Skip to main content
Top
Published in: BMC Medicine 1/2023

Open Access 01-12-2023 | Type 2 Diabetes | Research article

Early-life exposure to the Great Chinese Famine and gut microbiome disruption across adulthood for type 2 diabetes: three population-based cohort studies

Authors: Wanglong Gou, Huijun Wang, Xin-yi Tang, Yan He, Chang Su, Jiguo Zhang, Ting-yu Sun, Zengliang Jiang, Zelei Miao, Yuanqing Fu, Hui Zhao, Yu-ming Chen, Bing Zhang, Hongwei Zhou, Ju-Sheng Zheng

Published in: BMC Medicine | Issue 1/2023

Login to get access

Abstract

Background

The early life stage is critical for the gut microbiota establishment and development. We aimed to investigate the lifelong impact of famine exposure during early life on the adult gut microbial ecosystem and examine the association of famine-induced disturbance in gut microbiota with type 2 diabetes.

Methods

We profiled the gut microbial composition among 11,513 adults (18–97 years) from three independent cohorts and examined the association of famine exposure during early life with alterations of adult gut microbial diversity and composition. We performed co-abundance network analyses to identify keystone taxa in the three cohorts and constructed an index with the shared keystone taxa across the three cohorts. Among each cohort, we used linear regression to examine the association of famine exposure during early life with the keystone taxa index and assessed the correlation between the keystone taxa index and type 2 diabetes using logistic regression adjusted for potential confounders. We combined the effect estimates from the three cohorts using random-effects meta-analysis.

Results

Compared with the no-exposed control group (born during 1962–1964), participants who were exposed to the famine during the first 1000 days of life (born in 1959) had consistently lower gut microbial alpha diversity and alterations in the gut microbial community during adulthood across the three cohorts. Compared with the no-exposed control group, participants who were exposed to famine during the first 1000 days of life were associated with consistently lower levels of keystone taxa index in the three cohorts (pooled beta − 0.29, 95% CI − 0.43, − 0.15). Per 1-standard deviation increment in the keystone taxa index was associated with a 13% lower risk of type 2 diabetes (pooled odds ratio 0.87, 95% CI 0.80, 0.93), with consistent results across three individual cohorts.

