Computed tomography findings in 3,557 COVID-19 infected children: a systematic review

Introduction

Coronavirus disease 2019 (COVID-19), the newly emerged highly contagious disease that appeared in December 2019, is caused by the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) agent. SARS-CoV-2 is a member of the genus Betacoronavirus within the subfamily Coronavirinae (1). COVID-19 emerged in December 2019 in Wuhan, China, and since then, millions of people worldwide have contracted the disease. As of June 4, 2021, more than 172 million people worldwide have been infected with SARS-CoV-2, with more than 3,700,000 deaths related to this disease (2).

The common symptoms that the majority of patients with COVID-19 present with include cough (either with or without sputum), shortness of breath, fever, sore throat, chills, nasal congestion, fatigue or myalgia, dizziness, muscle pain, arthralgia, weakness, dyspnea, and chest tightness (3-7). However, the disease can also present with several atypical manifestations, such as acute coronary syndrome, myocardial dysfunction, acute kidney injury, or neurological, gastrointestinal, bleeding, and thrombotic or cutaneous symptoms (8-12). Although it was assumed in the early stages of the outbreak that the disease was uncommon among children, the number of cases of infected children has since increased significantly (13).

The diagnosis of COVID-19 is confirmed using the gold standard reverse transcriptase polymerase chain reaction (RT-PCR) test that has a quite good sensitivity (91%) along with a very high specificity (100%) for the diagnosis of COVID-19 (14-17). However, computed tomography (CT) scans also has been used in the diagnostic workup of patients who are suspected of having COVID-19, especially in cases of false-negative RT-PCR test results, when RT-PCR is not available, or when the results are delayed (18).

Since the emergence of the disease, a vast number of articles have been published that focus on the pathogenesis, clinical manifestations, laboratory and imaging findings, and treatment of the disease, as well as several systematic reviews that summarize all the related findings. However, as the pandemic continues, new aspects of the disease are being discovered, and there is still a need for further investigations to be performed. While several systematic review articles have examined the imaging features of COVID-19 in adults (19-29), only a few have performed such an analysis of child cases (30-33). The aim of this review was to compile the existing data on the CT characteristics of COVID-19 disease in children. Simultaneously, the clinical and laboratory findings of child COVID-19 cases will be summarized based on the articles reviewed.

Materials and methods

Literature search and study selection

We searched seven databases, including PubMed, Embase, Scopus, and Web of Science core collection databases (four databases, including SSCI, SCIE, AHCI, and ESCI) to find the original articles on the use of chest CT for the detection of COVID-19 in children published in English between December 1, 2019, and May 7, 2021.. We used the following queries: “corona virus” OR coronavirus OR “corona-virus” OR “covid_19” OR “covid-19” OR “SARS-cov-2” OR ncov* OR 2019-nCov OR novelcorona* AND child* OR pediat* OR paediat*OR neonate* OR newborn* OR infant* OR adolescen* AND CT OR “computed tomography” OR “computed-tomography” OR tomogram OR “CT-scan” OR “CT scan” OR “Computer Assisted Tomography” OR “Computer-Assisted Tomography” OR “Computerized Tomography.”

We also searched the reference lists of the included studies to identify additional articles.

Eligibility criteria

The inclusion criteria were as follows: (I) the age of the study population was 0–18 years; (II) COVID-19 infection was confirmed in patients using RT-PCR; (III) CT findings were mentioned, and (IV) the article was published in English. Articles without available English full text, that did not mention CT findings, that did not confirm cases of COVID-19 using PCR, and that reported CT findings only in adult patients were excluded. We did not exclude case reports or studies that included both adult and pediatric populations separately to widen our research scope.

Data extraction and quality assessment

Three independent radiologists extracted the data from the full text of all articles into a database (Excel; Microsoft, Redmond, WA). Disagreements were solved by discussion and consensus. Duplicates were deleted. Extracted data included the following factors: bibliography (such as the first author’s name, country, journal name), demographics (sample size, gender distribution, average age, exposure history), symptoms (asymptomatic, fever, sputum, runny nose, abdominal pain, etc.), lab data, and chest CT findings, including the following aspects: (I) lesion distribution (bilateral lung, peripheral, central, involved lobes); (II) lesion morphology (nodular, patchy, parenchymal band); (III) density of the lesions(GGO, consolidation, GGO mixed consolidation, crazy paving, halo sign); and (IV) accompanying signs (pleural effusion, pericardial effusion, lymphadenopathy).

