AIMS: To evaluate the prevalence of X-ray findings in hospitalized patients requiring hospitalization with suspected Coronavirus disease 2019 (COVID-19) infection and potential differences in the laboratory values and clinical outcomes related to the presence of abnormal chest X-ray (CXR) findings.
METHODS:
RESULTS:
CONCLUSION: CXR is a routine examination in all patients with symptoms of lower respiratory tract disease and its findings relate to in-hospital mortality and Pa

Karamouzos, Vasileios

Karanikolas, Menelaos

Lagadinou, Maria

Marangos, Markos

Oikonomou, Eleousa

Paraskevas, Themistoklis

Sampsonas, Fotios

Velissaris, Dimitrios

English

Digital Commons@Becker

Washington University School of Medicine Digital Commons@Becker Open Access Publications 9-1-2021 Evaluation of admission chest X-ray findings in patients with respiratory infection during the COVID-19 pandemic Dimitrios Velissaris Maria Lagadinou Themistoklis Paraskevas Eleousa Oikonomou Vasileios Karamouzos See next page for additional authors Follow this and additional works at: https://digitalcommons.wustl.edu/open_access_pubs Authors Dimitrios Velissaris, Maria Lagadinou, Themistoklis Paraskevas, Eleousa Oikonomou, Vasileios Karamouzos, Fotios Sampsonas, Markos Marangos, and Menelaos Karanikolas Review began  08/24/2021 Review ended  09/16/2021 Published 09/20/2021© Copyright 2021Velissaris et al. This is an open accessarticle distributed under the terms of theCreative Commons Attribution LicenseCC-BY 4.0., which permits unrestricteduse, distribution, and reproduction in anymedium, provided the original author andsource are credited.Evaluation of Admission Chest X-Ray Findings inPatients With Respiratory Infection During theCOVID-19 PandemicDimitrios Velissaris  , Maria Lagadinou  , Themistoklis Paraskevas  , Eleousa Oikonomou  , VasileiosKaramouzos  , Fotios Sampsonas  , Markos Marangos  , Menelaos Karanikolas 1. Department of Internal Medicine, University Hospital of Patras, Patras, GRC 2. Intensive Care Unit, UniversityHospital of Patras, Patras, GRC 3. Department of Respiratory Medicine, University Hospital of Patras, Patras, GRC 4.Department of Anaesthesiology, Washington University School of Medicine, Saint Louis, USACorresponding author: Dimitrios Velissaris, dimitrisvelissaris@yahoo.comAbstractAims: To evaluate the prevalence of X-ray findings in hospitalized patients requiring hospitalizationwith suspected Coronavirus disease 2019 (COVID-19) infection and potential differences in the laboratoryvalues and clinical outcomes related to the presence of abnormal chest X-ray (CXR) findings.Methods: A total of 117 patients suspected of COVID-19 pneumonia and hospitalized with symptomsof lower respiratory tract disease were included in this study. Patients were divided into subgroups accordingto COVID-19 diagnosis and statistical comparisons were made according to CXR findings.Results: In our cohort, CXR abnormalities were more common in patients with confirmed COVID-19diagnosis and were associated with increased mortality. Patients with abnormal chest X-rays had asignificantly lower PaO2/FiO2 ratio both in the COVID-19 and non-COVID-19 groups.Conclusion: CXR is a routine examination in all patients with symptoms of lower respiratory tractdisease and its findings relate to in-hospital mortality and PaO2/FiO2 ratio. Thus, it can be a significantmeasure of disease severity, especially in resource restrained settings and emergency situations such as theCOVID-19 pandemic.Categories: Emergency Medicine, Internal Medicine, Infectious DiseaseKeywords: thoracic radiography, chest x-ray (cx-ray), covid-19, pneumonia, emergency medicineIntroductionCoronavirus disease 2019 (COVID-19) has been declared a pandemic by the World Health Organization(WHO) since March 2020. After the partial retreat of the first wave, a second wave with an increased numberof infected people occurred worldwide since October 2020. The respiratory system is the most frequentlyaffected by severe acute respiratory syndrome Coronavirus 2 (SARS-CoV-2) and patients present with a