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Saddle pulmonary embolism in the setting of COVID-19 infection: A systematic review of case reports and case series

  • Hassan Choudry , Fateen Ata ORCID logo EMAIL logo , Wanis Ibrahim , Mohammad Omer Rehman Rana , Shoaib Ahmad , Asim Mehmood , Basir Afzaal Gill and Mahammed Khan Suheb
Published/Copyright: June 1, 2023
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Open Medicine
From the journal Open Medicine Volume 18 Issue 1

Abstract

Saddle pulmonary embolism (SPE) is a rare type of pulmonary embolism that can lead to hemodynamic compromise causing sudden deaths. Due to a dearth of large prospective studies in this area, little is known regarding the epidemiology, and prognosis and factors affecting the latter for COVID-19-associated SPE. We aimed to describe COVID-19-associated SPE and quantify and compare mortality and factors affecting mortality among the cases. We included a total of 25 publications with a total of 35 cases. The average age was 45 ± 16.3 years with 11 females and 24 males. Dyspnoea (82.5%), orthopnoea (43.5%), and cough (43.5%) were the most common symptoms, and obstructive shock was present in five (21.7%) patients. The average reported oxygen (O2) saturation was 85.8% ± 11.9 mm Hg. Hypertension (26.1%), diabetes (21.7%), and deep vein thrombosis (21.7%) were the most commonly reported comorbidities. Right heart strain was recognized in seven (30%) patients on electroencephalogram (S1QIIITIII) and 12 (52.2%) patients on echocardiogram. Anticoagulation, thrombolysis, and percutaneous intervention were tried in 21 (91.3%), 13 (56.5%), and 6 (26.1%) cases, respectively. Despite the aggressive management, 2 of 25 (8.7%) patients died in our smaller case report cohort. We conclude that despite aggressive management modalities, the mortality of SPE remains high in COVID-19.

Keywords: saddle pulmonary embolism; SPE; COVID-19; coronavirus disease 2019; SARS-CoV-2; severe acute respiratory syndrome-related coronavirus 2

1 Introduction

Saddle pulmonary embolism (SPE) is a large pulmonary embolism (PE) that straddles the bifurcation of the pulmonary trunk and extends into both the left and right pulmonary arteries. It is a rare type of PE that can cause sudden death. Higher incidences of cardiac arrest, cardiogenic shock, respiratory failure, and mean length of stay (LOS) have all been linked to SPE [1]. Consequently, SPE has historically been considered a condition associated with high mortality. PE-related death has been observed in the range of 1–7.0% in non-SPE patients [2]. SPE has been reported to occur in about 2.6–5.4% of all acute PE patients and is expected to predict poorer outcomes if not treated aggressively [3]. Standard anticoagulation (AC), systemic thrombolysis, catheter-directed thrombolysis and surgical embolectomy are all alternatives for the treatment.

Thrombotic events are one of the common features of coronavirus diseases 2019 (COVID-19) [4]. The underlying pathophysiological mechanisms are complex and involve two distinct mechanisms, namely, thromboembolism and immunothrombosis. The former is characterized by the activation of coagulation cascade due to endothelial cell damage, and the latter is characterized by intense inflammatory and immune reactions causing massive coagulation cascade activations and intense and prolonged fibrin degradation [5,6]. However, understanding this association and treating it promptly are critical for effectively managing this condition. The incidence of PE in COVID is known to be around at least 15% [4]. However, the incidence of SPE in COVID-19 is not widely known and needs further studies for its estimation. Some clinical features denoting severity in SPE, such as obstructive shock and right ventricular (RV) strain pattern, are associated with increased mortality [7]. Mortality in COVID-19 itself has been found to be associated with comorbidity status as well as PE [8]. The overall mortality of SPE in COVID-19 patients has also not been studied systematically in larger studies. More studies are needed on SPE in COVID-19 patients to estimate mortality and factors associated.

Cases of SPE in COVID-19 patients have also been reported with conflicting results concerning treatment success. In our recent systematic review of SPE, we reported that SPE mortality was 4.6% and found that AC, surgical thrombectomy, thrombolysis, and percutaneous treatment significantly increased the odds of survival in SPE patients [9]. In this focused systematic review, we aim to describe SPE in the context of COVID-19 and quantify and compare mortality, and possible factors affecting mortality among the cases.

2 Materials and methods

2.1 Literature search

PubMed, Scopus, and Google Scholar were searched for articles (any date up to February 28, 2022) reporting patients with SPE. Keyword as generated used advanced search function and was (“covid 19”[All Fields] OR “covid 19”[MeSH Terms] OR “covid 19 vaccines”[All Fields] OR “covid 19 vaccines”[MeSH Terms] OR “covid 19 serotherapy”[All Fields] OR “covid 19 serotherapy”[Supplementary Concept] OR “covid 19 nucleic acid testing”[All Fields] OR “covid 19 nucleic acid testing”[MeSH Terms] OR “covid 19 serological testing”[All Fields] OR “covid 19 serological testing”[MeSH Terms] OR “covid 19 testing”[All Fields] OR “covid 19 testing”[MeSH Terms] OR “sars cov 2”[All Fields] OR “sars cov 2”[MeSH Terms] OR “severe acute respiratory syndrome coronavirus 2”[All Fields] OR “ncov”[All Fields] OR “2019 ncov”[All Fields] OR ((“coronavirus”[MeSH Terms] OR “coronavirus”[All Fields] OR “cov”[All Fields]) AND 2019/11/01:3000/12/31[Date - Publication])) AND ((“saddle”[All Fields] OR “saddles”[All Fields]) AND (“pulmonary embolism”[MeSH Terms] OR (“pulmonary”[All Fields] AND “embolism”[All Fields]) OR “pulmonary embolism”[All Fields])). Scopus keywords and google scholar keywords were “COVID-19 AND Saddle Pulmonary Embolism” and “COVID-19 AND Saddle Pulmonary Embolism,” respectively.

