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Research Paper

Daily skin-to-skin contact alters microbiota development in healthy full-term infants

ORCID Icon, , , &
Article: 2295403 | Received 17 Jul 2023, Accepted 12 Dec 2023, Published online: 10 Jan 2024

References

  • Cerqueira FM, Photenhauer AL, Pollet RM, Brown HA, Koropatkin NM. Starch digestion by gut bacteria: crowdsourcing for carbs. Trends Microbiol. 2020;28(2):95–18. doi:10.1016/j.tim.2019.09.004.
  • Gensollen T, Iyer SS, Kasper DL, Blumberg RS. How colonization by microbiota in early life shapes the immune system. Science. 2016;352:539–544.
  • Zhang Y-J, Li S, Gan R-Y, Zhou T, Xu D-P, Li H-B. Impacts of gut bacteria on human health and diseases. Int J Mol Sci. 2015;16(12):7493–7519. doi:10.3390/ijms16047493.
  • Cryan JF, O’Riordan KJ, Cowan CSM, Sandhu KV, Bastiaanssen TFS, Boehme M, Codagnone MG, Cussotto S, Fulling C, Golubeva AV, et al. The microbiota-gut-brain axis. Physiol Rev. 2019;99(4):1877–2013. doi:10.1152/physrev.00018.2018.
  • Cryan JF, Dinan TG. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci. 2012;13:701–712.
  • Claesson MJ, Jeffery IB, Conde S, Power SE, O’Connor EM, Cusack S, Harris HMB, Coakley M, Lakshminarayanan B, O’Sullivan O, et al. Gut microbiota composition correlates with diet and health in the elderly. Nature. 2012;488:178–184.
  • Sekirov I, Russell SL, Antunes LCM, Finlay BB. Gut microbiota in health and disease. Physiol Rev. 2010;90(3):859–904. doi:10.1152/physrev.00045.2009.
  • Milani C, Duranti S, Bottacini F, Casey E, Turroni F, Mahony J, Belzer C, Delgado Palacio S, Arboleya Montes S, Mancabelli L, et al. The first microbial colonizers of the human gut: composition, activities, and health implications of the infant gut microbiota. Microbiol Mol Biol R. 2017;81:e00036–17.
  • Van Daele E, Knol J, Belzer C. Microbial transmission from mother to child: improving infant intestinal microbiota development by identifying the obstacles. Crit Rev Microbiol. 2019;45(5–6):613–648. doi:10.1080/1040841X.2019.1680601.
  • Yang L, Sakandar HA, Sun Z, Zhang H. Recent advances of intestinal microbiota transmission from mother to infant. J Funct Foods. 2021;87:104719.
  • Valles-Colomer M, Blanco-Míguez A, Manghi P, Asnicar F, Dubois L, Golzato D, Armanini F, Cumbo F, Huang KD, Manara S, et al. The person-to-person transmission landscape of the gut and oral microbiomes. Nature. 2023;614(7946):125–135. doi:10.1038/s41586-022-05620-1.
  • Hermes GDA, Eckermann HA, de Vos WM, de Weerth C. Does entry to center-based childcare affect gut microbial colonization in young infants? Sci Rep. 2020;10:10235.
  • Bäckhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P, Li Y, Xia Y, Xie H, Zhong H, et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host & Microbe. 2015;17(5):690–703. doi:10.1016/j.chom.2015.04.004.
  • Ou Y, Belzer C, Smidt H, de Weerth C. Development of the gut microbiota in healthy children in the first ten years of life: associations with internalizing and externalizing behavior. Gut Microbes. 2022;14:2038853.
  • Korpela K, Zijlmans MAC, Kuitunen M, Kukkonen K, Savilahti E, Salonen A, De Weerth C, De Vos WM. Childhood BMI in relation to microbiota in infancy and lifetime antibiotic use. Microbiome. 2017;5(1):26. doi:10.1186/s40168-017-0245-y.
  • WHO. Kangaroo mother care: a practical guide. Geneva: World Health Organization; 2003.
  • Beijers R, Cillessen L, Zijlmans MAC. An experimental study on mother-infant skin-to-skin contact in full-terms. Infant Behav Dev. 2016;43:58–65.
  • Cristóbal Cañadas D, Parrón Carreño T, Sánchez Borja C, Bonillo Perales A. Benefits of Kangaroo mother care on the physiological stress parameters of preterm infants and mothers in neonatal intensive care. Int J Envir Res & Pub Health. 2022;19(12):7183. doi:10.3390/ijerph19127183.
  • Ionio C, Ciuffo G, Landoni M. Parent and stress Regulation: a systematic Review of the literature. Int J Envir Res & Pub Health. 2021;18:4695.