Conclusions

These findings reveal a potential role of the gut microbiota in the developmental origins of health and disease (DOHaD) hypothesis, deepening our understanding about the etiology of type 2 diabetes.
Appendix
Available only for authorised users
Literature
2.
go back to reference van Abeelen AFM, Elias SG, Bossuyt PMM, Grobbee DE, van der Schouw YT, Roseboom TJ, et al. Famine exposure in the young and the risk of type 2 diabetes in adulthood. Diabetes. 2012;61:2255–60.PubMedPubMedCentralCrossRef van Abeelen AFM, Elias SG, Bossuyt PMM, Grobbee DE, van der Schouw YT, Roseboom TJ, et al. Famine exposure in the young and the risk of type 2 diabetes in adulthood. Diabetes. 2012;61:2255–60.PubMedPubMedCentralCrossRef
3.
go back to reference Zou Z, Li C, Patton GC. Early-life exposure to the Chinese Famine and subsequent T2DM. Nat Rev Endocrinol. 2020;16:124–5.PubMedCrossRef Zou Z, Li C, Patton GC. Early-life exposure to the Chinese Famine and subsequent T2DM. Nat Rev Endocrinol. 2020;16:124–5.PubMedCrossRef
4.
go back to reference Li J, Liu S, Li S, Feng R, Na L, Chu X, et al. Prenatal exposure to famine and the development of hyperglycemia and type 2 diabetes in adulthood across consecutive generations: a population-based cohort study of families in Suihua, China. Am J Clin Nutr. 2017;105:221–7.PubMedCrossRef Li J, Liu S, Li S, Feng R, Na L, Chu X, et al. Prenatal exposure to famine and the development of hyperglycemia and type 2 diabetes in adulthood across consecutive generations: a population-based cohort study of families in Suihua, China. Am J Clin Nutr. 2017;105:221–7.PubMedCrossRef
5.
go back to reference Meng R, Lv J, Yu C, Guo Y, Bian Z, Yang L, et al. Prenatal famine exposure, adulthood obesity patterns and risk of type 2 diabetes. Int J Epidemiol. 2018;47:399–408.PubMedCrossRef Meng R, Lv J, Yu C, Guo Y, Bian Z, Yang L, et al. Prenatal famine exposure, adulthood obesity patterns and risk of type 2 diabetes. Int J Epidemiol. 2018;47:399–408.PubMedCrossRef
6.
go back to reference Li Y, He Y, Qi L, Jaddoe VW, Feskens EJM, Yang X, et al. Exposure to the Chinese famine in early life and the risk of hyperglycemia and type 2 diabetes in adulthood. Diabetes. 2010;59:2400–6.PubMedPubMedCentralCrossRef Li Y, He Y, Qi L, Jaddoe VW, Feskens EJM, Yang X, et al. Exposure to the Chinese famine in early life and the risk of hyperglycemia and type 2 diabetes in adulthood. Diabetes. 2010;59:2400–6.PubMedPubMedCentralCrossRef
7.
go back to reference Neel JV. Diabetes mellitus: a “thrifty” genotype rendered detrimental by “progress”? Am J Hum Genet. 1962;14:353–62.PubMedPubMedCentral Neel JV. Diabetes mellitus: a “thrifty” genotype rendered detrimental by “progress”? Am J Hum Genet. 1962;14:353–62.PubMedPubMedCentral
8.
go back to reference McMillen IC, Robinson JS. Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev. 2005;85:571–633.PubMedCrossRef McMillen IC, Robinson JS. Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev. 2005;85:571–633.PubMedCrossRef
10.
go back to reference de Vos WM, Tilg H, Van Hul M, Cani PD. Gut microbiome and health: mechanistic insights. Gut. 2022;71:1020–32.PubMedCrossRef de Vos WM, Tilg H, Van Hul M, Cani PD. Gut microbiome and health: mechanistic insights. Gut. 2022;71:1020–32.PubMedCrossRef
11.
go back to reference Gou W, Ling C-W, He Y, Jiang Z, Fu Y, Xu F, et al. Interpretable machine learning framework reveals robust gut microbiome features associated with type 2 diabetes. Diabetes Care. 2021;44:358–66.PubMedCrossRef Gou W, Ling C-W, He Y, Jiang Z, Fu Y, Xu F, et al. Interpretable machine learning framework reveals robust gut microbiome features associated with type 2 diabetes. Diabetes Care. 2021;44:358–66.PubMedCrossRef
12.
