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Review Article

The association of infant and mother gut microbiomes with development of allergic diseases in children: a systematic review

, MD, , MD, , MD, , MD, , PhD, , PhD & , PhD show all
Received 20 Dec 2023, Accepted 15 Mar 2024, Published online: 04 Apr 2024

References

  • Mazur M, Czarnobilska M, Dyga W, Czarnobilska E. Trends in the epidemiology of allergic diseases of the airways in children growing up in an urban agglomeration. J Clin Med. 2022;11(8):2188.
  • Doll RJ, Joseph NI, McGarry D, Jhaveri D, Sher T, Hostoffer R. Epidemiology of allergic diseases. Allergy and asthma: the basics to best practices. Cham: Springer International Publishing; 2019:31–51.
  • Atopic Dermatitis. Atopic dermatitis: National Institute of Health. Available from : https://www.niams.nih.gov/health-topics/atopic-dermatitis#:∼:text=Atopic%20dermatitis%2C%20often%20referred%20to,the%20disease%20at%20any%20age.
  • Nutten S. Atopic dermatitis: global epidemiology and risk factors. Ann Nutr Metab. 2015;66 Suppl 1(Suppl. 1):8–16. doi:10.1159/000370220.
  • Flohr C, Mann J. New insights into the epidemiology of childhood atopic dermatitis. Allergy. 2014;69(1):3–16. doi:10.1111/all.12270.
  • Okada H, Kuhn C, Feillet H, Bach JF. The ‘hygiene hypothesis’ for autoimmune and allergic diseases: an update. Clin Exp Immunol. 2010;160(1):1–9. doi:10.1111/j.1365-2249.2010.04139.x.
  • Pfefferle PI, Keber CU, Cohen RM, Garn H. The hygiene hypothesis – learning from but not living in the past. Front Immunol. 2021;12:635935. doi:10.3389/fimmu.2021.635935.
  • Hou K, Wu ZX, Chen XY, Wang JQ, Zhang D, Xiao C, Zhu D, Koya JB, Wei L, Li J, et al. Microbiota in health and diseases. Signal Transduct Target Ther. 2022;7(1):135.
  • Ogunrinola GA, Oyewale JO, Oshamika OO, Olasehinde GI. The human microbiome and its impacts on health. Int J Microbiol. 2020;2020:8045646–8045647. doi:10.1155/2020/8045646.
  • Sun S, Wang H, Howard AG, Zhang J, Su C, Wang Z, Du S, Fodor AA, Gordon-Larsen P, Zhang B, et al. Loss of novel diversity in human gut microbiota associated with ongoing urbanization in China. Msystems. 2022;7(4):e00200-22. doi:10.1128/msystems.00200-22.
  • Winglee K, Howard AG, Sha W, Gharaibeh RZ, Liu J, Jin D, Fodor AA, Gordon-Larsen P. Recent urbanization in China is correlated with a westernized microbiome encoding increased virulence and antibiotic resistance genes. Microbiome. 2017;5(1):121. doi:10.1186/s40168-017-0338-7.
  • Gomaa EZ. Human gut microbiota/microbiome in health and diseases: a review. Antonie Van Leeuwenhoek. 2020;113(12):2019–2040. doi:10.1007/s10482-020-01474-7.
  • Fan Y, Pedersen O. Gut microbiota in human metabolic health and disease. Nat Rev Microbiol. 2021;19(1):55–71. doi:10.1038/s41579-020-0433-9.
  • Simonyte Sjödin K, Vidman L, Rydén P, West CE. Emerging evidence of the role of gut microbiota in the development of allergic diseases. Curr Opin Allergy Clin Immunol. 2016;16(4):390–395. doi:10.1097/ACI.0000000000000277.
  • Lee M-J, Kang M-J, Lee S-Y, Lee E, Kim K, Won S, Suh DI, Kim KW, Sheen YH, Ahn K, et al. Perturbations of gut microbiome genes in infants with atopic dermatitis according to feeding type. J Allergy Clin Immunol. 2018;141(4):1310–1319. doi:10.1016/j.jaci.2017.11.045.