  • Bergman N, Linley L, Fawcus S. Randomized controlled trial of skin-to-skin contact from birth versus conventional incubator for physiological stabilization in 1200- to 2199-gram newborns. Acta Paediatr. 2004;93(6):779–785. doi:10.1111/j.1651-2227.2004.tb03018.x.
  • Conde-Agudelo A, Díaz-Rossello JL. Kangaroo mother care to reduce morbidity and mortality in low birthweight infants. Cochrane Database Syst Rev. 2016;2017.
  • Feldman R, Rosenthal Z, Eidelman AI. Maternal-preterm skin-to-skin contact enhances child physiologic organization and cognitive control across the first 10 years of life. Biol Psychiatry. 2014;75(1):56–64. doi:10.1016/j.biopsych.2013.08.012.
  • Meder U, Tarjanyi E, Kovacs K, Szakmar E, Cseko AJ, Hazay T, Belteki G, Szabo M, Jermendy A. Cerebral oxygenation in preterm infants during maternal singing combined with skin-to-skin care. Pediatr Res. 2021;90(4):809–814. doi:10.1038/s41390-020-01235-2.
  • WHO Immediate KMC Study Group. Immediate “Kangaroo mother care” and survival of infants with low birth weight. N Engl J Med. 2021;384(21):2028–2038. doi:10.1056/NEJMoa2026486.
  • de Alencar AEMA, Arraes LC, de Albuquerque EC, Alves JGB. Effect of Kangaroo mother care on postpartum depression. J Trop Pediatr. 2007;55(1):36–38. doi:10.1093/tropej/fmn083.
  • Dombrowski MAS, Anderson GC, Santori C, Burkhammer M. Kangaroo (skin-to-skin) care with a postpartum Woman who Felt Depressed. MCN: Am J Maternal/Child Nurs. 2001;26(4):214–216. doi:10.1097/00005721-200107000-00012.
  • Feldman R, Eidelman AI, Sirota L, Weller A. Comparison of skin-to-skin (Kangaroo) and traditional care: parenting outcomes and preterm infant development. Pediatrics. 2002;110(1):16–26. doi:10.1542/peds.110.1.16.
  • Sinha B, Sommerfelt H, Ashorn P, Mazumder S, Taneja S, More D, Bahl R, Bhandari N. Effect of community-initiated Kangaroo mother care on postpartum depressive symptoms and stress among mothers of low-birth-weight infants: a randomized clinical trial. JAMA Netw Open. 2021;4(4):e216040. doi:10.1001/jamanetworkopen.2021.6040.
  • Moore ER, Bergman N, Anderson GC, Medley N. Early skin-to-skin contact for mothers and their healthy newborn infants. Cochrane Database Syst Rev. 2016;2016(11):2016. doi:10.1002/14651858.CD003519.pub4.
  • Feldman R, Eidelman AI. Skin-to-skin contact (Kangaroo care) accelerates autonomic and neurobehavioural maturation in preterm infants. Dev Med Child Neurol. 2003;45(04). doi:10.1017/S0012162203000525.
  • Föhe K, Kropf S, Avenarius S. Skin-to-skin contact improves gas exchange in premature infants. J Perinatol. 2000;20(5):311–315. doi:10.1038/sj.jp.7200378.
  • Charpak N, Tessier R, Ruiz JG, Hernandez JT, Uriza F, Villegas J, Nadeau L, Mercier C, Maheu F, Marin J, et al. Twenty-year follow-up of Kangaroo mother care versus traditional care. Pediatrics. 2017;139(1):e20162063. doi:10.1542/peds.2016-2063.
  • Ropars S, Tessier R, Charpak N, Uriza LF. The long-term effects of the Kangaroo mother care intervention on cognitive functioning: results from a longitudinal study. Dev Neuropsychol. 2018;43(1):82–91. doi:10.1080/87565641.2017.1422507.
  • Mehler K, Hucklenbruch-Rother E, Trautmann-Villalba P, Becker I, Roth B, Kribs A. Delivery room skin-to-skin contact for preterm infants—A randomized clinical trial. Acta Paediatr. 2020;109(3):518–526. doi:10.1111/apa.14975.
  • Walters MW, Boggs KM, Ludington-Hoe S, Price KM, Morrison B. Kangaroo Care at Birth for Full Term Infants: A Pilot Study. MCN: Am J Maternal/Child Nurs. 2007;32(6):375–381. doi:10.1097/01.NMC.0000298134.39785.6c.
  • Bigelow A, Power M, MacLellan-Peters J, Alex M, McDonald C. Effect of mother/infant skin-to-skin contact on postpartum depressive symptoms and maternal physiological stress. J Obstet, Gynecol Neonatal Nurs. 2012;41(3):369–382. doi:10.1111/j.1552-6909.2012.01350.x.