widespectrum of symptoms, from mild illness to more severe disease such as acute respiratory distress syndrome(ARDS) requiring intensive care unit (ICU) admission [1,2]. Reported mortality rates differ significantlyamong studies, ranging from 3% to 15%, probably due to different sample sizes, origin, diagnostic criteria,applied tests among investigations, and therapeutic approaches. In the age of COVID-19, suspected casesare often hospitalized in special wards and respiratory support must begin before the results of COVID-19reverse transcription-polymerase chain reaction (RT-PCR) are available.Chest X-ray (CXR) is a routine examination in such patients, but its clinical value is often underestimated. Inthis setting, CXR might play a prognostic role, while its diagnostic value seems uncertain due to the lowspecificity of its findings in the differentiation between the different infectious agents.The aim of this study was to evaluate the prevalence of X-ray abnormalities in hospitalized patients withsuspected COVID-19 and potential differences in the laboratory values and clinical outcomes related to thepresence of abnormal CXR findings.Materials And MethodsPatientsThis prospective observational study enrolled patients with signs and symptoms of lung lower respiratorytract disease hospitalized in the Department of Internal Medicine of a tertiary academic medical center inwestern Greece. Patients under 18 years old and patients who refused consent were excluded from this study.The patients were treated in a modified Ward with precautions due to the possible transmission of SARS-1 1 1 12 3 1 4 Open Access OriginalArticle  DOI: 10.7759/cureus.18114How to cite this articleVelissaris D, Lagadinou M, Paraskevas T, et al. (September 20, 2021) Evaluation of Admission Chest X-Ray Findings in Patients With RespiratoryInfection During the COVID-19 Pandemic. Cureus 13(9): e18114. DOI 10.7759/cureus.18114CoV-2 and were divided into two groups according to the polymerase chain reaction (PCR) results for SARS-CoV-2 infection. The study period was from January 1, 2021 until January 31, 2021, during the period of thesecond wave of the current COVID-19 pandemic in Greece. The two groups consisted of 30 COVID-19patients and 87 non-COVID-19 patients. Clinical examination and laboratory screening with inflammatorymarkers (white cell blood count (WBC), total number of lymphocytes, C-reactive protein (CRP), lactatedehydrogenase (LDH), d-dimers, ferritin, fibrinogen) were undertaken in all patients immediately uponadmission. Radiographic findings via CXR evaluation on admission were also assessed. All patients gaveconsent for participating in the study and the Ethics Committee of the General University Hospital of Patrasapproved the protocol (Protocol Number: 102/09-03-2021).Statistical analysisPatient data were analyzed by using Chi-square, Fisher’s Exact, and Mann Whitney U tests, as appropriate.Results are presented in tables as median (25th, 75th percentile). P-values less than 0.05 indicate statisticalsignificance. All data analysis was conducted using the SPSS statistical software package (IBM Corp.Released 2019. IBM SPSS Statistics for Windows, Version 26.0. Armonk, NY: IBM Corp).ResultsDemographic and laboratory values in patients with COVID-19 versus patients without COVID-19 areshown in Table 1. COVID-19 positive patients had a significantly lower number of total WBC, lower absolutenumber of lymphocytes, lower levels of d-dimers, and increased plasma levels of ferritin, LDH, and creatinephosphokinase (CPK). In addition, these patients also had a significantly lower PO2/FiO2 ratio (p=0.004) andlonger length of hospital stay (p=0.02) when compared to non-COVID-19 patients, but there was nosignificant difference with regards to mortality. COVID-19 positive (n=30) COVID-19 negative (n=87) P-valueAge (years) 65.5 (55,74) 69 (55, 80) 0.473Body mass index 27 (25, 31) 25 (23, 31) 0.127Gender (M/F) 20/10 56/31 0.82WBC (K/mL) 6105 (4310, 7710) 9060 (7485, 14,560) <0.001Total lymphocytes (K/mL) 840 (520, 1418) 1290 (750, 2135) 0.012CRP (mg/dL) 