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Original Studies

Acute Abdomen and Appendicitis in 1010 Pediatric Patients With COVID-19 or MIS-C: A Multinational Experience from Latin America

Yock-Corrales, Adriana MD*; Lenzi, Jacopo PhD; Ulloa-Gutiérrez, Rolando MD; Gómez-Vargas, Jessica MD*; Antúnez-Montes, Omar Yassef MD§; Rios Aida, Jorge Alberto MD; del Aguila, Olguita MD; Arteaga-Menchaca, Erick MD**; Campos, Francisco MD††; Uribe, Fadia MD††; Hernández Díaz, Roger††; Buitrago, Andrea Parra MD‡‡,§§; Londoño, Lina Maria Betancur MD‡‡; Kozicki, Verónica MD¶¶; Brizuela, Martin MD¶¶; Buonsenso, Danilo MD∥∥,***,†††

Author Information
The Pediatric Infectious Disease Journal: October 2021 - Volume 40 - Issue 10 - p e364-e369
doi: 10.1097/INF.0000000000003240
  • Free

Abstract

Clinical features of coronavirus disease 2019 (COVID-19) in children have resulted in a mild disease in the majority of patients.1 Abdominal pain is one of the most common reasons for child’s assessment in the pediatric emergency departments with over 1,345,000 annual visits in the US in under 15 years of age.2 Acute appendicitis (AA) is the most common abdominal surgical emergency in childhood with an incidence of 1–2 cases per 100,000 children per year between birth and 4 years to 25 cases for every 10,000 children between 10 and 17 years.3 Incidence of AA in children with COVID-19 is unknown, with sporadic publications of small case series.4 Also, surgical outcomes in this pediatric population with severe acute respiratory syndrome coronavirus 2 (SARS CoV-2) needing an abdominal surgery are not well studied.

Antibiotic therapy for uncomplicated appendicitis is an alternative option that can be safely used in selected patients with an increased risk of recurrent appendicitis in 20% of the cases, without increasing the likelihood of perforation.5 In the context of COVID-19, nonoperative management of AA is an alternative to surgery with low failure and complication rates.6

Delayed presentation in patients with AA during the pandemic has been reported, leading to major risk of perforation in younger patients and more complications during hospitalization.7,8 Children with COVID-19 may present with clinical features suggestive of appendicitis/AA in relation to terminal ileitis and it has not been clear whether appendicitis might occur as a complication of SARS-CoV-2 infection.9 Multisystem inflammatory syndrome in children (MIS-C), another entity related to SARS-CoV-2 infection, was also reported as a mimicker of AA.10,11

Since cases are constantly raising worldwide, it is expected that SARS-CoV-2 will circulate still for a long time; therefore, the appropriate management of children with COVID-19 is a priority. While the pandemic only determined a limited direct impact on children, delayed diagnosis of patients with AA and COVID-19 could lead to increased morbidity. Due to the gap in the available literature, we performed a multinational study in Latin America aiming to describe the presentation and possible delays of pediatric patients with AA and COVID-19.

MATERIALS AND METHODS

Study Design and Participants

This study is part of an ongoing independent, unfunded project that aims to provide urgent information on COVID-19 and MIS-C in Latin American children. The project was presented during the first peak in Latin America12 and led to the publication of different papers describing an initial group of 409 children with confirmed COVID-19,1 antibiotic uses in children with COVID-19 or with MIS-C,13 and the impact of sex on disease severity in children.14 For the current study, we aimed to assess the diagnoses of AA in children with COVID-19 or with MIS-C. We implemented the previously used dataset1,12–14 including specific variables for this aim: clinically diagnosed acute abdomen; abdominal ultrasound; abdominal radiograph; complete blood count and C-reactive protein (CRP); surgical findings; culture results from intraoperative specimens. Appendicitis with peritonitis or abdominal abscesses were considered as complicated. These adjunctive data were collected only for children with a clinical diagnosis of appendicitis, since the current emergency situation in Latin America and the burden on health workers, along with the lack of dedicated research resources in our Institutions, did not allow a comprehensive data collection for all children. The remaining variables were collected for all children and are those previously used and included: age, gender, symptoms, imaging, underlying medical conditions, need for hospital and neonatal intensive care unit/pediatric intensive care unit (PICU) admission, respiratory and cardiovascular support, other viral coinfections, drugs used to treat COVID-19, development of MIS-C and type of organ involvement, and outcome. SARS-CoV-2 infection was defined as a positive polymerase chain reaction (PCR) test on nasopharyngeal swab.

