	0.08
Score (Complete TUS) (IQR)	40	14 (14–14)	14 (14–17)	14 (14–14)	0.08
Subpleural consolidation (%)	40	4 (10)	2 (15)	2 (7)	0.43
Pleural effusion (%)	40	1 (3)	1 (8)	0 (0)	0.33
Shearwave elastography (IQR)	38	2.23 (1.765–2.755)	2.03 (1.625–2.59)	2.34 (1.875–2.835)	0.024
Spirometry
FEV1, L ± SD	40	3.1 ± 0.76	3.1 ± 0.52	3.11 ± 0.86	0.46
FEV1% of predicted) ± SD	40	101 ± 18	99 ± 14	102 ± 19	0.32
FVC, L ± SD	40	4.1 ± 1.07	4.1 ± 0.7	4.2 ± 1.21	0.43
FVC (% of predicted) ± SD	40	108 ± 18	104 ± 15	109 ± 19	0.18
FEV1/FVC ± SD	40	75.9 ± 6.34	75.6 ± 3.22	76.0 ± 7.45	0.42
DLCO-SB (% of predicted) ± SD	39	86 ± 18	85 ± 16	87 ± 19	0.40
DLCOc (% of predicted) ± SD	39	85 ± 17	83 ± 15	85 ± 19	0.36
6-min walk test
Distance, meters ± SD	38	518 ± 105	479 ± 93	538 ± 107	0.05
Oxygen saturation prior, % (IQR)	38	98 (96–98)	97 (96–98)	98 (96–98)	0.26
Oxygen saturation after, % (IQR)	38	96 (94–97)	95 (93.5–96)	96 (95–97.5)	0.05
Borg scale prior	38	0.5 (0–1)	0.5 (0–1)	0.5 (0–1)	0.90
Borg scale after	38	3 (1–4)	3 (0.75–5)	3 (1–4)	0.87
Sequelae
Interstitial lung sequelae	40	1	1	0	0.325
COPD/emphysematous sequelae	40	0	0	0	1.0
Asthmatic sequelae	40	3	1	2	0.54
Combined sequelae	40	0	0	0	1.0
Unspecific airway sequelae	40	2	2	0	0.1
Other	40	2	1	1	0.82

*Sensation of fatigue, irritability, depressive symptoms, increased need for sleep, anosmia. ^€Abdominal pain or bloating, changes in passage of stool, nausea. ^¥Feeling of muscular weakness or pain. FEV1: forced expiratory volume in 1 sec. FVC: forced vital capacity. DLCOc: diffusion capacity of the lung for carbon monoxide adjusted for hemoglobin. COPD: chronic obstructive pulmonary disorder.

Figure 2. Comparison of pulmonary function test results between patients with and without abnormal thoracic ultrasound findings.FEV1: Forced expiratory volume in 1 second. FVC: Forced vital capacity. DLCOc: diffusion capacity of the lung for carbon monoxide adjusted for hemoglobin. 6MWT: 6-minute walking distance.

Table 4. Correlations between thoracic ultrasound findings and pulmonary function tests.

Clinical variable for evaluation of correlation	N	r-coefficient
Total B-lines (Complete TUS)
FEV1, % of predicted	40	−0.133
FVC, % of predicted	40	−0.268
FEV1/FVC	40	0.025
DLCOc, % of predicted	39	−0.385
6-min walk test distance	38	−0.360
Oxygen saturation post exercise	38	−0.310
Borg scale post exercise	38	0.314
Mongodi score (Complete TUS)
FEV1, % of predicted	40	−0.092
FVC, % of predicted	40	−0.229
FEV1/FVC	40	0.021
DLCOc, % of predicted	39	−0.364
6-min walk test distance	38	−0.422
Oxygen saturation post exercise	38	−0.269
Borg scale post exercise	38	0.368

R = 0.00–0.10: negligible correlation. R = 0.10–0.39: weak correlation. R = 0.40–0.69: moderate correlation. R = 0.70–0.89 = strong correlation. R = 0.90–1.00: very strong correlation. FEV1: forced expiratory volume in 1 sec. FVC: forced vital capacity. DLCOc: diffusion capacity of the lung for carbon monoxide adjusted for hemoglobin.

Falster C, Jacobsen N, Wulff Madsen L, et al. Lung ultrasound may be a valuable aid in decision making for patients admitted with COVID-19 disease. Eur Clin Respir J. 2021;8(1): Taylor and Francis Ltd. doi: 10.1080/20018525.2021.1909521

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