2.2 Study selection and data extraction

Retrieved articles from the search strategy were uploaded to Rayyan.AI software for screening. HC and FA screened the articles independently. WI conducted an independent review of the disputed articles for a final decision. The extracted studies were initially screened from the title, abstract, and keywords, followed by a full-length screening.

2.3 Inclusion criteria

Studies published in English, reporting primary patient data (case reports, series, observational retrospective, prospective studies, and clinical trials) regarding SPE in the context of COVID-19 patients, were added to the systematic review.

2.4 Exclusion criteria

Exclusion criteria included studies in languages other than English. In addition, review articles with secondary patient data were excluded.

2.5 Quality assessment

FA and HC assessed the quality of the added studies independently. Case reports and series were assessed using the Joanna Briggs Institute case report appraisal checklist for inclusion in systematic reviews [10].

2.6 Data collection and analysis

Data on demographics, clinical characteristics, clinical observations, diagnostics results, LOS, management, and outcomes were extracted and analyzed. Data were collected in Microsoft Excel 2016, and analysis was performed in R Studio 2022.2.3. Dplyr, psych, and epitools packages were used for analysis in R Studio. We excluded the case series in the inferential statistics as the individual case data for each case were unavailable in these publications. The chi-square test and Mann-Whitney U tests were used where appropriate.

  1. Systematic Review Registration: The protocol has been registered in the International Prospective Register of Systematic Reviews (PROSPERO): CRD42021286270. https://www.crd.york.ac.uk/PROSPERO/display_record.php?RecordID=286270.

3 Results

A total of 25 publications (case reports and series) were identified with 35 cases (Figure 1). The average age was 45.6 ± 16.3 years, with 11 females (31.4%) and 24 males (68.6%). As discussed in Section 2, we included only the case reports for our descriptive and inferential analysis of clinical parameters, observations, diagnostic testing, treatment, and outcome. COVID-19 variant information was not available for any of the publications. All of our included cases, however, correspond to a time period from summer of 2020 to mid-summer of 2021. Hence, it is probable that alpha and delta strains were the most prevalent ones.

Figure 1 The Prisma flow diagram summarizing the inclusion and exclusion of relevant studies.
Figure 1

The Prisma flow diagram summarizing the inclusion and exclusion of relevant studies.

Only four publications mentioned prophylactic AC, despite which patients developed the PE [11–13]. Himwaze et al. in the autopsy study mentioned four patients being on AC prophylactically and still having the thrombotic event [11]. None, except one of the cases, Shazley et al. mentioned COVID-19 vaccination [14].

The basic characteristics of the patients, including clinical presentations, investigations, and treatment modalities, are all listed in Table 1. Dyspnoea (82.5%), orthopnoea (43.5%), and cough (43.5%) were the most common symptoms. Features of obstructive shock were reported in 5 (21.7%) patients. The average reported oxygen (O2) saturation was 85.8% ± 11.9. It was normal (≥94%) only in 2 of 14 patients (14.3%) and <90% in 6 of 14 (42.8%) cases.

Table 1

Clinical characteristics and outcomes of patients with SPE in the setting of COVID-19 infection (N = 35)

Gender Females: 11 (31.4%)
Male: 24 (68.5%)
Age Mean: 45 years
SD: 16.3
Clinical presentations Syncope 4/23 (14.7%)
Dyspnoea 19/23 (73%)
Chest pain 7/23 (29.4%)
Hemoptysis 2/23 (5.9%)
Cough 10/23 (29.4%)
Orthopnoea 10/23 (41.2%)
Unconscious on presentation 0
Lower limb pain 1 (5.9%)
Obstructive shock 5 (14.7%)
OBS Systolic blood pressure Mean: 110.9 ± 26.3  mm Hg
HR Mean: 129 ± 18.6
O2 saturation 85.8 ± 11.8%
Comorbidities Patent foramen ovale 3/23 (13.0%)
Any valvular disorder 2/23 (8.7%)
Diabetes 5/23 (21.7%)
Hypertension 6/23 (26.1%)
Lung disease 3/23 (13.0%)
Chronic kidney disease 1/23 (4.3%)
Malignancy 1/23 (4.3%)
Any comorbidity 10/23 (43.5%)
DVT 5/23 (21.7%)
History of PE 1/23(4.3%)
Diagnostics ECG findings Normal/not mentioned: 9 (39.1%)
Right heart strain (S1Q3T3): 7 (30.4%)
Other findings: 7 (30.4%)
Echocardiogram findings Right ventricular strain: 12 (52.2%)
Normal/not mentioned: 11 (47.8%)
Right heart strain (ECG or echo) Present: 16 (69.6%)
Not present or mentioned: 7 (30.4%)
CTPA Saddle thrombus: 20 (86.9%)
Other findings: 3 (13.1%)
Treatments employed Surgical removal 0
Catheter removal 6 (26.1%)
Thrombolysis 13 (56.5%)
Anticoagulation 21 (91.3%)
IVC filter 1 (4.3%)
Outcome LOS Mean: 9.8 days
SD: 8.9
ICU admissions 15/23 (65.2%)
Outcome (total)* Alive: 21 (61.8%)
Died: 13 (38.2%)
Total: 33 (100%)
Outcome (case reports) Alive: 21 (91.3%); died: 2 (8.7%)
Total: 23 (100%)

*Total outcome includes autopsy studies where all the patients were deceased.

