Bertran, Marta

Buszewicz, Marta

Dalrymple, Emma

Ford, Tamsin

Heyman, Isobel

Ladhani, Shamez N

Nugawela, Manjula D

Pereira, Snehal M Pinto

Segal, Terry Y

Shafran, Roz

Stephenson, Terence

Whittaker, Elizabeth

UCL Discovery

 Journal Pre-proofThe relationship between Post COVID symptoms in young peopleand their parentsMarta Bertran , Snehal M Pinto Pereira , Manjula D Nugawela ,Terence Stephenson , Roz Shafran , Tamsin Ford ,Marta Buszewicz , Elizabeth Whittaker , Isobel Heyman ,Terry Y Segal , Emma Dalrymple , Shamez N LadhaniPII: S0163-4453(22)00560-6DOI: https://doi.org/10.1016/j.jinf.2022.10.005Reference: YJINF 5727To appear in: Journal of InfectionAccepted date: 2 October 2022Please cite this article as: Marta Bertran , Snehal M Pinto Pereira , Manjula D Nugawela ,Terence Stephenson , Roz Shafran , Tamsin Ford , Marta Buszewicz , Elizabeth Whittaker ,Isobel Heyman , Terry Y Segal , Emma Dalrymple , Shamez N Ladhani , The relationship be-tween Post COVID symptoms in young people and their parents, Journal of Infection (2022), doi:https://doi.org/10.1016/j.jinf.2022.10.005This is a PDF file of an article that has undergone enhancements after acceptance, such as the additionof a cover page and metadata, and formatting for readability, but it is not yet the definitive version ofrecord. This version will undergo additional copyediting, typesetting and review before it is publishedin its final form, but we are providing this version to give early visibility of the article. Please note that,during the production process, errors may be discovered which could affect the content, and all legaldisclaimers that apply to the journal pertain.© 2022 Published by Elsevier Ltd on behalf of The British Infection Association.1   The relationship between Post COVID symptoms in young people and their parents Letter to the Editor | Letter to the Editor The relationship between Post COVID symptoms in young people and their parents Marta Bertran1, Snehal M Pinto Pereira2, Manjula D Nugawela3, Terence Stephenson3, Roz Shafran3, Tamsin Ford4, Marta Buszewicz5, Elizabeth Whittaker6, Isobel Heyman3, Terry Y Segal7, Emma Dalrymple3, Shamez N Ladhani1,8,* 1Immunisations and Vaccine Preventable Diseases Division, UK Health Security Agency, 61 Colindale Avenue, London NW9 5EQ, UK 2Division of Surgery & Interventional Science, Faculty of Medical Sciences, University College London, WC1E 6BT 3UCL Great Ormond Street Institute of Child Health, 30 Guilford Street, London, WC1N 1EH 4Department of Psychiatry, University of Cambridge, Hershel Smith Building Cambridge Biomedical Campus, CB2 0SZ 5Research Department of Primary Care & Population Health, University College London Medical School London UK 6Department of Paediatric Infectious Diseases, Imperial College Healthcare NHS Trust, London 7Paediatric and Adolescent division, University College London Hospitals NHS Foundation Trust, London 8Paediatric Infectious Diseases Research Group, St. George‟s University of London, Cranmer Terrace, London, SW17 0RE, UK          2  *Corresponding author: Dr. Shamez N Ladhani, UK Health Security Agency, Immunisations and Vaccine Preventable Diseases Division, 61 Colindale Avenue, London NW9 5EQ, United Kingdom, Phone: +44 (0) 20 8327 7155 E-mail: shamez.ladhani@ukhsa.gov.uk Keywords: LONG-COVID, SARS-CoV-2, children and young people, matched cohort study Dear Editor We read with interest the recent study on risk factors for long COVID. (1) Similar risk factors, including female gender, older age and higher number of symptoms, have been reported in children and young people (CYP).(2) In England, the CLoCk study was established to investigate long COVID in a cohort of >30,000 CYP aged 11-17 years with PCR-confirmed SARS-CoV-2 infection and a contemporaneous PCR-negative group, matched by age, sex, geography and time.(3) Outcomes at 3 months follow-up have been published.(4) Anecdotal information suggested many CYP with ongoing symptoms had other household members symptoms after COVID-19. We hypothesised that CYP reporting long COVID were more likely to have a parent with ongoing symptoms.  