Research Article
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Ultrasonographic evaluation of post-COVID long-term lung changes and relation to prolonged COVID symptoms: a prospective cross-sectional study

Year 2024, Volume: 10 Issue: 5, 490 - 500
https://doi.org/10.18621/eurj.1513218

Abstract

Objectives: This study aims to evaluate lung findings using lung ultrasonography (USG) in patients with PCR-positive COVID-19 pneumonia treated in the ward or intensive care unit and to explore the relationship with prolonged COVID-19 symptoms.

Methods: This prospective cross-sectional study was conducted at the University Medical Faculty Hospital outpatient clinic from December 2022 to April 2023. It involved 54 adult patients with PCR-positive COVID-19 pneumonia, treated and discharged from the ward or intensive care unit (ICU). Clinical and demographic data, lung ultrasonography results, and prolonged COVID-19 symptoms were recorded.

Results: Among the 54 patients, the ICU group had a mean age of 52.84 ± 12.30 years, while the ward group had a mean age of 58.80 ± 11.36 years (P=0.085). Shortness of breath was the most common prolonged symptom in both groups. The ICU group had significantly more right lung B lines than the ward group (P=0.002). Myalgia was more frequent in the ward group (P=0.024). No significant differences were observed in other variables (P>0.05). Prolonged COVID-19 symptoms were interrelated (P<0.05), and the total number of B lines was significantly associated with dyspnea (P=0.023).

Conclusions: Our study demonstrated that lung USG is a valuable tool in the assessment of lung injury after COVID-19 and in the management of long-term COVID-19 symptoms. B lines detected by lung USG are significantly associated with the long-term COVID symptom of shortness of breath, and the number of B lines may be an important biomarker in the management of shortness of breath.

Ethical Statement

Ethics committee approval for this study was obtained from the Trakya University Faculty of Medicine Ethics Committee on 14/06/2021, with decision number:13/35 and protocol code: TUTF-BAEK-2021/292