  • Bigelow AE, Power M. Mother–infant skin-to-skin contact: short- and long-term effects for mothers and their children born full-term. Front Psychol. 2020;11:1921. doi:10.3389/fpsyg.2020.01921.
  • Cooijmans KHM, Beijers R, Rovers AC, de Weerth C. Effectiveness of skin-to-skin contact versus care-as-usual in mothers and their full-term infants: study protocol for a parallel-group randomized controlled trial. BMC Pediatr. 2017;17(1):154. doi:10.1186/s12887-017-0906-9.
  • Cooijmans KHM, Beijers R, Brett BE, de Weerth C. Daily mother-infant skin-to-skin contact and maternal mental health and postpartum healing: a randomized controlled trial. Sci Rep. 2022;12(1):10225. doi:10.1038/s41598-022-14148-3.
  • Cooijmans KHM, Beijers R, Brett BE, Weerth C. Daily skin-to-skin contact in full-term infants and breastfeeding: secondary outcomes from a randomized controlled trial. Matern Child Nutr. 2022;18(1):18. doi:10.1111/mcn.13241.
  • Cooijmans KHM, Beijers R, De Weerth C. Daily skin-to-skin contact and crying and sleeping in healthy full-term infants: a randomized controlled trial. Dev Psychol. 2022;58(9):1629–1638. doi:10.1037/dev0001392.
  • Rheinheimer N, Beijers R, Bruinhof N, Cooijmans KHM, de Weerth C. Effects of daily full-term infant skin-to-skin contact on behavior and cognition at age three – secondary outcomes of a randomized controlled trial. J Child Psychol Psychiatry. 2022;64(1):pp.136–144. doi:10.1111/jcpp.13679.
  • Rheinheimer N, Beijers R, Cooijmans KHM, Brett BE, de Weerth C. Effects of skin-to-skin contact on full-term infants’ stress reactivity and quality of mother–infant interactions. Dev Psychobiol. 2022;64(7):64. doi:10.1002/dev.22308.
  • Browne PD, Aparicio M, Alba C, Hechler C, Beijers R, Rodríguez JM, Fernández L, de Weerth C. Human milk microbiome and maternal postnatal psychosocial distress. Front Microbiol. 2019;10:2333. doi:10.3389/fmicb.2019.02333.
  • Ziomkiewicz A, Babiszewska M, Apanasewicz A, Piosek M, Wychowaniec P, Cierniak A, Barbarska O, Szołtysik M, Danel D, Wichary S. Psychosocial stress and cortisol stress reactivity predict breast milk composition. Sci Rep. 2021;11(1):11576. doi:10.1038/s41598-021-90980-3.
  • van den Elsen LWJ, Garssen J, Burcelin R, Verhasselt V. Shaping the gut microbiota by breastfeeding: The Gateway to Allergy prevention? Front Pediatr. 2019;7:47. doi:10.3389/fped.2019.00047.
  • Bailey MT, Dowd SE, Galley JD, Hufnagle AR, Allen RG, Lyte M. Exposure to a social stressor alters the structure of the intestinal microbiota: implications for stressor-induced immunomodulation. Brain Behav Immun. 2011;25(3):397–407. doi:10.1016/j.bbi.2010.10.023.
  • O’Mahony SM, Clarke G, Dinan TG, Cryan JF. Early-life adversity and brain development: is the microbiome a missing piece of the puzzle? Neuroscience. 2017;342:37–54. doi:10.1016/j.neuroscience.2015.09.068.
  • de Weerth C. Do bacteria shape our development? Crosstalk between intestinal microbiota and HPA axis. Neurosci Biobehav Rev. 2017;83:458–471. doi:10.1016/j.neubiorev.2017.09.016.
  • Galley JD, Nelson MC, Yu Z, Dowd SE, Walter J, Kumar PS, Lyte M, Bailey MT. Exposure to a social stressor disrupts the community structure of the colonic mucosa-associated microbiota. BMC Microbiol. 2014;14(1):189. doi:10.1186/1471-2180-14-189.
  • Xu M, Wang C, Krolick KN, Shi H, Zhu J. Difference in post-stress recovery of the gut microbiome and its altered metabolism after chronic adolescent stress in rats. Sci Rep. 2020;10(1):3950. doi:10.1038/s41598-020-60862-1.
  • Dill-McFarland KA, Tang Z-Z, Kemis JH, Kerby RL, Chen G, Palloni A, Sorenson T, Rey FE, Herd P. Close social relationships correlate with human gut microbiota composition. Sci Rep. 2019;9(1):703. doi:10.1038/s41598-018-37298-9.
  • Drell T, Štšepetova J, Simm J, Rull K, Aleksejeva A, Antson A, Tillmann V, Metsis M, Sepp E, