Skip to main content
SpringerLink
Log in

Missing microbes in infants and children in the COVID-19 pandemic: a study of 1,126 participants in Beijing, China

  • Research Paper
  • Published:
Science China Life Sciences Aims and scope Submit manuscript

Abstract

The COVID-19 pandemic has caused many fatalities worldwide and continues to affect the health of the recovered patients in the form of long-COVID. In this study, we compared the gut microbiome of uninfected infants and children before the pandemic began (BEFORE cohort, n=906) to that of after the pandemic (AFTER cohort, n=220) to examine the potential impact of social distancing and life habit changes on infant/children gut microbiome. Based on 16S rRNA sequencing, we found a significant change in microbiome composition after the pandemic, with Bacteroides enterotype increasing to 35.45% from 30.46% before the pandemic. qPCR quantification indicated that the bacterial loads of seven keystone taxa decreased by 91.69%–19.58%. Quantitative microbiome profiling, used to enhance the resolution in detecting microbiome differences, revealed a greater explained variance of pandemic on microbiome compared to gender, as well as a significant decrease in bacterial loads in 15 of the 20 major genera. The random forest age-predictor indicated the gut microbiomes were less mature in the after-pandemic cohort than in the before-pandemic cohort in the children group (3–12 years old) and had features of a significantly younger age (average of 1.86 years). Lastly, body weight and height were significantly lower in the after-pandemic cohort than in the before-pandemic cohort in infants (<1 year of age), which was associated with a decrease in bacterial loads in the fecal microbiome.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Alsharairi, N.A. (2021). The role of short-chain fatty acids in mediating very low-calorie ketogenic diet-infant gut microbiota relationships and its therapeutic potential in obesity. Nutrients 13, 3702.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson, M.J. (2017). Permutational multivariate analysis of variance (PERMANOVA). Wiley Statsref, doi: https://doi.org/10.1002/9781118445112.stat07841.

  • Arumugam, M., Raes, J., Pelletier, E., Le Paslier, D., Yamada, T., Mende, D.R., Fernandes, G.R., Tap, J., Bruls, T., Batto, J.M., et al. (2011). Enterotypes of the human gut microbiome. Nature 473, 174–180.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Auchtung, T.A., Stewart, C.J., Smith, D.P., Triplett, E.W., Agardh, D., Hagopian, W. A., Ziegler, A.G., Rewers, M.J., She, J.X., Toppari, J., et al. (2022). Temporal changes in gastrointestinal fungi and the risk of autoimmunity during early childhood: the TEDDY study. Nat Commun 13, 3151.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bäckhed, F., Roswall, J., Peng, Y., Feng, Q., Jia, H., Kovatcheva-Datchary, P., Li, Y., Xia, Y., Xie, H., Zhong, H., et al. (2015). Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 17, 690–703.

    Article  PubMed  Google Scholar 

  • Ballering, A.V., van Zon, S.K.R., olde Hartman, T.C., and Rosmalen, J.G.M. (2022). Persistence of somatic symptoms after COVID-19 in the Netherlands: an observational cohort study. Lancet 400, 452–461.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57, 289–300.

    Article  Google Scholar 

  • Blanton, L.V., Charbonneau, M.R., Salih, T., Barratt, M.J., Venkatesh, S., Ilkaveya, O., Subramanian, S., Manary, M.J., Trehan, I., Jorgensen, J.M., et al. (2016). Gut bacteria that prevent growth impairments transmitted by microbiota from malnourished children. Science 351, aad3311.

    Article  PubMed  Google Scholar 

  • Bokulich, N.A., Chung, J., Battaglia, T., Henderson, N., Jay, M., Li, H., D. Lieber, A., Wu, F., Perez-Perez, G.I., Chen, Y., et al. (2016). Antibiotics, birth mode, and diet shape microbiome maturation during early life. Sci Transl Med 8, 343ra382.