6.18 (1.86, 10.18) 6.02 (2.10, 13.50) 0.528Lactate (mmol/L) 1.15 (0.80, 1.40) 1.20 (0.80, 1.80) 0.625Fibrinogen (mg/dL) 509 (404, 682) 569 (448, 661) 0.577D-Dimers (ng/mL) 1057 (460, 1890) 1270 (690, 2725) 0.257Ferritin (μg/L) 654.5 (336.5, 937) 149.5 (56, 384) <0.001LDH (U/L) 361 (238, 502) 241, (201.5, 309.5) 0.006CPK (U/L) 102.5 (71, 149) 71 (47, 128) 0.032PO2/FiO2 281.7 (174, 390) 379.8 (288.6, 441.2) 0.004Length of hospital stay 6.5 (4, 13) 3 (2, 6) 0.002Chest X-ray abnormalities (presence/absence) 25/5 37/50 <0.001Outcome (dead/alive) 6/24 8/79 0.116TABLE 1: Demographic and Laboratory data in COVID-19 positive versus COVID-19 negativepatients.Demographic and laboratory values in both groups of patients (with COVID-19 vs. without COVID-19). Values are listed as median (25th, 75thpercentile). WBC: white blood cells, CRP: C-reactive protein, LDH: lactate dehydrogenase, CPK: creatine phosphokinase.CXR findingsTwenty-five of 30 (83.33%) COVID-19 positive patients had abnormal findings in the CXR (bilateral lesions),2021 Velissaris et al. Cureus 13(9): e18114. DOI 10.7759/cureus.18114 2 of 5compared to 37 of 87 (42.53%) in COVID-19 negative patients, and the difference was highly significant(p<0.001).In our cohort, there was a significant increase in mortality (p=0.0014) and a decrease in the P/F ratio(p<0.01) in patients with CXR abnormalities.We further analyzed the data, by dividing COVID-19 positive patients into two sub-groups based on thepresence or absence of abnormal CVR findings. This analysis showed that mortality was 24% (6 of 25) inpatients with an abnormal CXR vs. 0% mortality (0 of 5) in patients with normal CXR. Although mortality ishigher in those with abnormal CXR, the difference did not reach significance (P=0.553), likely due to thesmall sample size. Length of hospital stay was not different among the two sub-groups. However, patientswith COVID-19 who had abnormal CXRs had significantly higher CRP, lactate, and LDH levels andsignificantly lower PO2/FiO2 compared to COVID-19 positive patients without CXR abnormalities. Thesefindings are presented in Table 2. COVID-19 patients with abnormal CXR (n=25) COVID-19 patients with normal CXR (n=5) P-valueAge (years) 66 (55.5, 79) 55 (37.5, 70.5) 0.251BMI 28 (24, 32) 27 (26.25, 27.75) 0.818Gender (M/F) 16/9 4/1 0.640WBC (K/mL) 6110 (4585, 7665) 6100 (2790, 11,250) 1.000Total lymphocytes (K/mL) 830 (510, 1404) 930 (540, 1835) 0.481CRP (mg/dL) 8.78 (3.41, 12.63) 1.01 (0.38, 2.10) 0.003Lactate (mmol/L) 1.2 (0.8, 1.9) 0.8 (0.45, 1.1) 0.042Fibrinogen (mg/dL) 521.5 (405, 682) 474 (381.5, 616.5) 0.482D-Dimers (ng/mL) 1130 (580, 1910) 380 (315, 2120) 0.136Ferritin (μg/L) 677 (324, 978) 432 (229, 1337) 0.727LDH (U/L) 388 (241, 569) 184 (159, 371.5) 0.042CPK (U/L) 100 (70, 151.5) 118 (75, 174.5) 0.787PO2/FiO2 260 (156, 342) 400 (397, 464) <0.001Length of hospital stay 7 (4, 14) 2 (2, 9) 0.136Outcome (dead/alive) 6/19 0/5 0.553TABLE 2: Demographic and laboratory values in COVID-19 positive patients with versus withoutchest infiltrates on CXRCOVID-19 patients based on the presence of chest infiltrations. Values are presented as median (25th, 75th percentile). CXR: chest X-ray, WBC:white blood cells, CRP: C-reactive protein, LDH: lactate dehydrogenase, CPK: creatine phosphokinase.In patients with abnormal CXRs who tested negative for SARS-CoV-2, mortality was 18.9% (7 of 37) inpatients with abnormal CXR, compared to 2% (1 of 50) in patients without CXR infiltrations and theobserved difference was highly significant (P=0.009). However, there was no significant difference inhospital length of stay. Demographic and laboratory results in the COVID-19 negative patients withversus without abnormal CXR findings are presented in Table 3. P/F ratio significantly differed between thetwo groups (p<0.01).2021 Velissaris et al. Cureus 13(9): e18114. DOI 10.7759/cureus.18114 3 of 5 Non-COVID-19 patients with abnormal CXR (n=37) Non-COVID-19 patients with normal CXR (n=50) P-valueAge (years) 71 (58, 80) 66.5 (53,80) 0.275BMI 25.5 (23, 31) 25 (2331.5) 0.775Gender (M/F) 27/10 29/21 