Statistical analysis

For categorical variable, we used frequency and percent and to estimate the 95% confidence interval we used binomial distribution. STATA 11 (Stata Corp., College Station, TX) used for analysis.

Results

Study selection

From the initial search of four databases (PubMed, Embase, ISI, and Scopus) that was performed on May 7, 2021, 2574 unique articles were identified (Figure 1). In addition, 18 articles were added after hand searching of the reference lists of previous systematic reviews after deleting duplicates, 1,681 records remained. Through screening the abstracts, reviews, meta-analyses, irrelevant studies, and studies in languages other than English were removed. Out of these articles, 1,013 records were retained for full-text review, and 81 studies met the inclusion criteria and were included in our analysis. A quality assessment of included articles was performed using the NIH Quality Assessment Tool (Table 1), and most of the articles were scored as fair according to these criteria.

Figure 1 Preferred reporting system for systematic reviews and meta-analyses (PRISMA) flow diagram. Diagram represents the review process and selection of included studies. Adopted from Moher et al. (doi.org/10.1371/journal.pmed.1000097)©2009, under terms of Creative Commons Attribution 4.0 International License (creativecommons.org/licences/by/4.0/legalcode).

Table 1 NIH quality assessment
Full table

Characteristics of included studies

The basic and bibliographic characteristics of the included papers are summarized in Table S1. The interested reader can find them in a supplementary appendix online. This review included 81 articles published in English that in total included 3,557 pediatric patients. Of these, 2 were from the USA (46,86), 1 was from Kore (58), 1 was worldwide (70), 5 were from Turkey (66,72,92,99,107), 7 were from Iran (43,69,71,95,97,104,106), 2 were from Italy (87,112), 2 were from Brazil (96,114), 1 was from Egypt (85), 1 was from the Latin America (108), 1 was from France (105), 2 was from the UAE (91,93), 1 was from Portugal (113) and the remained 55 studies were from China. All of them were published in 2020-21.

Among the 81 studies, 14 investigated children and adults (36,38,40,59,79,89,91,93,94,96,99,101,107,108), and the rest of them studied only children. There were 14 case reports (37,44,45,54,55,57,58,63,85,87,95,97), 8 case series (46,47,75,81,82,90,104,108), 2 letters (77,79), 1 brief report (36), 2 case-control study (49,101), 2 cohort studies (66,70), 1 observational (84) and 5 observational cohort study (80,93,99,100,113) and the remained articles were descriptive studies. A total of 84 variables were extracted for this review.

Demographic characteristics of the patients

The demographic characteristics and the clinical and laboratory findings are summarized in Table 2. Of the 3,557 cases, 1,926 (54.1%) were male, and 1,610 (45.2%) were female. In addition, 1,387 (39%) of these children had a recent exposure history to COVID-19-infected patients. The age of participants ranged from less than 1 month to 18 years. One study reported the median BMI of the patients, which was 17.4 (49).

Table 2 Demographic characteristics and clinical and laboratory findings
Full table

Among the 81 included papers, 27 studies reported accompanying comorbidities(such as immunocompromised status (post-transplant, immunosuppressive medication, malignancies), congenital heart diseases, long-term respiratory conditions (asthma, bronchial hyperreactivity, aspiration syndrome, preterm chronic lung disease), allergic rhinitis, atopic dermatitis, drug allergy, chronic kidney disease, neurological disorders, cardiovascular disease, liver cirrhosis, leukemia, polyarthritis, X-linked lymphoproliferative (XLP). According to these studies, 613 (17.2%) of the patients had underlying predisposing conditions. Moreover, co-infection with other agents [including CMV (Cytomegalovirus), influenza B, influenza A, mycoplasma, and Respiratory Syncytial Virus (RSV)] was detected in 36 (1%) of the patients (42,50,74,78,99).