    Article  Google Scholar 

  • Bolyen, E., Rideout, J.R., Dillon, M.R., Bokulich, N.A., Abnet, C.C., Al-Ghalith, G.A., Alexander, H., Alm, E.J., Arumugam, M., Asnicar, F., et al. (2019). Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37, 852–857.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., and Madden, T.L. (2009). BLAST+: architecture and applications. BMC Bioinf 10, 421.

    Article  Google Scholar 

  • Cani, P.D., Depommier, C., Derrien, M., Everard, A., and de Vos, W.M. (2022). Akkermansia muciniphila: paradigm for next-generation beneficial microorganisms. Nat Rev Gastroenterol Hepatol 19, 625–637.

    Article  PubMed  Google Scholar 

  • Cao, J., Wang, C., Zhang, Y., Lei, G., Xu, K., Zhao, N., Lu, J., Meng, F., Yu, L., Yan, J., et al. (2021). Integrated gut virome and bacteriome dynamics in COVID-19 patients. Gut Microbes 13, 1–2.

    Article  PubMed  Google Scholar 

  • Costea, P.I., Hildebrand, F., Arumugam, M., Bäckhed, F., Blaser, M.J., Bushman, F.D., de Vos, W.M., Ehrlich, S.D., Fraser, C.M., Hattori, M., et al. (2018). Enterotypes in the landscape of gut microbial community composition. Nat Microbiol 3, 8–16.

    Article  CAS  PubMed  Google Scholar 

  • de Goffau, M.C., Jallow, A.T., Sanyang, C., Prentice, A.M., Meagher, N., Price, D.J., Revill, P.A., Parkhill, J., Pereira, D.I.A., and Wagner, J. (2022). Gut microbiomes from Gambian infants reveal the development of a non-industrialized Prevotella-based trophic network. Nat Microbiol 7, 132–144.

    Article  CAS  PubMed  Google Scholar 

  • Dominguez-Bello, M.G., Costello, E.K., Contreras, M., Magris, M., Hidalgo, G., Fierer, N., and Knight, R. (2010). Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci USA 107, 11971–11975.

    Article  PubMed  PubMed Central  Google Scholar 

  • Dominguez-Bello, M.G., De Jesus-Laboy, K.M., Shen, N., Cox, L.M., Amir, A., Gonzalez, A., Bokulich, N.A., Song, S.J., Hoashi, M., Rivera-Vinas, J.I., et al. (2016). Partial restoration of the microbiota of cesarean-born infants via vaginal microbial transfer. Nat Med 22, 250–253.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Durack, J., and Lynch, S.V. (2019). The gut microbiome: Relationships with disease and opportunities for therapy. J Exp Med 216, 20–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao, S., and Wang, J. (2023). Maternal and infant microbiome: next-generation indicators and targets for intergenerational health and nutrition care. Protein Cell 14, 807–823.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gehrig, J.L., Venkatesh, S., Chang, H.W., Hibberd, M.C., Kung, V.L., Cheng, J., Chen, R.Y., Subramanian, S., Cowardin, C.A., Meier, M.F., et al. (2019). Effects of microbiota-directed foods in gnotobiotic animals and undernourished children. Science 365, eaau4732.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gensollen, T., Iyer, S.S., Kasper, D.L., and Blumberg, R.S. (2016). How colonization by microbiota in early life shapes the immune system. Science 352, 539–544.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giuntella, O., Hyde, K., Saccardo, S., and Sadoff, S. (2021). Lifestyle and mental health disruptions during COVID-19. Proc Natl Acad Sci USA 118, e2016632118.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guner, Y.S., Malhotra, A., Ford, H.R., Stein, J.E., and Kelly, L.K. (2009). Association of Escherichia coli O157:H7 with necrotizing enterocolitis in a full-term infant. Pediatr Surg Int 25, 459–463.

