key: cord-0769731-p3jd931d
authors: Shi, Guocheng; Huang, Jihong; Pi, Mingan; Chen, Xinxin; Li, Xiaofeng; Ding, Yiqun; Zhang, Hao
title: Impact of early COVID-19 pandemic on pediatric cardiac surgery in China
date: 2020-12-01
journal: J Thorac Cardiovasc Surg
DOI: 10.1016/j.jtcvs.2020.11.074
sha: ec17eed72a3484e57472dd659bc290f792d7fd2a
doc_id: 769731
cord_uid: p3jd931d

Objective This study aimed to provide an insight into the impact of early outbreak of the novel coronavirus disease 2019 (COVID-19) on the care management for patients with congenital heart disease. Methods This study respectively enrolled a cohort of surgical patients (patients undergoing surgery in 2018 [group I], 2019[group II], and 2020 [group III]) and a cohort of follow-up patients (patients having follow-up in 2017 [group A], 2018 [group B] and 2019 [group C]) from 13 children hospitals. Results During the COVID-19 era, there was a significant decrease in total surgical volume and a change in case mix in terms of an increase in the proportion of emergency operations. Decrease in migration scale index was correlated to the decrease in both surgical volume (r=0.64, p=0.02) and outpatient visit volume (r=0.61, p=0.03). There was a significantly higher proportion of patients who had follow-up through the internet or phone in group C (26.4% vs. 9.6% in group B and 8.9% in group A; p< 0.0001). There was no statistical difference in death or rehospitalization among the 3 follow-up groups (p=0.49). There was higher parents’ anxiety score (p < 0.0001) and more utilization of telemedicine (p = 0.004) in group C comparing to group A and B. Conclusion The COVID-19 pandemic has resulted in a considerable decrease in total surgical volume and a change of case mix, which seems to be related to the strict traffic ban. Follow-up through the online medical service appears to be an effective alternative to the conventional method.

The outbreak of novel coronavirus disease 2019 (COVID-19) has enormously 148 strained healthcare systems across the globe [1, 2] . Many hospitals, particularly those in 149 epicenter areas, have curtailed or postponed surgical procedures in an effort to mitigate 150 the disease transmission and preserve the resources to care for the COVID-19 infected 151 patients. In addition, patients' access to routine face-to-face visits are heavily restricted 152 owing to the aggressive actions taken by the local governments. 153

Congenital heart disease (CHD) remains a global public health concern [3] . The 154 majority of patients with CHD require surgical repair, further, a considerable proportion 155 of critically-ill neonates require emergency operations [4] . The ongoing worldwide 156 pandemic has greatly impacted the optimal treatments delivery to patients with CHDs 157 [5, 6] , potentially placing this population at increased risk for adverse outcomes. Of note, 158 postoperative cardiovascular and non-cardiovascular morbidity are common among this 159 subgroup patients, particularly in those with complex CHDs (CCHDs), emphasizing the 160 need for a structured follow-up surveillance [7] . Guidelines [8, 9] have stressed the 161 importance of maximizing optimization of care for surgical patients during the COVID-162 19 era, including appropriate triage of cases as well as resources allocation, tiered 163 precautions, use of telemedicine, and a detailed follow-up program. As management care 164 for CHD requires significant resources and organized regionalional system [10, 11] , 165 understanding how the current pandemic affects the congenital heart surgical program is 166 paramount. 167 J o u r n a l P r e -p r o o f in Wuhan since Jan 22, 2020 [12, 13] . And with the suppression of the outbreak of the new 169 coronavirus disease, there has been a gradual recovery in healthcare provision in most 170 areas since Wuhan lift outbound travel restrictions on April 8, 2020 . In the present study, 171

we recruited 13 participating pediatric cardiac surgery intuitions in China, representing 172 the major children hospitals in the National Association of Pediatric Cardiology and 173