Clinical features of the patients

Among all 3,557 cases, 658 patients (18.5%) were asymptomatic. Among the symptomatic patients, the main clinical features were fever, cough, dyspnea, gastrointestinal symptoms (including diarrhea, vomiting, nausea, abdominal pain, lack of appetite, and intussusception), sore throat, accounting for 1,104 (31%), 1,018 (28.6%), 313 (8.8%), 261 (7.3%), 175 (4.9%), and 171 (4.8%) cases, respectively. Fatigue was present in 92 (2.6%) of the cases, headache in 39 (1.1%), and lethargy or dizziness in 26 (0.7%).

Laboratory findings

Forty-four articles with a total of 986 cases reported the total white blood cell count, and it was decreased in 184 (18.6%) and increased in 125 (12.7%) of the patients. Forty-four studies with a total of 1,266 patients reported the lymphocyte count, and it was lower than normal in 207 (16.3%) and high in 229 (18%) of the patients. Only 36 articles reported CRP, which was normal in 921 (72.4%) of cases and increased in 351 (27.6%). O₂ saturation in breathing room air was mentioned in 20 papers for 208 patients, and it was decreased in 54 cases (26%).

Chest CT imaging features

Among the 3,557 Corona virus-infected patients, 2,202 have undergone a chest CT scan; 66% [1,451] of them had some abnormalities on their chest CT scans, while 34% [751] had normal chest CT scans. Among the 1,451 children with abnormal chest CT findings, the site of involvement was recorded in 63 articles, and around 53.6% (549/1,024) of cases had bilateral lung involvement, and the other 46.4% (475/1,024) had unilateral lung involvement. Based on these reports, the right lung was involved slightly more frequently than the left lung. When the left lung was involved, there was a predilection for lower lobe involvement, and when the right lung was involved, the infection sites in the order of frequency were the right lower, right upper, and right middle lobes. Thirty-three studies with a total of 352 cases reported the distribution of lung involvement, and summarizing these findings revealed that 81.2% had a peripheral pattern, about 15.6% had a diffuse pattern, and about 3.1% had a peribronchovascular pattern.

Regarding the type of lung lesions in children with COVID-19 infection and abnormal chest CT findings, ground glass opacities were observed in 54.7% (794/1,451) and consolidation in 10.2% (149/1,451) of the patients. Other common features were halo sign, discrete pulmonary nodules, interstitial abnormalities or reticulations, and vascular thickening shadows in 7.4%, 2.6%, 9.7%, and 1.7% of the patients, respectively. Based on these publications, a crazy paving pattern (0.6%), pleural effusion (2.7%), and lymphadenopathy (0.5%) were not common features in COVID-19-infected children (Table 3).

Table 3 Frequency of chest CT findings of COVID-19 in children (chest CT imaging features)
Full table

Additional findings

We also extracted the mean time between the onset and diagnosis of Corona virus infection in children. A total of 28 articles with a total of 1,139 cases recorded this item, and it ranged from 1.5 to 10 days.

Discussion

During the global spread of the coronavirus infection throughout the world, it was found that the previous epidemiologic knowledge that suggested relatively few cases were seen among children was not accurate (58) and many children were diagnosed infected with clinical manifestations of the disease such as dry cough, fever, dyspnea, tachypnea, and sore throat in addition to corresponding laboratory (e.g., changes in white blood cell count, lymphocyte count, CRP, O₂ saturation, …) and imaging findings including ground glass opacities and consolidations, and also less common features of halo sign, discrete pulmonary nodules, interstitial abnormalities or reticulations, and vascular thickening shadows.

Although RT-PCR is considered the gold standard tool for the diagnosis of COVID-19 infection, some studies have discussed the diagnostic role of chest CT scans. For example a study conducted by Ai and colleagues is the first study thus far to determine the diagnostic value of chest CT in patients with COVID-19. The authors analyzed 1,014 patients with suspected COVID-19, and all these patients underwent both chest CT scan and nucleic acid test (RT-PCR). Of the 1,014 patients, 601 (59%) had positive RT-PCR results, and positive chest CT findings were detected in 97% of the 601 patients. With RT-PCR as the diagnostic reference for COVID-19, their results depicted that the sensitivity, specificity, positive predictive value, and negative predictive value of CT were 97%, 25%, 65% and 83%, respectively. The high false positive of CT scan according to this study could be due to extensive overlap between imaging findings of corona virus lung infection and other kinds of pneumonia. Although as Ai et al. pointed out, their results may only be valid in epidemic areas with high pre-test probability for this disease and for milder cases, the chest CT positive rate will be much lower (25,115,116); however, it seems crucial to identify the imaging patterns of lung involvement and to determine the role of chest CT scan in pediatric infected patients.