    Article  PubMed  Google Scholar 

  • Holmes, Z.C., Silverman, J.D., Dressman, H.K., Wei, Z., Dallow, E.P., Armstrong, S.C., Seed, P.C., Rawls, J.F., AND David, L.A. (2020). Short-chain fatty acid production by gut microbiota from children with obesity differs according to prebiotic choice and bacterial community composition. mBio 11, e00914–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang, C., Huang, L., Wang, Y., Li, X., Ren, L., Gu, X., Kang, L., Guo, L., Liu, M., Zhou, X., et al. (2023). 6-Month consequences of COVID-19 in patients discharged from hospital: a cohort study. Lancet 401, e21–e33.

    Article  PubMed  PubMed Central  Google Scholar 

  • Huttenhower, C., Gevers, D., Knight, R., Abubucker, S., Badger, J.H., Chinwalla, A.T., Creasy, H.H., Earl, A.M., and Fitzgerald, M.G. (2012). Structure, function and diversity of the healthy human microbiome. Nature 486, 207–214.

    Article  CAS  Google Scholar 

  • Iddrisu, I., Monteagudo-Mera, A., Poveda, C., Pyle, S., Shahzad, M., Andrews, S., and Walton, G.E. (2021). Malnutrition and gut microbiota in children. Nutrients 13, 2727.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ignacio, A., Fernandes, M.R., Rodrigues, V.A.A., Groppo, F.C., Cardoso, A.L., Avila-Campos, M.J., and Nakano, V. (2016). Correlation between body mass index and faecal microbiota from children. Clin Microbiol Infect 22, 258.e1–258.e8.

    Article  CAS  PubMed  Google Scholar 

  • Isolauri, E. (2012). Development of healthy gut microbiota early in life. J Paediatr Child Health 48, 1–6.

    Article  PubMed  Google Scholar 

  • Korpela, K., Zijlmans, M.A.C., Kuitunen, M., Kukkonen, K., Savilahti, E., Salonen, A., de Weerth, C., and de Vos, W.M. (2017). Childhood BMI in relation to microbiota in infancy and lifetime antibiotic use. Microbiome 5, 26.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laursen, M.F., Sakanaka, M., von Burg, N., Mörbe, U., Andersen, D., Moll, J.M., Pekmez, C.T., Rivollier, A., Michaelsen, K.F., M0lgaard, C., et al. (2021). Bifidobacterium species associated with breastfeeding produce aromatic lactic acids in the infant gut. Nat Microbiol 6, 1367–1382.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lebeaux, R.M., Coker, M.O., Dade, E.F., Palys, T.J., Morrison, H.G., Ross, B.D., Baker, E.R., Karagas, M.R., Madan, J.C., and Hoen, A.G. (2021). The infant gut resistome is associated with E. coli and early-life exposures. BMC Microbiol 21, 201.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, X., Stokholm, J., Brejnrod, A., Vestergaard, G.A., Russel, J., Trivedi, U., Thorsen, J., Gupta, S., Hjelmsø, M.H., Shah, S.A., et al. (2021). The infant gut resistome associates with E. coli, environmental exposures, gut microbiome maturity, and asthma-associated bacterial composition. Cell Host Microbe 29, 975–987.e4.

    Article  CAS  PubMed  Google Scholar 

  • Lloréns-Rico, V., Gregory, A.C., Van Weyenbergh, J., Jansen, S., Van Buyten, T., Qian, J., Braz, M., Menezes, S.M., Van Mol, P., Vanderbeke, L., et al. (2021). Clinical practices underlie COVID-19 patient respiratory microbiome composition and its interactions with the host. Nat Commun 12, 6243.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lopez-Leon, S., Wegman-Ostrosky, T., Ayuzo del Valle, N.C., Perelman, C., Sepulveda, R., Rebolledo, P.A., Cuapio, A., and Villapol, S. (2022). Long-COVID in children and adolescents: a systematic review and meta-analyses. Sci Rep 12, 9950.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lopez-Siles, M., Duncan, S.H., Garcia-Gil, L.J., and Martinez-Medina, M. (2017). Faecalibacterium prausnitzii: from microbiology to diagnostics and prognostics. ISME J 11, 841–852.

