COVID-19 and Pulmonary Thrombosis-An Unresolved Clinical Puzzle: A Single-Center Cohort Study

Loris Močibob, Frano Šušak, Maja Šitum, Klaudija Višković, Neven Papić, Adriana Vince, Loris Močibob, Frano Šušak, Maja Šitum, Klaudija Višković, Neven Papić, Adriana Vince

Abstract

Pulmonary thrombosis (PT) is a frequent complication of COVID-19. However, the risk factors, predictive scores, and precise diagnostic guidelines on indications for CT pulmonary angiography (CTPA) are still lacking. This study aimed to analyze the clinical and laboratory characteristics associated with PT in patients with COVID-19. We conducted a cohort study of consecutively hospitalized adult patients with COVID-19 who underwent CTPA at the University Hospital for Infectious Diseases in Zagreb, Croatia between 1 April and 31 December 2021. Of 2078 hospitalized patients, 575 (27.6%) underwent CTPA. PT was diagnosed in 178 (30.9%) patients (69.6% males, median age of 61, IQR 50-69 years). The PT group had a higher CRP, LDH, D-dimer, platelets, and CHOD score. PT was more frequent in patients requiring ≥15 L O2/min (25.0% vs. 39.7%). In multivariable analysis, only D-dimer ≥ 1.0 mg/L (OR 1.78, 95%CI 1.12-2.75) and O2 ≥ 15 L (OR 1.89, 95%CI 1.26-2.84) were associated with PT. PT was not associated with in-hospital mortality. In conclusion, our data confirmed a high incidence of PT in hospitalized patients with COVID-19, however, no correlation with traditional risk factors and mortality was found. CTPA should be performed in patients requiring high-flow supplemental oxygen or those with increased D-dimer levels.

Keywords: COVID-19; CTPA; D-dimer; pulmonary angiography; pulmonary thrombosis; venous thromboembolism.

Conflict of interest statement

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

Figures

Figure 1
Figure 1
Frequency of patients with PT stratified by the respiratory support level. PT—pulmonary thrombosis, HFNC—high flow nasal cannula, NIV—non-invasive ventilation, IMV—invasive mechanic ventilation, ECMO—extracorporeal membrane oxygenation.

