Different from previous pneumonia transmissions caused by influenza virus [3,10,12], COVID–19 is characterized by rapid transmission, high infection rate and high lethality. In addition to chest X-ray and CT scan, ultrasound can also be used for the diagnosis and treatment. It has been confirmed that COVID–19 can be transmitted by droplets and direct contact; therefore, ultrasonic device has advantages over CT and DR in disinfection and smaller area of contact with patients. In particular, 9–15 MHz high-frequency linear array probe can clearly display the morphology and changes of subpleural lesions, and the changes of air and water contents in consolidated peripulmonary tissues [6.13]. It has been reported that 3–17 MHz high-frequency linear array probe can show air bronchogram sign in unconsolidated lung tissues caused by intra-pulmonary hemorrhage , which is of great significance for the close observation of peripulmonary lesions. Color flow Doppler technique can show the blood supply and lesion progression in peripulmonary consolidation, which has special clinical significance . Therefore, ultrasound is playing an indispensable role in the diagnosis, treatment and efficacy evaluation of severe acute pneumonia [7,16].
Since few studies investigated the ultrasonic manifestations of non-critical COVID–19 [2.3.9–12], this study focuses on the ultrasonic manifestations and characteristics and their relationship with CT images. Currently, ultrasound is largely limited in the diagnosis and treatment of central lung diseases and bone-occlusion lung diseases due to the attenuation of sound waves by normal lung and bone tissues. Therefore, lung ultrasound relies on the artifacts of peripulmonary lesions to make the diagnosis [17,18], while the artifacts occur because of the abnormal sound wave reflection caused by changes in the ratio of air and water contents in alveoli and interstitial tissues due to peripulmonary lesions. Based on this speculation, this study used abdominal convex array ultrasound combined with 3–17 MHz high frequency linear array probe to observe the pulmonary lesions and artifacts. The authors believed that B lines emerged mainly because in the COVID–19 cases enrolled, most of the lesions were observed under the peripulmonary pleura, which resulted in the thickening and edema of interstitial tissues, reduced air content in alveoli, and artifacts caused by ultrasonic ringing effects.
Ultrasound images showed that the subpleural lesions in the course of non-critical COVID–19 were significantly different from other lesions reported in literature [8,17], such as bacterial pneumonia, pulmonary abscess, tuberculosis, compression and obstructive atelectasis, pneumothorax, benign and malignant tumors, and so on. Lung ultrasound revealed the following radiographic features of non-critical COVID–19:
Lesions were mostly located in the posterior fields of both lungs. Multiple discontinuous or continuous fused B lines (waterfall sign) under the pleural line were visible as shown in Figure 2, or diffused B lines (white lung sign), and the A lines disappeared as shown in Figure 4. Compared with the B lines caused by cardiogenic pulmonary edema, the B lines here were more likely to be fused and fixed. The B lines had blurred edges and no bifurcation signs. The origination point of the subpleural lesion was more obtuse (convex array probe) compared with that of B lines of pulmonary edema, as shown in Figure 6.
High frequency ultrasound showed that the pleural line was unsmooth and rough, as shown in Figure 8 and 10, and interrupted as shown in Figure 12, mainly due to the decreased gas content and sound wave reflection in the subpleural alveoli and interstitial lesions.
Multiple small patchy consolidations were observed in the subpleural lesion, as shown in Figure 13, and strip consolidation was shown in Figure 16.
The echogenicity in the lesions was homogeneous or inhomogeneous, and air bronchiologram sign was visible (mostly early and progressive stages as shown in Figure 19, because secondary pulmonary lobules were involved by interstitial inflammation, the interstitial tissues were thickened and swollen, some bronchioles and alveoli were not involved by high gas content) or air bronchogram sign (visible in severe cases or local consolidation, possibly because local inflammation storm caused the consolidation and edema of most bronchioles and alveoli, and only large bronchi and part of the alveoli were not involved, as shown in Figure 20, 21, 22), diffuse B lines. Some patients had long onset and the symptoms improved, then CT images showed nodule consolidation, and ultrasound showed irregular nodule subpleural echo shadow, with fused B lines in fixed position, as shown in Figure 23.
High frequency ultrasound also showed the localized pleural thickening and local pleural effusion around the subpleural lesion. Linear array probe clearly showed that most patients’ pleural thickening was about 1–2mm, and the subpleural effusion was about 2–3mm, which changed with the progress of disease, as shown in Figure 24.
CDFI ultrasound showed insensitivity of blood flow signals in subpleural consolidation as shown in Figure 13 and 25. Although ultrasonic devices of different brands were used, the signal of blood flow was still poor, possibly due to the pathological nature and progression of lesions. Great attention should be paid to this, because pulmonary consolidation caused by common inflammation generally shows abundant blood flow signals and the prognosis is good, but COVID–19 progresses rapidly and may cause death. Whether lung tissues are unable to quickly establish microvessel exchange mechanism has yet to be further studied, but color Doppler ultrasound, compared with other medical equipment, can more effectively detect the blood supply in consolidation, and therefore is more useful for clinicians to prejudge the prognosis and process of the disease.
Comparing CT images and ultrasound images of patients with non-critical COVID–19, we can find that the two types of images were highly consistent, but CT showed more clear and complete intrapulmonary and apical lesions than ultrasound. Meanwhile, ground glass opacity, nodule shadow, consolidation shadow and air bronchogram sign all had special manifestations in ultrasonic images as shown in Figure 1, 3, 5, 7, 9, 11, 14, 15, 17, 18, 20 and 21. However, CT is inferior to ultrasound in showing the smaller peripulmonary lesions and pleural and peripulmonary effusion. On the other hand, ultrasound can produce real-time and dynamic images, and is therefore more advantageous in distinguishing interstitial lesions and showing the distribution of blood flow and angiogenesis in inflammatory lesions.
In summary, the COVID–19 foci are mainly observed in the posterior fields in both lungs, especially the posterior and inferior fields. Fused B lines and waterfall signs are visible. The pleural line is unsmooth, discontinuous or interrupted. The subpleural lesions show patchy, strip, and nodule consolidation, in which air bronchogram sign or air bronchiologram sign can be seen. The involved interstitial tissues show obvious thickening and edema, the pleura shows localized thickening, and there is localized pleural effusion around the lesions. CDFI ultrasound shows insufficient blood supply in the lesions. High frequency linear array probe is suggested to be used for minor subpleural lesions, for it can provide rich information and improve the diagnostic accuracy. Our study indicated that ultrasound can show typical manifestations and has advantages over CT in the clinical diagnosis and treatment of non-critical COVID–19, but it cannot replace CT. Ultrasound can be used as a supplementary method. This study has some limitations: the sample size is small, the changes of ultrasonic images are not carefully examined, and no control studies are conducted. Further large sample studies remain to be conducted.