Cardiac Surgery (the annualized case volume in each hospital in this association 174 constitutes more than 60% of the CHD surgeries in the provinces/cities where these 175 hospitals are located). Additionally, these 13 centers were located in the provinces where 176

there was a reportedly considerable number of patients were diagnosed as COVID-19 177

infected. This study sought to evaluate the impact of early COVD-19 outbreak on the 178 congenital heart surgery program and the outcomes of repaired CCHD patients during 179 this peak time when the COVID-19 forced significant changes in medical services in 180

China. 181

This multi-center observational cohort study included 13 pediatric tertiary cardiac 184 centers (Supplemental Figure 1) to survey the running of the CHD surgery as well 185 follow-up program during the COVID-19 pandemic. The Ethics Committee has 186 approved this study and informed consent was obtained. Data including the clinic and 187 surgical information were retrospectively collected. Follow-up data including mortality 188 and unplanned rehospitalization within six months after surgery were retrieved from the 189 follow-up databases. Patients undergoing operations (surgical cohort) were classified 190 discharged alive after surgical repair of CCHD and had follow-up (follow-up cohort) 193

were also classified into three groups. Group A and B respectively refer to patients 194 having follow-up between September.1st and December. 31st in 2017 and 2018; group C 195 refers to patients having follow-up between September 1st, 2019 and January 23rd, 2020. 196 Of note, there was a higher population in group C than group A and B because additional 197 data from January 1st to 23rd, 2020 was collected in group C, tending to better-illustrate 198 the impact of COVID-19. For patients discharged in 2017 and 2018, follow-up data 199 including mortality and unplanned rehospitalization within six months after surgery, 200

were retrieved from the follow-up databases. Elven (2.7%) and 13 (2.9%) patients were 201 lost to follow-up in group A and group B. 202

Baidu migration [14] is an open-source big data project characterizing population 203 migration. Leveraging its location-based services system and Baidu Tianyan system, we 204 obtained the daily migration scale index (MSI) from January 23rd to April 8th in 2020 205

and 2019 of the cities where each recruited center is located. Haodaifu(Good-doctor) 206 is one of the biggest online health services platform, which provide online consult 207 service for patients [16] . The number of network visit for each center from Jan 23rd to 208

April 8th in 2018,2019 and 2020 was obtained from the customer service department as 209 requested. Given the lack of nucleic acid testing outside the epicenter during this study 210 period, each enrolled hospital followed a strict institutional protocol to control the spread 211 of COVID-19, the principle of which included (1) a 14-day quarantine duration before 212 surgery (including patients and their parents) and (2) negative pressure operation room S2). During the 14-day quarantine duration, all patients and their parents were required 215 to keep social distancing in a specific hotel near the hospitals and every-day evaluation 216 was made by specialized stuff. During the hospital admission, clinical evaluation was 217 made on patients and their parents. Additionally, examination including x-ray or 218 computed tomography scan and serologic testing was also required. These principles 219 were in line with the expert-consensus guideline issued by the Chinese Medical 220

Association for Pediatric Surgery [17, 18] and the policy of local Health Bureau in 2020. 221 Due to the impact of COVID-19, follow-up data for children in group C was 222 collected from the parents by phone call and/or social media app (WeChat). We first 223 send questionnaires (Supplemental Table S1 ) to parents or guardians and collect the 224 feedback data. In case of no feedback, we re-contact the parents via phone or WeChat to 225 complete the follow-up. If we are unable to contact the parents or guardian by telephone 226

and WeChat, and cannot obtain follow-up records, this case is considered to be lost to 227 follow-up. Besides, we contact all of the survivors' parents or guardians, asking about 228 the follow-up modes and the degree of family anxiety during the COVID-19 outbreak. 229

The definition of CCHD and detailed types have been previously reported by our group 230 [18] . 231

For the follow-up cohort, the composite endpoint was all-cause mortality and 233 unplanned readmission events during follow-up. All-cause mortality was defined as 234 death from any causes that occurred after discharge. Unplanned readmission was defined 235 as admission to a health-care facility for any unexpected reason during follow-up. The 236