0.149WBC (K/mL) 10,640 (7490, 15,675) 8515 (7352, 13,647) 0.238Total Lymphocytes (K/mL) 1430 (800, 2050) 1245 (685, 2207) 0.680CRP (mg/dL) 7.06 (1.95, 13.5) 4.50 (2.1, 14.9) 0.990Lactate (mmol/L) 1.10 (0.80, 1.70) 1.29 (0.80, 1.83) 0.419Fibrinogen (mg/dL) 568.5 (372, 684) 569.5 (376, 648) 0.188D-Dimers (ng/mL) 1400 (585, 2510) 1265 (747.5, 3205) 0.843Ferritin (μg/L) 138 (50, 338.5) 186 (59, 482.5) 0.420LDH (U/L) 251 (200.5, 306.5) 235.5 (200, 323) 0.734CPK (U/L) 93 (51, 176) 66.5 (42, 125) 0.139PO2/FiO2 309 (192.5, 392.4) 400 (376, 452) <0.001Length of Hospital Stay 4 (2,7) 3 (2, 5.5) 0.747Outcome (dead/alive) 7/30 1/49 0.009TABLE 3: Demographic and laboratory values in COVID-19 negative patients with and withoutchest infiltrates on CXRNon-COVID-19 patients based on the presence of chest infiltrations. Values are presented as median (25th, 75th percentile). CXR: chest X-ray, WBC:white blood cells, CRP: C-reactive protein, LDH: lactate dehydrogenase, CPK: creatine phosphokinase.DiscussionIn this study, we report that in the setting of hospitalized patients with symptoms of lower respiratory tractinfection suspected with COVID-19, patients with a diagnosis of COVID-19 have a significantly higherproportion of abnormal CXR, compared to those with a diagnosis of non-COVID-19 pneumonia. In addition,we found that irrespective of COVID-19 diagnosis, patients with an abnormal CXR have a lower P/F ratio,which corresponds to increased disease severity. Lastly, in our cohort, there was a significant difference inlaboratory biomarkers (CRP, LDH, lactate) in patients with abnormal CXR compared to patients withoutchest infiltrates, only among the patients with COVID-19.CXR is a fast and cheap diagnostic tool, which can be performed in the majority of patients even in theemergency department with the help of portable X-ray units. Modified radiological scores have been used toevaluate the prognosis of COVID-19 patients [3,4], but due to the lack of specific findings in COVID-19patients, its use is limited [5]. The prognostic capabilities of CXR and its use as a triage tool in non-severeCOVID-19 patients are highlighted in a study by Sempere-Gonzales [6]. Computed tomography is being usedto identify abnormalities in patients with COVID-19, but it is not available in all clinical settings and iscostly compared to CXR [7,8]. Nevertheless, computed tomography findings are related to clinical severityand prognosis, thus making it a useful supplemental tool for patients’ evaluation [9,10]In COVID-19 patients, several changes in commonly used laboratory parameters are described. In the studyby Broman, IL-6 and CRP were the strongest predictors of severity in hospitalized patients with COVID-19 [11], while in another study, it was shown that abnormal levels of neutrophil to lymphocyte ratio (NLR),LDH, d-dimers, CRP, fibrinogen, and ferritin can be identified early on admission COVID-19 and can predictthe severity of the disease [12]. In our study, we identify the presence of combined abnormalities of commonlaboratory parameters and CXR infiltrations in COVID-19 patients. Predictive scores that integrate easilyavailable radiological and laboratory markers could be of great significance in resource-constrained settingsand emergency situations [13].The main limitation of our study is the small number of patients enrolled and that it is a single-center study.Additionally, the exact pathogen was not identified in patients with non-COVID-19 pneumonia, but they2021 Velissaris et al. Cureus 13(9): e18114. DOI 10.7759/cureus.18114 4 of 5were considered and treated as bacterial pneumonia. On the contrary, there were no signs of superimposedbacterial infection in any of the COVID-19 patients in our cohort.ConclusionsIn our study, the presence of abnormalities in the CXR of COVID-19 and non-COVID-19 patients wasassociated with reduced P/F ratio and increased in-hospital mortality. As CXR is a routine examination in allpatients with symptoms of lower respiratory tract infection, it can be a significant measure of diseaseseverity, especially in resource