Supporting Institution

Trakya University Scientific Research Project

Project Number

2022/131

References

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  • 4. Mahase E. Covid-19: What do we know about "long covid"? BMJ. 2020;370:m2815. doi: 10.1136/bmj.m2815.
  • 5. Baris SA, Toprak OB, Cetinkaya PD, et al. The predictors of long-COVID in the cohort of Turkish Thoracic Society-TURCOVID multicenter registry: One year follow-up results. Asian Pac J Trop Med. 2022;15(9):400-409. doi: 10.4103/1995-7645.354422.
  • 6. Rocca E, Zanza C, Longhitano Y, et al. Lung Ultrasound in Critical Care and Emergency Medicine: Clinical Review. Adv Respir Med. 2023;91(3):203-223. doi: 10.3390/arm91030017.
  • 7. Walden A, Campbell A, Miller A, Wise M, eds. Ultrasound in the Critically Ill: A Practical Guide. 1st ed. Springer Nature; 2022: pp. 41-67. doi: 10.1007/978-3-030-71742-1.
  • 8. Haaksma ME, Smit JM, Heldeweg MLA, Pisani L, Elbers P, Tuinman PR. Lung ultrasound and B-lines: B careful!. Intensive Care Med. 2020;46(3):544-545. doi: 10.1007/s00134-019-05911-8.
  • 9. Xirouchaki N, Magkanas E, Vaporidi K, et al. Lung ultrasound in critically ill patients: comparison with bedside chest radiography. Intensive Care Med. 2011;37(9):1488-1493. doi: 10.1007/s00134-011-2317-y.
  • 10. Volpicelli G, Elbarbary M, Blaivas M, et al. International Liaison Committee on Lung Ultrasound (ILC-LUS) for International Consensus Conference on Lung Ultrasound (ICC-LUS). International evidence-based recommendations for point-of-care lung ultrasound. Intensive Care Med. 2012;38(4):577-591. doi: 10.1007/s00134-012-2513-4.
  • 11. Turkish Ministry of Health. e-Nabız Personal Health System. Available at: https://www.enabiz.gov.tr/. Accessed April 24, 2024.
  • 12. Tabakoglu NT, Celik M. Evaluation of Health-Related Quality of Life in Patients with Euthyroid Hashimoto's Thyroiditis under Long-Term Levothyroxine Therapy: A Prospective Case-Control Study. J Clin Med. 2024;13(11):3082. doi: 10.3390/jcm13113082.
  • 13. Ekström M, Sundh J, Andersson A, et al. Exertional breathlessness related to medical conditions in middle-aged people: the population-based SCAPIS study of more than 25,000 men and women. Respir Res. 2024;25(1):127. doi: 10.1186/s12931-024-02766-6.
  • 14. Tabakoglu NT, Üstündağ S. Comparison of Prevalence and Severity of Depressive Symptoms in Hemodialysis Patients Before and During the COVID-19 Pandemic. Balkan Sağlık Bilimleri Dergisi. 2024;2(3):131-139. doi: 10.61830/balkansbd.1399034.
  • 15. DePace NL, Colombo J. Long-COVID Syndrome and the Cardiovascular System: A Review of Neurocardiologic Effects on Multiple Systems. Curr Cardiol Rep. 2022;24(11):1711-1726. doi: 10.1007/s11886-022-01786-2.
  • 16. Bilgin S, Yamanoğlu A, Kayalı A, et al. Long COVID symptoms among outpatients with COVID-19: a descriptive study. Cukurova Med J. 2023;48(1):243-252. doi: 10.17826/cumj.1216943.
  • 17. Carfì A, Bernabei R, Landi F; Gemelli Against COVID-19 Post-Acute Care Study Group. Persistent Symptoms in Patients After Acute COVID-19. JAMA. 2020;324(6):603-605. doi: 10.1001/jama.2020.12603.
  • 18. Fidan A, Cömert ŞŞ, Tokmak M, Saraç G, Salepçi B, Kıral N. [Retrospective analysis of aspiration pneumonia cases]. Kartal Eğitim ve Araştırma Hastanesi Tıp Dergisi. 2008;19(3):113-116. [Article in Turkish]
  • 19. Grewal JS, Carlsten C, Johnston JC, Shah AS, Wong AW, Ryerson CJ. Post-COVID dyspnea: prevalence, predictors, and outcomes in a longitudinal, prospective cohort. BMC Pulm Med. 2023;23(1):84. doi: 10.1186/s12890-023-02376-w.
  • 20. Garrigues E, Janvier P, Kherabi Y, et al. Post-discharge persistent symptoms and health-related quality of life after hospitalization for COVID-19. J Infect. 2020;81(6):e4-e6. doi: 10.1016/j.jinf.2020.08.029.