    Article  PubMed  PubMed Central  Google Scholar 

  • Magne, F., Gotteland, M., Gauthier, L., Zazueta, A., Pesoa, S., Navarrete, P., and Balamurugan, R. (2020). The Firmicutes/Bacteroidetes ratio: a relevant marker of gut dysbiosis in obese patients? Nutrients 12, 1474.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mariat, D., Firmesse, O., Levenez, F., Guimarăes, V.D., Sokol, H., Doré, J., Corthier, G., and Furet, J.P. (2009). The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol 9, 123.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mu, Q., Tavella, V.J., and Luo, X.M. (2018). Role of Lactobacillus reuteri in human health and diseases. Front Microbiol 9, 757.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mueller, N.T., Bakacs, E., Combellick, J., Grigoryan, Z., and Dominguez-Bello, M.G. (2015). The infant microbiome development: mom matters. Trends Mol Med 21, 109–117.

    Article  PubMed  Google Scholar 

  • Nakakubo, S., Kishida, N., Okuda, K., Kamada, K., Iwama, M., Suzuki, M., Yokota, I., Ito, Y.M., Nasuhara, Y., Boucher, R.C., et al. (2023). Associations of COVID-19 symptoms with omicron subvariants BA.2 and BA.5, host status, and clinical outcomes in Japan: a registry-based observational study. Lancet Infect Dis 23, 1244–1256.

    Article  CAS  PubMed  Google Scholar 

  • National Health Commission of the People’s Republic of China. (2022). Growth standard for children under 7 years of age. Available from URL: http://www.nhc.gov.cn/wjw/fyjk/202211/16d8b049fdf547978a910911c19bf389/files/87dabeb-c66e1421b903f20c5db53ac07.pdf.

  • Olm, M.R., Dahan, D., Carter, M.M., Merrill, B.D., Yu, F.B., Jain, S., Meng, X., Tripathi, S., Wastyk, H., Neff, N., et al. (2022). Robust variation in infant gut microbiome assembly across a spectrum of lifestyles. Science 376, 1220–1223.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., and Glöckner, F.O. (2013). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41, D590–D596.

    Article  CAS  PubMed  Google Scholar 

  • Raman, A.S., Gehrig, J.L., Venkatesh, S., Chang, H.W., Hibberd, M.C., Subramanian, S., Kang, G., Bessong, P.O., Lima, A.A.M., Kosek, M.N., et al. (2019). A sparse covarying unit that describes healthy and impaired human gut microbiota development. Science 365, eaau4735.

    Article  PubMed  PubMed Central  Google Scholar 

  • Reyman, M., van Houten, M.A., Watson, R.L., Chu, M.L.J.N., Arp, K., de Waal, W.J., Schiering, I., Plötz, F.B., Willems, R.J.L., van Schaik, W., et al. (2022). Effects of early-life antibiotics on the developing infant gut microbiome and resistome: a randomized trial. Nat Commun 13, 893.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruohtula, T., de Goffau, M.C., Nieminen, J.K., Honkanen, J., Siljander, H., Hämäläinen, A.M., Peet, A., Tillmann, V., Ilonen, J., Niemelä, O., et al. (2019). Maturation of gut microbiota and circulating regulatory T cells and development of IgE sensitization in early life. Front Immunol 10, 2494.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sarkar, A., Yoo, J.Y., Valeria Ozorio Dutra, S., Morgan, K.H., and Groer, M. (2021). The association between early-life gut microbiota and long-term health and diseases. J Clin Med 10, 459.

    Article  PubMed  PubMed Central  Google Scholar 

  • Segers, M.E., and Lebeer, S. (2014). Towards a better understanding of Lactobacillus rhamnosus GG—host interactions. Microb Cell Fact 13, S7.

    Article  PubMed  PubMed Central  Google Scholar 

  • Serafini, G., Parmigiani, B., Amerio, A., Aguglia, A., Sher, L., and Amore, M. (2020). The psychological impact of COVID-19 on the mental health in the general population. QJM 113, 531–537.

