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Clinical and Laboratory Follow-up After Hospitalization for COVID-19 at an Italian Tertiary Care Center

Clinical and Laboratory Follow-up After Hospitalization for COVID-19 at an Italian Tertiary Care... Downloaded from https://academic.oup.com/ofid/article/8/3/ofab049/6128632 by DeepDyve user on 09 March 2021 applyparastyle “fig//caption/p[1]” parastyle “FigCapt” Open Forum Infectious Diseases BRIEF REPORT and an intensive level of treatment, being at higher risk of severe Clinical and Laboratory Follow-up complications, such as septic shock, thromboembolic events, Aer H ft ospitalization for COVID-19 at and acute kidney injury [5]. Initial reports are emerging about the persistence of a sig- an Italian Tertiary Care Center nificant symptom burden in the aer ft math of recovery from 1,2, 1 1 1 2 Michele Spinicci, Iacopo Vellere, Lucia Graziani, Marta Tilli, Beatrice Borchi, 2 2 1 3 acute COVID-19; this phenomenon has been called “long Jessica Mencarini, Irene Campolmi, Leonardo Gori, Laura Rasero, 1,4 1,5 1,6 Francesco Fattirolli, Iacopo Olivotto, Federico Lavorini, COVID” [6–8]. More insight about the short- and long-term 1,6, 1,2, 1,2 Niccolò Marchionni, Lorenzo Zammarchi, and Alessandro Bartoloni ; for the consequences of SARS-CoV-2 infection is essential to prop- Careggi Post-acute COVID-19 Study Group erly inform follow-up programs for patients who experienced Department of Experimental & Clinical Medicine, University of Florence, Florence, Italy, Infectious and Tropical Diseases Unit, Careggi University and Hospital, Florence, Italy, symptoms of COVID-19 [9]. An earlier clinical review within 3 4 Department of Health Science, University of Florence, Florence, Italy, Cardiac Rehabilitation 5 4–8 weeks postdischarge has been recommended, at least in pa- Unit, Careggi University Hospital, Florence, Italy, Cardiomyopathy Unit, Careggi University Hospital, Florence, Italy, and Department of Cardiothoracovascular Medicine, Careggi tients who experienced more severe symptoms [10]. In Tuscany, Hospital, Florence, Italy Italy, a comprehensive 12-month follow-up, including multidis- ciplinary evaluations according to disease severity and patient We evaluated 100 postacute coronavirus disease 2019 (COVID- characteristics, is guaranteed to all individuals diagnosed with 19) patients a median (interquartile range) of 60 (48–67) days SARS-CoV-2 infection [11]. aer ft discharge from the Careggi University Hospital, Italy. Eighty-four (84%) had at least 1 persistent symptom, irrespec- In this paper, we report the results of the first step of the fol- tive of COVID-19 severity. A considerable number of hospital low-up program for postacute COVID-19 patients discharged readmissions (10%) and/or infectious diseases (14%) during the from Careggi University Hospital, Florence, Italy, consisting postdischarge period were reported. of a clinical and biochemical assessment 8 weeks aer h ft ospital Keywords. COVID-19; follow-up; sequelae, SARS-CoV-2; discharge. long-term. METHODS On December 31, 2019, the world received the first notice of a Since May 20, 2020—soon after the end of the epidemic phase— cluster of atypical pneumonia cases due to a novel coronavirus, an outpatient service dedicated to the follow-up of postdischarge later named severe acute respiratory syndrome 2 (SARS-CoV-2) COVID-19 patients has been active at the Careggi University [1]. Twelve months later, nearly 90 million cases of coronavirus Hospital, Florence, Italy, in accordance with the program of the disease 2019 (COVID-19) have been reported worldwide, with Tuscany Region. Several specialists from different disciplines almost 2 million deaths [2]. are involved with this program, including infectious diseases Clinical presentation can be variable, ranging from SARS- specialists, pulmonologists, cardiologists, immunologists, and CoV-2 asymptomatic carriers to life-threatening and fatal dis- physiotherapists. ease. The most common symptoms include fever, cough, and All patients discharged from the hospital were oer ff ed a clin- shortness of breath. Musculoskeletal symptoms, such as my- ical visit. Exclusion criteria were (i) patients discharged for more algia, joint pain, headache, and fatigue have also been reported, than 10 weeks; (ii) patients unable to attend the visit because of as well as enteric symptoms (abdominal pain, vomiting, and hospitalization or residents in care facilities; (iii) patient refusal. diarrhea), anosmia, and dysgeusia [3, 4]. Critically ill patients Data on subjects’ death aer di ft scharge were collected. oen r ft equire prolonged hospital stay, mechanical ventilation, Data on previous hospital admissions were retrieved from electronic medical records. Disease severity was classified as mild, moderate, severe, and critical, according to World Health Received 15 December 2020; editorial decision 25 January 2021; accepted 28 January 2021. Organization (WHO) definitions [12]. A detailed postdischarge *The members of the Careggi Post-acute COVID-19 Study Group are listed in the Acknowledgments. clinical history was collected through