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Cardiovascular Ultrasound
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* Published: 19 January 2022

PILOT STUDY ON THE VALUE OF ECHOCARDIOGRAPHY COMBINED WITH LUNG ULTRASOUND TO
EVALUATE COVID-19 PNEUMONIA

* Jing Han1 na1,
* Xi Yang2 na1,
* Wei Xu3,
* Ronghua Jin4,
* Weiyuan Liu1,
* Lei Ding1,
* Sha Meng5,
* Yuan Zhang1,
* Jin Li6,
* Ying Zheng1,
* …
* Haowen Li7 &
* Fankun Meng1

Show authors

Cardiovascular Ultrasound volume 20, Article number: 2 (2022) Cite this article

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ABSTRACT

BACKGROUND

This study aimed to investigate the relationship between echocardiography
results and lung ultrasound score (LUS) in coronavirus disease 2019 (COVID-19)
pneumonia patients and evaluate the impact of the combined application of these
techniques in the evaluation of COVID-19 pneumonia.

METHODS

Hospitalized COVID-19 pneumonia patients who underwent daily lung ultrasound and
echocardiography were included in this study. Patients with tricuspid
regurgitation within three days of admission were enrolled. Moreover, the
correlation and differences between their pulmonary artery pressure (PAP) and
LUS on days 3, 8, and 13 were analyzed. The inner diameter of the pulmonary
artery root as well as the size of the atria and ventricles were also
considered.

RESULTS

The PAP on days 3, 8, and 13 of hospitalization was positively correlated with
the LUS (r = 0.448, p = 0.003; r = 0.738, p < 0.001; r = 0.325, p = 0.036,
respectively). On day 8, the values of both PAP and LUS were higher than on days
3 and 13 (p < 0.01). Similarly, PAP and LUS were significantly increased in
92.9% (39/42) and 90.5% (38/42) of patients, respectively, and at least one of
these two values was positive in 97.6% (41/42) of cases. The inner diameters of
the right atrium, right ventricle, and pulmonary artery also differed
significantly from their corresponding values on days 3 and 13 (p < 0.05).

CONCLUSIONS

PAP is positively correlated with LUS in COVID-19 pneumonia. The two values
could be combined for a more precise assessment of disease progression and
recovery status.

Peer Review reports

BACKGROUND

On February 11, 2020, the World Health Organization (WHO) declared the emergence
of coronavirus disease 2019 (COVID-19) caused by severe acute respiratory
syndrome (SARS) coronavirus-2 in Wuhan, Hubei, China [1]. With the rapid
worldwide spread of COVID-19 [2, 3], real-time reverse-transcriptase polymerase
chain reaction (RT-PCR) and high-resolution chest computed tomography (CT) have
become progressively insufficient to meet diagnostic demands. Several countries
and regions have gradually adopted ultrasonography as the basic examination
method [4,5,6], especially Italy [7]; hence, improvements in the ultrasound
diagnostic value for COVID-19 pneumonia are required. At present, some reports
in the literature [8, 9] describe the combination of pulmonary and cardiac
ultrasound to evaluate patients with COVID-19 pneumonia. However, the
correlation between pulmonary arterial pressure and lung ultrasound score (LUS)
has not been investigated in detail. If these two values are related, the
results of one of these investigations may reflect the results of the other,
thereby reducing the burden of work in a specific environment. The present study
aimed to examine the correlations between these values for the progression
evaluation and treatment monitoring of patients with COVID-19 pneumonia.

METHODS

STUDY DESIGN

This study was supported by the Ministry of Science and Technology of the
People’s Republic of China (grant number: 2020YFC0844900). The study was
approved by the Ethics Committee of Beijing You An Hospital, affiliated with the
Capital Medical University ([2020]020). Informed consent was obtained from all
patients included in the study. In accordance with the WHO guidelines for
COVID-19 spread prevention, our hospital’s infection prevention and control
procedures were strictly implemented, ensuring that none of the health workers
involved in the study were infected with the disease.