In the current review, we evaluated the chest CT findings in 2,202 children, from 81 articles, with a positive COVID-19 RT-PCR test result (ages ranged from less than one month to 18 years), as well as the demographic characteristics and clinical and laboratory manifestations. This is the largest systematic review to date to survey all of these items in COVID-19-infected children. According to the quality assessment of included articles using the NIH Quality Assessment Tool, 20 studies were of poor quality due to imperfect clinical and CT scan data, and the others were scored as fair or good.

We also included 10 case reports conducted during the first months of epidemic when it was believed that children were not susceptible to COVID-19. In addition, most of the studies were descriptive, but we included 7 cohort studies, which provided information about the use of CT scans during the follow-up of pediatric COVID-19-infected patients; although most radiologists believe that CT scan, because of its relatively high radiation dose, should not be used for follow-up in corona virus infected children and considering the much lower radiation effect, serial chest radiographs can be used for monitoring of the disease regression or progression (117).

In this review, 55 articles were from China, representing 1,760 cases, and 26 articles from other countries, representing 1,797 cases. These values regarding the latest Worldometer statistics of total cases of about 90,973 in China, which is a small percentage of the total worldwide cases compared to that of several other countries, indicates that Chinese authors have made more of an effort to report on pediatric patients with the corona virus infection. Thus, it would be of value if other countries with a high number of total cases, such as the USA, India, and Brazil, would publish investigations on the corona virus infection in children. A Multilanguage systematic review of local databases would be of great help in this area. In this review, 18.5% of COVID-19-infected children were asymptomatic, while for adult patients, this rate has been reported to be about 13.3% (115,116) to 15.6% (118). However, we need also to emphasize the background where these data were collected. Most studies were conducted in tertiary hospitals, and the results from hospital-based patients usually do not represent the patients in general population, where the proportion of asymptomatic virus carriers and mild cases must be much higher (116).

According to Wang et al., COVID-19 patients commonly have symptoms of fever, fatigue, dry cough, dyspnea, chest tightness, nasal congestion, runny nose or other upper respiratory symptoms (119). In our review, the most prevalent symptoms in pediatric patients were fever and cough, in 35.0% and 31.8% of patients, respectively, while 9.2% of patients had dyspnea. These manifestations are nearly similar to the most common symptoms reported in adults, although the frequencies of fever and cough were higher in adult, and about 80% and 60%, respectively (8). Gastrointestinal findings, including diarrhea and abdominal pain, were fairly common in children with COVID-19 infection (12%), possibly because during the pathogenesis of COVID-19, the SARS-CoV-2 virus attaches to the ACE2 receptor, which is highly expressed in the GI tract (29).

We evaluated the laboratory findings of COVID-19-infected children, and the most common findings were decreased numbers of leukocytes and lymphocytes, in 18.4% and 15.4% of patients respectively, whereas in adults, these findings are more frequently reported (41%) (120). Increased WBC and lymphocyte counts are rare findings in adult patients (1–2%) (26), but they were reported in 12.7% and 18.1% of pediatric patients, respectively. Overall, normal CRP was more prevalent in children (72.4%) than in adults (13–44%) (26,29).

Based on these studies, 34% of COVID-19-infected children had normal chest CT scans, in contrast to only 2% of infected adults (26). The most common finding in the chest CT scans of the pediatric patients with COVID-19 was GGO without consolidation (54.7%), indicating that the patients were in the early stage of the disease or the lesions had started to heal (121). The second most common feature in the chest CT scans of the patients was consolidation (10.2%), and progression to consolidation indicates that the immune system of the patient is not strong enough to defeat the virus, potentially increasing the risk of pulmonary fibrosis (121). Furthermore, a consolidative pattern might be indicative of a more severe disease (19). The prevalences of these two features in children were slightly lower than those reported in adult patients; a review by Wan et al. reported rates of 86% and 47% for GOO and consolidation, respectively, and a review by Vieeto Ojha et al. reported rates of 50.2% and 24% for GGO and consolidation, respectively (21,29).