MIS-C due to SARS-CoV-2 was defined according to the Centers for Disease Control and Prevention criteria. The study was reviewed and approved by the CoviD in sOuth aMerIcaN children—study GrOup core group and approved by the ethics committee of the coordinating center and by each participating center (Mexico: COMINVETICA-30072020-CEI0100120160207; Colombia: PE-CEI-FT-06; Peru: No. 42-IETSI-ESSALUD-2020 and Costa Rica: CEC-HNN-243-2020). The study was conducted in accordance with the Declaration of Helsinki and its amendments. No personal or identifiable data were collected during the conduct of this study.

Statistical Analysis

Summary statistics were presented as counts and percentages. Crude comparisons between groups were evaluated with the chi-squared test or Fisher’s exact test, as appropriate. The association of relevant demographic characteristics and clinical factors with the diagnosis of appendicitis was assessed through logistic regression analysis; the effect size of covariates was expressed by odds ratios with 95% confidence intervals (CIs), and the presence of systematic differences (i.e., statistical significance) was assessed using the 2-sided Wald test. Standard errors were adjusted for clustering of patients within hospitals (m = 8). All data were analyzed using Stata version 15 (StataCorp. 2017. Stata Statistical Software: Release 15. College Station, TX: StataCorp LP). The significance level was set at 5%.

RESULTS

Study Population

A total of 1010 children were enrolled: 941 children (93.2%) with COVID-19 and 69 children (6.8%) with MIS-C: Peru (n = 391, 38.7%), Costa Rica (n = 303, 30%), Argentina (n = 260, 25.7%), Colombia (n = 44, 4.4%) and Mexico (n = 12, 1.2%).

The demographic and clinical characteristics of the 1010 study patients, and according to the final diagnosis of appendicitis or not, are summarized in Table 1. Four hundred ninety-four (48.9%) were female. A total of 323 (32%) children were admitted to the hospital and 47 (4.7%) required admission to a PICU.