IVC: inferior vena cava; SD: standard deviation; HR: heart rate; LOS: length of stay; ICU: intensive care unit; CTPA: computed tomography pulmonary angiogram; ECG: electrocardiogram; Echo: echocardiogram; DVT: deep vein thrombosis; PE: pulmonary embolism; O2: oxygen.

The most common comorbidities were hypertension present in 6 (26.1%) and diabetes mellitus in 5 (21.7%) cases, followed by lung disease and patent foramen ovale (PFO) in 3 (13.0%) cases each. Deep vein thrombosis (DVT) was reported in five cases (21.7%), with two being bilateral and three unilateral.

Right heart strain pattern on electroencephalogram (ECG) (S1QIII TIII) was identified in seven (30%) patients, while another seven (30%) cases had abnormal ECG with findings other than the RV strain pattern. Echocardiography revealed RV strain in 12 (52.2%) patients. Initial computed tomography pulmonary angiogram (CTPA) revealed SPE in 20 (86.9%) of cases, whereas 8 cases mentioned additional non-SPEs upon imaging.

The average hospital stay was 9.8 ± 8.9 days, with 15 reported admissions to the intensive care unit (ICU). The most common treatment modality was AC, reported in 21 (91.3%) cases, while thrombolysis and percutaneous thrombectomy percutaneous intervention (PCI) were tried in 13 (56.5%) and 6 (26.1%) cases, respectively. Alteplase (r-tpa) and tPA were two reported thrombolytic agents used in six and four cases, respectively. An inferior vena cava filter was reported in one case for recurrent thromboembolism.

The outcome was 2 of 21 (8.7%) deaths in our smaller case report cohort.

3.1 Inferential statistics

Statistical analysis was performed to assess the relationship of outcome with gender, age, clinical presentations, comorbidity status, and diagnostic findings and treatment. We found no statistical difference between any of the variables mentioned earlier in terms of outcome (p > 0.05), as presented in Table 2. Comorbidity status (defined as the presence of either of the following: hypertension, diabetes, chronic kidney disease, lung disease, any valvular disorder, PFO, or history of PE) was also unrelated to the outcome (P = 0.34). The mean age of alive and dead was 45.7 and 61.0 years, respectively, but the difference was statistically insignificant (P = 0.23). Gender also did not influence the outcome in our small cohort (P = 1).

Table 2

Inferential statistics of patients with SPE and COVID-19 based on mortality (N = 24)

Variable Alive (21) vs dead (2) P value
Gender: male vs female 15 vs 1 6 vs 1 1
Syncope 4 vs 0 1
Dyspnea 17 vs 2 1
Chest pain 7 vs 0 0.86
Hemoptysis 2 vs 0 1
Cough 8 vs 2 0.35
Orthopnea 10 vs 0 0.58
Lower limb pain 1 vs 0 1
Obstructive shock 5 vs 0 —
SBP (mm of Hg) 106 vs 174 0.20
O2 saturation 88 vs 57 0.12
Any valvular disorder 2 vs 0 1
Diabetes 4 vs 1 0.90
Hypertension 4 vs 2 0.09
Lung disease 2 vs 1 0.60
Any comorbidity 8 vs 2 0.35
ECG (RV strain) 7 vs 0 0.86
Echo (RV strain) 10 vs 2 0.49
CTPA (SPE) 19 vs 2 1
PCI 4 vs 2 0.09
Thrombolysis 13 vs 0 0.3
Anticoagulation 19 vs 2 1
IVC filter 1 vs 0 1

PCI: percutaneous intervention, IVC filter: inferior vena cava filter, SBP: systolic BP; RV strain: right ventricular strain; SPE: saddle pulmonary embolism.

4 Discussion

Historically, SPE has been reportedly associated with a higher (9.2–65%) in-hospital mortality in multiple studies [1,15] compared with a relatively lower overall mortality of non-SPE cases, which varies from 0.2 to 6% depending on the clinical context [16–20]. Pathak et al. compared outcomes of hospitalizations due to PE in the United States and reported that SPE represented only 0.16% of all PE-related hospitalizations [21]. They reported similar outcomes but higher rates of cardiogenic shock, respiratory failure, thrombolysis, and LOS in the SPE group. Multiple comparative studies have reported similar outcomes in SPE and non-SPE [3,22].

To the best of our knowledge, our study represents the first systematic review of SPE in COVID-19 cases, charting the prevalence of mortality and possible prognostic factors. Our recent systematic review discussed the prognostic factors among SPE cases and found an overall mortality of 4.6% [9]. We report a slightly higher mortality of 8.7% in our current small cohort of patients with SPE in the context of COVID-19, excluding the post-mortem studies for apparent bias.

