Abstract

We conducted two surveys to evaluate the health-seeking behaviors of individuals with acute respiratory infections (ARI) during the COVID-19 outbreak in Wuhan, China. Among 351 participants reporting ARI (10.3%, 351/3,411), 36.5% sought medical assistance. Children were more likely to seek medical assistance than other age-groups (66.1% vs. 28.0%-35.1%). This population-based study demonstrates that the majority of patients with ARI symptoms did not seek medical assistance during the COVID-19 outbreak in Wuhan. These findings may be used to refine the estimates of disease burden and clinical severity of COVID-19 and to plan for health resources allocation.


Authors

Yang, Juan;  Gong, Hui;  Chen, Xinhua;  Chen, Zhiyuan;  Deng, Xiaowei;  Qian, Mengcen;  Hou, Zhiyuan;  Ajelli, Marco;  Viboud, Cecile;  Yu, Hongjie

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  • pre-publication peer review (FINAL ROUND)
    Decision Letter
    2020/08/18

    18-Aug-2020

    Dear Prof. Yu:

    It is a pleasure to accept your manuscript entitled "Health seeking behaviors of patients with acute respiratory infections during the outbreak of novel coronavirus disease 2019 in Wuhan, China" in its current form for publication in Influenza and Other Respiratory Viruses.

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    Author Response
    2020/08/17

    Manuscript number: IRV-2020-224
    Title: Health seeking behaviors of patients with acute respiratory infections during the outbreak of novel coronavirus disease 2019 in Wuhan, China

    Response to reviewers’ and editors’ comments
    We would like to thank the editor for giving us the opportunity to revise our manuscript. We would also like to thank the two reviewers for their in-depth assessment and useful suggestions. Our point-by-point responses to the reviewers’ comments are given below. Page and line numbers refer to the clean version of our revised manuscript.

    Reviewers' comments:
    Reviewer: 1
    Comments to the Corresponding Author
    The authors conducted two cross-sectional surveys among adults and children residing in Wuhan, China to evaluate health-seeking behaviours of individuals with ARI during COVID-19 outbreak. The authors reported only one third of participants reporting ARI sought medical care, which showed the possibility of a large proportion of mild cases did not seek medical care could potentially be COVID-19 cases but were undetectable. The manuscript is brief and written with appropriate conclusions.
    Response: We would like to thank the reviewer for the positive evaluation of our manuscript and the useful comments that helped us improve our work.

    1.1 If the authors are able to perform some estimations, what would be the expected actual number of COVID-19 cases in Wuhan, China during the survey period?
    Response: The reviewer rose a very interesting point. In the current study we provide a key metric (i.e., probability of seeking medical help) to estimate the disease burden and assess the severity of COVID-19 outbreak in Wuhan. However, only using this parameter is not enough. In addition to health seeking behaviors, factors like the sensitivity of laboratory assays and community-based screening rates for individuals with fever should be also accounted for to adjust the reported COVID-19 cases by the local passive surveillance system. We already dedicated much effort on this topic and submitted a separate paper specific on this topic back in April. In case the reviewer is interested in the obtained results, we include a brief summary hereafter.
    A total of 50,333 COVID-19 cases were reported in Wuhan from December 1, 2019 to March 31, 2020. We adjusted estimates for sensitivity of laboratory assays and accounted for prospective community screenings and healthcare seeking behaviors. Then, the estimated actual number of symptomatic COVID-19 cases was 85,200 (95%CI 75,200-104,500) in Wuhan. Rates of symptomatic cases, medical consultations, hospitalizations, and deaths were estimated at 796 (95%CI: 703-977), 489 (472-509), 370 (358-384), and 36.2 (35.0-37.3) per 100,000 persons, respectively. The obtained age-specific results show that the most affected age group was 60+ years with an estimated incidence of 2,386 (95%CI: 2,047-3,188) symptomatic cases per 100,000 individuals.
    1.2 Convenience sampling and respond through self-reporting are major limitations of the study. Generalisability of study findings to the whole population in Wuhan, China is concerned.
    Response: The reviewer rose two good points that we did not stress enough in the previous version of the paper and we would like to thank her/him for the careful reading.
    In the telephone-and-online survey among adults, we randomly dialed Wuhan mobile phone numbers to invite the participants through a computer-assisted interviewing system. While for the online survey of children, an online link to our questionnaire was randomly sent to Wuhan families with children through emails. Therefore, our study population could not be generalized to the whole population in Wuhan. Instead, we extrapolated the results to the population who owns a mobile phone and has access to the Internet based on the corresponding age structure. The families with better education background and higher income are more likely to have emails. Accordingly, the health seeking behaviors in children may better represent those from families with better education background and higher income.
    We also agree that we cannot exclude that the recall bias have affected our results. As such, we have now included a discussion on both topics and acknowledge them as study limitations. In particular,
    Page 7, line 102-106: Adjusting for the age structure of the Wuhan population who owns a mobile phone and has access to the Internet4, the overall proportion of patients with ARI was 10.5% (95%CI 9.4%-11.6%), and the adjusted proportion of seeking medical assistance for ARI was 39.0% (95%CI 32.3%-46.7%).
    Page 10-11, line 177-197: First, for the telephone-and-online survey among adults, the study participants were those who owns a mobile phone and has access to the Internet. While for the online survey of children, the study participants were from Wuhan families with emails. The families with better education background and higher income are more likely to have emails. Accordingly, the health seeking behaviors could not represent that of the whole population in Wuhan. Using the age profile of the population who owns a mobile phone and has access to the Internet, we could partially adjust the probability of health seeking behaviors…Third, as it was a retrospective study, and the ARI illness and the corresponding health seeking behaviors were all self-reported, recall bias was inevitable and was difficult to be quantified.