The present study included hospitalized COVID-19 pneumonia patients (with
diagnosis confirmed by RT-PCR and CT) who underwent dynamic lung ultrasound and
echocardiographic observation upon hospital admission. The combined use of the
two modalities for evaluating lung lesions was assessed, and the correlations
between the data provided were calculated.

A total of 138 patients with COVID-19 pneumonia were treated at our hospital.
According to the Chinese government policy, these patients must be hospitalized
for observation and treatment upon diagnosis confirmation; therefore, the
hospitalization rate of patients with COVID-19 pneumonia is 100%. Among this
group, we selected patients with tricuspid valve regurgitation. Since the
proportion of patients with this disorder increased by the third day of
hospitalization, we included patients with evident tricuspid regurgitation
within 3 days of admission (42 cases). Afterward, LUS assessment and
echocardiographic examinations were conducted daily. Other studies, including
our previous research, suggest that the interval between the appearance of
symptoms and the most severe stage of the disease is approximately 10 days [10,
11], and hospitalization is required approximately 2 days after the onset of the
first symptoms. The mean hospital stay duration was 15 days. Accordingly, days
3, 8, and 13 were selected to compare LUS, pulmonary arterial pressures, and
atrial and ventricular diameters. General symptoms, including fever, cough, and
dyspnea, were recorded, as well as the history of underlying heart and lung
disease. The sample size of this study was determined using R [R Core Team
(2019), Version 3.6.1] with RStudio (Version 1.2.5019) and Pwr Package prior to
commencing the experiment with a view of obtaining a power of 80%. Calculation
was based on the lines of Cohen (1988) using in particular the same notations
for effect sizes [12]. The estimated sample size needed to reach 80% power on
the 0.05 significance level (two-sided test) with a correlation coefficient (r)
smaller than 0.5, leaded to a sample size of 28 cases.

LUNG ULTRASOUND

Rouby [13] proposed to divide one lung into six zones each for examination. In
the present study, the lungs were both divided into three areas, with the
anterior and posterior axillary lines as the boundaries: anterior, middle, and
posterior (Fig. 1). Each area was further divided into superior and inferior
regions. The results were recorded as the following four basic types (Fig. 2):
type N: ≤ 2 separated B-lines, indicating good lung inflation; type B1: multiple
B-lines, separated by approximately 7 mm (B7 lines); type B2: multiple B-lines,
separated by ≤3 mm (B3 lines); and type C: hepatization or fragmentation, with
dynamic bronchial inflation sign, and with or without pleural effusion,
indicating lung consolidation. The LUS was based on the above four types: N = 0,
B1 = 1, B2 = 2, and C = 3. In each region, the most severe sign was considered
the final score. All patients underwent lung ultrasonographic examination, and
the sum of the scores of the 12 regions was recorded. All lung ultrasound scans
were performed by two experienced sonologists.

Fig. 1

Correlation between LUS and pulmonary arterial pressure in 42 patients with
COVID-19 pneumonia: (a) day 3; (b) day 8; (c) day 13

Full size image
Fig. 2

Parameters of a 60-year-old male patient with pulmonary hypertension, presenting
with tricuspid regurgitation on color Doppler echocardiography. The systolic
pulmonary artery pressure was estimated on days 3 (a), 8 (b), and 13 (c), using
the gradient of tricuspid regurgitation pressure. The patient remained on
extracorporeal membrane oxygenation support and exhibited low fever with stable
heart rate and breathing

Full size image

ECHOCARDIOGRAPHY

All the patients underwent echocardiographic examinations daily. Routine
parasternal, apical, and other cardiac section scans were performed. The
European Society of Cardiology (ESC) and the European Respiratory Society (ERS)
indicated the guidelines for diagnosing pulmonary hypertension (PH). The
screening criteria for PH are mainly based on the tricuspid regurgitation peak
velocity and systolic pulmonary artery pressure [14, 15]. Left atrial volume
(LAV), left ventricular volume, and right atrial volume (RAV) were estimated
using the disk summation algorithm (Simpson’s technique) following a biplanar
approach from the four apical chambers [16, 17]. The pulmonary artery (PA) root
diameter, right ventricular base diameter, and right ventricular internal
dimension were recorded.

STATISTICAL ANALYSIS

The sample size (42 > 28cases) was deemed sufficient for this study. Continuous
data were expressed as mean ± standard deviation. Non-parametric tests were used
to assess non-normally distributed data. The Mann–Whitney U test was used to
compare two independent samples, and the Kruskal–Wallis test for multiple
independent samples. Pearson’s correlational analysis was performed to assess
the correlations between LUS and pulmonary artery pressure. The analysis of
variance was used to analyze the differential distribution of data between more
than two groups (LAV), with subsequent post hoc correction for multiple
comparisons. A p-value < 0.05 was deemed statistically significant. The
statistical software SPSS 26.0 (IBM, Armonk, NY, USA) was used for data
analysis.

RESULTS

A total of 42 patients were included in the cohort (24 males and 18 females),
with a mean age of 47.8 ± 10.8 years. Extracorporeal membrane oxygenation
support was provided in one case, ventilator support in three, and oxygen masks
in nine. None of the participants had a history of heart disease or chronic
respiratory disease. The patients’ demographic characteristics, clinical
features, and relevant medical history are shown in Table 1.

Table 1 Demographic characteristics, clinical features, and relevant medical
history of the patients (n = 42)
Full size table

LUS and pulmonary arterial pressure in all patients changed significantly as the
disease progressed. The two parameters were positively correlated within three
days of admission, and the correlation was stronger in patients with more severe
disease (on days 3, 8, and 13: r = 0.448, p = 0.003; r = 0.738, p < 0.001;
r = 0.325, p = 0.036, respectively; Fig. 1).

The LUS directly reflects the degree of lung disease, whereas the pulmonary
arterial pressure is an indirect indicator. Increased pulmonary arterial
pressure can directly cause dilation of the pulmonary artery trunk, with
consequent enlargement of the right ventricle and right atrium, leading to the
exacerbation of tricuspid regurgitation. One case of this occurrence is shown in
Fig. 2, illustrating the relationship between pulmonary artery changes and
tricuspid regurgitation on days 3, 8, and 13. There were significant differences
in the LUS between the 3 days considered. Differences in the inner diameters of
the atria, ventricles, and pulmonary artery are shown in Tables 2 and 3.

Table 2 Overall differences in LUS, pulmonary arterial pressure, and atrial
diameter on days 3, 8, and 13
Full size table
Table 3 Differences in LUS, pulmonary artery pressure, and atrial diameter on
days 3, 8, and 13
Full size table

All patients exhibited an overall increase in both pulmonary arterial pressure
and LUS on day 8; however, at that point in time there were four patients
without any significant increase in the pulmonary arterial pressure and three
without any significant increase in LUS. Comparisons of CT findings on day 8
revealed increased severity compared to day 3 in six patients, suggesting that
these six patients were false negatives. In one (1/7) patient there was no
substantial difference between the CT findings acquired on day 3 and those
acquired on day 8, indicating a negative result in this case. There were
41/42(97.6%) cases in which the two in combination were positive (Table 4).

Table 4 Positivity rates of LUS and pulmonary arterial pressure values,
considered alone or in combination
Full size table

DISCUSSION

In the present study, the LUS was positively correlated with pulmonary arterial
pressure, with the correlation becoming stronger as the disease severity
worsens. Increased pulmonary arterial pressure may be caused by several
pathologies [15, 18, 19]. Patients with a history of underlying cardiopulmonary
disease were excluded from the present study; the changes observed in the
pulmonary arterial pressure were assumed to be related to the current lung
disease. During lung inflammation, inflammatory infiltration and alveolar
exudate reduce the alveolar surface area available for diffusion, thereby
prolonging the diffusion time. Hypoxic acidosis may cause pulmonary endothelial
edema and vasospasm, leading to PH [15, 20].