go back to reference Ruuskanen MO, Erawijantari PP, Havulinna AS, Liu Y, Méric G, Tuomilehto J, et al. Gut microbiome composition is predictive of incident type 2 diabetes in a population cohort of 5,572 Finnish adults. Diabetes Care. 2022;45:811–8.PubMedPubMedCentralCrossRef Ruuskanen MO, Erawijantari PP, Havulinna AS, Liu Y, Méric G, Tuomilehto J, et al. Gut microbiome composition is predictive of incident type 2 diabetes in a population cohort of 5,572 Finnish adults. Diabetes Care. 2022;45:811–8.PubMedPubMedCentralCrossRef
13.
go back to reference Wang H, Gou W, Su C, Du W, Zhang J, Miao Z, et al. Association of gut microbiota with glycaemic traits and incident type 2 diabetes, and modulation by habitual diet: a population-based longitudinal cohort study in Chinese adults. Diabetologia. 2022;65:1145–56.PubMedPubMedCentralCrossRef Wang H, Gou W, Su C, Du W, Zhang J, Miao Z, et al. Association of gut microbiota with glycaemic traits and incident type 2 diabetes, and modulation by habitual diet: a population-based longitudinal cohort study in Chinese adults. Diabetologia. 2022;65:1145–56.PubMedPubMedCentralCrossRef
14.
go back to reference Robertson RC, Manges AR, Finlay BB, Prendergast AJ. The human microbiome and child growth - first 1000 days and beyond. Trends Microbiol. 2019;27:131–47.PubMedCrossRef Robertson RC, Manges AR, Finlay BB, Prendergast AJ. The human microbiome and child growth - first 1000 days and beyond. Trends Microbiol. 2019;27:131–47.PubMedCrossRef
15.
go back to reference Reyman M, van Houten MA, Watson RL, Chu MLJN, Arp K, de Waal WJ, et al. Effects of early-life antibiotics on the developing infant gut microbiome and resistome: a randomized trial. Nat Commun. 2022;13:1–12.CrossRef Reyman M, van Houten MA, Watson RL, Chu MLJN, Arp K, de Waal WJ, et al. Effects of early-life antibiotics on the developing infant gut microbiome and resistome: a randomized trial. Nat Commun. 2022;13:1–12.CrossRef
16.
go back to reference Gou W, Ling C-W, He Y, Jiang Z, Fu Y, Xu F, et al. Westlake Gut Project: a consortium of microbiome epidemiology for the gut microbiome and health research in China. Med Microecol. 2022;14:100064.CrossRef Gou W, Ling C-W, He Y, Jiang Z, Fu Y, Xu F, et al. Westlake Gut Project: a consortium of microbiome epidemiology for the gut microbiome and health research in China. Med Microecol. 2022;14:100064.CrossRef
17.
go back to reference Zhang Z-Q, He L-P, Liu Y-H, Liu J, Su Y-X, Chen Y-M. Association between dietary intake of flavonoid and bone mineral density in middle aged and elderly Chinese women and men. Osteoporos Int. 2014;25:2417–25.PubMedCrossRef Zhang Z-Q, He L-P, Liu Y-H, Liu J, Su Y-X, Chen Y-M. Association between dietary intake of flavonoid and bone mineral density in middle aged and elderly Chinese women and men. Osteoporos Int. 2014;25:2417–25.PubMedCrossRef
18.
go back to reference He Y, Wu W, Zheng H-M, Li P, McDonald D, Sheng H-F, et al. Regional variation limits applications of healthy gut microbiome reference ranges and disease models. Nat Med. 2018;24:1532–5.PubMedCrossRef He Y, Wu W, Zheng H-M, Li P, McDonald D, Sheng H-F, et al. Regional variation limits applications of healthy gut microbiome reference ranges and disease models. Nat Med. 2018;24:1532–5.PubMedCrossRef
19.
go back to reference Popkin BM, Du S, Zhai F, Zhang B. Cohort profile: the China Health and Nutrition Survey–monitoring and understanding socio-economic and health change in China, 1989–2011. Int J Epidemiol. 2010;39:1435–40.PubMedCrossRef Popkin BM, Du S, Zhai F, Zhang B. Cohort profile: the China Health and Nutrition Survey–monitoring and understanding socio-economic and health change in China, 1989–2011. Int J Epidemiol. 2010;39:1435–40.PubMedCrossRef
20.
go back to reference Yang DT. China’s agricultural crisis and famine of 1959–1961: a survey and comparison to Soviet famines. Comp Econ Stud. 2008;50:1–29.CrossRef Yang DT. China’s agricultural crisis and famine of 1959–1961: a survey and comparison to Soviet famines. Comp Econ Stud. 2008;50:1–29.CrossRef
21.