    1.3 Would the findings be relatable to the results from serosurveillance study conducted in the city?
    Response: This is another very nice point. Unfortunately, no studies have reported the seroprevalence of COVID-19 among general population in Wuhan until now. We found three studies reporting seroprevalence estimates for specific groups in Wuhan: healthcare workers, hospital patients, and general workers who return to work and did not show respiratory symptoms during the epidemic (Lin et al., medRxiv, https://doi.org/10.1101/2020.06.16.20132423; Liu et al., medRxiv, https://www.medrxiv.org/content/10.1101/2020.06.13.20130252v1.full.pdf; Yu et al., https://papers.ssrn.com/sol3/papers.cfm?abstract_id=3608054). Those studies reported that the seroprevalence of IgG was 3.3%-4.6% among asymptomatic general workers who return to work, 2.1%-4.0% in healthcare providers, and 1.0% in non-COVID-19 patients. Unfortunately, these particular groups of the population are not representative of the general population and thus cannot be used to estimate the number of infections. Nonetheless, if we make the simplistic assumption that the seroprevalence in general population is the same as in the workers sampled in Lin et al., we would obtain an estimate of 363,000-506,000 SARS-CoV-2 infected individuals in Wuhan. On the basis of estimated 85,200 symptomatic COVID-19 cases provided in the response to Point 1.1, we could conclude that 17%-23% of COVID-19 infections were symptomatic cases. As stated in the reply to Point 1.1, this goes beyond the scope of the current study and, honestly, we feel that the assumption that the workers analyzed in Lin et al. are representative of the general population is too simplistic. In light of these reasons, we do not report these estimations in the revised version of the manuscript.

    Reviewer: 2
    Comments to the Corresponding Author
    General comments:
    This article reports findings from population surveys of healthcare usage for acute respiratory infection in Wuhan, China. While I appreciate the need to understand healthcare usage patterns during the COVID-19 epidemic, and that these findings may be of local policy interest, it wasn’t clear to me that this manuscript contains sufficient substantive material to merit a publication in itself. It effectively presents an age-standardised estimate of healthcare usage among individuals with self-reported ARI in the previous 3 months from a potentially highly skewed sample of survey respondents, as well as age-specific estimates in fairly coarse age groupings. The discussion is lacking some consideration of key limitations, and I feel some of the conclusions are rather tenuous.
    Response: We would like to thank the reviewer for the many useful comments that helped us improve our work.