COVID-19 pneumonia and the 2003 SARS outbreaks were both caused by members of
the coronavirus family. Angiotensin-converting enzyme-2 is a component of the
renin-angiotensin system that protects blood vessels and possibly a functional
receptor for coronaviruses on epithelial cells [21,22,23]. Another component of
the renin-angiotensin system is angiotensin II, which causes inflammation and
damage of the alveolar epithelium. The lung alterations associated with COVID-19
may be due to the upregulation of angiotensin II and reduced
angiotensin-converting enzyme-2 levels, resulting in increased pulmonary
vasoconstriction. The results of the present study suggest that these factors
may be associated with higher LUSs and higher pulmonary arterial pressure.

The assessment of pulmonary artery pressure can be performed using several
methodologies. Right heart catheterization is an advanced and reliable method
for this task; however, it is performed only in specific cases due to its
invasive nature [16, 24]. Abbas et al. developed an algorithm to calculate the
PVR of patients with pre occipital PH; however, this method may lead to
false-positive results [25]. The most commonly used method in clinical practice
is the calculation of maximum pulmonary systolic pressure [17, 26, 27] using the
tricuspid regurgitation velocity [28]. This method has been widely used and is
based on the clear guidelines of the ESC and ERS. Therefore, we opted to use
these guidelines to evaluate the pulmonary artery pressure in our study;
however, this method requires good image quality and sufficient Doppler signal.
These characteristics may not always be present, though all the images of the
patients selected for the study met the requirements.

Several studies [15,16,17,18,19] investigated pulmonary arterial hypertension
caused by pneumonia; however, there are no reports on the use of pulmonary
arterial pressure to predict the LUS. In the present study, the LUS was
dynamically evaluated, and echocardiography was performed simultaneously. The
LUS was positively correlated with disease severity. Echocardiography indicated
that the amount of tricuspid regurgitation increased with aggravating disease
conditions; the pulmonary arterial pressure and the inner diameters and volumes
of the pulmonary artery, right ventricle, and right atrium also increased. All
these parameters exhibited statistically significant changes during disease
progression, and all of them decreased with improving conditions (Tables 2 and
3). These results suggest that changes in LUS and pulmonary arterial pressure
can reflect the severity of lung lesions.

Hemodynamic principles indicate that increased pulmonary arterial pressure leads
to increased right ventricular ejection resistance and, consequently, increased
inner diameters of the right atrium, right ventricle, and pulmonary artery.
Dynamic echocardiography can be used to monitor changes in pulmonary arterial
pressure and the size of each heart chamber in real time; therefore, the disease
progression can be assessed efficiently. The positive correlation between
pulmonary arterial pressure and LUS in the current study also indicates a
tendency for LUS. There were no significant changes in left heart size during
the entire course of the disease, indicating a low probability of left heart
involvement, consistent with previous studies.

In the present study, the positivity rate for increased pulmonary arterial
pressure on day 8 was 92.9%. Three patients (7.1%) had stable pulmonary arterial
pressure, possibly indicating compensation by the pulmonary blood vessels [13,
20]. The positivity rate for LUS increase on day 8 was 90.5%, though the scores
of four patients (9.5%) did not increase with aggravating disease conditions. In
conjunction with CT findings, this result suggests that the regions of lesion
exacerbation in these cases were located in the innermost pulmonary areas,
beyond ultrasound detection range, which are consistent with the principles of
lung ultrasound. The positivity rate for the two parameters combined was 97.6%,
improving the accuracy of disease progression evaluation. Currently, no reports
have examined this aspect.