  • Nylund L, Nermes M, Isolauri E, Salminen S, de Vos WM, Satokari R. Severity of atopic disease inversely correlates with intestinal microbiota diversity and butyrate-producing bacteria. Allergy. 2015;70(2):241–244. doi:10.1111/all.12549.
  • Mueller NT, Bakacs E, Combellick J, Grigoryan Z, Dominguez-Bello MG. The infant microbiome development: mom matters. Trends Mol Med. 2015;21(2):109–117. doi:10.1016/j.molmed.2014.12.002.
  • Khodayar-Pardo P, Mira-Pascual L, Collado MC, Martínez-Costa C. Impact of lactation stage, gestational age and mode of delivery on breast milk microbiota. J Perinatol. 2014;34(8):599–605. doi:10.1038/jp.2014.47.
  • Cabrera-Rubio R, Collado MC, Laitinen K, Salminen S, Isolauri E, Mira A. The human milk microbiome changes over lactation and is shaped by maternal weight and mode of delivery. Am J Clin Nutr. 2012;96(3):544–551. doi:10.3945/ajcn.112.037382.
  • Rey-Mariño A, Francino MP. Nutrition, gut microbiota, and allergy development in infants. Nutrients. 2022;14(20):4316. doi:10.3390/nu14204316.
  • Noverr MC, Huffnagle GB. The ‘microflora hypothesis’ of allergic diseases. Clin Exp Allergy. 2005;35(12):1511–1520. doi:10.1111/j.1365-2222.2005.02379.x.
  • Cukrowska B, Bierła JB, Zakrzewska M, Klukowski M, Maciorkowska E. The relationship between the infant gut microbiota and allergy. The role of bifidobacterium breve and prebiotic oligosaccharides in the activation of anti-allergic mechanisms in early life. Nutrients. 2020;12(4):946. doi:10.3390/nu12040946.
  • Łoś-Rycharska E, Gołębiewski M, Grzybowski T, Rogalla-Ładniak U, Krogulska A. The microbiome and its impact on food allergy and atopic dermatitis in children. Postepy Dermatol Alergol. 2020;37(5):641–650. doi:10.5114/ada.2019.90120.
  • Borre YE, O'Keeffe GW, Clarke G, Stanton C, Dinan TG, Cryan JF. Microbiota and neurodevelopmental windows: implications for brain disorders. Trends Mol Med. 2014;20(9):509–518. doi:10.1016/j.molmed.2014.05.002.
  • Vallès Y, Francino MP. Air pollution, early life microbiome, and development. Curr Environ Health Rep. 2018;5(4):512–521. doi:10.1007/s40572-018-0215-y.
  • Lee YC. Synergistic effect of various regulatory factors in TH1/TH2 balance; immunotherapeutic approaches in asthma. Int J Biomed Sci. 2008;4(1):8–13. doi:10.59566/IJBS.2008.4008.
  • Vernocchi P, Del Chierico F, Fiocchi AG, El Hachem M, Dallapiccola B, Rossi P, Putignani L. Understanding probiotics’ role in allergic children: the clue of gut microbiota profiling. Curr Opin Allergy Clin Immunol. 2015;15(5):495–503. doi:10.1097/ACI.0000000000000203.
  • Round JL, Mazmanian SK. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci U S A. 2010;107(27):12204–12209. doi:10.1073/pnas.0909122107.
  • Geuking MB, Cahenzli J, Lawson MAE, Ng DCK, Slack E, Hapfelmeier S, McCoy KD, Macpherson AJ. Intestinal bacterial colonization induces mutualistic regulatory T cell responses. Immunity. 2011;34(5):794–806. doi:10.1016/j.immuni.2011.03.021.
  • Tanaka M, Nakayama J. Development of the gut microbiota in infancy and its impact on health in later life. Allergol Int. 2017;66(4):515–522. doi:10.1016/j.alit.2017.07.010.
  • Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, Shamseer L, Tetzlaff JM, Akl EA, Brennan SE, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71. doi:10.1136/bmj.n71.
  • Arrieta M-C, Arévalo A, Stiemsma L, Dimitriu P, Chico ME, Loor S, Vaca M, Boutin RCT, Morien E, Jin M, et al. Associations between infant fungal and bacterial dysbiosis and childhood atopic wheeze in a nonindustrialized setting. J Allergy Clin Immunol. 2018;142(2):424–434.e10. doi:10.1016/j.jaci.2017.08.041.