References

    1. Jiménez D., García-Sanchez A., Rali P., Muriel A., Bikdeli B., Ruiz-Artacho P., Le Mao R., Rodríguez C., Hunt B.J., Monreal M. Incidence of VTE and Bleeding Among Hospitalized Patients With Coronavirus Disease 2019: A Systematic Review and Meta-analysis. Chest. 2021;159:1182–1196. doi: 10.1016/j.chest.2020.11.005.
    1. Katsoularis I., Fonseca-Rodríguez O., Farrington P., Jerndal H., Lundevaller E.H., Sund M., Lindmark K., Connolly A.-M.F. Risks of deep vein thrombosis, pulmonary embolism, and bleeding after COVID-19: Nationwide self-controlled cases series and matched cohort study. BMJ. 2022;377:e069590. doi: 10.1136/bmj-2021-069590.
    1. Cui L.-Y., Cheng W.-W., Mou Z.-W., Xiao D., Li Y.-Y., Li Y.-J., Li W.-T., Chen Z.-M. Risk factors for pulmonary embolism in patients with COVID-19: A systemic review and meta-analysis. Int. J. Infect. Dis. 2021;111:154–163. doi: 10.1016/j.ijid.2021.08.017.
    1. Colling M.E., Kanthi Y. COVID–19-associated coagulopathy: An exploration of mechanisms. Vasc. Med. 2020;25:471–478. doi: 10.1177/1358863X20932640.
    1. Varga Z., Flammer A.J., Steiger P., Haberecker M., Andermatt R., Zinkernagel A.S., Mehra M.R., Schuepbach R.A., Ruschitzka F., Moch H. Endothelial cell infection and endotheliitis in COVID-19. Lancet. 2020;395:1417–1418. doi: 10.1016/S0140-6736(20)30937-5.
    1. Słomka A., Kowalewski M., Żekanowska E. Hemostasis in Coronavirus Disease 2019—Lesson from Viscoelastic Methods: A Systematic Review. Thromb. Haemost. 2021;121:1181–1192. doi: 10.1055/a-1346-3178.
    1. Kirsch B., Aziz M., Kumar S., Burke M., Webster T., Immadi A., Sam M., Lal A., Estrada-Y-Martin R.M., Cherian S., et al. Wells Score to Predict Pulmonary Embolism in Patients with Coronavirus Disease 2019. Am. J. Med. 2021;134:688–690. doi: 10.1016/j.amjmed.2020.10.044.
    1. Kwee R.M., Adams H.J.A., Kwee T.C. Pulmonary embolism in patients with COVID-19 and value of D-dimer assessment: A meta-analysis. Eur. Radiol. 2021;31:8168–8186. doi: 10.1007/s00330-021-08003-8.
    1. Huda W. Radiation Doses and Risks in Chest Computed Tomography Examinations. Proc. Am. Thorac. Soc. 2007;4:316–320. doi: 10.1513/pats.200611-172HT.
    1. Raji H., Moosavi S.A.J., Dastoorpoor M., Mohamadipour Z., Ghanavati P.M. Overuse and underuse of pulmonary CT angiography in patients with suspected pulmonary embolism. Med. J. Islam. Repub. Iran. 2018;32:13–17. doi: 10.14196/mjiri.32.3.
    1. Van Dam L., Kroft L., van der Wal L., Cannegieter S., Eikenboom J., de Jonge E., Huisman M., Klok F. Clinical and computed tomography characteristics of COVID-19 associated acute pulmonary embolism: A different phenotype of thrombotic disease? Thromb. Res. 2020;193:86–89. doi: 10.1016/j.thromres.2020.06.010.
    1. Mestre-Gómez B., Lorente-Ramos R.M., Rogado J., Franco-Moreno A., Obispo B., Salazar-Chiriboga D., Saez-Vaquero T., Torres-Macho J., Abad-Motos A., Cortina-Camarero C., et al. Incidence of pulmonary embolism in non-critically ill COVID-19 patients. Predicting factors for a challenging diagnosis. J. Thromb. Thrombolysis. 2021;51:40–46. doi: 10.1007/s11239-020-02190-9.
    1. Gratz J., Wiegele M., Maleczek M., Herkner H., Schöchl H., Chwala E., Knöbl P., Schaden E. Risk of Clinically Relevant Venous Thromboembolism in Critically Ill Patients With COVID-19: A Systematic Review and Meta-Analysis. Front. Med. 2021;8:647917. doi: 10.3389/fmed.2021.647917.
    1. Kreidieh F., Temraz S. Anticoagulation for COVID-19 Patients: A Bird’s-Eye View. Clin. Appl. Thromb. 2021;27:10760296211039288. doi: 10.1177/10760296211039288.
    1. Assessing SARS-CoV-2 Circulation, Variants of Concern, Non-Pharmaceutical Interventions and Vaccine Rollout in the EU/EEA, 16th update. [(accessed on 29 October 2022)]. Available online: .
    1. García-Ortega A., Oscullo G., Calvillo P., López-Reyes R., Méndez R., Gómez-Olivas J.D., Bekki A., Fonfría C., Trilles-Olaso L., Zaldívar E., et al. Incidence, risk factors, and thrombotic load of pulmonary embolism in patients hospitalized for COVID-19 infection. J. Infect. 2021;82:261–269. doi: 10.1016/j.jinf.2021.01.003.
    1. Loffi M., Regazzoni V., Toselli M., Cereda A., Palmisano A., Vignale D., Moroni F., Pontone G., Andreini D., Mancini E.M., et al. Incidence and characterization of acute pulmonary embolism in patients with SARS-CoV-2 pneumonia: A multicenter Italian experience. PLoS ONE. 2021;16:e0245565. doi: 10.1371/journal.pone.0245565.