Data normality was tested for each continuous variable. Summary statistics were 

Of the 13 hospitals, 5 hospitals were designated as hospitals to treat pediatric 250 patients with COVID-19. A total of 47 (7.5%) nurses were assigned to support other 251 departments in the same hospital, such as the infectious department or fever clinic while 252 no pediatric cardiologist and surgeon was assigned to support other departments. Only 253 one hospital's congenital heart surgery program subsidiary intensive care unit was 254 requisitioned for the treatment of COVID-19 infected children. There was scarcity of 255 nucleic acid and serologic antibody testing during the study period so that majority of the 256 stuff except those in Wuhan Children's Hospital were not screened with swabs or 257 serologic testing. both emergent and elective surgery during the pandemic was less than those in the last 2 267 years (Table 1, Figure 2 ). There was a change in case mix during the COVID-19 era 268 ( Figure 3A) . First, as a proportion of total surgical volume, there was a relative increase 269 of emergency operations (6.3% in group III vs. 3.1% in group I and 2.9% in group II). During the COVID-19 pandemic, there was a substantial reduction in total number 276 of outpatient visit ( Table 1) . The median number of transshipments received by the 277 centers from other hospitals was 0-1, significantly lower than that in 2019 (p=0.004) 278 (Table 1) Of the 1475 patients in follow-up group, 44 (3%) were lost to follow-up, including 286 11 cases in group A, 13 in group B, and 20 in group C. There was no significant 287 difference in age, weight, and primary diagnosis among the three groups ( Table 2) . 288

A and B (p= 0·019). The median duration of follow-up time in group C was 155 days 290 (IQR,110-180). There was a higher proportion of online or telephone follow-up in group 291 C than in group A and B. There was no difference in cumulative probability of death or 292 unplanned readmission during the first 180 days among the three groups (p= 0.52) 293

( Figure 3B ). The scores of anxiety index of the patients' parents in group C were 3.5 294 times higher than that in group A and B. And the patients' parents from group C had the 295 highest frequency to use phone or internet for follow-up. 296

To our best knowledge, this is the first nationwide multicenter study to investigate 298 the impact of COVID-19 on pediatric congenital heart program. Our main findings 299 include that (1) COVID-19 disease has greatly impacted the perioperative care for CHD 300 patients, including a substantial number of case delay and limited access to routine 301 follow-up hospital visit and (2) tele and network follow-up might be an effective 302 alternative to the conventional hospital visit in terms of potentially mitigating the risk of 303 post-repair adverse outcomes.

of diagnosis and treatment offered by the tertiary center in China was dramatically 306 dropped by 51% during the COVD-19 era [19] . Correspondingly, there was also a 307 substantial decrease in pediatric congenital heart surgery as compared with the same 308 period in 2018 and 2019. Further, as a proportion of total surgical volume, there was a 309 relative increase of emergency operations. Such change in case mix may largely ascribe 310

to the strict restriction placed on each enrolled hospital that elective operation for patients 311 with asymptomatic simple CHDs was not allowed during the COVID-19 era. Further 312 subdivided by the disease category, a significant difference can only be found in those 313 with coarctation of aorta (CoA) and Tetralogy of Fallot (ToF). However; there was a 314 trend for higher percentage of patients in the other categories and failure to find statistical 315 differences may be partly due to the relatively low prevalence of these diseases. Notably, 316

given the regionalization of congenital heart surgery services in China where there is a 317 growing CHD population with limited specialist resources, the majority of CHD patients 318 moved from other cities or rural areas to undergo surgical repair in a few tertiary centers 319 [20] . During the COVID-19 era, such patient transfer was greatly restricted by the travel 320 ban, explaining for the decrease in surgeries, even in emergency cases. Additionally, 321

parents' reluctance to seek care during this pandemic and the 14-day pre-admission 322 quarantine before surgery are other potential impendent to such decrease. Chinese 323 government has implemented aggressive actions [13, 21] to control the spread of COVID-19, 324

including strict control of entering or leaving from cities and rural areas, 325 reducing/shutting down the city public transportation, and inter-city airline or high-speed 326 railways. The decrease in emergent surgery raises substantial concerns. Critical CHDs in which dramatic changes after birth may lead to rapid hemodynamic compromise and 329 preoperative attrition. From the standpoint of clinical practice, there is only a narrow 330 temporal window for these patients and timely life-saving surgical intervention is 331 definitely required. Lack of surgical care in early life potentially poses a big threat to this 332 patient population. 333