a standardized question- Correspondence: Michele Spinicci, MD, Dipartimento di Medicina Sperimentale e Clinica, naire focused on persistence of symptoms potentially related Largo Brambilla 3, 50141, Firenze, Italy (michele.spinicci@unifi.it). to recent SARS-CoV-2 infection. Symptom count included any Open Forum Infectious Diseases 2021 © The Author(s) 2021. Published by Oxford University Press on behalf of Infectious Diseases self-reported symptom persisting at the time of the follow-up Society of America. This is an Open Access article distributed under the terms of the Creative visit. Postdischarge symptoms resolved before the visit were Commons Attribution-NonCommercial-NoDerivs licence (http://creativecommons.org/licenses/ by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any not considered in the count. The symptom inventory question- medium, provided the original work is not altered or transformed in any way, and that the naire used for the study is shown in the Supplementary Data. work is properly cited. For commercial re-use, please contact journals.permissions@oup.com DOI: 10.1093/ofid/ofab049 Moreover, hospital readmissions and postdischarge infections BRIEF REPORT • ofid • 1 Downloaded from https://academic.oup.com/ofid/article/8/3/ofab049/6128632 by DeepDyve user on 09 March 2021 Table 1. Baseline Characteristics and Data on COVID-19-Related were ascertained by medical record review, or, alternatively, Hospitalization of the Studied Population (n = 100 Patients) they were self-reported and supported by all available medical documentation. A full physical examination was performed. Baseline Characteristics Total (n = 100) Laboratory tests included complete blood count, coagula- Gender female, No. (%) 41 (41) tion profile, serum biochemical tests and serum inflammatory Age, y markers, and arterial blood gas test. Median (IQR) 67.5 (56–78.5) Descriptive analysis was used to illustrate population charac- Range 24–90 Charlson comorbidity index, median (IQR) 3 (1–4) teristics. Categorical variables were evaluated with the Pearson Hypertension, No. (%) 50 (50) chi-square/Fisher exact test, as appropriate. Continuous vari- Diabetes, No. (%) 21 (21) ables were evaluated with the Mann-Whitney test. A multivar- COPD, No. (%) 12 (12) iate logistic regression was performed, aiming to investigate CHD, No. (%) 12 (12) the association between symptom persistence (categorical) and CKD, No. (%) 7 (7) demographic factors (age, gender), comorbidity burden (by Obesity, No. (%) 25 (25) Length of hospital stay, median (IQR), d 16 (8–27) Charlson comorbidity index), and clinical severity of COVID- Time to microbiological cure, median (IQR), d 27 (14–44) 19 (as per WHO classification). Treatments, No. (%) Antiretrovirals (LPV/r, DRV/c) 76 (76) Patient Consent Statement Hydroxychloroquine 88 (88) Data collection was approved by the local ethics committee Remdesivir 9 (9) (17104_oss). Patient consent was obtained. The study was Immune-modulators 48 (48) High-dose steroid (≥1 mg/kg 6-MP) 26 (26) performed in accordance with the ethical principles of the Antibiotics 49 (49) Declaration of Helsinki and with the International Conference ICU admission, No. (%) 31 (31) on Harmonization Good Clinical Practice guidelines. Highest oxygen supplementation, No. (%) No support 13 (13) Standard oxygen therapy 33 (33) RESULTS High flow nasal cannulae 7 (7) Noninvasive ventilation 26 (26) Between May 20 and August 26, 2020, 178 patients were potentially Mechanical ventilation 21 (21) eligible for the 8-week follow-up review, of whom 71 presented at COVID-19 severity (WHO), No. (%) least 1 exclusion criterion (41 residents of health care facilities, 7 Mild 9 (9) patients readmitted to the hospital, 3 already followed by other Moderate 32 (32) outpatient services, 20 refused or did not answer). In addition, 7 Severe 12 (12) patients died after discharge. One hundred patients (41% female; Critical 47 (47) Follow-up timing, median (IQR) median age [interquartile range {IQR}], 67.5 [56–78.5] years) at- Days since symptoms onset 82 (70–101) tended the postdischarge follow-up visit. Baseline characteristics Days since hospital discharge 60 (48–67) and data on the COVID-19-related hospitalization of the 100 pa- Days since microbiological cure 50 (36–66) tients are reported in detail in Table 1. In brief, 12/100 (12%) and Abbreviations: CHD, coronary heart disease; CKD, chronic kidney disease; COPD, chronic 47/100 (47%) experienced severe and critical COVID-19, respec- obstructive pulmonary disease; COVID-19, coronavirus disease 2019; LPV/r, lopinavir/ ritonavir; DRV/c, darunavir/cobicistat; ICU, intensive care unit; IQR, interquartile range; tively; the median hospital length of stay (IQR) was 16 (8–27) days, WHO, World Health Organization. with 31/100 (31%) admitted to the intensive care unit (ICU). Most Time from the first positive to the first negative nasopharyngeal swab. of the evaluated subjects received antiretrovirals (76/100, 76%) and/or hydroxychloroquine (88/100, 88%). Immune-modulator (11%), hair loss (8%), and impaired hearing (6%), were also drugs (such as tocilizumab and