The current study had some limitations. Some patients required oxygen therapy
for dyspnea; compared with patients who did not require such, the estimation of
pulmonary arterial pressure may be biased. Moreover, since the frequency of CT
examinations was lower than that of ultrasound, not all patients have
corresponding CT data at the three time-points considered, causing a lack of
basis for comparison. However, the corresponding CT data were available for the
seven negative patients for either parameter, providing a reliable reference for
diagnosis. Some previous studies [8, 9] describe the use of LUS and
echocardiography in patients with COVID-19 pneumonia. On the other hand, cardiac
reports [9] focus on intensive care unit (ICU) patients, while most of the
patients we evaluated were non-ICU patients. Our comprehensive pulmonary
evaluation (bilateral LUS) may reflect the disease progression more accurately,
as the change in pulmonary hemodynamics in patients with COVID-19 pneumonia is
evident. Moreover, we found the modification in pulmonary arterial pressure to
be a sensitive indicator at the early stage of the disease. In patients on
ventilator support, when it is challenging to obtain double lung scoring, the
pulmonary arterial pressure can be measured to assess the severity of lung
disease. This knowledge may help clinicians in the management of patients with
severe disease.

CONCLUSIONS

In COVID-19 pneumonia patients, the pulmonary arterial pressure and LUS are
positively correlated. For those who are unable to be transferred or relocated,
the pulmonary arterial pressure may be measured to reflect the degree of lung
lesions indirectly. Combining these two parameters could improve the accuracy of
lung disease progression assessment, providing an important guiding role for
treatment decisions.

AVAILABILITY OF DATA AND MATERIALS

The datasets generated and/or analysed during the current study are not publicly
available due [REASON WHY DATA ARE NOT PUBLIC] but are available from the
corresponding author on reasonable request.

ABBREVIATIONS

COVID-19:

Coronavirus disease 2019

CT:

Computed tomography

LUS:

Lung ultrasound score

RT-PCR:

Reverse transcriptase polymerase chain reaction

REFERENCES

1. 1.

WH O. WHO director-General's remarks at the media briefing on 2019-nCoV on
11 Feb 2020. 2020.

2. 2.

Han Y, Yang H. The transmission and diagnosis of 2019 novel coronavirus
infection disease (COVID-19): a Chinese perspective. J Med Virol.
2020;92(6):639–44.

CAS Article Google Scholar

3. 3.

World Health Organization. COVID-19 weekly epidemiological update 14
January. 2022. https://covid19.who.in.

4. 4.

Soldati G, Smargiassi A, Inchingolo R, Buonsenso D, Perrone T, Briganti DF,
et al. Proposal for international standardization of the use of lung
ultrasound for patients with COVID-19 a simple, quantitative. Reproducible
Method J Ultras Med. 2020;39(7):1413–9.

Google Scholar

5. 5.

Soldati G, Smargiassi A, Inchingolo R, Buonsenso D, Perrone T, Briganti DF,
et al. Is there a role for lung ultrasound during the COVID-19 pandemic? J
Ultras Med. 2020;39(7):1459–62.

Article Google Scholar

6. 6.

Kalafat E, Yaprak E, Cinar G, Varli B, Ozisik S, Uzun C, et al. Lung
ultrasound and computed tomographic findings in pregnant woman with
COVID-19. Ultrasound Obst Gyn. 2020;55(6):835–7.

CAS Article Google Scholar

7. 7.

Vetrugno L, Bove T, Orso D, Barbariol F, Bassi F, Boero E, et al. Our
Italian experience using lung ultrasound for identification, grading and
serial follow-up of severity of lung involvement for management of patients
with COVID-19. Echocardiogr-J Card. 2020;37:625–7.

Article Google Scholar

8. 8.

Edgar GC, Daniel MS, Rafael RS, Rodrigo GN, Ricardo LBC, Antonio JR, et al.
Critical care ultrasonography during COVID-19 pandemic: the ORACLE
protocol. Echocardiography. 2020;37(9):1353–61.