We examined this in a subset of CLoCk participants who completed their six-month questionnaire after a positive or negative SARS-CoV-2 PCR-test between October 2020 and March 2021 (n=14,377). We excluded CYP with subsequent SARS-CoV-2 infections (48/6,878 PCR-positive at baseline, 317/7,499 PCR-negative at baseline), those who returned the questionnaire after 34 weeks (n=1,063) and those who did not answer the question of interest (n=161). The final sample included 12,788 CYP (6,334 PCR-positives, 6,454 PCR negatives).  The questionnaire included demographics, elements of the International Severe Acute Respiratory and Emerging Infection Consortium (ISARIC) questionnaire,(4) 21 symptoms as well as the Strengths and Difficulties questionnaire (SDQ) (6) embedded within it, the EQ5D-         3  Y scale,(5) Short Warwick Edinburgh Mental Health Wellbeing scale (SWEMBS),(6) Chalder Fatigue Scale,(7) and the following question: “Has COVID-19 affected family members (in your house): Does anyone have ongoing problems from Covid-19? If so, can you tell us who?”. We grouped responses as „no‟, „ongoing problems in parents‟, or „other‟ if ongoing symptoms were reported in other family members or if the relationship was unclear (e.g., specific names given). The Delphi consensus research definition of long COVID adapted to CYP was used: experiencing ≥1 symptom AND problems with mobility, self-care, doing usual activities or having pain/discomfort or feeling very worried/sad, based on the EQ-5D-Y scale, at the time of questionnaire completion around 6 months after their PCR-test.(8) We assessed the association between on-going symptoms in CYP and their parents having on-going symptoms using a logistic regression model that adjusted for age, sex, deprivation (index of multiple deprivation [IMD] quintiles) and SARS-CoV-2 PCR-test status. All analyses were done in Stata v17. Among test-positive CYP, 19.1% (1,207/6,334) reported having a parent with ongoing problems after COVID-19. In this group, the prevalence of long COVID six months post-test in CYP reporting a parent with ongoing problems was 33.3% (402/1,207) compared to 22.6% (1,156/5,127) in CYP who did not report parents having ongoing problems after COVID-19 (Table).  The same pattern, albeit with lower prevalence, was observed among SARS-CoV-2 PCR-negative CYP, where 5.5% (354/6,454) reported having parents with ongoing COVID-19 related symptoms. In this group, the prevalence of long COVID six months post-test in CYP reporting a parent with symptoms was 28.0% (99/354) compared to 17.3% (1,052/6,100) in CYP not reporting parents having ongoing symptoms (Table).           4  In the logistic regression model including age, sex and deprivation and SARS-CoV-2 status, CYP reporting parents with ongoing symptoms were 1.79-times (95% CI, 1.58-2.02) more likely to have long COVID at 6 months than CYP who did not report parents having ongoing symptoms, independently of age, sex, deprivation and SARS-CoV-2 PCR-test results. Notably, Chalder Fatigue Scale, SWEMBS and SDQ scores (for total difficulties as well as subscales) were broadly similar, irrespective of the CYP‟ SARS-CoV-2 PCR-status or parental ongoing symptom status (Table). In summary, this association between having a parent with ongoing symptoms after COVID-19 and CYP experiencing long COVID 6 months after their SARS-CoV-2 test was present in test-positive and test-negatives CYP albeit at a lower prevalence among the latter. Possible explanations for the increased risk of long COVID in CYP with PCR-confirmed SARS-CoV-2 infection who reported parents with ongoing symptoms include exposure to an increased viral load when infected and shared genetic vulnerability to post-COVID syndrome, such as viral persistence. There could also be shared environmental and genetic factors related to pre-existing poor physical and mental health among both test positive and test negative participants, such as  those arising from socioeconomic status, including higher living density which may increase exposure to viral shedding even in those testing negative.