PE is risk stratified for management decisions and prognostic determination using the PE severity index (PESI), a widely validated risk score [23]. This scale has historically been based on epidemiological variables (age and gender), comorbidity status (cancer, heart failure, and lung failure), as well as vital instability [7]. A simplified PESI later on excluded gender and some of the vitals [24]. In terms of clinical severity, it is classified into high risk (massive), intermediate risk (submassive), and low risk based on hemodynamic instability, demonstration of RV dysfunction on echocardiogram or CTPA, PESI score, and elevated troponins. There is a significant difference in outcomes between these severity classes with massive PE mortality ranging from 20 to 65% and submassive with 5–25% [1,25]. Low-risk PE has been reported to carry a mortality risk of close to 1%. Although hemodynamic instability was not a common feature for most of our patients, RV dysfunction on Echo and Saddle embolus on CTPA was demonstrable in 70 and 86% of patients in our cohort, respectively (Table 1). Almost all of our cases constitute an intermediate risk, as all had a CTPA elucidated defect straddling the bifurcation of vessels, with the exception of five (14%) who presented with hemodynamic instability.

Two of our case series were post-mortem and represented 12 patients in our cohort [11,26]. Mucheleng’anga et al. described 21 cases in a post-mortem case series of COVID-19 patients from Zambia, Africa [26]. They mentioned eight (38%) cases with SPE among their cohort, while details were given for 7, which we eventually included in this study. PE in one form or another (shower, saddle, non-saddle) was diagnosed on autopsy in 17 patients (81%), while the remaining were found to have changes consistent with severe pneumonia. The authors later from the same region presented another case series of 29 cases with 5 (17%) cases of SPE. Because of the nature of these studies and the type of data presented, it was not possible to include these cases in the inferential statistics (Table 3).

Table 3

Available clinical details of all 25 included studies

Sr no. Author Epidemiology, presentations Comorbidities Investigations Treatment Outcome
1 Cristoforo et al. [31] 11 M Nephrotic syndrome Diagnosed on CT, ECG: RV strain Discharged
2 Teklie et al. [32] 20 M Elevation of 50% of complement Heparin infusion, bilateral PA catheter Discharged
3 Molina et al. [33] 23 M Nitric oxide inhalation ECG: Sinus tachy, RBBB, ECHO: RV strain, B/L DVT Thrombolysis (tPA) Alive
4 Atallah et al. [30] 29 M Autism ICU MV, CT angio Thrombolysis (tPA) Discharged
5 Kharazmi et al. [34] 32 M PFO Echo: RVS, TIT, IVC clot Thrombolysis (r-tPA) Discharged
6 Hoilat et al. [35] 32 M CT angiography ICU MV, mechanical embolectomy Discharged
7 Vyas et al. [36] 32 M CT angiography Mechanical thrombectomy
8 Himwaze et al. [11] 33 M with dyspnoea and fever HIV Died (Autopsy)
9 36 M dyspnoea/Abdo pain, abdominal TB Died (Autopsy)
10 47 F saddle emboli, heavy lungs (>1,000 g each), Deep venous thrombosis, and diffuse alveolar damage Died (autopsy)
11 65 M CVA Died (autopsy)
12 70 F Hypertension DVT, thrombosed mesenteric arteries Died (autopsy)
13 Pendower et al. [37] 64 F syncope, SOB, dizziness Old DVT Echo: RVS. Infusion catheter (alteplase) Discharged
CT Angio,
14 Flemming et al. [38] 47 M ECG: Normal Catheter thrombolysis Discharged
Echo: RVS, CT angio
15 Jafari et al. [39] 50 F saddle after 3 days stay in hospital CTPA, AC Discharged
16 Ali et al. [40] 52 F SPE 7 days after discharge ECG: S1Q3T3 r-tPA Discharged
CTPA syncope ICU
Anticoagulation (enoxaparin)
17 Shazley and Alshazley [14] 52 M after J&J vaccine Hypertension, diabetes, obesity Bilateral DVT CTPA ICU MV Death in 1 month
PCI
18 Valencia-Manrique et al. [12] 52 F Diabetes, obesity S1Q3T3 ICU, anticoagulation (enoxaparin)
19 Ismail et al. [41] 52 M with left weakness DVT ECG: bifascular block, Anticoagulation (IV heparin) Recovered
Echo: RV embolus, third-degree AV block,
20 Yu et al. [42] 55 M syncope Hypertension, diabetes Echo: intracardiac shunt, CTPA Catheter-directed thrombolysis Discharged
(t-PA), Anticoagulation (IV heparin)
21 Aaron et al. [43] 56 M DVT Echo: RV strain CTPA ICU MV Discharged
tPA (resolution) Saddle PE again in 1 week: tPA
22 Khurram et al. [44] 61 M End-stage renal disease, OSA, diabetes, CVA, BPH, superior ophthalmic vein thrombosis CTPA ICU Anticoagulation (LMWH) Discharged
23 Bhatt et al. [45] 65 M DVT DVT CTPA Anticoagulation (IV heparin) Discharged
24 Aoi et al. [13] 70 F Hypertension, DM, history of SVT ECG: S1Q3T3 PCI + Cath thrombolysis Died
Echo: RVS
CTPA: CIT
25 Fujikura et al. [46] 77 F DVT, discharged → missed apixaban → dyspnea again CVA, DM, PFO, DVT, history of cancer Echo: RV strain. Anticoagulation (IV heparin) Discharged
CTPA
Re-echo: B/l atrial RA CIT
26 Chang and Segura [47] 43 M CTPA ICU MV Discharged
tPA
Cardiac support
27 Nehme et al. [48] 56 M CTPA multiple Pes, tracheal necrotic flap Thrombolysis (alteplase) Discharged
ICU MV
VAP
28 Namburu et al. [49] 69, ST elevation, Takasubo cardiomyopathy Cath: Takasubo Cardiomyopathy Thrombolysis Discharge
Echo: Enlarged right ventricles, atrial thrombus, CTPA
29 Mucheleng’anga et al. [26] 32 M Headache and diarrhea Died
30 37 M chest pain dyspnoea Died
31 51 M Chest pain and dyspnoea Died
32 20 M Dyspnea and painful legs Died
33 39 F Chest pain Died
34 38 M Died
35 25 F Convulsions DVT Died