    Main comments:
    1. Some key issues are the very low participation. For example, for the child questionnaires, only 4% of those sent were retained, and of these nearly half could not be used in the analysis. Similarly, for adults, of the 15% who initially agreed to participate, nearly two-thirds did not result in a completed questionnaire. The potential for bias in responses and lack of representativeness is therefore high, even with age-standardisation, but there is no comment on this in the discussion. Figure 1 is rather confusing. Given that the child and adult samples were, as I understand it, completely independent, it would be clearer to keep the left and right-hand sides of this diagram separate, rather than linking the boxes at the bottom, which creates confusion about the participant flow. The percentages are also quite misleading, since the denominators change at every stage. The lower tier also shows the age composition of respondents, rather than the final participation by age group.
    Response: The reviewer is right about the low participation rate and we apologize for the lack of discussion on this study limitation. Low participation is a common weakness of telephone and online surveys in mainland China. Similar response rates were observed in previous telephone studies. For example, the response rate was 17.6% in a telephone survey conducted by Chinese Center for Disease Control and Prevention in 2013/14 on economic burden of patients with hand, foot and mouths (Zheng Y, PLoS One 2017), and the response rate was only 7.4-7.6% for surveys on economic burden of influenza patients (Yang J, Infectious Diseases of Poverty 2015). Even so, we used a telephone and online survey other than a community-based field investigation since that was the only feasible option during the lockdown period in Wuhan. Nonetheless, we agree that this is a limitation in our study. We added the following paragraph to comment on this.
    Page 11, line 184-194: Second, the low response rate in our survey may lead to a potential bias towards individuals who paid more attention on health and thus were more likely to participate in our study. This may have led to overestimate the probability of health seeking medical assistance. We were unable to evaluate the representativeness of the study participants since the demographic characteristics of those who did not participate in the present study were not available. Although we adjusted the probability of seeking medical care using the actual age structure of Wuhan population who owns a mobile phone and has access to the Internet to minimize the bias, factors like socio-economic status, medical insurance, and education level were not accounted for. Accordingly, it should be prudent to generalize study findings to the whole population of Wuhan.

    About Figure 1, the reviewer is right. Child and adult sample were completely independent. As suggested, we revised the Figure 1 by: 1) separating the left and right-hand sides of the diagram; 2) presenting the age profile of the final participants; 3) removing some boxes such as “participants recruited” and aggregating information in the box “included in the analysis”. The percentage shows the proportion of persons between two adjacent stages. The denominators are the number of persons in the former stage. For example, for the adult questionnaires, 15.5% of those who were called agreed to participate, and 34.2% of those who agreed to participate were qualified for the analysis. This has now been clarified in the caption.

    2.1 The outcome isn’t clearly defined in the paper, though from the questionnaire ARI includes fever and/or any respiratory symptom – this should be clearly stated in the methods, and the discussion needs some mention of the limitations of such a non-specific case definition, particularly with a recall period of 3 months, which has a lot of potential for error. The authors seem to imply that all these reported episodes are infectious in nature, but the definition is compatible with allergic rhinitis, asthmatic wheezing and numerous other non-infectious conditions.
    Response: We apologize for the lack of clarity. In Section Methods, we previously gave the definition of ARI (presence of fever and/or any respiratory symptoms, e.g., cough and sore throat) in Section Methods. In the revised manuscript, we moved the definition to the first sentence in Section Methods (page 4, line 51-53).
    The primary objective of this study was to understand the health seeking behaviors of ARI patients in the COVID-19 pandemic context, which could reveal the impact of the COVID-19 pandemic on routine medical services and health seeking behaviors for a wide range of groups of population with specific symptoms instead of only a specific disease. For this objective, we did not relate ARI patients with COVID-19. Second, our study could provide key metrics (i.e., the probability of seeking medical help) that can be instrumental to estimate the disease burden and assess the full severity pyramid of COVID-19. As the reviewer mentioned, the case definition is purposely non-specific, and thus there are limitations to use the health seeking behaviors of ARI patients as a proxy for COVID-19 patients.
    According to the reviewer’s suggestion, we deeply revised the Discussion. First, we explained the primary implications of the results (Page 8, line 136-153), then we discussed the potential value of the results for estimating disease burden and severity of COVID-19 (Page 9, line 154-164). Finally, we stressed the limitations of using the health seeking behaviors of ARI patients for estimating disease burden and severity of COVID-19 (Page 10, line 165-176). As suggested, we have also added comments about the recall-bias as a study limitation (Page 11, line 194-197).