Article Google Scholar

9. 9.

Guarracino F, Vetrugno L, Forfori F, Corradi F, Orso D, Bertini P, et al.
Lung, Heart, Vascular, and Diaphragm Ultrasound Examination of COVID-19
Patients: A Comprehensive Approach. J Cardiothorac Vasc Anesth.
2020;S1053–0770(20):30519-X.

Google Scholar

10. 10.

Zu ZY, Jiang MD, Xu PP, Chen W, Ni QQ, Lu GM, et al. Coronavirus disease
2019 (COVID-19): a perspective from China. Radiology. 2020;296(2):E15–25.

Article Google Scholar

11. 11.

Zhou S, Wang Y, Zhu T, Xia L. CT features of coronavirus disease 2019
(COVID-19) pneumonia in 62 patients in Wuhan. China AJR Am J Roentgenol.
2020;214:1287–94.

Article Google Scholar

12. 12.

Cohen J. Statistical power analysis for the behavioral sciences. 2nd ed.
Hillsdale: N.J.: L. Erlbaum Associates; 1988.

Google Scholar

13. 13.

Caltabeloti FP, Rouby JJ. Lung ultrasound: a useful tool in the weaning
process? Rev Bras Ter Intensiva. 2016;28:5–7.

Article Google Scholar

14. 14.

Galie N, Humbert M, Vachiery JL, Gibbs S, Lang I, Torbicki A, et al. 2015
ESC/ERS guidelines for the diagnosis and treatment of pulmonary
hypertension. Kardiol Pol. 2016;69(2):177.

Google Scholar

15. 15.

Galie N, Hoeper MM, Humbert M, Torbicki A, Vachiery JL, Barbera JA, et al.
Guidelines for the diagnosis and treatment of pulmonary hypertension: the
task force for the diagnosis and treatment of pulmonary hypertension of the
European Society of Cardiology (ESC) and the European Respiratory Society
(ERS), endorsed by the International Society of Heart and Lung
Transplantation (ISHLT). Eur Heart J. 2009;30:2493–537.

Article Google Scholar

16. 16.

Vladislav C, Nicola RP, Claudia T, Elisa P, Valentina S, Andrea B, et al. A
novel echocardiographic method for estimation of pulmonary artery wedge
pressure and pulmonary vascular resistance. ESC Heart Fail.
2021;8(2):1216–29.

Article Google Scholar

17. 17.

Lang RM, Badano LP, Mor-Avi V, Afilalo J, Armstrong A, Ernande L, et al.
Recommendations for cardiac chamber quantification by echocardiography in
adults: an update from the American Society of Echocardiography and the
European Association of Cardiovascular Imaging. J Am Soc Echocardiogr.
2015;28:1–39.e14.

Article Google Scholar

18. 18.

Parasuraman S, Walker S, Loudon BL, Gollop ND, Wilson AM, Lowery C, et al.
Assessment of pulmonary artery pressure by echocardiography-a comprehensive
review. Int J Cardiol Heart Vasc. 2016;12:45–51.

PubMed PubMed Central Google Scholar

19. 19.

Dunham-Snary KJ, Wu D, Sykes EA, Thakrar A, Parlow LRG, Mewburn JD, et al.
Hypoxic pulmonary vasoconstriction: from molecular mechanisms to medicine.
Chest. 2017;151:181–92.

Article Google Scholar

20. 20.

Tuder RM, Archer SL, Dorfmuller P, Erzurum SC, Guignabert C, Michelakis E,
et al. Relevant issues in the pathology and pathobiology of pulmonary
hypertension. J Am Coll Cardiol. 2013;62:D4–12.

Article Google Scholar

21. 21.

Li W, Moore MJ, Vasilieva N, Sui J, Wong SK, Berne MA, et al.
Angiotensin-converting enzyme 2 is a functional receptor for the SARS
coronavirus. Nature. 2003;426:450–4.