DM: diabetes mellitus CVA: cerebrovascular accident, DVT: deep venous thrombosis, CTPA: CT pulmonary angiogram, MV: mechanical ventilation, VAP: ventilation associated pneumonia, Cath: catheterization (Coronary), RV: right ventricle, BPH: benign prostatic hyperplasia, SVT: supraventricular tachycardia, TB: tuberculosis, SOB: shortness of breath.

The proportion of SPE among PE patients has largely been found to be 2–5% [15]. The two autopsy studies we included describe the share of SPE to be ranged from 17 to 38% among all patients who died of COVID [11,26]. It would be prudent to keep in mind the nature of these two studies, which included only the COVID patients who died and hence likely to overestimate the SPE proportion. Similarly, prophylactic AC, which was rare during the first wave of the COVID-19 pandemic and became commonplace later, is also very likely to affect this number [27].

In one of the interesting studies on COVID and PE, Hobohm et al. reported a 1.9% prevalence of PE in hospitalized patients with COVID-19. More than 33% of COVID patients with PE had ICU admission. They also reported a significantly higher case fatality rate in COVID patients with PE vs COVID without PE (28.7% vs 17.7%). Another interesting trend was higher case fatality in COVID and PE patients versus patients with PE without COVID (28.7% vs 12.5%) [8]. In the current systematic review, ICU admission was reported for 15 (76% of smaller cohort) cases, which is much higher but in line with the clinical instability and interventions required for this subset of PE (saddle).

The pathophysiology of PE in COVID is complex and multifactorial. The distinct angiocentric feature of COVID-19 was recognized relatively early in the pandemic [28]. Two distinct mechanisms have been elucidated for the overall pathogenesis of thrombosis in COVID-19. The first mechanism is the classic thromboembolism that arises due to sepsis and endothelial dysfunction, leading to tissue factor expression, thrombosis cascade activation, and finally classic thromboembolism [6]. The second mechanism, somewhat novel, involved micro-thrombosis due to the activation of immune pathways causing severe organ damage in lungs, kidneys, skin (blue toes), and other organs [29]. The latter severe type causing widespread immune-mediated microthrombi was reported to be found in patients on prophylactic AC. We found that three of the publications (with a total of six patients) mentioned PE despite prophylactic AC [11,13,30]. PE, one of the sequelae of the angiocentric activity of the disease, has been found in most COVID-19 patients upon autopsy. The prevalence of any pulmonary thromboembolism in the two autopsy studies in our cohort was 80.9 and 48.3% among those deceased [11,26]. It was also one of the leading causes of death among those.

Treatment modalities in our sample did not affect the outcomes. We believe that this is because of the small number in one group, i.e., the deceased. Our general SPE study earlier recognized that all interventions affected mortality in the SPE. However, we are unsure if this is due to forward or reverse causation, i.e., the severity of SPE (upon presentation) discouraging operators or not allowing enough time for clinicians to perform any intervention [9]. Undoubtedly more studies, clinical trials, in particular, are needed to look at the impact of different treatment modalities on the recovery and outcome of SPE in COVID patients.

Our study has several limitations. The small sample size of our study makes our data less reliable, as the statistical inferences are not generalizable. The types of studies included (case reports and series) and the cases they represented suffer multiple biases, including publication and survival ones. These studies may be a source of selection bias in our sample, something inherent for most systematic reviews, which include these types of studies. Barring the aforementioned limitations, we believe our study is free from any systematic biases. Nevertheless, this is the first systematic review highlighting an important and clinically significant combination of SPE with COVID-19 infection and opening doors to further research on the topic.

5 Conclusion

SPE is relatively common in COVID-19 cases and is associated with high mortality. More extensive data are needed to understand the association between COVID-19 infection and SPE.

Acknowledgments

The publication of this article was funded by the Qatar National Library.

  1. Funding information: This study was not funded.

  2. Author contributions: HC: conceptualization, methodology, data collection, data analysis, data interpretation, literature review, writing original draft, critical review, and revisions in the manuscript; FA: conceptualization, methodology, data collection, literature review, writing original draft, critical review, and revisions in the manuscript; MR, SA, AM, BG, MK: data collection, literature review, and manuscript writing; WI: conceptualization, supervision, manuscript review, and revisions. All authors reviewed and approved the final version of this manuscript.