TABLE 1. - Characteristics of the Study Sample, Overall and by Diagnosis of Appendicitis
Characteristic All (n = 1010) Appendicitis P value
Yes (n = 34) No (n = 976)
n % n % n %
Female sex 494 48.9 13 38.2 481 49.3 0.205
Age group <0.001
 0 yr 202 20.0 0 0.0 202 20.7
 1–2 yr 229 22.7 0 0.0 229 23.5
 3–5 yr 146 14.5 5 14.7 141 14.4
 6–11 yr 259 25.6 22 64.7 237 24.3
 12–17 yr 174 17.2 7 20.6 167 17.1
Delay between onset and diagnosis 0.061
 0–1 d 448 44.4 20 58.8 428 43.9
 2–7 d 469 46.4 14 41.2 455 46.6
 >7 d 93 9.2 0 0.0 93 9.5
Likely index case 0.220
 Parent 290 28.7 14 41.2 276 28.3
 Sibling 14 1.4 0 0.0 14 1.4
 Other 120 11.9 1 2.9 119 12.2
 Unknown 586 58.0 19 55.9 567 58.1
Medical history
 Known history of BCG vaccine 760 75.2 34 100.0 726 74.4 0.001
 Pre-existing medical conditions 133 13.2 7 20.6 126 12.9 0.196
 Immunosuppressants at the time of diagnosis 11 1.1 0 0.0 11 1.1 1.000
 Primary or secondary immunodeficiency 8 0.8 0 0.0 8 0.8 1.000
 Chemotherapy over the last 6 months 8 0.8 0 0.0 8 0.8 1.000
Admitted to the hospital 323 32.0 34 100.0 289 29.6 <0.001
Intensive care during hospital stay 47 4.7 1 2.9 46 4.7 1.000
Symptoms
 Pyrexia (≥38.0/≥100.4°C/°F) 692 68.5 24 70.6 668 68.4 0.791
 Upper respiratory tract infection 468 46.3 3 8.8 465 47.6 <0.001
 Diarrhea and/or vomiting 321 31.8 34 100.0 287 29.4 <0.001
 Lower respiratory tract infection 217 21.5 5 14.7 212 21.7 0.328
 Headache 105 10.4 1 2.9 104 10.7 0.246
 Acute abdomen 42 4.2 33 97.1 9 0.9 <0.001
Chest radiograph 0.257
 Negative 194 19.2 3 8.8 191 19.6
 Positive (pneumonia* and/or ARDS) 93 9.2 4 11.8 89 9.1
 Not performed 723 71.6 27 79.4 696 71.3
Respiratory support
 Oxygen support 118 11.7 5 14.7 113 11.6 0.584
 Mechanical ventilation 31 3.1 1 2.9 30 3.1 1.000
 Continuous positive airway pressure (CPAP) 11 1.1 0 0.0 11 1.1 1.000
 Extracorporeal membrane oxygenation (ECMO) 0 0.0 0 0.0 0 0.0 ·
Administration of inotropes 29 2.9 2 5.9 27 2.8 0.255
Coinfections detected in respiratory samples(s) 15 1.5 1 2.9 14 1.4 0.404
Abdominal surgery 38 3.8 34 100.0 4 0.4 <0.001
Drug administration
 Systemic corticosteroids 90 8.9 2 5.9 88 9.0 0.761
 Intravenous immunoglobulin (IVIG) 60 5.9 3 8.8 57 5.8 0.449
 Hydroxychloroquine 9 0.9 0 0.0 9 0.9 1.000
 Oseltamivir 8 0.8 0 0.0 8 0.8 1.000
 Lopinavir or ritonavir 3 0.3 0 0.0 3 0.3 1.000
 Noncorticosteroid immunosuppressants 3 0.3 0 0.0 3 0.3 1.000
 Favipiravir 2 0.2 0 0.0 2 0.2 1.000
 Remdesivir 2 0.2 0 0.0 2 0.2 1.000
MIS-C diagnosis 0.300
 No 941 93.2 31 91.2 910 93.2
 Yes, with no cardiac or joint involvement 33 3.3 3 8.8 30 3.1
 Yes, with cardiac involvement§ 23 2.3 0 0.0 23 2.4
 Yes, with joint involvement 11 1.1 0 0.0 11 1.1
 Yes, with cardiac and joint involvement§ 2 0.2 0 0.0 2 0.2
 Tocilizumab administration to treat MIS-C 8 0.8 0 0.0 8 0.8 1.000
Current status 0.040
 All symptoms resolved 989 97.9 32 94.1 957 98.1
 Dead 8 0.8 0 0.0 8 0.8
 Still symptomatic 7 0.7 0 0.0 7 0.7
 Long-term sequelae 6 0.6 2 5.9 4 0.4
Country 0.737
 Peru 391 38.7 11 32.4 380 38.9
 Costa Rica 303 30.0 14 41.2 289 29.6
 Argentina 260 25.7 8 23.5 252 25.8
 Colombia 44 4.4 1 2.9 43 4.4
 Mexico 12 1.2 0 0.0 12 1.2
*Forty-five cases of interstitial disease, 31 cases of consolidation, 4 cases of pleural effusion and 13 unspecified diagnoses.
†Three cases of interstitial disease, 3 cases of consolidation and 10 unspecified diagnoses.
‡Eight mycoplasmas, 4 rhinoviruses, 1 cytomegalovirus, 1 Epstein–Barr virus and 1 unspecified virus.
§Ten cases of pericardial effusion, 6 cases of coronary dilatation, 5 cases of myocarditis and 4 cases of “other” cardiac involvement.
¶Mean time from symptom onset to death was 14 ± 8 days, ranging from 3 to 27.
ARDS indicates acute respiratory distress syndrome; BCG, bacillus Calmette–Guérin; COVID-19, coronavirus disease 2019; IgG, immunoglobulin G; MIS-C, multisystem inflammatory syndrome; PCR, polymerase chain reaction; SARS-CoV-2, severe acute respiratory syndrome coronavirus 2.

Forty-two children (4.2%) had a clinical diagnosis of acute abdomen. Of them, 4 (9.5%) were diagnosed with MIS-C and did not undergo surgery. The remaining 38 children (3.8% of the study population) underwent abdominal surgery due to suspected appendicitis, 34 of them (89.7%) had an intraoperative diagnosis of AA, while 4 of them had nonsurgical findings (mesenteric adenitis in 2 cases, and normal abdominal findings in the remaining 2). The 2 children with mesenteric adenitis but no appendicitis who underwent surgery, were eventually diagnosed with MIS-C with myocarditis. Eight children died (0.8%), none of them being diagnosed with appendicitis. Further details are described in Table 1.

Characteristics of Children With Acute Appendicitis

Children with AA were significantly older than those without (P < 0.0001) and did not experience a delay at diagnoses, compared with the other group (Table 1).

Table 2 describes details of the cohort of children with appendicitis and according to the presence of surgical complications or not (peritonitis, abdominal abscesses). Children with complicated appendicitis had more frequently fever (85.7% vs. 60%), intestinal distension on the abdominal radiograph (7.1% vs. none), leukocytosis (85.7% vs. 40%) and high levels of CRP (35.7% vs. 5%), although differences were not statistically significant probably due to the overall low number of children with appendicitis. On multivariate analyses (Table 3), age >5 years was associated with a higher risk of appendicitis (P < 0.001, 95% CI: 4.17–32.83), while the presence of upper respiratory tract symptoms with a reduced risk (P = 0.019, 95% CI: 0.02–0.71).