go back to reference Li Y, Li Y, Gurol ME, Liu Y, Yang P, Shi J, et al. In utero exposure to the Great Chinese Famine and risk of intracerebral hemorrhage in midlife. Neurology. 2020;94:e1996-2004.PubMedPubMedCentralCrossRef Li Y, Li Y, Gurol ME, Liu Y, Yang P, Shi J, et al. In utero exposure to the Great Chinese Famine and risk of intracerebral hemorrhage in midlife. Neurology. 2020;94:e1996-2004.PubMedPubMedCentralCrossRef
22.
go back to reference Zhang X, Wang G, Forman MR, Fu Q, Rogers CJ, Wu S, et al. In utero and childhood exposure to the Great Chinese Famine and risk of cancer in adulthood: the Kailuan Study. Am J Clin Nutr. 2021;114:2017–24.PubMedCrossRef Zhang X, Wang G, Forman MR, Fu Q, Rogers CJ, Wu S, et al. In utero and childhood exposure to the Great Chinese Famine and risk of cancer in adulthood: the Kailuan Study. Am J Clin Nutr. 2021;114:2017–24.PubMedCrossRef
23.
go back to reference Canivell S, Gomis R. Diagnosis and classification of autoimmune diabetes mellitus. Autoimmun Rev. 2014;13:403–7.PubMedCrossRef Canivell S, Gomis R. Diagnosis and classification of autoimmune diabetes mellitus. Autoimmun Rev. 2014;13:403–7.PubMedCrossRef
24.
go back to reference Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R. O, R.B., Simpson, G.L., Solymos, P., Henry, H., Wagner S. vegan: community ecology package. 2015. https://cran.r-project.org. Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R. O, R.B., Simpson, G.L., Solymos, P., Henry, H., Wagner S. vegan: community ecology package. 2015. https://​cran.​r-project.​org.
25.
go back to reference Zmora N, Suez J, Elinav E. You are what you eat: diet, health and the gut microbiota. Nat Rev Gastroenterol Hepatol. 2019;16:35–56.PubMedCrossRef Zmora N, Suez J, Elinav E. You are what you eat: diet, health and the gut microbiota. Nat Rev Gastroenterol Hepatol. 2019;16:35–56.PubMedCrossRef
26.
go back to reference Li C, Lumey LH. Exposure to the Chinese Famine of 1959–61 in early life and long-term health conditions: a systematic review and meta-analysis. Int J Epidemiol. 2017;46:1157–70.PubMedCrossRef Li C, Lumey LH. Exposure to the Chinese Famine of 1959–61 in early life and long-term health conditions: a systematic review and meta-analysis. Int J Epidemiol. 2017;46:1157–70.PubMedCrossRef
27.
go back to reference Peschel S, Müller CL, von Mutius E, Boulesteix A-L, Depner M. NetCoMi: network construction and comparison for microbiome data in R. Brief Bioinform. 2021;22:bbaa290.PubMedCrossRef Peschel S, Müller CL, von Mutius E, Boulesteix A-L, Depner M. NetCoMi: network construction and comparison for microbiome data in R. Brief Bioinform. 2021;22:bbaa290.PubMedCrossRef
28.
go back to reference Palarea-Albaladejo J, Martín-Fernández JA. zCompositions—R package for multivariate imputation of left-censored data under a compositional approach. Chemom Intell Lab Syst. 2015;143:85–96.CrossRef Palarea-Albaladejo J, Martín-Fernández JA. zCompositions—R package for multivariate imputation of left-censored data under a compositional approach. Chemom Intell Lab Syst. 2015;143:85–96.CrossRef
29.
go back to reference Clauset A, Newman MEJ, Moore C. Finding community structure in very large networks. Phys Rev E. 2004;70:066111.CrossRef Clauset A, Newman MEJ, Moore C. Finding community structure in very large networks. Phys Rev E. 2004;70:066111.CrossRef
30.
go back to reference Li C, Tobi EW, Heijmans BT, Lumey LH. The effect of the Chinese Famine on type 2 diabetes mellitus epidemics. Nat Rev Endocrinol. 2019;15:313–4.PubMedCrossRef Li C, Tobi EW, Heijmans BT, Lumey LH. The effect of the Chinese Famine on type 2 diabetes mellitus epidemics. Nat Rev Endocrinol. 2019;15:313–4.PubMedCrossRef
32.
go back to reference Kurtz ZD, Müller CL, Miraldi ER, Littman DR. Sparse and compositionally robust inference of microbial ecological networks. PLoS Comput Biol. 2015;11:e1004226.PubMedPubMedCentralCrossRef Kurtz ZD, Müller CL, Miraldi ER, Littman DR. Sparse and compositionally robust inference of microbial ecological networks. PLoS Comput Biol. 2015;11:e1004226.PubMedPubMedCentralCrossRef