  • 21. Iwakura K, Onishi T. A practical guide to the lung ultrasound for the assessment of congestive heart failure. J Echocardiogr. 2021;19(4):195-204. doi: 10.1007/s12574-021-00528-7.
  • 22. Volpicelli G, Mussa A, Garofalo G, et al. Bedside lung ultrasound in the assessment of alveolar-interstitial syndrome. Am J Emerg Med. 2006;24(6):689-696. doi: 10.1016/j.ajem.2006.02.013.
  • 23. Kimmig LM, Rako ZA, Ziegler S, et al. Long-term comprehensive cardiopulmonary phenotyping of COVID-19. Respir Res. 2022;23(1):263. doi: 10.1186/s12931-022-02173-9.
  • 24. Scaramuzzo G, Ronzoni L, Campo G, et al. Long-term dyspnea, regional ventilation distribution and peripheral lung function in COVID-19 survivors: a 1 year follow up study. BMC Pulm Med. 2022;22(1):408. doi: 10.1186/s12890-022-02214-5.
  • 25. Herndon CM, Nguyen V. Patterns of Viral Arthropathy and Myalgia Following COVID-19: A Cross-Sectional National Survey. J Pain Res. 2022;15:3069-3077. doi: 10.2147/JPR.S373295.
  • 26. Ferrandi PJ, Alway SE, Mohamed JS. The interaction between SARS-CoV-2 and ACE2 may have consequences for skeletal muscle viral susceptibility and myopathies. J Appl Physiol (1985). 2020;129(4):864-867. doi: 10.1152/japplphysiol.00321.2020.
  • 27. Partridge LJ, Urwin L, Nicklin MJH, James DC, Green LR, Monk PN. ACE2-Independent Interaction of SARS-CoV-2 Spike Protein with Human Epithelial Cells Is Inhibited by Unfractionated Heparin. Cells. 2021;10(6):1419. doi: 10.3390/cells10061419.
  • 28. Sarkesh A, Sorkhabi AD, Sheykhsaran E, et al. Extrapulmonary Clinical Manifestations in COVID-19 Patients. Am J Trop Med Hyg. 2020;103(5):1783-1796. doi: 10.4269/ajtmh.20-0986.
  • 29. Morley JE, Kalantar-Zadeh K, Anker SD. COVID-19: a major cause of cachexia and sarcopenia? J Cachexia Sarcopenia Muscle. 2020;11(4):863-865. doi: 10.1002/jcsm.12589.
  • 30. Disser NP, De Micheli AJ, Schonk MM, et al. Musculoskeletal Consequences of COVID-19. J Bone Joint Surg Am. 2020;102(14):1197-1204. doi: 10.2106/JBJS.20.00847.
  • 31. Nakanishi N, Liu K, Kawakami D, et al. Post-Intensive Care Syndrome and Its New Challenges in Coronavirus Disease 2019 (COVID-19) Pandemic: A Review of Recent Advances and Perspectives. J Clin Med. 2021;10(17):3870. doi: 10.3390/jcm10173870.
  • 32. Smith EM, Lee ACW, Smith JM, Thiele A, Zeleznik H, Ohtake PJ. COVID-19 and post-intensive care syndrome: community-based care for ICU survivors. Home Health Care Manag Pract. 2021;33(2):117-124. doi: 10.1177/1084822320974956.
  • 33. Fakili F, Cetinkaya PD, Baydar O. Post-discharge mortality in the first wave of COVID-19 in Turkey. Asian Pac J Trop Med. 2022;15(11):479-484. doi: 10.4103/1995-7645.361853.
  • 34. Karacaer C, Karabay O, Gunduz Y, Yaylacı S, Guclu E. Correlation of Lung Ultrasound and Computed Tomography Findings in COVID-19 Pneumonia. J Coll Physicians Surg Pak. 2020;30(10):147-152. doi: 10.29271/jcpsp.2020.supp2.S147.
  • 35. Soldati G, Smargiassi A, Inchingolo R, et al. Is There a Role for Lung Ultrasound During the COVID-19 Pandemic? J Ultrasound Med. 2020;39(7):1459-1462. doi: 10.1002/jum.15284.
  • 36. Sofia S, Boccatonda A, Montanari M, et al. Thoracic ultrasound and SARS-COVID-19: a pictorial essay. J Ultrasound. 2020;23(2):217-221. doi: 10.1007/s40477-020-00458-7.
  • 37. Smith MJ, Hayward SA, Innes SM, Miller ASC. Point-of-care lung ultrasound in patients with COVID-19 - a narrative review. Anaesthesia. 2020;75(8):1096-1104. doi: 10.1111/anae.15082.
  • 38. Convissar DL, Gibson LE, Berra L, Bittner EA, Chang MG. Application of Lung Ultrasound During the COVID-19 Pandemic: A Narrative Review. Anesth Analg. 2020;131(2):345-350. doi: 10.1213/ANE.0000000000004929.
Year 2024, Volume: 10 Issue: 5, 490 - 500
https://doi.org/10.18621/eurj.1513218