(9) Another explanation relevant to both groups might be an increased focus on symptoms among families with ongoing symptoms, potentially resulting in increased symptoms or reporting by their children. Additionally, this could result in proxy selection bias: parents with ongoing COVID-19 problems may have encouraged their children to participate in the study. The lack of substantial differences in mental health and wellbeing symptoms suggests that the increased risk of long COVID in CYP of parents with ongoing symptoms is not associated with the child‟s current mental wellbeing.          5  Strengths and limitations of the study methodology have been discussed previously.(4) Using a national dataset with PCR-confirmed test-positives and matched test-negatives is a strength of this analysis, highlighting the higher prevalence of symptoms in children of parents with ongoing problems independently of the children‟s own SARS-CoV-2 infection status. We excluded CYP who were (re)infected between their original PCR-test and questionnaire completion but acknowledge misclassification may still exist. Although CYP reported their own symptoms, there is a risk of selection bias as described above. Reporting bias might occur if children of parents with ongoing problems were hypervigilant regarding the same symptoms. Finally, we also have no information about the symptoms, duration or severity of on-going problems in parents.  In conclusion, we have identified an association between having a parent with ongoing problems after COVID-19 problems and long COVID at six months post-test in CYP, irrespective of their SARS-CoV-2 positivity status. At present, services for post-COVID syndromes are separate for adults and children. The importance of working with the family in CYP clinics is highlighted. There may be some benefit for integrated joint services focussing on holistic strategies and interventions for the whole family unit, as is currently in place for other infections such as viral hepatitis and HIV. Ethical approval The study was approved by Yorkshire and the Humber–South Yorkshire Research Ethics Committee (REC reference: 21/YH/0060; IRAS project ID: 293495). UKHSA has legal permission, provided by Regulation 3 of The Health Service (Control of Patient Information) Regulations 2002, to process patient confidential information for national surveillance of communicable diseases. Individual patient consent is not required for initial invitation to the study.          6  Data availability Data are sensitive and not publicly available. All requests for data will be reviewed by the Children & young people with LONG-COVID (CLoCk) study team, to verify whether the request is subject to any intellectual property or confidentiality obligations. Requests for access to the participant-level data from this study can be submitted via email to clock@ukhsa.gov.uk with detailed proposals for approval. A signed data access agreement with the CLoCK team is required before accessing shared data. Code is not made available as we have not used custom code or algorithms central to our conclusions. Declaration of Competing Interest TS is Chair of the Health Research Authority and therefore recused himself from the research ethics application. All other authors declare no competing interests. Table 1. Number of CYP with LONG-COVID, number of symptoms and scores from the SDQ questionnaire, SWEMBS and Chalder fatigue scale six months post-test stratified by SARS-CoV-2 status and ongoing COVID-19 problmes in parents (number and percentages)  CYP SARS-CoV-2 positive at baseline only (n=6,334) CYP SARS-CoV-2 negative since baseline (n=6,454)  Parents with ongoing COVID-19 problems Parents with ongoing COVID-19 problems  Yes No Yes No  1,207 (19.1%) 5,127 (80.9%) 354 (5.5%) 6,100 (94.5%) LONG-COVID* in CYP     Yes 402 (33.3%) 1,156 (22.6%) 99 (28.0%) 1,052 (17.3%)          7  No 805 (66.7%) 3,3971 (77.5%) 255 (72.0%) 5,048 (82.8%) No of symptoms (CYP)         0 363 (30.1%) 2,111 (41.2%) 163 (46.1%) 3,505 (57.5%) 1 221 (18.3%) 1,120 (21.9%) 56 (15.8%) 1,151 (18.9%) 2 179 (14.8%) 594 (11.6%) 30 (8.5%) 523 (8.6%) 3 130 (10.8%) 437 (8.5%) 25 (7.1%) 290 (4.8%) 4 95 (7.9%) 291 (5.7%) 20 (5.7%) 195 (3.2%) 5+ 219 (18.1%) 574 (11.2%) 60 (17.0%) 436 (7.2%) SDQ     SDQ Total Difficulties     Median 11 10 12 11 (25th, 75th) (7,16) (6,15) (2,18) (6,16) SDQ Emotional symptoms     Median 4 3 4 3 (25th, 75th) (2,6) (1,5) (2,6) (1,5) SDQ Conduct problems     Median 1 1 2 1 (25th, 75th) (0,2) (0,2) (1,3) (0,2) SDQ Hyperactivity/inattention     Median (25th, 75th) 4 4 4 4 (2,6) (2,6) (2,6) (3,6) SDQ peer relationship problem              8  Median 2 2 2 2 (25th, 75th) (1,3) (1,3) (1,3) (1,3) SWEMBS     Median 21.5 21.5 20.0 20.7 (25th, 75th) (18.5,24.1) (18.5,24.1) (18.0,23.2) (18.6,24.1) Chalder fatigue scale     Median 13 12 13 11 (25th, 75th) (11,15) (11,18) (11,17) (11,15) *Using data from the questionnaire on symptoms and the EQ-5D-Y scale at the time of the questionnaire (i.e., approximately 6 months after the PCR-test), LONG-COVID was operationalized as having at least 1 symptom and experiencing some/a lot of problems with respect to mobility, self-care, doing usual activities or having pain/discomfort or feeling very worried/sad. Funding and acknowledgements This work was supported by the Department of Health and Social Care, in their capacity as the National Institute for Health Research (NIHR), and by the UK Research and Innovation (UKRI) who have awarded funding grant number COVLT0022. All research at Great Ormond Street Hospital NHS Foundation Trust and UCL Great Ormond Street Institute of Child Health is made possible by the NIHR Great Ormond Street Hospital Biomedical Research Centre. SMPP is supported by a UK Medical Research Council Career Development Award (ref: MR/P020372/1). References          9  1 Righi E, Mirandola M, Mazzaferri F, Dossi G, Razzaboni E, Zaffagnini A, et al. Determinants of persistence of symptoms and impact on physical and mental wellbeing in Long COVID: A prospective cohort study. J Infect. 2022;84(4):566-72. 2 Behnood SA, Shafran R, Bennett SD, Zhang AXD, O'Mahoney LL, Stephenson TJ, et al. Persistent symptoms following SARS-CoV-2 infection amongst children and young people: A meta-analysis of controlled and uncontrolled studies. J Infect. 2022;84(2):158-70. 3 Stephenson T, Shafran R, De Stavola B, Rojas N, Aiano F, Amin-Chowdhury Z, et al. Long COVID and the mental and physical health of children and young people: national matched cohort study protocol (the CLoCk study). BMJ Open. 2021;11(8):e052838. 4 Stephenson T, Pinto Pereira SM, Shafran R, de Stavola BL, Rojas N, McOwat K, et al. Physical and mental health 3 months after SARS-CoV-2 infection (long COVID) among adolescents in England (CLoCk): a national matched cohort study. Lancet Child Adolesc Health. 2022;6(4):230-9. 5 Ravens-Sieberer U, Wille N, Badia X, Bonsel G, Burström K, Cavrini G, et al. Feasibility, reliability, and validity of the EQ-5D-Y: results from a multinational study. Qual Life Res. 2010;19(6):887-97. 6 Tennant R, Hiller L, Fishwick R, Platt S, Joseph S, Weich S, et al. The Warwick-Edinburgh Mental Well-being Scale (WEMWBS): development and UK validation. Health and Quality of Life Outcomes. 2007;5(1):63. 7 Chalder T, Berelowitz G, Pawlikowska T, Watts L, Wessely S, Wright D, et al. Development of a fatigue scale. J Psychosom Res. 1993;37(2):147-53. 8 Stephenson T, Allin B, Nugawela MD, Rojas N, Dalrymple E, Pinto Pereira S, et al. Long COVID (post-COVID-19 condition) in children: a modified Delphi process. Archives of Disease in Childhood. 2022;107(7):674-80.          10  9 Cerami C, Popkin-Hall ZR, Rapp T, Tompkins K, Zhang H, Muller MS, et al. Household Transmission of Severe Acute Respiratory Syndrome Coronavirus 2 in the United States: Living Density, Viral Load, and Disproportionate Impact on Communities of Color. Clinical Infectious Diseases. 2021;74(10):1776-85.             

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The relationship between Post COVID symptoms in young people and their parents

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The relationship between Post COVID symptoms in young people and their parents

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