  3. Conflict of interest: This manuscript is original work and has not been submitted or is not under consideration for publication elsewhere. All the authors have reviewed the manuscript and approved it before submission. The authors declare that they have no competing interest.

  4. Data availability statement: Data sharing not applicable.

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Received: 2023-01-06
Revised: 2023-05-02
Accepted: 2023-05-02
Published Online: 2023-06-01

© 2023 the author(s), published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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  181. A comparative study on the overlapping effects of clinically applicable therapeutic interventions in patients with central nervous system damage
  182. Low intensity extracorporeal shockwave therapy for chronic pelvic pain syndrome: Long-term follow-up
  183. The diagnostic accuracy of touch imprint cytology for sentinel lymph node metastases of breast cancer: An up-to-date meta-analysis of 4,073 patients
  184. Mortality associated with Sjögren’s syndrome in the United States in the 1999–2020 period: A multiple cause-of-death study
  185. CircMMP11 as a prognostic biomarker mediates miR-361-3p/HMGB1 axis to accelerate malignant progression of hepatocellular carcinoma
  186. Analysis of the clinical characteristics and prognosis of adult de novo acute myeloid leukemia (none APL) with PTPN11 mutations
  187. KMT2A maintains stemness of gastric cancer cells through regulating Wnt/β-catenin signaling-activated transcriptional factor KLF11
  188. Evaluation of placental oxygenation by near-infrared spectroscopy in relation to ultrasound maturation grade in physiological term pregnancies
  189. The role of ultrasonographic findings for PIK3CA-mutated, hormone receptor-positive, human epidermal growth factor receptor-2-negative breast cancer
  190. Construction of immunogenic cell death-related molecular subtypes and prognostic signature in colorectal cancer
  191. Long-term prognostic value of high-sensitivity cardiac troponin-I in patients with idiopathic dilated cardiomyopathy
  192. Establishing a novel Fanconi anemia signaling pathway-associated prognostic model and tumor clustering for pediatric acute myeloid leukemia patients
  193. Integrative bioinformatics analysis reveals STAT2 as a novel biomarker of inflammation-related cardiac dysfunction in atrial fibrillation
  194. Adipose-derived stem cells repair radiation-induced chronic lung injury via inhibiting TGF-β1/Smad 3 signaling pathway
  195. Real-world practice of idiopathic pulmonary fibrosis: Results from a 2000–2016 cohort
  196. lncRNA LENGA sponges miR-378 to promote myocardial fibrosis in atrial fibrillation
  197. Diagnostic value of urinary Tamm-Horsfall protein and 24 h urine osmolality for recurrent calcium oxalate stones of the upper urinary tract: Cross-sectional study
  198. The value of color Doppler ultrasonography combined with serum tumor markers in differential diagnosis of gastric stromal tumor and gastric cancer
  199. The spike protein of SARS-CoV-2 induces inflammation and EMT of lung epithelial cells and fibroblasts through the upregulation of GADD45A
  200. Mycophenolate mofetil versus cyclophosphamide plus in patients with connective tissue disease-associated interstitial lung disease: Efficacy and safety analysis
  201. MiR-1278 targets CALD1 and suppresses the progression of gastric cancer via the MAPK pathway
  202. Metabolomic analysis of serum short-chain fatty acid concentrations in a mouse of MPTP-induced Parkinson’s disease after dietary supplementation with branched-chain amino acids
  203. Cimifugin inhibits adipogenesis and TNF-α-induced insulin resistance in 3T3-L1 cells
  204. Predictors of gastrointestinal complaints in patients on metformin therapy
  205. Prescribing patterns in patients with chronic obstructive pulmonary disease and atrial fibrillation
  206. A retrospective analysis of the effect of latent tuberculosis infection on clinical pregnancy outcomes of in vitro fertilization–fresh embryo transferred in infertile women
  207. Appropriateness and clinical outcomes of short sustained low-efficiency dialysis: A national experience
  208. miR-29 regulates metabolism by inhibiting JNK-1 expression in non-obese patients with type 2 diabetes mellitus and NAFLD
  209. Clinical features and management of lymphoepithelial cyst
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  211. ENPP1 ameliorates vascular calcification via inhibiting the osteogenic transformation of VSMCs and generating PPi
  212. Significance of monitoring the levels of thyroid hormone antibodies and glucose and lipid metabolism antibodies in patients suffer from type 2 diabetes
  213. The causal relationship between immune cells and different kidney diseases: A Mendelian randomization study
  214. Interleukin 33, soluble suppression of tumorigenicity 2, interleukin 27, and galectin 3 as predictors for outcome in patients admitted to intensive care units
  215. Identification of diagnostic immune-related gene biomarkers for predicting heart failure after acute myocardial infarction