Abstract

Project Number

2022/131

References

  • 1. World Health Organization. WHO Coronavirus (COVID-19) Dashboard. Available at: https://covid19.who.int/. Accessed September 17, 2023.
  • 2. Soriano JB, Murthy S, Marshall JC, Relan P, Diaz JV; WHO Clinical Case Definition Working Group on Post-COVID-19 Condition. A clinical case definition of post-COVID-19 condition by a Delphi consensus. Lancet Infect Dis. 2022;22(4):e102-e107. doi: 10.1016/S1473-3099(21)00703-9.
  • 3. Akar MN. Prolonged COVID. In: TOBB ETU Publications, 1st ed. Ankara, Ankara: TOBB ETÜ Publications; 2023: pp. 3-15.
  • 4. Mahase E. Covid-19: What do we know about "long covid"? BMJ. 2020;370:m2815. doi: 10.1136/bmj.m2815.
  • 5. Baris SA, Toprak OB, Cetinkaya PD, et al. The predictors of long-COVID in the cohort of Turkish Thoracic Society-TURCOVID multicenter registry: One year follow-up results. Asian Pac J Trop Med. 2022;15(9):400-409. doi: 10.4103/1995-7645.354422.
  • 6. Rocca E, Zanza C, Longhitano Y, et al. Lung Ultrasound in Critical Care and Emergency Medicine: Clinical Review. Adv Respir Med. 2023;91(3):203-223. doi: 10.3390/arm91030017.
  • 7. Walden A, Campbell A, Miller A, Wise M, eds. Ultrasound in the Critically Ill: A Practical Guide. 1st ed. Springer Nature; 2022: pp. 41-67. doi: 10.1007/978-3-030-71742-1.
  • 8. Haaksma ME, Smit JM, Heldeweg MLA, Pisani L, Elbers P, Tuinman PR. Lung ultrasound and B-lines: B careful!. Intensive Care Med. 2020;46(3):544-545. doi: 10.1007/s00134-019-05911-8.
  • 9. Xirouchaki N, Magkanas E, Vaporidi K, et al. Lung ultrasound in critically ill patients: comparison with bedside chest radiography. Intensive Care Med. 2011;37(9):1488-1493. doi: 10.1007/s00134-011-2317-y.
  • 10. Volpicelli G, Elbarbary M, Blaivas M, et al. International Liaison Committee on Lung Ultrasound (ILC-LUS) for International Consensus Conference on Lung Ultrasound (ICC-LUS). International evidence-based recommendations for point-of-care lung ultrasound. Intensive Care Med. 2012;38(4):577-591. doi: 10.1007/s00134-012-2513-4.
  • 11. Turkish Ministry of Health. e-Nabız Personal Health System. Available at: https://www.enabiz.gov.tr/. Accessed April 24, 2024.
  • 12. Tabakoglu NT, Celik M. Evaluation of Health-Related Quality of Life in Patients with Euthyroid Hashimoto's Thyroiditis under Long-Term Levothyroxine Therapy: A Prospective Case-Control Study. J Clin Med. 2024;13(11):3082. doi: 10.3390/jcm13113082.
  • 13. Ekström M, Sundh J, Andersson A, et al. Exertional breathlessness related to medical conditions in middle-aged people: the population-based SCAPIS study of more than 25,000 men and women. Respir Res. 2024;25(1):127. doi: 10.1186/s12931-024-02766-6.
  • 14. Tabakoglu NT, Üstündağ S. Comparison of Prevalence and Severity of Depressive Symptoms in Hemodialysis Patients Before and During the COVID-19 Pandemic. Balkan Sağlık Bilimleri Dergisi. 2024;2(3):131-139. doi: 10.61830/balkansbd.1399034.
  • 15. DePace NL, Colombo J. Long-COVID Syndrome and the Cardiovascular System: A Review of Neurocardiologic Effects on Multiple Systems. Curr Cardiol Rep. 2022;24(11):1711-1726. doi: 10.1007/s11886-022-01786-2.
  • 16. Bilgin S, Yamanoğlu A, Kayalı A, et al. Long COVID symptoms among outpatients with COVID-19: a descriptive study. Cukurova Med J. 2023;48(1):243-252. doi: 10.17826/cumj.1216943.
  • 17. Carfì A, Bernabei R, Landi F; Gemelli Against COVID-19 Post-Acute Care Study Group. Persistent Symptoms in Patients After Acute COVID-19. JAMA. 2020;324(6):603-605. doi: 10.1001/jama.2020.12603.
  • 18. Fidan A, Cömert ŞŞ, Tokmak M, Saraç G, Salepçi B, Kıral N. [Retrospective analysis of aspiration pneumonia cases]. Kartal Eğitim ve Araştırma Hastanesi Tıp Dergisi. 2008;19(3):113-116. [Article in Turkish]
  • 19. Grewal JS, Carlsten C, Johnston JC, Shah AS, Wong AW, Ryerson CJ. Post-COVID dyspnea: prevalence, predictors, and outcomes in a longitudinal, prospective cohort. BMC Pulm Med. 2023;23(1):84. doi: 10.1186/s12890-023-02376-w.
  • 20. Garrigues E, Janvier P, Kherabi Y, et al. Post-discharge persistent symptoms and health-related quality of life after hospitalization for COVID-19. J Infect. 2020;81(6):e4-e6. doi: 10.1016/j.jinf.2020.08.029.
  • 21. Iwakura K, Onishi T. A practical guide to the lung ultrasound for the assessment of congestive heart failure. J Echocardiogr. 2021;19(4):195-204. doi: 10.1007/s12574-021-00528-7.