restrained settings and emergency situations. Multi-center studies areneeded to identify the prognostic value of the combined presence of abnormal laboratory parametersand CXR abnormalities in COVID-19.Additional InformationDisclosuresHuman subjects: Consent was obtained or waived by all participants in this study. Ethics Commitee of theGeneral University Hospital of Patras issued approval 102/09-03-2021. Animal subjects: All authors haveconfirmed that this study did not involve animal subjects or tissue. Conflicts of interest: In compliancewith the ICMJE uniform disclosure form, all authors declare the following: Payment/services info: Allauthors have declared that no financial support was received from any organization for the submitted work.Financial relationships: All authors have declared that they have no financial relationships at present orwithin the previous three years with any organizations that might have an interest in the submitted work.Other relationships: All authors have declared that there are no other relationships or activities that couldappear to have influenced the submitted work.References1. Tay MZ, Poh CM, Rénia L, MacAry PA, Ng LF: The trinity of COVID-19: immunity, inflammation andintervention. Nat Rev Immunol. 2020, 20:363-74. 10.1038/s41577-020-0311-82. Guan WJ, Ni ZY, Hu Y, et al.: Clinical characteristics of Coronavirus disease 2019 in China . N Engl J Med.2020, 382:1708-20. 10.1056/NEJMoa20020323. Balbi M, Caroli A, Corsi A, et al.: Chest X-ray for predicting mortality and the need for ventilatory support inCOVID-19 patients presenting to the emergency department. Eur Radiol. 2021, 31:1999-2012.10.1007/s00330-020-07270-14. Adarve Castro A, Díaz Antonio T, Cuartero Martínez E, García Gallardo MM, Bermá Gascón ML, DomínguezPinos D: Usefulness of chest X-rays for evaluating prognosis in patients with COVID-19 [PREPRINT](Utilidad de la radiografía de tórax para evaluar el pronóstico de pacientes con). Radiologia. 2021,10.1016/j.rx.2021.05.0025. Kerpel A, Apter S, Nissan N, et al.: Diagnostic and prognostic value of chest radiographs for COVID-19 atpresentation. West J Emerg Med. 2020, 21:1067-75. 10.5811/westjem.2020.7.488426. Sempere-González A, Llaneras-Artigues J, Pinal-Fernández I, et al.: Radiography-based triage for COVID-19in the emergency department in a Spanish cohort of patients [PREPRINT]. Med Clin (Barc). 2021,10.1016/j.medcli.2021.05.0137. Fred HL: Drawbacks and limitations of computed tomography: views from a medical educator . Tex HeartInst J. 2004, 31:345-348.8. Alsharif W, Qurashi A: Effectiveness of COVID-19 diagnosis and management tools: A review . Radiography(Lond). 2021, 27:682-7. 10.1016/j.radi.2020.09.0109. Zhao W, Zhong Z, Xie X, Yu Q, Liu J: Relation between chest CT findings and clinical conditions ofCoronavirus disease (COVID-19) pneumonia: a multicenter study. AJR Am J Roentgenol. 2020, 214:1072-7.10.2214/AJR.20.2297610. Ai T, Yang Z, Hou H, et al.: Correlation of chest CT and RT-PCR testing for Coronavirus disease 2019(COVID-19) in China: a report of 1014 cases. Radiology. 2020, 296:E32-40. 10.1148/radiol.202020064211. Broman N, Rantasärkkä K, Feuth T, et al.: IL-6 and other biomarkers as predictors of severity in COVID-19 .Ann Med. 2021, 53:410-2. 10.1080/07853890.2020.184062112. Lagadinou M, Salomou EE, Zareifopoulos N, Marangos M, Gogos C, Velissaris D: Prognosis of COVID- 19:changes in laboratory parameters. Infez Med. 2020, 28:89-95.13. Huespe I, Carboni Bisso I, Di Stefano S, Terrasa S, Gemelli NA, Las Heras M: COVID-19 Severity Index: apredictive score for hospitalized patients [PREPRINT]. Med Intensiva (Engl Ed). 2020,10.1016/j.medin.2020.12.0012021 Velissaris et al. Cureus 13(9): e18114. DOI 10.7759/cureus.18114 5 of 5

Evaluation of admission chest X-ray findings in patients with respiratory infection during the COVID-19 pandemic

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Evaluation of admission chest X-ray findings in patients with respiratory infection during the COVID-19 pandemic

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