Guidelines related to adult patients undergoing cardiac surgery [22] or heart transplant 334 and Society guidance statements [24] have also stressed the necessity of deferring elective 337 surgeries in efforts to (1) control the spreading of COVID-19 and (2) preserve or redirect 338 limited resources and personnel for the treatment of patients infected by COVID-19. 339

Although there was an expected decrease in elective surgery in this cohort, some may still 340 argue that maintaining elective surgery is not appropriate given that the potential harm in 341 terms of COVID-19 transmission would seem extremely high and clearly absolutely 342 unjustified when compared with the benign prognosis associated with deferring elective 343 pediatric cardiac operations. First of all, we should clarify that surgery for patients with 344 asymptomatic simple CHDs was heavily restricted. The elective cases in this study 345 includes some patients with TOF or CoA who presented with relatively stable clinical 346 manifestations, infantile patients with large VSD or complete atrioventricular septal 347 defect (CAVSD) who had a sign of impaired heart function and a history of recurrent 348 repertory infection as well as failure to thrive. Postponing surgery in these patients might 349 result in cyanotic spell and severe heart failure during the waiting time, potentially 350 increasing the perioperative mortality. Actually, the implications of deferred cardiac 351 surgical operations remain unknow [25] , and comprehensive as well as careful risk-benefit 352 evaluation should be made instead of making decision solely based on COVID-associated 353 risks [26] . The policy-makers should not prioritize needs to maximize the number of 354 patients care at the cost of disregarding care for vulnerable individuals [27] . On the other 355 hand, we do recognize that the significance of the potential damage of COVID-19 in 356 patients undergoing cardiac surgery cannot be underestimated. In face of the lack of 357 availability of nucleic acid testing during early COVID-19 outbreak, every elective case 358 as well as their parents must be observed for 2 weeks before surgeries given the rationale 359 that incubation period of COVID-19 is generally within 14 days following exposure. 360

According to the results, resource scarcities and the phenomenon of medical system 361 breakdown were less common. For instance, resources in cardiac intensive care unit and 362 the ECMO facilities were not allocated to those infected cases in majority of the recruited 363 hospitals. And only a very small portion of doctors/nurses were assigned to assist the care 364 management for patients infected by COVID-19, which is in line with a recent report that 365 a small fraction of pediatric cardiologists from 56 U.S. centers are reassigned to provide 366 clinical services outside their scope of practice [6] . There may be several explanations. 367

First, the study period can be considered as an early phase in which resources were 368 relatively plentiful as compared with the peak phase [28] and majority of the hospitals were 369 not at the epicenter. Second, pediatric patients constitute relatively a small portion of 370 cases infected by COVID-19 as compared with adult patients [29] . Thus, there was a lower 371 burden of hospitalized patients with COVID-19 in children's hospital. However, these 372 results should be interpreted with caution because as this pandemic continues to a peak time, postponing the elective surgery after careful patient triage should undoubtedly be 374 advocated in efforts to preserve the scarce resources. Of note, although there was a 375 substantial decrease in blood donation during the COVID-19 era, it did not appear to be a 376 main reason for the decrease in surgical volume given the liberal use of priming without 377 blood and blood salvage in congenital heart surgery [30] . 378