  • Low JSY, Soh S-E, Lee YK, Kwek KYC, Holbrook JD, Van der Beek EM, Shek LP, Goh AEN, Teoh OH, Godfrey KM, et al. Ratio of klebsiella/bifidobacterium in early life correlates with later development of paediatric allergy. Benef Microbes. 2017;8(5):681–695. doi:10.3920/BM2017.0020.
  • Stiemsma LT, Arrieta M-C, Dimitriu PA, Cheng J, Thorson L, Lefebvre DL, Azad MB, Subbarao P, Mandhane P, Becker A, et al. Shifts in Lachnospira and Clostridium sp. in the 3-month stool microbiome are associated with preschool age asthma. Clin Sci (Lond). 2016;130(23):2199–2207. doi:10.1042/CS20160349.
  • Ismail IH, Boyle RJ, Licciardi PV, Oppedisano F, Lahtinen S, Robins-Browne RM, Tang MLK. Early gut colonization by Bifidobacterium breve and B. catenulatum differentially modulates eczema risk in children at high risk of developing allergic disease. Pediatr Allergy Immunol. 2016;27(8):838–846. doi:10.1111/pai.12646.
  • West CE, Rydén P, Lundin D, Engstrand L, Tulic MK, Prescott SL. Gut microbiome and innate immune response patterns in IgE-associated eczema. Clin Exp Allergy. 2015;45(9):1419–1429. doi:10.1111/cea.12566.
  • Arrieta M-C, Stiemsma LT, Dimitriu PA, Thorson L, Russell S, Yurist-Doutsch S, Kuzeljevic B, Gold MJ, Britton HM, Lefebvre DL, et al. Early infancy microbial and metabolic alterations affect risk of childhood asthma. Sci Transl Med. 2015;7(307):307ra152. doi:10.1126/scitranslmed.aab2271.
  • Wang M, Karlsson C, Olsson C, Adlerberth I, Wold AE, Strachan DP, Martricardi PM, Aberg N, Perkin MR, Tripodi S, et al. Reduced diversity in the early fecal microbiota of infants with atopic eczema. J Allergy Clin Immunol. 2008;121(1):129–134. doi:10.1016/j.jaci.2007.09.011.
  • Gore C, Munro K, Lay C, Bibiloni R, Morris J, Woodcock A, Custovic A, Tannock GW. Bifidobacterium pseudocatenulatum is associated with atopic eczema: a nested case-control study investigating the fecal microbiota of infants. J Allergy Clin Immunol. 2008;121(1):135–140. doi:10.1016/j.jaci.2007.07.061.
  • Tanabe H, Sakurai K, Nakanishi Y, Kato T, Kawasaki Y, Nakano T, Yamaide F, Taguchi-Atarashi N, Shiko Y, et al. Association of the maternal gut microbiota/metabolome with cord blood CCL17. Nutrients. 2021;13(8):2837. doi:10.3390/nu13082837.
  • Seppo AE, Bu K, Jumabaeva M, Thakar J, Choudhury RA, Yonemitsu C, Bode L, Martina CA, Allen M, Tamburini S, et al. Infant gut microbiome is enriched with Bifidobacterium longum ssp. infantis in Old Order Mennonites with traditional farming lifestyle. Allergy. 2021;76(11):3489–3503. doi:10.1111/all.14877.
  • Schei K, Simpson MR, Øien T, Salamati S, Rudi K, Ødegård RA. Allergy-Related diseases and early gut fungal and bacterial microbiota abundances in children. Clin Transl Allergy. 2021;11(5):e12041. doi:10.1002/clt2.12041.
  • Lehtimäki J, Thorsen J, Rasmussen MA, Hjelmsø M, Shah S, Mortensen MS, Trivedi U, Vestergaard G, Bønnelykke K, Chawes BL, et al. Urbanized microbiota in infants, immune constitution, and later risk of atopic diseases. J Allergy Clin Immunol. 2021;148(1):234–243. doi:10.1016/j.jaci.2020.12.621.