ruxolitinib) and high-dose steroids reported. Other neurological disorders included mental con- (methylprednisolone equivalent ≥1 mg/kg/d) were used in 48/100 fusion (10%), peripheral neuropathies (5%), and vertigo (3%). (48%) and 26/100 (26%) cases, respectively; 90/100 (90%) required Furthermore, 4% of patients had psychological symptoms, such oxygen supplementation, including high-flow nasal cannulae as anxiety and depression (Figure 1). (7/100, 7%), noninvasive ventilation (26/100, 26%), and mechan- e p Th ersistence of symptoms was not associated with ical ventilation (21/100, 21%). COVID-19 severity (83% vs 85% in patients with mild/mod- At the time of the follow-up visit, a median (IQR) of 60 (48– erate vs severe/critical disease, respectively; P = .807) or with 67) days aer h ft ospital discharge, 84/100 (84%) had at least 1 ICU admission (84% vs 84% in ICU- vs non-ICU-admitted pa- persistent symptom, and 36/100 (36%) reported >2 symptoms. tients, respectively; P = .981) or with length of hospital stay (16 e Th more frequent symptoms were fatigue (46%), dyspnea vs 13.5 days in patients with and without persistent symptoms, (30%), insomnia (26%), anosmia (20%), and dysgeusia and palpitation (15%). Unusual symptoms, such as visual disorders respectively; P = .559) (Table 2). 2 • ofid • BRIEF REPORT Downloaded from https://academic.oup.com/ofid/article/8/3/ofab049/6128632 by DeepDyve user on 09 March 2021 Likewise, no statistical difference was observed between pa- respiratory failure (pO2 < 60 mmHg). Fifteen patients (15/100, tients with and without symptom persistence by gender, fre- 15%) were discharged with long-term oxygen therapy (LTOT), quency of comorbidities (including hypertension, diabetes, 5 of whom (5/100, 5%) were still on LTOT at the time of the chronic obstructive pulmonary disease, coronary heart disease, follow-up visit (2 were already on LTOT before SARS-CoV-2 chronic kidney disease, and obesity), or median Charlson co- infection). morbidity index. By multivariate analysis, only age was asso- DISCUSSION ciated with an increased risk of symptom persistence (odds ratio, 1.09 for each 1-year increase; 95% CI, 1.02–1.16) (data We analyzed clinical and laboratory results from follow-up not shown). reviews of 100 COVID-19 patients a median of 60  days after Some patients required hospital readmission (10/100, 10%). hospital discharge. At the time of the visit, a high percentage Causes for hospital readmission included cardiac disease, such of patients (84%) complained of 1 or more persistent symp- as heart failure and myocardial infarction (n = 5), infectious toms. Similar findings have been observed in recent studies, diseases (n = 2), respiratory symptoms (n = 1), and neuro- based on face-to-face reviews or telephone/web surveys, on logic disorders (n = 2). Overall, 14 patients (14%) experi- both COVID-19 inpatient and outpatient populations [6–8, enced an infection during the postdischarge period, including 13–14]. In our study, persistence of symptoms was not related urinary tract infections, skin and soft tissue infections, and to COVID-19 severity, ICU admission, or length of hospital Clostridioides difficile colitis. Nineteen (19%) presented rectal stay. Among demographic and clinical characteristics, only colonization with multidrug-resistant bacteria (vancomycin- increasing age was independently associated with higher risk resistant Enterococcus spp. and/or carbapenem-resistant of SARS-CoV-2 infection sequelae. Moreover, in most cases, Enterobacterales) during the hospital stay, with a higher risk in symptoms were not accompanied by blood test abnormalities, more severe patients (16/59, 27%) in comparison with milder as median values of lymphocyte count, D-dimer, and inflam- cases (3/41, 7%; P = .010), and ICU-admitted patients (11/31, mation markers resulted in range and abnormal results oc- 5%) in comparison with non-ICU patients (8/69, 12%; P = .016) curred in a minority of patients. Fatigue was the most frequent (Table 2). self-reported symptom (46%). Persistent fatigue has been al- No significant alteration was observed in the median values ready reported as a common sequela following SARS-CoV-2 of the blood test (Table 2). In our population, 22% (22/100) infection, raising concern that SARS-CoV-2 has the potential and 14% (14/100) showed persistence of elevated C-reactive to trigger postviral chronic fatigue syndrome, similarly to other protein and ferritin, respectively. Thirteen (13%) patients pre- infectious diseases [15]. In the same study, postviral fatigue was sented high D-dimer values (>1000  ng/mL). None presented associated with female gender and a preexisting diagnosis of Fatigue 46% Dyspnea 30% Insomnia 26% Anosmia 20% Palpitation 15% Dysgeusia 15% Chest pain 12% Cough 12% Visual disorders 11% Mental confusion 10% Diarrhea 9% Hair loss 8% Fever 7% Impaired hearing 6% Neuropatic 5% Myalgia 4% Depression/anxiety 4% Vertigo 3% 0% 5% 10% 15% 20% 25% 20% 35% 40% 45% 50% Figure 1. Persistent symptoms reported among 100 postacute coronavirus disease 2019 patients a median of 60 days after hospital discharge. BRIEF REPORT • ofid • 3 Downloaded from https://academic.oup.com/ofid/article/8/3/ofab049/6128632 by DeepDyve user on 09 March 2021 depression/anxiety, while no correlation was observed with the than concurrent complications of underlying conditions, more in- severity of initial SARS-CoV-2 infection, nor with inflamma- formation about burden and risk factors for COVID-19 patients’ tory biomarker abnormalities. readmission is needed to inform both clinical practice and public e a Th vailable data suggest that chronic sequelae are not lim- health decisions [19–20]. However, postdischarge cardiopulmo- ited to more severe COVID-19 cases. The results of a multistate nary manifestations, such as dyspnea, palpitations, and chest pain, telephone survey in the United States confirmed that return to require careful consideration, especially in elderly patients with baseline health aer C ft OVID-19 can take a long time, even in multiple comorbidities. e w Th ide range of reported symptoms young adults with milder diseases and no chronic conditions reflects the multi-organ involvement of COVID-19, mediated by [13]. Age, female gender, obesity, and burden of comorbidities direct tissue damage, hyperinflammation, and COVID-19-related have been variously identified as predictors of long-term coagulopathy. A number of symptoms reported in our study, like symptom persistence during follow-up assessment performed chemosensory dysfunction, insomnia, mental confusion, and from a few weeks to 6 months aer ac ft ute illness [7 , 16–17]. vertigo, belong to the neuropsychiatric sphere. SARS-CoV-2 tro- Hospital readmission aer a ft n initial COVID-19 hospitalization pism of the central nervous system (CNS), likely due to wide- was experienced in 10% of the patients in our population. A large spread angiotensin-converting enzyme 2 (ACE2) expression in the nationwide US study, including more than 100 000 electronical brain tissue, has been documented [21]. Long-term neurological records of COVID-19 patients’ hospitalizations, found a 9% rate sequelae in patients with previous SARS-CoV-2 infection will be of readmission to the same hospital within 2 months of discharge fully understood only in the coming months, when longitudinal [18]. The odds of hospital readmission increased with age and assessments will be performed. in the presence of chronic conditions, such as chronic obstruc- In addition, several patients complained of unusual symptoms, tive pulmonary disease, heart failure, diabetes, chronic kidney like visual disorders, impaired hearing, and hair loss. Vision and disease, and obesity. In our study, heart failure and other cardiac hearing impairment may be part of peripheral nervous system conditions accounted for half of hospital readmissions within manifestations [22]. A  high frequency of male pattern hair loss the 8-week postdischarge period, including an 82-year-old man among patients hospitalized for COVID-19 has been observed diagnosed with heart failure and referred to the emergency room in Spain, suggesting that androgen expression might be a clue to during the follow-up visit. Moreover, at least 1 case of sudden COVID-19 severity [23]. Although the aforementioned symptoms death due to heart attack was recorded close to the follow-up visit are not life-threatening conditions, they can ae ff ct patients’ overall in a 70-year-old man with a previous history of coronary heart well-being and functional status. disease. Although it is hard to definitively establish whether these Finally, 14% of patients had an infectious event aer di ft scharge. events are due to direct or indirect effects of COVID-19, rather Immune system damage induced by SARS-CoV-2 infection, Table 2. Clinical and Laboratory Findings at Follow-up in a Postacute COVID-19 Population (n = 100 Patients) Total (n = 100), Mild to Moderate Severe to Critical Non-ICU (n = 69), ICU (n = 31), P Persistent Symptoms No. (%) (n = 41), No. (%) (n = 59), No. (%) P Value No. (%) No. (%) Value No 16 (16) 7 (17) 9 (15) .807 11 (16) 5 (16) .981 Yes 84 (84) 34 (83) 50 (85) .342 58 (84) 26 (84) No. of symptoms 0 17 (17) 7 (17) 10 (17) 11 (16) 5 (17) 1–2 47 (47) 16 (39) 31 (53) 30 (43) 17 (59) >2 36 (36) 18 (44) 18 (30) 28 (41) 7 (24) .362 Postdischarge infectious 14 (14) 5 (12) 9 (15) .665 9 (13) 5 (16) .681 diseases Rectal colonization 19 (19) 3 (7) 16 (27) .018 8 (12) 11 (35) .005 Blood Test at Follow-up Reference Values Median Values (IQR) White blood cell, 10 cells per L 4.0–10.0 6.65 (5.38–7.72) Neutrophil count, 10 cells per L 1.5–7.5 3.98 (3.13–5.84) Lymphocyte count, 10 cells per L 0.5–5.0 1.84 (1.47–2.22) Platelet count, 10 cells per L 140–440 239 (194–290) ALT, U/L 10–50 15 (12–21) Creatinine mg/dL 0.7–1.2 0.9 (0.8–1.1) D-dimer, mg/L <500 444 (302–816) C-reactive protein, mg/L 0–5 4 (4–5) Serum ferritin, μg/L 30–400 152 (69–276) Lactate dehydrogenase, U/L 135–225 194 (174–219) Abbreviations: ALT, alanine aminotransferase; COVID-19, coronavirus disease 2019; ICU, intensive care unit; IQR, interquartile range. 4 • ofid • BRIEF REPORT Downloaded from https://academic.oup.com/ofid/article/8/3/ofab049/6128632 by DeepDyve user on 09 March 2021 3. 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Clinical and Laboratory Follow-up After Hospitalization for COVID-19 at an Italian Tertiary Care Center