  • 22. Volpicelli G, Mussa A, Garofalo G, et al. Bedside lung ultrasound in the assessment of alveolar-interstitial syndrome. Am J Emerg Med. 2006;24(6):689-696. doi: 10.1016/j.ajem.2006.02.013.
  • 23. Kimmig LM, Rako ZA, Ziegler S, et al. Long-term comprehensive cardiopulmonary phenotyping of COVID-19. Respir Res. 2022;23(1):263. doi: 10.1186/s12931-022-02173-9.
  • 24. Scaramuzzo G, Ronzoni L, Campo G, et al. Long-term dyspnea, regional ventilation distribution and peripheral lung function in COVID-19 survivors: a 1 year follow up study. BMC Pulm Med. 2022;22(1):408. doi: 10.1186/s12890-022-02214-5.
  • 25. Herndon CM, Nguyen V. Patterns of Viral Arthropathy and Myalgia Following COVID-19: A Cross-Sectional National Survey. J Pain Res. 2022;15:3069-3077. doi: 10.2147/JPR.S373295.
  • 26. Ferrandi PJ, Alway SE, Mohamed JS. The interaction between SARS-CoV-2 and ACE2 may have consequences for skeletal muscle viral susceptibility and myopathies. J Appl Physiol (1985). 2020;129(4):864-867. doi: 10.1152/japplphysiol.00321.2020.
  • 27. Partridge LJ, Urwin L, Nicklin MJH, James DC, Green LR, Monk PN. ACE2-Independent Interaction of SARS-CoV-2 Spike Protein with Human Epithelial Cells Is Inhibited by Unfractionated Heparin. Cells. 2021;10(6):1419. doi: 10.3390/cells10061419.
  • 28. Sarkesh A, Sorkhabi AD, Sheykhsaran E, et al. Extrapulmonary Clinical Manifestations in COVID-19 Patients. Am J Trop Med Hyg. 2020;103(5):1783-1796. doi: 10.4269/ajtmh.20-0986.
  • 29. Morley JE, Kalantar-Zadeh K, Anker SD. COVID-19: a major cause of cachexia and sarcopenia? J Cachexia Sarcopenia Muscle. 2020;11(4):863-865. doi: 10.1002/jcsm.12589.
  • 30. Disser NP, De Micheli AJ, Schonk MM, et al. Musculoskeletal Consequences of COVID-19. J Bone Joint Surg Am. 2020;102(14):1197-1204. doi: 10.2106/JBJS.20.00847.
  • 31. Nakanishi N, Liu K, Kawakami D, et al. Post-Intensive Care Syndrome and Its New Challenges in Coronavirus Disease 2019 (COVID-19) Pandemic: A Review of Recent Advances and Perspectives. J Clin Med. 2021;10(17):3870. doi: 10.3390/jcm10173870.
  • 32. Smith EM, Lee ACW, Smith JM, Thiele A, Zeleznik H, Ohtake PJ. COVID-19 and post-intensive care syndrome: community-based care for ICU survivors. Home Health Care Manag Pract. 2021;33(2):117-124. doi: 10.1177/1084822320974956.
  • 33. Fakili F, Cetinkaya PD, Baydar O. Post-discharge mortality in the first wave of COVID-19 in Turkey. Asian Pac J Trop Med. 2022;15(11):479-484. doi: 10.4103/1995-7645.361853.
  • 34. Karacaer C, Karabay O, Gunduz Y, Yaylacı S, Guclu E. Correlation of Lung Ultrasound and Computed Tomography Findings in COVID-19 Pneumonia. J Coll Physicians Surg Pak. 2020;30(10):147-152. doi: 10.29271/jcpsp.2020.supp2.S147.
  • 35. Soldati G, Smargiassi A, Inchingolo R, et al. Is There a Role for Lung Ultrasound During the COVID-19 Pandemic? J Ultrasound Med. 2020;39(7):1459-1462. doi: 10.1002/jum.15284.
  • 36. Sofia S, Boccatonda A, Montanari M, et al. Thoracic ultrasound and SARS-COVID-19: a pictorial essay. J Ultrasound. 2020;23(2):217-221. doi: 10.1007/s40477-020-00458-7.
  • 37. Smith MJ, Hayward SA, Innes SM, Miller ASC. Point-of-care lung ultrasound in patients with COVID-19 - a narrative review. Anaesthesia. 2020;75(8):1096-1104. doi: 10.1111/anae.15082.
  • 38. Convissar DL, Gibson LE, Berra L, Bittner EA, Chang MG. Application of Lung Ultrasound During the COVID-19 Pandemic: A Narrative Review. Anesth Analg. 2020;131(2):345-350. doi: 10.1213/ANE.0000000000004929.
There are 38 citations in total.

Details

Primary Language English
Subjects Chest Diseases
Journal Section Original Articles
Authors

Nilgün Tan Tabakoğlu 0000-0001-9282-5971

Pervin Hancı Yılmaztürk 0000-0002-7207-2041

İlker Yılmam 0000-0003-4349-5771

Necdet Süt 0000-0001-6678-482X

Osman Nuri Hatipoğlu 0000-0002-2772-8654

Project Number 2022/131
Early Pub Date August 16, 2024
Publication Date
Submission Date July 9, 2024
Acceptance Date August 3, 2024
Published in Issue Year 2024 Volume: 10 Issue: 5

Cite

AMA Tan Tabakoğlu N, Hancı Yılmaztürk P, Yılmam İ, Süt N, Hatipoğlu ON. Ultrasonographic evaluation of post-COVID long-term lung changes and relation to prolonged COVID symptoms: a prospective cross-sectional study. Eur Res J. 10(5):490-500. doi:10.18621/eurj.1513218

e-ISSN: 2149-3189 


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