  • Vuillermin PJ, O'Hely M, Collier F, Allen KJ, Tang MLK, Harrison LC, Carlin JB, Saffery R, Ranganathan S, Sly PD, et al. Maternal carriage of Prevotella during pregnancy associates with protection against food allergy in the offspring. Nat Commun. 2020;11(1):1452. doi:10.1038/s41467-020-14552-1.
  • Chan CWH, Yuet Wa Chan J, Leung TF, Choi KC, Tsui SKW, Wong CL, et al. Altered gut microbiome and environmental factors associated with development of eczema in Hong Kong infants: a 4-month pilot study. Int J Environ Res Public Health. 2020;17(20):7634.
  • Tanabe H, Sakurai K, Kato T, Kawasaki Y, Nakano T, Yamaide F, Taguchi-Atarashi N, Watanabe M, Ochiai S, Ohno H, et al. Association of the maternal microbiome in Japanese pregnant women with the cumulative prevalence of dermatitis in early infancy: a pilot study from the Chiba study of Mother and Child Health birth cohort. World Allergy Organ J. 2019;12(10):100065. doi:10.1016/j.waojou.2019.100065.
  • Simonyté Sjödin K, Hammarström M-L, Rydén P, Sjödin A, Hernell O, Engstrand L, West CE. Temporal and long-term gut microbiota variation in allergic disease: a prospective study from infancy to school age. Allergy. 2019;74(1):176–185. doi:10.1111/all.13485.
  • Stokholm J, Blaser MJ, Thorsen J, Rasmussen MA, Waage J, Vinding RK, Schoos A-MM, Kunøe A, Fink NR, Chawes BL, et al. Maturation of the gut microbiome and risk of asthma in childhood. Nat Commun. 2018;9(1):141. doi:10.1038/s41467-017-02573-2.
  • Chua H-H, Chou H-C, Tung Y-L, Chiang B-L, Liao C-C, Liu H-H, Ni Y-H. Intestinal dysbiosis featuring abundance of Ruminococcus gnavus associates with allergic diseases in infants. Gastroenterology. 2018;154(1):154–167. doi:10.1053/j.gastro.2017.09.006.
  • Tun HM, Konya T, Takaro TK, Brook JR, Chari R, Field CJ, Guttman DS, Becker AB, Mandhane PJ, Turvey SE, et al. Exposure to household furry pets influences the gut microbiota of infants at 3–4 months following various birth scenarios. Microbiome. 2017;5(1):40. doi:10.1186/s40168-017-0254-x.
  • Fujimura KE, Sitarik AR, Havstad S, Lin DL, Levan S, Fadrosh D, Panzer AR, LaMere B, Rackaityte E, Lukacs NW, et al. Neonatal gut microbiota associates with childhood multisensitized atopy and T cell differentiation. Nat Med. 2016;22(10):1187–1191. doi:10.1038/nm.4176.
  • Carvalho-Queiroz C, Johansson MA, Persson J-O, Jörtsö E, Kjerstadius T, Nilsson C, Saghafian-Hedengren S, Sverremark-Ekström E. Associations between EBV and CMV seropositivity, early exposures, and gut microbiota in a prospective birth cohort: a 10-year follow-up. Front Pediatr. 2016;4:93. doi:10.3389/fped.2016.00093.
  • Abrahamsson TR, Jakobsson HE, Andersson AF, Björkstén B, Engstrand L, Jenmalm MC. Low gut microbiota diversity in early infancy precedes asthma at school age. Clin Exp Allergy. 2014;44(6):842–850. doi:10.1111/cea.12253.
  • Nermes M, Niinivirta K, Nylund L, Laitinen K, Matomäki J, Salminen S, Isolauri E. Perinatal pet exposure, faecal microbiota, and wheezy bronchitis: is there a connection? ISRN Allergy. 2013;2013:827934–827936. doi:10.1155/2013/827934.
  • Gosalbes MJ, Llop S, Vallès Y, Moya A, Ballester F, Francino MP. Meconium microbiota types dominated by lactic acid or enteric bacteria are differentially associated with maternal eczema and respiratory problems in infants. Clin Exp Allergy. 2013;43(2):198–211. doi:10.1111/cea.12063.
  • Rudi K, Storrø O, Oien T, Johnsen R. Modelling bacterial transmission in human allergen-specific IgE sensitization. Lett Appl Microbiol. 2012;54(5):447–454. doi:10.1111/j.1472-765X.2012.03229.x.