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Downloaded from https://academic.oup.com/ofid/article/8/3/ofab049/6128632 by DeepDyve user on 09 March 2021 applyparastyle “fig//caption/p[1]” parastyle “FigCapt” Open Forum Infectious Diseases BRIEF REPORT and an intensive level of treatment, being at higher risk of severe Clinical and Laboratory Follow-up complications, such as septic shock, thromboembolic events, Aer H ft ospitalization for COVID-19 at and acute kidney injury [5]. Initial reports are emerging about the persistence of a sig- an Italian Tertiary Care Center nificant symptom burden in the aer ft math of recovery from 1,2, 1 1 1 2 Michele Spinicci, Iacopo Vellere, Lucia Graziani, Marta Tilli, Beatrice Borchi, 2 2 1 3 acute COVID-19; this phenomenon has been called “long Jessica Mencarini, Irene Campolmi, Leonardo Gori, Laura Rasero, 1,4 1,5 1,6 Francesco Fattirolli, Iacopo Olivotto, Federico Lavorini, COVID” [6–8]. More insight about the short- and long-term 1,6, 1,2, 1,2 Niccolò Marchionni, Lorenzo Zammarchi, and Alessandro Bartoloni ; for the consequences of SARS-CoV-2 infection is essential to prop- Careggi Post-acute COVID-19 Study Group erly inform follow-up programs for patients who experienced Department of Experimental & Clinical Medicine, University of Florence, Florence, Italy, Infectious and Tropical Diseases Unit, Careggi University and Hospital, Florence, Italy, symptoms of COVID-19 [9]. An earlier clinical review within 3 4 Department of Health Science, University of Florence, Florence, Italy, Cardiac Rehabilitation 5 4–8 weeks postdischarge has been recommended, at least in pa- Unit, Careggi University Hospital, Florence, Italy, Cardiomyopathy Unit, Careggi University Hospital, Florence, Italy, and Department of Cardiothoracovascular Medicine, Careggi tients who experienced more severe symptoms [10]. In Tuscany, Hospital, Florence, Italy Italy, a comprehensive 12-month follow-up, including multidis- ciplinary evaluations according to disease severity and patient We evaluated 100 postacute coronavirus disease 2019 (COVID- characteristics, is guaranteed to all individuals diagnosed with 19) patients a median (interquartile range) of 60 (48–67) days SARS-CoV-2 infection [11]. aer ft discharge from the Careggi University Hospital, Italy. Eighty-four (84%) had at least 1 persistent symptom, irrespec- In this paper, we report the results of the first step of the fol- tive of COVID-19 severity. A considerable number of hospital low-up program for postacute COVID-19 patients discharged readmissions (10%) and/or infectious diseases (14%) during the from Careggi University Hospital, Florence, Italy, consisting postdischarge period were reported. of a clinical and biochemical assessment 8 weeks aer h ft ospital Keywords. COVID-19; follow-up; sequelae, SARS-CoV-2; discharge. long-term. METHODS On December 31, 2019, the world received the first notice of a Since May 20, 2020—soon after the end of the epidemic phase— cluster of atypical pneumonia cases due to a novel coronavirus, an outpatient service dedicated to the follow-up of postdischarge later named severe acute respiratory syndrome 2 (SARS-CoV-2) COVID-19 patients has been active at the Careggi University [1]. Twelve months later, nearly 90 million cases of coronavirus Hospital, Florence, Italy, in accordance with the program of the disease 2019 (COVID-19) have been reported worldwide, with Tuscany Region. Several specialists from different disciplines almost 2 million deaths [2]. are involved with this program, including infectious diseases Clinical presentation can be variable, ranging from SARS- specialists, pulmonologists, cardiologists, immunologists, and CoV-2 asymptomatic carriers to life-threatening and fatal dis- physiotherapists. ease. The most common symptoms include fever, cough, and All patients discharged from the hospital were oer ff ed a clin- shortness of breath. Musculoskeletal symptoms, such as my- ical visit. Exclusion criteria were (i) patients discharged for more algia, joint pain, headache, and fatigue have also been reported, than 10 weeks; (ii) patients unable to attend the visit because of as well as enteric symptoms (abdominal pain, vomiting, and hospitalization or residents in care facilities; (iii) patient refusal. diarrhea), anosmia, and dysgeusia [3, 4]. Critically ill patients Data on subjects’ death aer di ft scharge were collected. oen r ft equire prolonged hospital stay, mechanical ventilation, Data on previous hospital admissions were retrieved from electronic medical records. Disease severity was classified as mild, moderate, severe, and critical, according to World Health Received 15 December 2020; editorial decision 25 January 2021; accepted 28 January 2021. Organization (WHO) definitions [12]. A detailed postdischarge *The members of the Careggi Post-acute COVID-19 Study Group are listed in the Acknowledgments. clinical history was collected through a standardized question- Correspondence: Michele