    1. Ventura-Díaz S., Quintana-Pérez J.V., Gil-Boronat A., Herrero-Huertas M., Gorospe-Sarasúa L., Montilla J., Acosta-Batlle J., Blázquez-Sánchez J., Vicente-Bártulos A. A higher D-dimer threshold for predicting pulmonary embolism in patients with COVID-19: A retrospective study. Emerg. Radiol. 2020;27:679–689. doi: 10.1007/s10140-020-01859-1.
    1. Kollias A., Kyriakoulis K.G., Lagou S., Kontopantelis E., Stergiou G.S., Syrigos K. Venous thromboembolism in COVID-19: A systematic review and meta-analysis. Vasc. Med. 2021;26:415–425. doi: 10.1177/1358863X21995566.
    1. Fauvel C., Weizman O., Trimaille A., Mika D., Pommier T., Pace N., Douair A., Barbin E., Fraix A., Bouchot O., et al. Pulmonary embolism in COVID-19 patients: A French multicentre cohort study. Eur. Heart J. 2020;41:3058–3068. doi: 10.1093/eurheartj/ehaa500.
    1. Cueto-Robledo G., Navarro-Vergara D.-I., Roldan-Valadez E., Garcia-Cesar M., Graniel-Palafox L.-E., Cueto-Romero H.-D., Perez-Calatayud A.-A., Enriquez-Garcia R., Casillas-Suarez C. Pulmonary Embolism (PE) Prevalence in Mexican-Mestizo Patients With Severe SARS-Cov-2 (COVID-19) Pneumonia At A Tertiary-Level Hospital: A Review. Curr. Probl. Cardiol. 2022;20:101208. doi: 10.1016/j.cpcardiol.2022.101208.
    1. Antithrombotic Therapy in Patients With COVID-19. [(accessed on 29 October 2022)]; Available online:
    1. Lawler P.R., Goligher E.C., Berger J.S., Neal M.D., McVerry B.J., Nicolau J.C. Therapeutic Anticoagulation with Heparin in Noncritically Ill Patients with COVID-19. New Engl. J. Med. 2021;385:790–802. doi: 10.1056/nejmoa2105911.
    1. Goligher E.C., Bradbury C.A., McVerry B.J., Lawler P.R., Berger J.S., Gong M.N. Therapeutic Anticoagulation with Heparin in Critically Ill Patients with COVID-19. New Engl. J. Med. 2021;385:777–789. doi: 10.1056/nejmoa2103417.
    1. Halmaciu I., Arbănași E.M., Kaller R., Mureșan A.V., Arbănași E.M., Bacalbasa N., Suciu B.A., Cojocaru I.I., Runcan A.I., Grosu F., et al. Chest CT Severity Score and Systemic Inflammatory Biomarkers as Predictors of the Need for Invasive Mechanical Ventilation and of COVID-19 Patients’ Mortality. Diagnostics. 2022;12:2089. doi: 10.3390/diagnostics12092089.
    1. Strazzulla A., Ben Halima S.A., Chouchane I., Rezek M., Stiebler M.P., Hamrouni S., Maalaoui M., Ghriss N., Guedec-Ghelfi R., Moini C., et al. The Predictive Value of Cell Blood Count Parameters to Diagnose Pulmonary Embolism in Patients with SARS-CoV-2 Infection: A Case Control Study. Antibiotics. 2022;11:60. doi: 10.3390/antibiotics11010060.
    1. Lax S.F., Skok K., Zechner P., Kessler H.H., Kaufmann N., Koelblinger C., Vander K., Bargfrieder U., Trauner M. Pulmonary Arterial Thrombosis in COVID-19 With Fatal Outcome: Results From a Prospective, Single-Center, Clinicopathologic Case Series. Ann. Intern. Med. 2020;173:350–361. doi: 10.7326/M20-2566.
    1. Bompard F., Monnier H., Saab I., Tordjman M., Abdoul H., Fournier L., Sanchez O., Lorut C., Chassagnon G., Revel M.-P. Pulmonary embolism in patients with COVID-19 pneumonia. Eur. Respir. J. 2020;56:2001365. doi: 10.1183/13993003.01365-2020.
    1. Cau R., Pacielli A., Fatemeh H., Vaudano P., Arru C., Crivelli P., Stranieri G., Suri J.S., Mannelli L., Conti M., et al. Complications in COVID-19 patients: Characteristics of pulmonary embolism. Clin. Imaging. 2021;77:244–249. doi: 10.1016/j.clinimag.2021.05.016.
    1. Bledsoe J.R., Knox D., Peltan I.D., Woller S.C., Lloyd J.F., Snow G.L., Horne B.D., Connors J.M., Kline J.A. D-dimer Thresholds to Exclude Pulmonary Embolism among COVID-19 Patients in the Emergency Department: Derivation with Independent Validation. Clin. Appl. Thromb. 2022;28:10760296221117997. doi: 10.1177/10760296221117997.
    1. Zhou X., Pu Y., Zhang D., Xia Y., Guan Y., Liu S., Fan L. CT findings and dynamic imaging changes of COVID-19 in 2908 patients: A systematic review and meta-analysis. Acta Radiol. 2022;63:291–310. doi: 10.1177/0284185121992655.
    1. Da Silveira W.C., Ramos L.E.F., Silva R.T., de Paiva B.B.M., Pereira P.D., Schwarzbold A.V., Garbini A.F., Barreira B.S.M., de Castro B.M., Ramos C.M., et al. Predictors of venous thromboembolism in COVID-19 patients: Results of the COVID-19 Brazilian Registry. Intern. Emerg. Med. 2022;17:1863–1878. doi: 10.1007/s11739-022-03002-z.

Source: PubMed

3
Iratkozz fel