  • Lange NE, Celedón JC, Forno E, Ly NP, Onderdonk A, Bry L, Delaney ML, DuBois AM, Gold DR, Weiss ST, et al. Maternal intestinal flora and wheeze in early childhood. Clin Exp Allergy. 2012;42(6):901–908. doi:10.1111/j.1365-2222.2011.03950.x.
  • Sekirov I, Russell SL, Antunes LC, Finlay BB. Gut microbiota in health and disease. Physiol Rev. 2010;90(3):859–904. doi:10.1152/physrev.00045.2009.
  • Kang YB, Cai Y, Zhang H. Gut microbiota and allergy/asthma: from pathogenesis to new therapeutic strategies. Allergol Immunopathol (Madr). 2017;45(3):305–309. doi:10.1016/j.aller.2016.08.004.
  • West CE. Gut microbiota and allergic disease: new findings. Curr Opin Clin Nutr Metab Care. 2014;17(3):261–266. doi:10.1097/MCO.0000000000000044.
  • Bridgman SL, Kozyrskyj AL, Scott JA, Becker AB, Azad MB. Gut microbiota and allergic disease in children. Ann Allergy Asthma Immunol. 2016;116(2):99–105. doi:10.1016/j.anai.2015.10.001.
  • Nogal A, Valdes AM, Menni C. The role of short-chain fatty acids in the interplay between gut microbiota and diet in cardio-metabolic health. Gut Microbes. 2021;13(1):1–24. doi:10.1080/19490976.2021.1897212.
  • Patrick DM, Sbihi H, Dai DLY, Al Mamun A, Rasali D, Rose C, Marra F, Boutin RCT, Petersen C, Stiemsma LT, et al. Decreasing antibiotic use, the gut microbiota, and asthma incidence in children: evidence from population-based and prospective cohort studies. Lancet Respir Med. 2020;8(11):1094–1105. doi:10.1016/S2213-2600(20)30052-7.
  • Demirci M, Tokman HB, Uysal HK, Demiryas S, Karakullukcu A, Saribas S, Cokugras H, Kocazeybek BS. Reduced Akkermansia muciniphila and Faecalibacterium prausnitzii levels in the gut microbiota of children with allergic asthma. Allergol Immunopathol (Madr). 2019;47(4):365–371. doi:10.1016/j.aller.2018.12.009.
  • Dzidic M, Abrahamsson TR, Artacho A, Björkstén B, Collado MC, Mira A, Jenmalm MC. Aberrant IgA responses to the gut microbiota during infancy precede asthma and allergy development. J Allergy Clin Immunol. 2017;139(3):1017–1025.e14. doi:10.1016/j.jaci.2016.06.047.
  • Candela M, Rampelli S, Turroni S, Severgnini M, Consolandi C, De Bellis G, Masetti R, Ricci G, Pession A, Brigidi P, et al. Unbalance of intestinal microbiota in atopic children. BMC Microbiol. 2012;12(1):95. doi:10.1186/1471-2180-12-95.
  • Penders J, Gerhold K, Stobberingh EE, Thijs C, Zimmermann K, Lau S, Hamelmann E. Establishment of the intestinal microbiota and its role for atopic dermatitis in early childhood. J Allergy Clin Immunol. 2013;132(3):601–607.e8. doi:10.1016/j.jaci.2013.05.043.
  • Nylund L, Satokari R, Nikkilä J, Rajilić-Stojanović M, Kalliomäki M, Isolauri E, Salminen S, de Vos WM. Microarray analysis reveals marked intestinal microbiota aberrancy in infants having eczema compared to healthy children in at-risk for atopic disease. BMC Microbiol. 2013;13(1):12. doi:10.1186/1471-2180-13-12.
  • Petersen EBM, Skov L, Thyssen JP, Jensen P. Role of the gut microbiota in atopic dermatitis: a systematic review. Acta Derm Venereol. 2019;99(1):5–11. doi:10.2340/00015555-3008.