Spinicci, MD, Dipartimento di Medicina Sperimentale e Clinica, naire focused on persistence of symptoms potentially related Largo Brambilla 3, 50141, Firenze, Italy (michele.spinicci@unifi.it). to recent SARS-CoV-2 infection. Symptom count included any Open Forum Infectious Diseases 2021 © The Author(s) 2021. Published by Oxford University Press on behalf of Infectious Diseases self-reported symptom persisting at the time of the follow-up Society of America. This is an Open Access article distributed under the terms of the Creative visit. Postdischarge symptoms resolved before the visit were Commons Attribution-NonCommercial-NoDerivs licence (http://creativecommons.org/licenses/ by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any not considered in the count. The symptom inventory question- medium, provided the original work is not altered or transformed in any way, and that the naire used for the study is shown in the Supplementary Data. work is properly cited. For commercial re-use, please contact journals.permissions@oup.com DOI: 10.1093/ofid/ofab049 Moreover, hospital readmissions and postdischarge infections BRIEF REPORT • ofid • 1 Downloaded from https://academic.oup.com/ofid/article/8/3/ofab049/6128632 by DeepDyve user on 09 March 2021 Table 1. Baseline Characteristics and Data on COVID-19-Related were ascertained by medical record review, or, alternatively, Hospitalization of the Studied Population (n = 100 Patients) they were self-reported and supported by all available medical documentation. A full physical examination was performed. Baseline Characteristics Total (n = 100) Laboratory tests included complete blood count, coagula- Gender female, No. (%) 41 (41) tion profile, serum biochemical tests and serum inflammatory Age, y markers, and arterial blood gas test. Median (IQR) 67.5 (56–78.5) Descriptive analysis was used to illustrate population charac- Range 24–90 Charlson comorbidity index, median (IQR) 3 (1–4) teristics. Categorical variables were evaluated with the Pearson Hypertension, No. (%) 50 (50) chi-square/Fisher exact test, as appropriate. Continuous vari- Diabetes, No. (%) 21 (21) ables were evaluated with the Mann-Whitney test. A multivar- COPD, No. (%) 12 (12) iate logistic regression was performed, aiming to investigate CHD, No. (%) 12 (12) the association between symptom persistence (categorical) and CKD, No. (%) 7 (7) demographic factors (age, gender), comorbidity burden (by Obesity, No. (%) 25 (25) Length of hospital stay, median (IQR), d 16 (8–27) Charlson comorbidity index), and clinical severity of COVID- Time to microbiological cure, median (IQR), d 27 (14–44) 19 (as per WHO classification). Treatments, No. (%) Antiretrovirals (LPV/r, DRV/c) 76 (76) Patient Consent Statement Hydroxychloroquine 88 (88) Data collection was approved by the local ethics committee Remdesivir 9 (9) (17104_oss). Patient consent was obtained. The study was Immune-modulators 48 (48) High-dose steroid (≥1 mg/kg 6-MP) 26 (26) performed in accordance with the ethical principles of the Antibiotics 49 (49) Declaration of Helsinki and with the International Conference ICU admission, No. (%) 31 (31) on Harmonization Good Clinical Practice guidelines. Highest oxygen supplementation, No. (%) No support 13 (13) Standard oxygen therapy 33 (33) RESULTS High flow nasal cannulae 7 (7) Noninvasive ventilation 26 (26) Between May 20 and August 26, 2020, 178 patients were potentially Mechanical ventilation 21 (21) eligible for the 8-week follow-up review, of whom 71 presented at COVID-19 severity (WHO), No. (%) least 1 exclusion criterion (41 residents of health care facilities, 7 Mild 9 (9) patients readmitted to the hospital, 3 already followed by other Moderate 32 (32) outpatient services, 20 refused or did not answer). In addition, 7 Severe 12 (12) patients died after discharge. One hundred patients (41% female; Critical 47 (47) Follow-up timing, median (IQR) median age [interquartile range {IQR}], 67.5 [56–78.5] years) at- Days since symptoms onset 82 (70–101) tended the postdischarge follow-up visit. Baseline characteristics Days since hospital discharge 60 (48–67) and data on the COVID-19-related hospitalization of the 100 pa- Days since microbiological cure 50 (36–66) tients are reported in detail in Table 1. In brief, 12/100 (12%) and Abbreviations: CHD, coronary heart disease; CKD, chronic kidney disease; COPD, chronic 47/100 (47%) experienced severe and critical COVID-19, respec- obstructive pulmonary disease; COVID-19, coronavirus disease 2019; LPV/r, lopinavir/ ritonavir; DRV/c, darunavir/cobicistat; ICU, intensive care unit; IQR, interquartile range; tively; the median hospital length of stay (IQR) was 16 (8–27) days, WHO, World Health Organization. with 31/100 (31%) admitted to the intensive care unit (ICU). Most Time from the first positive to the first negative nasopharyngeal swab. of the evaluated subjects received antiretrovirals (76/100, 76%) and/or hydroxychloroquine (88/100, 88%). Immune-modulator (11%), hair loss (8%), and impaired hearing (6%), were also drugs (such as tocilizumab and ruxolitinib) and high-dose steroids reported. Other