Other reported lesions in the chest CT scans of COVID-19-infected children were interstitial abnormalities or reticulation, halo sign, vascular thickening shadows, and pulmonary nodules, in 9.7%, 7.4%, 1.7%, and 2.6% of patients, respectively. Among these, halo sign has not been reported in adults, and the other patterns has been reported more frequently in adult patients (9–27%) (21,26,29). A crazy paving pattern, a feature of the severe involvement of the lungs, was not found as frequently as it is in adult patients, as it was reported in only 0.6% of pediatric cases in our review versus reported rates of 12%, 15%, and 19.5% in adults (21,26,29). Pleural effusion and lymphadenopathy are rare findings in chest CT scans for both children and adult patients, with rates of 2.7% and 0.5%, respectively (21,26).

In our review, around 549 (37.8%) of cases had bilateral lung involvement, and the other 475 (32.7%) had unilateral lung involvement. In adults, however, bilateral disease is much more common than a unilateral pattern, with rates of 80% and 20%, respectively (26); this is consistent with the milder symptoms of disease observed in the pediatric age group. In children, the distribution of the disease in the lungs is mostly peripheral, which is similar to the distribution seen in adults (26,29).

Some CT scan findings that have been detected in adult patients were rare or not seen in children in our review. For example, Roncon et al. analyzed 7,178 patients with COVID-19 (mean age 60.4 years) and reported that 14.7% of hospitalized patients had PE (or pulmonary thrombosis) (122), but based on our review, PE was not seen in the chest CT scans of pediatric patients.

Generally in our review, we noticed that the CT findings of COVID-19 are mild in most of the pediatric population, especially in comparison to adult patients. So, as we need to keep the patients’ radiation exposure as low as possible, particularly in children who are much more sensitive than adults to the induction of cancer by radiation, the application of CT scan as a diagnostic tool may be unjustified among regions with low COVID-19 prevalence (119). Considering the radiation exposure exists for chest CT exams (WHO guideline mentions a typical effective dose of 3.5 mSv for a chest CT in a 10-year-old child) (123) and thanks to the improvements in technical aspects of performing RT-PCR for detection of COVID-19 infected cases, it seems that performing chest CT scan should be limited to individual cases that its benefits outweigh the risks such as selected suspected cases where RT-PCR tests have been negative more than once (119), suspected cases with severe symptoms or when the CT results are supposed to affect the treatment plan.

One of the weak points of our review was that the number of published studies reporting chest CT scan findings in COVID-19-infected children was not very large, the patient populations in the included studies were not very diverse, and most of them had a small sample size. In addition, the majority of the studies were retrospective and descriptive in nature. Another limitation was that the timing of the CT scan was not the same among the studies; for example, in one study, it was done on the first day that clinical symptoms manifested, and in another, it was obtained several days later. In this review, we found that the reporting template of the CT scan findings was not identical among studies. In many articles, ambiguous terms were used, or the site and expanse of the lesions were not clear. Furthermore, a diagnosis of coronavirus infection based on a chest CT scan is dependent on the radiologist’s experience. In most of the articles, the severity of the illness and the imaging and laboratory findings were not recorded separately for each patient, so it was not possible to assess the correlation between the disease severity and pattern of chest CT scan findings.

Moreover, in this review, we included studies with CT scan findings for children who had positive RT-PCR test results. Thus, considering the fact that the median false-negative rate of RT-PCR for the detection of coronavirus infection is about 10.1% (124), there might have been some children with flu-like symptoms, negative RT-PCR test results, and imaging findings indicating coronavirus infection in their chest CT scans, possibly increasing the risk of bias in interpreting the chest CT scan findings.

Conclusions

CT scan plays a pivotal diagnostic role in patients suspicious of COVID-19 that their PCR tests failed to show positive results and their disease is severe and life-threatening. However, as the overwhelming majority of COVID-19 positive children only show mild CT scan findings and CT results possibly do not affect their treatment, given the risk of radiation exposure, CT seems unjustifiable in children and could be replaced by CXR in most patients except for individual cases when its benefits outweigh the risks.

Acknowledgments

We sincerely appreciate the support and assistance of Dr. Zeinab Shateri Amiri throughout her contribution in a part of data analysis.

Funding: None.

Footnote

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://dx.doi.org/10.21037/qims-20-1410). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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