33.
go back to reference Gil A, Rueda R, Ozanne SE, van der Beek EM, van Loo-Bouwman C, Schoemaker M, et al. Is there evidence for bacterial transfer via the placenta and any role in the colonization of the infant gut? - a systematic review. Crit Rev Microbiol. 2020;46:493–507.PubMedCrossRef Gil A, Rueda R, Ozanne SE, van der Beek EM, van Loo-Bouwman C, Schoemaker M, et al. Is there evidence for bacterial transfer via the placenta and any role in the colonization of the infant gut? - a systematic review. Crit Rev Microbiol. 2020;46:493–507.PubMedCrossRef
34.
go back to reference Bäckhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P, et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe. 2015;17:690–703.PubMedCrossRef Bäckhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P, et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe. 2015;17:690–703.PubMedCrossRef
35.
go back to reference Roswall J, Olsson LM, Kovatcheva-Datchary P, Nilsson S, Tremaroli V, Simon M-C, et al. Developmental trajectory of the healthy human gut microbiota during the first 5 years of life. Cell Host Microbe. 2021;29:765-776.e3.PubMedCrossRef Roswall J, Olsson LM, Kovatcheva-Datchary P, Nilsson S, Tremaroli V, Simon M-C, et al. Developmental trajectory of the healthy human gut microbiota during the first 5 years of life. Cell Host Microbe. 2021;29:765-776.e3.PubMedCrossRef
36.
go back to reference Subramanian S, Huq S, Yatsunenko T, Haque R, Mahfuz M, Alam MA, et al. Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature. 2014;510:417–21.PubMedPubMedCentralCrossRef Subramanian S, Huq S, Yatsunenko T, Haque R, Mahfuz M, Alam MA, et al. Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature. 2014;510:417–21.PubMedPubMedCentralCrossRef
37.
go back to reference Blanton L V, Charbonneau MR, Salih T, Barratt MJ, Venkatesh S, Ilkaveya O, et al. Gut bacteria that prevent growth impairments transmitted by microbiota from malnourished children. Science. 2016;351:10.1126/science.aad3311. Blanton L V, Charbonneau MR, Salih T, Barratt MJ, Venkatesh S, Ilkaveya O, et al. Gut bacteria that prevent growth impairments transmitted by microbiota from malnourished children. Science. 2016;351:10.1126/science.aad3311.
38.
go back to reference Sarkar A, Yoo JY, Valeria Ozorio Dutra S, Morgan KH, Groer M. The association between early-life gut microbiota and long-term health and diseases. J Clin Med. 2021;10:459.PubMedPubMedCentralCrossRef Sarkar A, Yoo JY, Valeria Ozorio Dutra S, Morgan KH, Groer M. The association between early-life gut microbiota and long-term health and diseases. J Clin Med. 2021;10:459.PubMedPubMedCentralCrossRef
39.
40.
go back to reference Fan Y, Pedersen O. Gut microbiota in human metabolic health and disease. Nat Rev Microbiol. 2021;19:55–71.PubMedCrossRef Fan Y, Pedersen O. Gut microbiota in human metabolic health and disease. Nat Rev Microbiol. 2021;19:55–71.PubMedCrossRef
41.
go back to reference Chen Z, Radjabzadeh D, Chen L, Kurilshikov A, Kavousi M, Ahmadizar F, et al. Association of insulin resistance and type 2 diabetes with gut microbial diversity: a microbiome-wide analysis from population studies. JAMA Netw Open. 2021;4:e2118811.PubMedPubMedCentralCrossRef Chen Z, Radjabzadeh D, Chen L, Kurilshikov A, Kavousi M, Ahmadizar F, et al. Association of insulin resistance and type 2 diabetes with gut microbial diversity: a microbiome-wide analysis from population studies. JAMA Netw Open. 2021;4:e2118811.PubMedPubMedCentralCrossRef
42.
go back to reference Banerjee S, Schlaeppi K, van der Heijden MGA. Keystone taxa as drivers of microbiome structure and functioning. Nat Rev Microbiol. 2018;16:567–76.PubMedCrossRef Banerjee S, Schlaeppi K, van der Heijden MGA. Keystone taxa as drivers of microbiome structure and functioning. Nat Rev Microbiol. 2018;16:567–76.PubMedCrossRef
43.