neurological disorders included mental con- (methylprednisolone equivalent ≥1 mg/kg/d) were used in 48/100 fusion (10%), peripheral neuropathies (5%), and vertigo (3%). (48%) and 26/100 (26%) cases, respectively; 90/100 (90%) required Furthermore, 4% of patients had psychological symptoms, such oxygen supplementation, including high-flow nasal cannulae as anxiety and depression (Figure 1). (7/100, 7%), noninvasive ventilation (26/100, 26%), and mechan- e p Th ersistence of symptoms was not associated with ical ventilation (21/100, 21%). COVID-19 severity (83% vs 85% in patients with mild/mod- At the time of the follow-up visit, a median (IQR) of 60 (48– erate vs severe/critical disease, respectively; P = .807) or with 67) days aer h ft ospital discharge, 84/100 (84%) had at least 1 ICU admission (84% vs 84% in ICU- vs non-ICU-admitted pa- persistent symptom, and 36/100 (36%) reported >2 symptoms. tients, respectively; P = .981) or with length of hospital stay (16 e Th more frequent symptoms were fatigue (46%), dyspnea vs 13.5 days in patients with and without persistent symptoms, (30%), insomnia (26%), anosmia (20%), and dysgeusia and palpitation (15%). Unusual symptoms, such as visual disorders respectively; P = .559) (Table 2). 2 • ofid • BRIEF REPORT Downloaded from https://academic.oup.com/ofid/article/8/3/ofab049/6128632 by DeepDyve user on 09 March 2021 Likewise, no statistical difference was observed between pa- respiratory failure (pO2 < 60 mmHg). Fifteen patients (15/100, tients with and without symptom persistence by gender, fre- 15%) were discharged with long-term oxygen therapy (LTOT), quency of comorbidities (including hypertension, diabetes, 5 of whom (5/100, 5%) were still on LTOT at the time of the chronic obstructive pulmonary disease, coronary heart disease, follow-up visit (2 were already on LTOT before SARS-CoV-2 chronic kidney disease, and obesity), or median Charlson co- infection). morbidity index. By multivariate analysis, only age was asso- DISCUSSION ciated with an increased risk of symptom persistence (odds ratio, 1.09 for each 1-year increase; 95% CI, 1.02–1.16) (data We analyzed clinical and laboratory results from follow-up not shown). reviews of 100 COVID-19 patients a median of 60  days after Some patients required hospital readmission (10/100, 10%). hospital discharge. At the time of the visit, a high percentage Causes for hospital readmission included cardiac disease, such of patients (84%) complained of 1 or more persistent symp- as heart failure and myocardial infarction (n = 5), infectious toms. Similar findings have been observed in recent studies, diseases (n = 2), respiratory symptoms (n = 1), and neuro- based on face-to-face reviews or telephone/web surveys, on logic disorders (n = 2). Overall, 14 patients (14%) experi- both COVID-19 inpatient and outpatient populations [6–8, enced an infection during the postdischarge period, including 13–14]. In our study, persistence of symptoms was not related urinary tract infections, skin and soft tissue infections, and to COVID-19 severity, ICU admission, or length of hospital Clostridioides difficile colitis. Nineteen (19%) presented rectal stay. Among demographic and clinical characteristics, only colonization with multidrug-resistant bacteria (vancomycin- increasing age was independently associated with higher risk resistant Enterococcus spp. and/or carbapenem-resistant of SARS-CoV-2 infection sequelae. Moreover, in most cases, Enterobacterales) during the hospital stay, with a higher risk in symptoms were not accompanied by blood test abnormalities, more severe patients (16/59, 27%) in comparison with milder as median values of lymphocyte count, D-dimer, and inflam- cases (3/41, 7%; P = .010), and ICU-admitted patients (11/31, mation markers resulted in range and abnormal results oc- 5%) in comparison with non-ICU patients (8/69, 12%; P = .016) curred in a minority of patients. Fatigue was the most frequent (Table 2). self-reported symptom (46%). Persistent fatigue has been al- No significant alteration was observed in the median values ready reported as a common sequela following SARS-CoV-2 of the blood test (Table 2). In our population, 22% (22/100) infection, raising concern that SARS-CoV-2 has the potential and 14% (14/100) showed persistence of elevated C-reactive to trigger postviral chronic fatigue syndrome, similarly to other protein and ferritin, respectively. Thirteen (13%) patients pre- infectious diseases [15]. In the same study, postviral fatigue was sented high D-dimer values (>1000  ng/mL). None presented associated with female gender and a preexisting diagnosis of Fatigue 46% Dyspnea 30% Insomnia 26% Anosmia 20% Palpitation 15% Dysgeusia 15% Chest pain 12% Cough 12% Visual disorders 11% Mental confusion 10% Diarrhea 9% Hair loss 8% Fever 7% Impaired hearing 6% Neuropatic 5% Myalgia 4% Depression/anxiety 4% Vertigo 3% 0% 5% 10% 15% 20% 25% 20% 35% 40% 45% 50% Figure 1. Persistent symptoms reported among 100 postacute coronavirus disease 2019 patients a median of 60 days after hospital discharge. BRIEF REPORT • ofid • 3 Downloaded from https://academic.oup.com/ofid/article/8/3/ofab049/6128632 