    2.2 The main result implies that about >40% of the population would have an episode of ARI in a year. Is this expected and compatible with other data sources? If so, some supporting evidence from other studies would be useful.
    Response: Thanks for the useful comment. In the revised manuscript, we compared our estimate with that in Wuhan in the same period (December 2009-March 2010) in 2009/2010.
    Page 10, line 171-176: As compared to a study conducted in Wuhan, during the 2009 H1N1 influenza pandemic 15, we found a larger proportion of ARI cases in the study populations (10.3% vs. 4.9%). This suggests that a faction of our ARI cases may be attributed to SARS-CoV-2 infections (also in light of the low circulation of other ARI-associated pathogens such as influenza virus during the study period16).
    We would like to stress that we found that 10.3% of the study populations reported ARI during the COVID-19 outbreak in Wuhan (i.e., the first quarter of 2020 only). We guess the reviewer estimated about that >40% of the population would have an episode of ARI per year by multiplying 10.3% by four. However, as the reviewer properly pointed out, ARI could be caused by many pathogens and subject to strong seasonal patterns. Therefore, we do not provide an estimate of the proportion of population reporting an ARI episode per year.

    1. I feel some of the conclusions are unwarranted. For example, the authors mention that their findings highlight the relevance of self-isolation. I don’t think this is at all evident from their study, since there is no way to know whether any of these self-reported ARI episodes were related to COVID-19, or whether the ARI prevalence estimates and healthcare usage fractions were any different to the period before December 2019.
      Response: We agree with the reviewer that our results do not provide a direct support to the conclusion about the relevance of self-isolation. Therefore, this sentence has been removed. In addition, the Discussion has been deeply revised and all conclusions not directly supported by our findings have been removed as well.

    2. The authors mention that fear of nosocomial infections was a major reason for children not seeking care. From the questionnaire, the relevant question seems to be rather leading. Firstly, it’s not clear to me that ‘nosocomial’ infection is a commonly understood term among the lay public. But among the response options offered are ‘mild illness’, ‘fear of nosocomial infection’, and ‘hospital suspension during the epidemic’. There are a multitude of reasons why parents would not take children to see a doctor when symptomatic – I can see that it would be of interest to know whether people are put off visiting health centres because of the epidemic, but asking the question in this way leaves a lot of room for biased responses, particularly given that offering other reasons involves considerably more work from respondents.
      Response: First of all, we apologize for the lack of clarity. The survey was performed in Chinese and in the text we did not put enough attention on the translation of the questions. In particular, we did not use the term ‘nosocomial infection’ in the Chinese version. Instead, a better translation of the question could read as follows: “Fear of acquiring COVID-19 when visiting a hospital”. For publication, we translated it into English. The translation was not exactly correct. We revised the text in the supplementary appendix accordingly:
      What is the main reason that your child did not go to medical institutions after onset of the above symptoms?
      a. Self-rated mild illness
      b. Fear of acquiring COVID-19 when visiting a hospital
      c. Hospital suspension during the COVID-19 epidemic
      d. Other

    Second, we apologize for the lack of clarity about this question. Indeed, the participants neither have to specify the reasons in case they replied “other” nor answer further questions. We would like to stress that this question was included only for informative purposes and added at the very end of the questionnaire. The results of the main analysis presented here (i.e., estimating the age-specific health seeking behavior of individuals affected by ARI) are not affected by this question.



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  • pre-publication peer review (ROUND 1)
    Decision Letter
    2020/07/09

    09-Jul-2020

    Dear Prof. Yu

    Manuscript ID IRV-2020-224 entitled "Health seeking behaviors of patients with acute respiratory infections during the outbreak of novel coronavirus disease 2019 in Wuhan, China" which you submitted to the Influenza and Other Respiratory Viruses, has been reviewed. The comments of the reviewers and Associate Editor are included at the bottom of this letter.