  • Bartosik T, Jensen SA, Afify SM, Bianchini R, Hufnagl K, Hofstetter G, Berger M, Bastl M, Berger U, Rivelles E, et al. Ameliorating atopy by compensating micronutritional deficiencies in immune cells: a double-blind placebo-controlled pilot study. J Allergy Clin Immunol Pract. 2022;10(7):1889–1902. e9. doi:10.1016/j.jaip.2022.02.028.
  • Petje L-M, Jensen SA, Szikora S, Sulzbacher M, Bartosik T, Pjevac P, Hausmann B, Hufnagl K, Untersmayr E, Fischer L, et al. Functional iron-deficiency in women with allergic rhinitis is associated with symptoms after nasal provocation and lack of iron-sequestering microbes. Allergy. 2021;76(9):2882–2886. doi:10.1111/all.14960.
  • Roduit C, Frei R, Ferstl R, Loeliger S, Westermann P, Rhyner C, Schiavi E, Barcik W, Rodriguez-Perez N, Wawrzyniak M, et al. High levels of butyrate and propionate in early life are associated with protection against atopy. Allergy. 2019;74(4):799–809. doi:10.1111/all.13660.
  • Venter C, Palumbo MP, Glueck DH, Sauder KA, O'Mahony L, Fleischer DM, Ben-Abdallah M, Ringham BM, Dabelea D. The maternal diet index in pregnancy is associated with offspring allergic diseases: the healthy start study. Allergy. 2022;77(1):162–172. doi:10.1111/all.14949.
  • Zakrzewski M, Wilkins SJ, Helman SL, Brilli E, Tarantino G, Anderson GJ, Frazer DM. Supplementation with Sucrosomial® iron leads to favourable changes in the intestinal microbiome when compared to ferrous sulfate in mice. Biometals. 2022;35(1):27–38. doi:10.1007/s10534-021-00348-3.
  • Chen H, Wu W, Tang S, Fu R, Gong X, Hou H, Xu J. Altered fecal microbial and metabolic profile reveals potential mechanisms underlying iron deficiency anemia in pregnant women in China. Bosn J Basic Med Sci. 2022;22(6):923–933. doi:10.17305/bjbms.2022.7091.
  • Seo H, Yoon SY, Ul-Haq A, Jo S, Kim S, Rahim MA, Park H-A, Ghorbanian F, Kim MJ, Lee M-Y, et al. The effects of iron deficiency on the gut microbiota in women of childbearing age. Nutrients. 2023;15(3):691. doi:10.3390/nu15030691.
  • Soriano-Lerma A, García-Burgos M, Alférez MJM, Pérez-Carrasco V, Sanchez-Martin V, Linde-Rodríguez Á, Ortiz-González M, Soriano M, García-Salcedo JA, López-Aliaga I, et al. Gut microbiome-short-chain fatty acids interplay in the context of iron deficiency anaemia. Eur J Nutr. 2022;61(1):399–412. doi:10.1007/s00394-021-02645-6.
  • Delgadinho M, Ginete C, Santos B, Mendes J, Miranda A, Vasconcelos J, Brito M. Microbial gut evaluation in an angolan paediatric population with sickle cell disease. J Cell Mol Med. 2022;26(21):5360–5368. doi:10.1111/jcmm.17402.
  • Lane ER, Zisman TL, Suskind DL. The microbiota in inflammatory bowel disease: current and therapeutic insights. J Inflamm Res. 2017;10:63–73. doi:10.2147/JIR.S116088.
  • Shim JO. Gut microbiota in inflammatory bowel disease. Pediatr Gastroenterol Hepatol Nutr. 2013;16(1):17–21. doi:10.5223/pghn.2013.16.1.17.
  • Miyoshi J, Chang EB. The gut microbiota and inflammatory bowel diseases. Transl Res. 2017;179:38–48. doi:10.1016/j.trsl.2016.06.002.
  • Abrahamsson TR, Wu RY, Jenmalm MC. Gut microbiota and allergy: the importance of the pregnancy period. Pediatr Res. 2015;77(1-2):214–219. doi:10.1038/pr.2014.165.
  • Sjögren YM, Jenmalm MC, Böttcher MF, Björkstén B, Sverremark-Ekström E. Altered early infant gut microbiota in children developing allergy up to 5 years of age. Clin Exp Allergy. 2009;39(4):518–526. doi:10.1111/j.1365-2222.2008.03156.x.

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