by DeepDyve user on 09 March 2021 depression/anxiety, while no correlation was observed with the than concurrent complications of underlying conditions, more in- severity of initial SARS-CoV-2 infection, nor with inflamma- formation about burden and risk factors for COVID-19 patients’ tory biomarker abnormalities. readmission is needed to inform both clinical practice and public e a Th vailable data suggest that chronic sequelae are not lim- health decisions [19–20]. However, postdischarge cardiopulmo- ited to more severe COVID-19 cases. The results of a multistate nary manifestations, such as dyspnea, palpitations, and chest pain, telephone survey in the United States confirmed that return to require careful consideration, especially in elderly patients with baseline health aer C ft OVID-19 can take a long time, even in multiple comorbidities. e w Th ide range of reported symptoms young adults with milder diseases and no chronic conditions reflects the multi-organ involvement of COVID-19, mediated by [13]. Age, female gender, obesity, and burden of comorbidities direct tissue damage, hyperinflammation, and COVID-19-related have been variously identified as predictors of long-term coagulopathy. A number of symptoms reported in our study, like symptom persistence during follow-up assessment performed chemosensory dysfunction, insomnia, mental confusion, and from a few weeks to 6 months aer ac ft ute illness [7 , 16–17]. vertigo, belong to the neuropsychiatric sphere. SARS-CoV-2 tro- Hospital readmission aer a ft n initial COVID-19 hospitalization pism of the central nervous system (CNS), likely due to wide- was experienced in 10% of the patients in our population. A large spread angiotensin-converting enzyme 2 (ACE2) expression in the nationwide US study, including more than 100 000 electronical brain tissue, has been documented [21]. Long-term neurological records of COVID-19 patients’ hospitalizations, found a 9% rate sequelae in patients with previous SARS-CoV-2 infection will be of readmission to the same hospital within 2 months of discharge fully understood only in the coming months, when longitudinal [18]. The odds of hospital readmission increased with age and assessments will be performed. in the presence of chronic conditions, such as chronic obstruc- In addition, several patients complained of unusual symptoms, tive pulmonary disease, heart failure, diabetes, chronic kidney like visual disorders, impaired hearing, and hair loss. Vision and disease, and obesity. In our study, heart failure and other cardiac hearing impairment may be part of peripheral nervous system conditions accounted for half of hospital readmissions within manifestations [22]. A  high frequency of male pattern hair loss the 8-week postdischarge period, including an 82-year-old man among patients hospitalized for COVID-19 has been observed diagnosed with heart failure and referred to the emergency room in Spain, suggesting that androgen expression might be a clue to during the follow-up visit. Moreover, at least 1 case of sudden COVID-19 severity [23]. Although the aforementioned symptoms death due to heart attack was recorded close to the follow-up visit are not life-threatening conditions, they can ae ff ct patients’ overall in a 70-year-old man with a previous history of coronary heart well-being and functional status. disease. Although it is hard to definitively establish whether these Finally, 14% of patients had an infectious event aer di ft scharge. events are due to direct or indirect effects of COVID-19, rather Immune system damage induced by SARS-CoV-2 infection, Table 2. Clinical and Laboratory Findings at Follow-up in a Postacute COVID-19 Population (n = 100 Patients) Total (n = 100), Mild to Moderate Severe to Critical Non-ICU (n = 69), ICU (n = 31), P Persistent Symptoms No. (%) (n = 41), No. (%) (n = 59), No. (%) P Value No. (%) No. (%) Value No 16 (16) 7 (17) 9 (15) .807 11 (16) 5 (16) .981 Yes 84 (84) 34 (83) 50 (85) .342 58 (84) 26 (84) No. of symptoms 0 17 (17) 7 (17) 10 (17) 11 (16) 5 (17) 1–2 47 (47) 16 (39) 31 (53) 30 (43) 17 (59) >2 36 (36) 18 (44) 18 (30) 28 (41) 7 (24) .362 Postdischarge infectious 14 (14) 5 (12) 9 (15) .665 9 (13) 5 (16) .681 diseases Rectal colonization 19 (19) 3 (7) 16 (27) .018 8 (12) 11 (35) .005 Blood Test at Follow-up Reference Values Median Values (IQR) White blood cell, 10 cells per L 4.0–10.0 6.65 (5.38–7.72) Neutrophil count, 10 cells per L 1.5–7.5 3.98 (3.13–5.84) Lymphocyte count, 10 cells per L 0.5–5.0 1.84 (1.47–2.22) Platelet count, 10 cells per L 140–440 239 (194–290) ALT, U/L 10–50 15 (12–21) Creatinine mg/dL 0.7–1.2 0.9 (0.8–1.1) D-dimer, mg/L <500 444 (302–816) C-reactive protein, mg/L 0–5 4 (4–5) Serum ferritin, μg/L 30–400 152 (69–276) Lactate dehydrogenase, U/L 135–225 194 (174–219) Abbreviations: ALT, alanine aminotransferase; COVID-19, coronavirus disease 2019; ICU, intensive care unit; IQR, interquartile range. 4 • ofid • BRIEF REPORT Downloaded from https://academic.oup.com/ofid/article/8/3/ofab049/6128632 by DeepDyve user on 09 March 2021 3. 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