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    Associate Editor
    Comments to the Corresponding Author:
    The second reviewer raised some more serious concerns about the value of this study, please consider carefully how to respond to these.

    Reviewer(s)' Comments to Author:

    Reviewer: 1

    Comments to the Corresponding Author
    The authors conducted two cross-sectional surveys among adults and children residing in Wuhan, China to evaluate health-seeking behaviours of individuals with ARI during COVID-19 outbreak. The authors reported only one third of participants reporting ARI sought medical care, which showed the possibility of a large proportion of mild cases did not seek medical care could potentially be COVID-19 cases but were undetectable. The manuscript is brief and written with appropriate conclusions.

    If the authors are able to perform some estimations, what would be the expected actual number of COVID-19 cases in Wuhan, China during the survey period?

    Convenience sampling and respond through self-reporting are major limitations of the study. Generalisability of study findings to the whole population in Wuhan, China is concerned.

    Would the findings be relatable to the results from serosurveillance study conducted in the city?

    Reviewer: 2

    Comments to the Corresponding Author
    IRV-2020-224: "Health seeking behaviors of patients with acute respiratory infections during the outbreak of novel coronavirus disease 2019 in Wuhan, China"
    General comments:
    This article reports findings from population surveys of healthcare usage for acute respiratory infection in Wuhan, China. While I appreciate the need to understand healthcare usage patterns during the COVID-19 epidemic, and that these findings may be of local policy interest, it wasn’t clear to me that this manuscript contains sufficient substantive material to merit a publication in itself. It effectively presents an age-standardised estimate of healthcare usage among individuals with self-reported ARI in the previous 3 months from a potentially highly skewed sample of survey respondents, as well as age-specific estimates in fairly coarse age groupings. The discussion is lacking some consideration of key limitations, and I feel some of the conclusions are rather tenuous.
    Main comments:
    1. Some key issues are the very low participation. For example, for the child questionnaires, only 4% of those sent were retained, and of these nearly half could not be used in the analysis. Similarly, for adults, of the 15% who initially agreed to participate, nearly two-thirds did not result in a completed questionnaire. The potential for bias in responses and lack of representativeness is therefore high, even with age-standardisation, but there is no comment on this in the discussion. Figure 1 is rather confusing. Given that the child and adult samples were, as I understand it, completely independent, it would be clearer to keep the left and right-hand sides of this diagram separate, rather than linking the boxes at the bottom, which creates confusion about the participant flow. The percentages are also quite misleading, since the denominators change at every stage. The lower tier also shows the age composition of respondents, rather than the final participation by age group.
    2. The outcome isn’t clearly defined in the paper, though from the questionnaire ARI includes fever and/or any respiratory symptom – this should be clearly stated in the methods, and the discussion needs some mention of the limitations of such a non-specific case definition, particularly with a recall period of 3 months, which has a lot of potential for error. The authors seem to imply that all these reported episodes are infectious in nature, but the definition is compatible with allergic rhinitis, asthmatic wheezing and numerous other non-infectious conditions. The main result implies that about >40% of the population would have an episode of ARI in a year. Is this expected and compatible with other data sources? If so, some supporting evidence from other studies would be useful.
    3. I feel some of the conclusions are unwarranted. For example, the authors mention that their findings highlight the relevance of self-isolation. I don’t think this is at all evident from their study, since there is no way to know whether any of these self-reported ARI episodes were related to COVID-19, or whether the ARI prevalence estimates and healthcare usage fractions were any different to the period before December 2019.
    4. The authors mention that fear of nosocomial infections was a major reason for children not seeking care. From the questionnaire, the relevant question seems to be rather leading. Firstly, it’s not clear to me that ‘nosocomial’ infection is a commonly understood term among the lay public. But among the response options offered are ‘mild illness’, ‘fear of nosocomial infection’, and ‘hospital suspension during the epidemic’. There are a multitude of reasons why parents would not take children to see a doctor when symptomatic – I can see that it would be of interest to know whether people are put off visiting health centres because of the epidemic, but asking the question in this way leaves a lot of room for biased responses, particularly given that offering other reasons involves considerably more work from respondents.