Preoperative and postoperative nucleic acid testing are both important because a 379 recent case report found that COVID-19 infection was confirmed on postoperative day 13 380 in a patient undergoing Fontan operation. There was a lack of enough testing kits at the 381 early period of COVID-19 outbreak, and it was not until April 24th, 2020 can the nucleic 382 acid testing be uniformly performed in China [31] . Hence, majority of the patients in this 383 cohort did not undergo regular preoperative and postoperative testing. Although we had 384 taken strict methods to try to control the spread of COVID-19 in patients undergoing 385 congenital heart surgery in this series, we cannot rule out the possibility that there may be 386 asymptomatic carrier because preoperative nucleic acid testing for COVID-19 was not 387 routinely performed in patients and their parents. We do recognize the significance of the 388 potential damage of COVID-19 in patients undergoing cardiac surgery, however; as 389 aforementioned, the balance between postponing or curtailing surgery and potentially 390 putting the vulnerable individuals in deterioration of some specific congenital heart 391 diseases requires a second ethical consideration. There was still a high overall surgical 392 volume performed during the COVID-19 era in this series. There are several potential 393 rationales and reasons for our relatively aggressive attitude towards performing surgery 394 for those who may have a high risk of mortality and morbidity during the waiting time. Orchestrated follow-up mechanism is crucial to the patients undergoing complex 416 congenital heart surgery [33] . In this study, the aforementioned traffic control, social 417 distancing policy, and parents' anxiety in being infected by COVID-19 were associated First, data regarding the number of neonates born with CHD during the study period 441 cannot be obtained so that detailed information regarding neonatal patients who died from a lack of healthcare cannot be made. It is possible that lack of access to timely 443 surgical intervention in some neonates with critical CHDs may result in an increased 444 mortality. Second, we lack information about the patients who potentially require surgical 445 interventions during the COVID-19 era so that the association between their parent' s 446 psychological factors and the decrease in surgical volumes cannot be identified. Third, 447

we only follow-up the patients via telephone or social media app during the COVID-19 448 era so that we cannot definitely verify the death or unplanned readmission in group C. 449

were both national children's medical center so that there were more patients coming 451 from other areas to seek treatments for CHD in these 2 hospitals. There may be variation 452 in institutional management care (e.g., surgical experiences, post-repair intensive care) 453 which may bias the results. Fifth, further study is required to obtain more robust data (e.g., The main findings of this study include: (1) The COVID-19 pandemic has resulted in a 634 substantial decrease in total surgical volume as well as a redistribution of the case mix; (2) 635

Online follow-up care strategy appears to be effective during the COVID-19 era. Our 636 results provide a platform for further study of better serving CHD patients in terms of 637 patient triage, tiered precautions and optimizing allocation of resources during the 638 COVID-19 era. CHD, congenital heart disease. 639 Values are n (%) or median (IQR). *p values compare values across all three groups. The GAD-7 score is calculated by assigning scores of 0, 1, 2, and 3, to the response categories of 'not at all,' 'several days,' 'more than half the days,' and 'nearly every day,' respectively. Scores of 5, 10, and 15 represent cut points for mild, moderate, and severe anxiety, respectively. 

Hospitalized Patients With 2019 Novel Coronavirus-Infected Pneumonia in Wuhan

Congenital heart disease: a global public health concern

Prevalence and number of children 495 living in institutional care: global, regional, and country estimates

COVID-19: crisis management in congenital heart surgery

Changes in contact 501 patterns shape the dynamics of the COVID-19 outbreak in China

Chronic disease burden 504 after congenital heart surgery: a 47-year population-based study with 99% follow-up

Resource allocation and decision making for pediatric and congenital cardiac 508 catheterization during the novel coronavirus SARS-CoV-2 (COVID-19) pandemic: A 509

multi-institutional perspective

Adult 511 (p=0.52). CHD, congenital heart disease, F/U, follow-up. ASD, atrial septal defect

patent ductus arteriosus; VSD, ventricular septal defect

AVSD, atrioventricular septal defect

aortic coarctation; IAA, interrupted aortic 625 arch; Misc., Miscellaneous; SV

TAPVC, total anomalous pulmonary 626 venous connection; PAPVC, partial anomalous pulmonary venous; conotruncal defects 627 including DORV (double outlet right ventricle), PA (pulmonary atresia)

Supplemental Figure 1. Distribution of enrolled thirteen pediatric heart centers. A. The 657 geographic location of the 13 centers; B The number of surgical cases in each center and 658 the number of COVID-19 confirmed cases in the province where the center is located 659 from

Supplemental Figure 2. The protocol of surgical program of surgical repair for 662 congenital heart diseases during January 23 to April 8 in the enrolled centers across 663

COVD-19: coronavirus disease 2019; PPE: Personal Protective Equipment; CDC: 664 Centers for