TABLE 2. - Characteristics of the Study Patients Diagnosed With Appendicitis, Overall and by Presence of Complications
Characteristic All (n = 34) Complicated appendicitis P value
Yes (n = 14) No (n = 20)
n % n % n %
Female sex 13 38.2 5 35.7 8 40.0 0.800
Age group 0.302
 3–5 yr 5 14.7 2 14.3 3 15.0
 6–11 yr 22 64.7 11 78.6 11 55.0
 12–17 yr 7 20.6 1 7.1 6 30.0
Pre-existing medical conditions 7 20.6 1 7.1 6 30.0 0.198
Intensive care during hospital stay 1 2.9 0 0.0 1 5.0 1.000
Symptoms
 Pyrexia (≥38.0/≥100.4°C/°F) 24 70.6 12 85.7 12 60.0 0.141
 Upper respiratory tract infection 3 8.8 1 7.1 2 10.0 1.000
 Lower respiratory tract infection 5 14.7 0 0.0 5 25.0 0.063
 Headache 1 2.9 0 0.0 1 5.0 1.000
 Acute abdomen 33 97.1 14 100.0 19 95.0 1.000
Chest radiograph 0.255
 Negative 3 8.8 1 7.1 2 10.0
 Positive (pneumonia and/or ARDS) 4 11.8 0 0.0 4 20.0
 Not performed 27 79.4 13 92.9 14 70.0
Abdominal ultrasound 0.097
 Appendicitis 4 11.8 0 0.0 4 20.0
 Mesenteric adenitis 2 5.9 0 0.0 2 10.0
 Abdominal distension 1 2.9 0 0.0 1 5.0
 Fluid 1 2.9 0 0.0 1 5.0
 Hepatic abscess 1 2.9 1 7.1 0 0.0
 Not performed 25 73.5 13 92.9 12 60.0
Abdominal radiograph 0.412
 Distended bowel loop 1 2.9 1 7.1 0 0.0
 Not performed 33 97.1 13 92.9 20 100.0
Microbiologic findings 0.328
 Negative 10 29.4 2 14.3 8 40.0
Escherichia coli 4 11.8 2 14.3 2 10.0
E. coli + Enterobacter cloacae 1 2.9 0 0.0 1 5.0
 Not detected 19 55.9 10 71.4 9 45.0
White blood cells 0.008
 ≤15.0 × 109/L 14 41.2 2 14.3 12 60.0
 >15.0 × 109/L 20 58.8 12 85.7 8 40.0
C-reactive protein 0.111
 <100 mg/L 10 29.4 3 21.4 7 35.0
 ≥100 mg/L 6 17.6 5 35.7 1 5.0
 Not detected 18 52.9 6 42.9 12 60.0
Respiratory support
 Oxygen support 5 14.7 1 7.1 4 20.0 0.379
 Mechanical ventilation 1 2.9 0 0.0 1 5.0 1.000
Administration of inotropes 2 5.9 0 0.0 2 10.0 0.501
Coinfections detected in respiratory samples(s) 1 2.9 0 0.0 1 5.0 1.000
Drug administration
 Systemic corticosteroids 2 5.9 0 0.0 2 10.0 0.501
 Intravenous immunoglobulin (IVIG) 3 8.8 0 0.0 3 15.0 0.251
MIS-C diagnosis (no cardiac/joint involvement) 3 8.8 0 0.0 3 15.0 0.251
Current status 0.501
 All symptoms resolved 32 94.1 14 100.0 18 90.0
 Long-term sequelae 2 5.9 0 0.0 2 10.0
Country 0.061
 Peru 11 32.4 5 35.7 6 30.0
 Costa Rica 14 41.2 3 21.4 11 55.0
 Argentina 8 23.5 6 42.9 2 10.0
 Colombia 1 2.9 0 0.0 1 5.0
ARDS indicates acute respiratory distress syndrome; MIS-C, multisystem inflammatory syndrome.