    Decision letter by
    Cite this decision letter
    Reviewer report
    2020/06/21

    IRV-2020-224: "Health seeking behaviors of patients with acute respiratory infections during the outbreak of novel coronavirus disease 2019 in Wuhan, China"
    General comments:
    This article reports findings from population surveys of healthcare usage for acute respiratory infection in Wuhan, China. While I appreciate the need to understand healthcare usage patterns during the COVID-19 epidemic, and that these findings may be of local policy interest, it wasn’t clear to me that this manuscript contains sufficient substantive material to merit a publication in itself. It effectively presents an age-standardised estimate of healthcare usage among individuals with self-reported ARI in the previous 3 months from a potentially highly skewed sample of survey respondents, as well as age-specific estimates in fairly coarse age groupings. The discussion is lacking some consideration of key limitations, and I feel some of the conclusions are rather tenuous.
    Main comments:
    1. Some key issues are the very low participation. For example, for the child questionnaires, only 4% of those sent were retained, and of these nearly half could not be used in the analysis. Similarly, for adults, of the 15% who initially agreed to participate, nearly two-thirds did not result in a completed questionnaire. The potential for bias in responses and lack of representativeness is therefore high, even with age-standardisation, but there is no comment on this in the discussion. Figure 1 is rather confusing. Given that the child and adult samples were, as I understand it, completely independent, it would be clearer to keep the left and right-hand sides of this diagram separate, rather than linking the boxes at the bottom, which creates confusion about the participant flow. The percentages are also quite misleading, since the denominators change at every stage. The lower tier also shows the age composition of respondents, rather than the final participation by age group.
    2. The outcome isn’t clearly defined in the paper, though from the questionnaire ARI includes fever and/or any respiratory symptom – this should be clearly stated in the methods, and the discussion needs some mention of the limitations of such a non-specific case definition, particularly with a recall period of 3 months, which has a lot of potential for error. The authors seem to imply that all these reported episodes are infectious in nature, but the definition is compatible with allergic rhinitis, asthmatic wheezing and numerous other non-infectious conditions. The main result implies that about >40% of the population would have an episode of ARI in a year. Is this expected and compatible with other data sources? If so, some supporting evidence from other studies would be useful.
    3. I feel some of the conclusions are unwarranted. For example, the authors mention that their findings highlight the relevance of self-isolation. I don’t think this is at all evident from their study, since there is no way to know whether any of these self-reported ARI episodes were related to COVID-19, or whether the ARI prevalence estimates and healthcare usage fractions were any different to the period before December 2019.
    4. The authors mention that fear of nosocomial infections was a major reason for children not seeking care. From the questionnaire, the relevant question seems to be rather leading. Firstly, it’s not clear to me that ‘nosocomial’ infection is a commonly understood term among the lay public. But among the response options offered are ‘mild illness’, ‘fear of nosocomial infection’, and ‘hospital suspension during the epidemic’. There are a multitude of reasons why parents would not take children to see a doctor when symptomatic – I can see that it would be of interest to know whether people are put off visiting health centres because of the epidemic, but asking the question in this way leaves a lot of room for biased responses, particularly given that offering other reasons involves considerably more work from respondents.

    Reviewed by
    Cite this review
    Reviewer report
    2020/06/12

    The authors conducted two cross-sectional surveys among adults and children residing in Wuhan, China to evaluate health-seeking behaviours of individuals with ARI during COVID-19 outbreak. The authors reported only one third of participants reporting ARI sought medical care, which showed the possibility of a large proportion of mild cases did not seek medical care could potentially be COVID-19 cases but were undetectable. The manuscript is brief and written with appropriate conclusions.

    If the authors are able to perform some estimations, what would be the expected actual number of COVID-19 cases in Wuhan, China during the survey period?

    Convenience sampling and respond through self-reporting are major limitations of the study. Generalisability of study findings to the whole population in Wuhan, China is concerned.

    Would the findings be relatable to the results from serosurveillance study conducted in the city?

    Reviewed by
    Cite this review
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