CAS Article Google Scholar

22. 22.

Jia H. Pulmonary angiotensin-converting enzyme 2 (ACE2) and inflammatory
lung disease. Shock. 2016;46:239–48.

CAS Article Google Scholar

23. 23.

Zhang J, Dong J, Martin M, He M, Gongol B, Marin TL, et al. AMP-activated
protein kinase phosphorylation of angiotensin-converting enzyme 2 in
endothelium mitigates pulmonary hypertension. Am J Respir Crit Care Med.
2018;198:509–20.

CAS Article Google Scholar

24. 24.

Hummel YM, Liu LCY, Lam CSP, Fonseca-Munoz DF, Damman K, Rienstra M, et al.
Echocardiographic estimation of left ventricular and pulmonary pressures in
patients with heart failure and preserved ejection fraction: a study
utilizing simultaneous echocardiography and invasive measurements. Eur J
Heart Fail. 2017;19:1651–60.

Article Google Scholar

25. 25.

Abbas AE, Franey LM, Marwick T, Maeder MT, Kaye DM, Vlahos AP, et al.
Noninvasive assessment of pulmonary vascular resistance by Doppler
echocardiography. J Am Soc Echocardiogr. 2013;26:1170–7.

Article Google Scholar

26. 26.

Bossone E, D'Andrea A, D'Alto M, Citro R, Argiento P, Ferrara F.
Echocardiography in pulmonary arterial hypertension: from diagnosis to
prognosis. J Am Soc Echocardiogr. 2013;26:1–14.

Article Google Scholar

27. 27.

Nagueh SF, Smiseth OA, Appleton CP, Byrd BF III, Dokainish H, Edvardsen T.
Recommendations for the evaluation of left ventricular diastolic function
by echocardiography: an update from the American Society of
Echocardiography and the European Association of Cardiovascular Imaging. J
Am Soc Echocardiogr. 2016;29:277–314.

Article Google Scholar

28. 28.

Dokainish H, Nguyen JS, Bobek J, Goswami R, Lakkis NM. Assessment of the
American Society of Echocardiography-European Association of
Echocardiography guidelines for diastolic function in patients with
depressed ejection fraction: an echocardiographic and invasive haemodynamic
study. Eur J Echocardiogr. 2011;12:857–64.

Article Google Scholar

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ACKNOWLEDGEMENTS

We would like to thank Editage (www.editage.cn) for English language editing.

FUNDING

This work was supported by the Ministry of Science and Technology of the
People’s Republic of China (grant number 2020YFC0844900).

AUTHOR INFORMATION

Author notes

1. Jing Han and Xi Yang contributed equally to the writing of this article and
should be considered as co-first authors.

AFFILIATIONS

1. Ultrasound and Functional Diagnosis Center, Beijing You An Hospital, Capital
Medical University, Beijing, 100069, China

Jing Han, Weiyuan Liu, Lei Ding, Yuan Zhang, Ying Zheng & Fankun Meng

2. Department of ultrasound, Hanyang Hospital Affiliated to Wuhan University of
science and technology, Wuhan, 430050, China

Xi Yang

3. Key Laboratory of Carcinogenesis and Translational Research (Ministry of
Education/Beijing), Department of Hepato-Pancreato-Biliary Surgery, Peking
University Cancer Hospital & Institute, Beijing, 100142, China

Wei Xu

4. Beijing You An Hospital, Capital Medical University, Beijing, 100069, China

Ronghua Jin

5. Department of Science and Technology Department, Beijing You An Hospital,
Capital Medical University, Beijing, 100069, China

Sha Meng

6. Department of Ultrasound, Beijing Hospital of Chinese Traditional and
Western Medicine, Beijing, 100069, China

Jin Li

7. Ultrasonography, China Aerospace Science & Industry Corporation 731
Hospital, Beijing, 100074, China

Haowen Li

Authors
1. Jing Han
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