TABLE 3. - Multivariable Logistic Regression Analysis of Appendicitis Diagnosis (n = 1010)
Characteristic Odds ratio P value 95% Confidence interval
Lower bound Upper bound
Sex
 Male Ref.
 Female 0.60 0.067 0.35 1.04
Age group
 ≤5 yr Ref.
 >5 yr 11.71 <0.001 4.17 32.83
Hospitalization
 No Ref.
 Yes, without intensive care 5.07 0.024 1.24 20.71
 Yes, with intensive care 1.29 0.749 0.27 6.15
Pyrexia (≥38.0/≥100.4°C/°F)
 No Ref.
 Yes 2.55 0.289 0.45 14.41
Upper respiratory tract infection
 No Ref.
 Yes 0.13 0.019 0.02 0.71
Lower respiratory tract infection
 No Ref.
 Yes 0.29 0.299 0.03 3.00
Headache
 No Ref.
 Yes 0.15 0.177 0.01 2.36
Chest radiograph abnormalities (pneumonia and/or ARDS)
 No Ref.
 Yes 2.13 0.323 0.48 9.53
Oxygen support, mechanical ventilation and/or CPAP
 No Ref.
 Yes 0.98 0.974 0.27 3.59
Administration of systemic corticosteroids
 No Ref.
 Yes 0.57 0.343 0.18 1.81
MIS-C diagnosis
 No Ref.
 Yes 0.57 0.252 0.22 1.49
Covariates that predict the outcome perfectly (immunosuppressants/immunodeficiency/chemo and diarrhea/vomiting) were excluded from the model.
ARDS indicates acute respiratory distress syndrome; CPAP, continuous positive airway pressure.

DISCUSSION

Abdominal pain is one of the clinical manifestations in children with COVID-19 and the MIS associated with SARS CoV-2 infection. According to available literature, it has been shown that patients with MIS-C could present in up to 30% as an acute abdomen.15–17 To our knowledge, this is the first multinational study assessing the outcomes of AA in children with COVID-19 and MIS-C. We found that a non-negligible percentage of children with COVID-19 or MIS-C presented with the acute abdomen (42 children, 4.2%) and 34 had AA. Interestingly, 4 children underwent surgery without finding surgical reasons for the abdominal pain, suggesting that COVID-19 and MIS-C can both present with acute abdomen and simulate appendicitis. In fact, a recent case series clearly showed that MIS-C can have a similar presentation with acute enteritis or acute abdomen for surgical reasons and the conditions may be misdiagnosed.18

There are reports of case series of pediatric patients with AA during COVID-19 and MIS-C which describe the relationship between this infection and delays in diagnosis and management.4,19,20 In our study, we found a low prevalence of diagnosis of AA (4.2%) but higher than other reported series.21 Gastrointestinal symptoms were present in a third of all COVID-19 patients and present in all patients with the diagnosis of AA. Similar findings were reported by Tullie et al and Meyer et al.19,22

The delay in the approach and treatment of patients with AA implies a higher risk of perforation and complications leading to an increased length of stay.8 However, we did not find that a delay in the diagnosis of appendicitis in these patients was associated with a higher incidence of complications (41.1%). Complications rate in Israel were reported in 22% associated with parental concern in contracting COVID-19 in the hospital, inadequate clinical evaluation and settings for clinical evaluation (telemedicine), and the lack of healthcare worker’s instructions in regard to the time to seek medical advice8

About the management of AA, 81% of our patients underwent surgery as the preferred modality of treatment; this differs from the practice reported in some hospitals that suggest conservative management of patients with the diagnosis of SARS-CoV-2 and acute abdomen.6,7 Some centers have used more conservative approaches for uncomplicated cases of AA in patients with COVID-19, including home care and nonoperative management with antibiotics.23

Reports of patients with AA and MIS-C has been described as part of the clinical features of the inflammatory syndrome.4,22,24 In our study, we found 4 patients with MIS-C and a clinical diagnosis of the acute abdomen who were treated with nonoperative management with no overall complications, suggesting that appendicitis was not the cause of abdominal pain. Interestingly, we also found 4 children who underwent but had not intra-operative findings of appendicitis, suggesting that the inflammatory response was the cause of pain rather than appendicitis. Two of these patients had mesenteric adenitis and were eventually diagnosed with MIS-C, supporting the evidence that AA may be one of the presenting symptoms of MIS-C and the difficulty in distinguishing the 2 conditions.

Our study has some limitations to address. We could not determine the time from diagnosis and the surgical management, limiting the result of the association between delayed treatment and complications. The small number of patients with AA and COVID-19 could be less than the real number of patients with these 2 conditions because a large proportion of children have not been tested with PCR test on nasopharyngeal test due to unavailability of them during certain periods of the pandemic, as may have happened in low-to-middle income countries settings worldwide. Despite these limitations, this study provides the largest overview of AA in children with COVID-19 and MIS-C to date.

In conclusion, our study found that both MIS-C and COVID-19 can present acute abdomen, with or without appendicitis. Further studies are needed to better recognize these cohorts of children and optimize diagnosis and both conservative or surgical treatment.

REFERENCES

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Keywords:

COVID-19; SARS-CoV-2; appendicitis; children

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