  216. Long-term administration of probiotics prevents gastrointestinal mucosal barrier dysfunction in septic mice partly by upregulating the 5-HT degradation pathway
  217. miR-192 inhibits the activation of hepatic stellate cells by targeting Rictor
  218. Diagnostic and prognostic value of MR-pro ADM, procalcitonin, and copeptin in sepsis
  219. Review Articles
  220. Prenatal diagnosis of fetal defects and its implications on the delivery mode
  221. Electromagnetic fields exposure on fetal and childhood abnormalities: Systematic review and meta-analysis
  222. Characteristics of antibiotic resistance mechanisms and genes of Klebsiella pneumoniae
  223. Saddle pulmonary embolism in the setting of COVID-19 infection: A systematic review of case reports and case series
  224. Vitamin C and epigenetics: A short physiological overview
  225. Ebselen: A promising therapy protecting cardiomyocytes from excess iron in iron-overloaded thalassemia patients
  226. Aspirin versus LMWH for VTE prophylaxis after orthopedic surgery
  227. Mechanism of rhubarb in the treatment of hyperlipidemia: A recent review
  228. Surgical management and outcomes of traumatic global brachial plexus injury: A concise review and our center approach
  229. The progress of autoimmune hepatitis research and future challenges
  230. METTL16 in human diseases: What should we do next?
  231. New insights into the prevention of ureteral stents encrustation
  232. VISTA as a prospective immune checkpoint in gynecological malignant tumors: A review of the literature
  233. Case Reports
  234. Mycobacterium xenopi infection of the kidney and lymph nodes: A case report
  235. Genetic mutation of SLC6A20 (c.1072T > C) in a family with nephrolithiasis: A case report
  236. Chronic hepatitis B complicated with secondary hemochromatosis was cured clinically: A case report
  237. Liver abscess complicated with multiple organ invasive infection caused by hematogenous disseminated hypervirulent Klebsiella pneumoniae: A case report
  238. Urokinase-based lock solutions for catheter salvage: A case of an upcoming kidney transplant recipient
  239. Two case reports of maturity-onset diabetes of the young type 3 caused by the hepatocyte nuclear factor 1α gene mutation
  240. Immune checkpoint inhibitor-related pancreatitis: What is known and what is not
  241. Does total hip arthroplasty result in intercostal nerve injury? A case report and literature review
  242. Clinicopathological characteristics and diagnosis of hepatic sinusoidal obstruction syndrome caused by Tusanqi – Case report and literature review
  243. Synchronous triple primary gastrointestinal malignant tumors treated with laparoscopic surgery: A case report
  244. CT-guided percutaneous microwave ablation combined with bone cement injection for the treatment of transverse metastases: A case report
  245. Malignant hyperthermia: Report on a successful rescue of a case with the highest temperature of 44.2°C
  246. Anesthetic management of fetal pulmonary valvuloplasty: A case report
  247. Rapid Communication
  248. Impact of COVID-19 lockdown on glycemic levels during pregnancy: A retrospective analysis
  249. Erratum
  250. Erratum to “Inhibition of miR-21 improves pulmonary vascular responses in bronchopulmonary dysplasia by targeting the DDAH1/ADMA/NO pathway”
  251. Erratum to: “Fer exacerbates renal fibrosis and can be targeted by miR-29c-3p”
  252. Retraction
  253. Retraction of “Study to compare the effect of casirivimab and imdevimab, remdesivir, and favipiravir on progression and multi-organ function of hospitalized COVID-19 patients”
  254. Retraction of “circ_0062491 alleviates periodontitis via the miR-142-5p/IGF1 axis”
  255. Retraction of “miR-223-3p alleviates TGF-β-induced epithelial-mesenchymal transition and extracellular matrix deposition by targeting SP3 in endometrial epithelial cells”
  256. Retraction of “SLCO4A1-AS1 mediates pancreatic cancer development via miR-4673/KIF21B axis”
  257. Retraction of “circRNA_0001679/miR-338-3p/DUSP16 axis aggravates acute lung injury”
  258. Retraction of “lncRNA ACTA2-AS1 inhibits malignant phenotypes of gastric cancer cells”
  259. Special issue Linking Pathobiological Mechanisms to Clinical Application for cardiovascular diseases
  260. Effect of cardiac rehabilitation therapy on depressed patients with cardiac insufficiency after cardiac surgery
  261. Special issue The evolving saga of RNAs from bench to bedside - Part I
  262. FBLIM1 mRNA is a novel prognostic biomarker and is associated with immune infiltrates in glioma
  263. Special Issue Computational Intelligence Methodologies Meets Recurrent Cancers - Part III
  264. Development of a machine learning-based signature utilizing inflammatory response genes for predicting prognosis and immune microenvironment in ovarian cancer
https://doi.org/10.1515/med-2023-0724
Keywords for this article
saddle pulmonary embolism; SPE; COVID-19; coronavirus disease 2019; SARS-CoV-2; severe acute respiratory syndrome-related coronavirus 2
Creative Commons
BY 4.0