    Article  PubMed  Google Scholar 

  • Shane, A.L. (2014). Missing microbes: how the overuse of antibiotics is fueling our modern plagues. Emerg Infect Dis 20, 1961.

    Article  PubMed Central  Google Scholar 

  • Stokholm, J., Blaser, M.J., Thorsen, J., Rasmussen, M.A., Waage, J., Vinding, R.K., Schoos, A.M.M., Kunøe, A., Fink, N.R., Chawes, B.L., et al. (2018). Maturation of the gut microbiome and risk of asthma in childhood. Nat Commun 9, 141.

    Article  PubMed  PubMed Central  Google Scholar 

  • The Lancet (2023). Long COVID: 3 years in. Lancet 401, 795.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • The Novel Coronavirus Pneumonia Emergency Response Epidemiology Team. (2020). The epidemiological characteristics of an outbreak of 2019 novel coronavirus diseases (COVID-19) in China. China CDC Weekly 2, 113–122.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turnbaugh, P.J., Ley, R.E., Mahowald, M.A., Magrini, V., Mardis, E.R., and Gordon, J. I. (2006). An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444, 1027–1031.

    Article  PubMed  Google Scholar 

  • Vandeputte, D., Kathagen, G., D’hoe, K., Vieira-Silva, S., Valles-Colomer, M., Sabino, J., Wang, J., Tito, R.Y., De Commer, L., Darzi, Y., et al. (2017). Quantitative microbiome profiling links gut community variation to microbial load. Nature 551, 507–511.

    Article  CAS  PubMed  Google Scholar 

  • Vieira-Silva, S., Sabino, J., Valles-Colomer, M., Falony, G., Kathagen, G., Caenepeel, C., Cleynen, I., van der Merwe, S., Vermeire, S., and Raes, J. (2019). Quantitative microbiome profiling disentangles inflammation- and bile duct obstruction-associated microbiota alterations across PSC/IBD diagnoses. Nat Microbiol 4, 1826–1831.

    Article  CAS  PubMed  Google Scholar 

  • Vieira-Silva, S., Falony, G., Belda, E., Nielsen, T., Aron-Wisnewsky, J., Chakaroun, R., Forslund, S.K., Assmann, K., Valles-Colomer, M., Nguyen, T.T.D., et al. (2020). Statin therapy is associated with lower prevalence of gut microbiota dysbiosis. Nature 581, 310–315.

    Article  CAS  PubMed  Google Scholar 

  • Wang, B., Zhang, L., Wang, Y., Dai, T., Qin, Z., Zhou, F., and Zhang, L. (2022a). Alterations in microbiota of patients with COVID-19: potential mechanisms and therapeutic interventions. Sig Transduct Target Ther 7, 143.

    Article  CAS  Google Scholar 

  • Wang, H., Paulson, K.R., Pease, S.A., Watson, S., Comfort, H., Zheng, P., Aravkin, A. Y., Bisignano, C., Barber, R.M., Alam, T., et al. (2022b). Estimating excess mortality due to the COVID-19 pandemic: a systematic analysis of COVID-19-related mortality, 2020–21. Lancet 399, 1513–1536.

    Article  CAS  Google Scholar 

  • Ward, D.V., Scholz, M., Zolfo, M., Taft, D.H., Schibler, K.R., Tett, A., Segata, N., and Morrow, A.L. (2016). Metagenomic sequencing with strain-level resolution implicates uropathogenic E. coli in necrotizing enterocolitis and mortality in preterm infants. Cell Rep 14, 2912–2924.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wong, E., Lui, K., Day, A.S., and Leach, S.T. (2022). Manipulating the neonatal gut microbiome: current understanding and future perspectives. Arch Dis Child Fetal Neonatal Ed 107, 346–350.

    Article  PubMed  Google Scholar 

  • World Health Organization. (2022). Mental health and COVID-19: Early evidence of the pandemic’s impact: Scientific brief, 2 march 2022. Available from URL: https://apps.who.int/iris/handle/10665/352189.