go back to reference Liang S, Sin ZY, Yu J, Zhao S, Xi Z, Bruzzone R, et al. Multi-cohort analysis of depression-associated gut bacteria sheds insight on bacterial biomarkers across populations. Cell Mol Life Sci. 2022;80:9.PubMedCrossRef Liang S, Sin ZY, Yu J, Zhao S, Xi Z, Bruzzone R, et al. Multi-cohort analysis of depression-associated gut bacteria sheds insight on bacterial biomarkers across populations. Cell Mol Life Sci. 2022;80:9.PubMedCrossRef
45.
go back to reference Vojinovic D, Radjabzadeh D, Kurilshikov A, Amin N, Wijmenga C, Franke L, et al. Relationship between gut microbiota and circulating metabolites in population-based cohorts. Nat Commun. 2019;10:5813.PubMedPubMedCentralCrossRef Vojinovic D, Radjabzadeh D, Kurilshikov A, Amin N, Wijmenga C, Franke L, et al. Relationship between gut microbiota and circulating metabolites in population-based cohorts. Nat Commun. 2019;10:5813.PubMedPubMedCentralCrossRef
46.
go back to reference Atzeni A, Bastiaanssen TFS, Cryan JF, Tinahones FJ, Vioque J, Corella D, et al. Taxonomic and functional fecal microbiota signatures associated with insulin resistance in non-diabetic subjects with overweight/obesity within the frame of the PREDIMED-Plus study. Front Endocrinol. 2022;13:804455.CrossRef Atzeni A, Bastiaanssen TFS, Cryan JF, Tinahones FJ, Vioque J, Corella D, et al. Taxonomic and functional fecal microbiota signatures associated with insulin resistance in non-diabetic subjects with overweight/obesity within the frame of the PREDIMED-Plus study. Front Endocrinol. 2022;13:804455.CrossRef
47.
go back to reference Cui J, Ramesh G, Wu M, Jensen ET, Crago O, Bertoni AG, et al. Butyrate-producing bacteria and insulin homeostasis: the Microbiome and Insulin Longitudinal Evaluation Study (MILES). Diabetes. 2022;71:2438–46.PubMedCrossRef Cui J, Ramesh G, Wu M, Jensen ET, Crago O, Bertoni AG, et al. Butyrate-producing bacteria and insulin homeostasis: the Microbiome and Insulin Longitudinal Evaluation Study (MILES). Diabetes. 2022;71:2438–46.PubMedCrossRef
48.
go back to reference Parker BJ, Wearsch PA, Veloo ACM, Rodriguez-Palacios A. The genus Alistipes: gut bacteria with emerging implications to inflammation, cancer, and mental health. Front Immunol. 2020;11:906.PubMedPubMedCentralCrossRef Parker BJ, Wearsch PA, Veloo ACM, Rodriguez-Palacios A. The genus Alistipes: gut bacteria with emerging implications to inflammation, cancer, and mental health. Front Immunol. 2020;11:906.PubMedPubMedCentralCrossRef
49.
go back to reference Chng KR, Ghosh TS, Tan YH, Nandi T, Lee IR, Ng AHQ, et al. Metagenome-wide association analysis identifies microbial determinants of post-antibiotic ecological recovery in the gut. Nat Ecol Evol. 2020;4:1256–67.PubMedCrossRef Chng KR, Ghosh TS, Tan YH, Nandi T, Lee IR, Ng AHQ, et al. Metagenome-wide association analysis identifies microbial determinants of post-antibiotic ecological recovery in the gut. Nat Ecol Evol. 2020;4:1256–67.PubMedCrossRef
50.
go back to reference St Clair D, Xu M, Wang P, Yu Y, Fang Y, Zhang F, et al. Rates of adult schizophrenia following prenatal exposure to the Chinese famine of 1959–1961. JAMA. 2005;294:557–62.PubMedCrossRef St Clair D, Xu M, Wang P, Yu Y, Fang Y, Zhang F, et al. Rates of adult schizophrenia following prenatal exposure to the Chinese famine of 1959–1961. JAMA. 2005;294:557–62.PubMedCrossRef
Metadata
Title
Early-life exposure to the Great Chinese Famine and gut microbiome disruption across adulthood for type 2 diabetes: three population-based cohort studies
Authors
Wanglong Gou
Huijun Wang
Xin-yi Tang
Yan He
Chang Su
Jiguo Zhang
Ting-yu Sun
Zengliang Jiang
Zelei Miao
Yuanqing Fu
Hui Zhao
Yu-ming Chen
Bing Zhang
Hongwei Zhou
Ju-Sheng Zheng
Publication date
01-12-2023
Publisher
BioMed Central
Published in
BMC Medicine / Issue 1/2023
Electronic ISSN: 1741-7015
DOI
https://doi.org/10.1186/s12916-023-03123-y

Other articles of this Issue 1/2023

BMC Medicine 1/2023 Go to the issue