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  204. Predictors of gastrointestinal complaints in patients on metformin therapy
  205. Prescribing patterns in patients with chronic obstructive pulmonary disease and atrial fibrillation
  206. A retrospective analysis of the effect of latent tuberculosis infection on clinical pregnancy outcomes of in vitro fertilization–fresh embryo transferred in infertile women
  207. Appropriateness and clinical outcomes of short sustained low-efficiency dialysis: A national experience
  208. miR-29 regulates metabolism by inhibiting JNK-1 expression in non-obese patients with type 2 diabetes mellitus and NAFLD
  209. Clinical features and management of lymphoepithelial cyst
  210. Serum VEGF, high-sensitivity CRP, and cystatin-C assist in the diagnosis of type 2 diabetic retinopathy complicated with hyperuricemia
  211. ENPP1 ameliorates vascular calcification via inhibiting the osteogenic transformation of VSMCs and generating PPi
  212. Significance of monitoring the levels of thyroid hormone antibodies and glucose and lipid metabolism antibodies in patients suffer from type 2 diabetes
  213. The causal relationship between immune cells and different kidney diseases: A Mendelian randomization study
  214. Interleukin 33, soluble suppression of tumorigenicity 2, interleukin 27, and galectin 3 as predictors for outcome in patients admitted to intensive care units
  215. Identification of diagnostic immune-related gene biomarkers for predicting heart failure after acute myocardial infarction
  216. Long-term administration of probiotics prevents gastrointestinal mucosal barrier dysfunction in septic mice partly by upregulating the 5-HT degradation pathway
  217. miR-192 inhibits the activation of hepatic stellate cells by targeting Rictor
  218. Diagnostic and prognostic value of MR-pro ADM, procalcitonin, and copeptin in sepsis
  219. Review Articles
  220. Prenatal diagnosis of fetal defects and its implications on the delivery mode
  221. Electromagnetic fields exposure on fetal and childhood abnormalities: Systematic review and meta-analysis
  222. Characteristics of antibiotic resistance mechanisms and genes of Klebsiella pneumoniae
  223. Saddle pulmonary embolism in the setting of COVID-19 infection: A systematic review of case reports and case series
  224. Vitamin C and epigenetics: A short physiological overview
  225. Ebselen: A promising therapy protecting cardiomyocytes from excess iron in iron-overloaded thalassemia patients
  226. Aspirin versus LMWH for VTE prophylaxis after orthopedic surgery
  227. Mechanism of rhubarb in the treatment of hyperlipidemia: A recent review
  228. Surgical management and outcomes of traumatic global brachial plexus injury: A concise review and our center approach
  229. The progress of autoimmune hepatitis research and future challenges
  230. METTL16 in human diseases: What should we do next?
  231. New insights into the prevention of ureteral stents encrustation
  232. VISTA as a prospective immune checkpoint in gynecological malignant tumors: A review of the literature
  233. Case Reports
  234. Mycobacterium xenopi infection of the kidney and lymph nodes: A case report
  235. Genetic mutation of SLC6A20 (c.1072T > C) in a family with nephrolithiasis: A case report
  236. Chronic hepatitis B complicated with secondary hemochromatosis was cured clinically: A case report
  237. Liver abscess complicated with multiple organ invasive infection caused by hematogenous disseminated hypervirulent Klebsiella pneumoniae: A case report
  238. Urokinase-based lock solutions for catheter salvage: A case of an upcoming kidney transplant recipient
  239. Two case reports of maturity-onset diabetes of the young type 3 caused by the hepatocyte nuclear factor 1α gene mutation
  240. Immune checkpoint inhibitor-related pancreatitis: What is known and what is not
  241. Does total hip arthroplasty result in intercostal nerve injury? A case report and literature review
  242. Clinicopathological characteristics and diagnosis of hepatic sinusoidal obstruction syndrome caused by Tusanqi – Case report and literature review
  243. Synchronous triple primary gastrointestinal malignant tumors treated with laparoscopic surgery: A case report
  244. CT-guided percutaneous microwave ablation combined with bone cement injection for the treatment of transverse metastases: A case report
  245. Malignant hyperthermia: Report on a successful rescue of a case with the highest temperature of 44.2°C
  246. Anesthetic management of fetal pulmonary valvuloplasty: A case report
  247. Rapid Communication
  248. Impact of COVID-19 lockdown on glycemic levels during pregnancy: A retrospective analysis
  249. Erratum
  250. Erratum to “Inhibition of miR-21 improves pulmonary vascular responses in bronchopulmonary dysplasia by targeting the DDAH1/ADMA/NO pathway”
  251. Erratum to: “Fer exacerbates renal fibrosis and can be targeted by miR-29c-3p”
  252. Retraction
  253. Retraction of “Study to compare the effect of casirivimab and imdevimab, remdesivir, and favipiravir on progression and multi-organ function of hospitalized COVID-19 patients”
  254. Retraction of “circ_0062491 alleviates periodontitis via the miR-142-5p/IGF1 axis”
  255. Retraction of “miR-223-3p alleviates TGF-β-induced epithelial-mesenchymal transition and extracellular matrix deposition by targeting SP3 in endometrial epithelial cells”
  256. Retraction of “SLCO4A1-AS1 mediates pancreatic cancer development via miR-4673/KIF21B axis”
  257. Retraction of “circRNA_0001679/miR-338-3p/DUSP16 axis aggravates acute lung injury”
  258. Retraction of “lncRNA ACTA2-AS1 inhibits malignant phenotypes of gastric cancer cells”
  259. Special issue Linking Pathobiological Mechanisms to Clinical Application for cardiovascular diseases
  260. Effect of cardiac rehabilitation therapy on depressed patients with cardiac insufficiency after cardiac surgery
  261. Special issue The evolving saga of RNAs from bench to bedside - Part I
  262. FBLIM1 mRNA is a novel prognostic biomarker and is associated with immune infiltrates in glioma
  263. Special Issue Computational Intelligence Methodologies Meets Recurrent Cancers - Part III
  264. Development of a machine learning-based signature utilizing inflammatory response genes for predicting prognosis and immune microenvironment in ovarian cancer
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