  • World Health Organization. (2023). WHO coronavirus disease (COVID-19) dashboard. Available from URL: https://covid19.who.int/.

  • Wu, D., Zhou, K., Xiao, M., Liu, Z., and Zhang, S. (2022). Differences in intestinal microbiome are associated with the mortality of COVID-19 patients in intensive care units. Sci China Life Sci 65, 1040–1042.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu, H., Esteve, E., Tremaroli, V., Khan, M.T., Caesar, R., Mannerås-Holm, L., Ståhlman, M., Olsson, L.M., Serino, M., Planas-Fèlix, M., et al. (2017). Metformin alters the gut microbiome of individuals with treatment-naive type 2 diabetes, contributing to the therapeutic effects of the drug. Nat Med 23, 850–858.

    Article  CAS  PubMed  Google Scholar 

  • Xiao, L., Wang, J., Zheng, J., Li, X., and Zhao, F. (2021). Deterministic transition of enterotypes shapes the infant gut microbiome at an early age. Genome Biol 22, 243.

    Article  PubMed  PubMed Central  Google Scholar 

  • Xiao, M., Lu, B., Ding, R., Liu, X., Wu, X., Li, Y., Liu, X., Qiu, L., Zhang, Z., Xie, J., et al. (2022). Metatranscriptomic analysis of host response and vaginal microbiome of patients with severe COVID-19. Sci China Life Sci 65, 1473–1476.

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang, I., Corwin, E.J., Brennan, P.A., Jordan, S., Murphy, J.R., and Dunlop, A. (2016). The infant microbiome. Nurs Res 65, 76–88.

    Article  PubMed  PubMed Central  Google Scholar 

  • Yeoh, Y.K., Zuo, T., Lui, G.C.Y., Zhang, F., Liu, Q., Li, A.Y., Chung, A.C., Cheung, C.P., Tso, E.Y., Fung, K.S., et al. (2021). Gut microbiota composition reflects disease severity and dysfunctional immune responses in patients with COVID-19. Gut 70, 698–706.

    Article  CAS  PubMed  Google Scholar 

  • Yilmaz, P., Parfrey, L.W., Yarza, P., Gerken, J., Pruesse, E., Quast, C., Schweer, T., Peplies, J., Ludwig, W., and Glöckner, F.O. (2014). The SILVA and “All-species Living Tree Project (LTP)” taxonomic frameworks. Nucl Acids Res 42, D643–D648.

    Article  CAS  PubMed  Google Scholar 

  • Zeng, W., Yang, F., Shen, W.L., Zhan, C., Zheng, P., and Hu, J. (2022). Interactions between central nervous system and peripheral metabolic organs. Sci China Life Sci 65, 1929–1958.

    Article  PubMed  Google Scholar 

Download references

Acknowledgement

This work was supported by the National Key Research and Development Program of China (2022YFC2303200).

Author information

Authors and Affiliations

  1. CAS Key Lab for Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, 100101, China

    Jiejing Wang, Yuejuan Li & Jun Wang

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Jiejing Wang, Yuejuan Li & Jun Wang

  3. Beijing Dr. CUIYUTAO Clinic, Beijing, 100028, China

    Yu Mu, Kefei Huang & Yutao Cui

  4. R-Institute Co. Ltd., Beijing, 100011, China

    Danyi Li & Canhui Lan

Authors
  1. Jiejing Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuejuan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yu Mu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kefei Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Danyi Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Canhui Lan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yutao Cui
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jun Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Yutao Cui or Jun Wang.

Ethics declarations

The author(s) declare that they have no conflict of interest. This study was approved by the Ethics Committee of Institute of Microbiology, Chinese Academy of Science (APIMCAS2022105).

Supplementary File for

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, J., Li, Y., Mu, Y. et al. Missing microbes in infants and children in the COVID-19 pandemic: a study of 1,126 participants in Beijing, China. Sci. China Life Sci. (2024). https://doi.org/10.1007/s11427-023-2488-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11427-023-2488-0

Search

Navigation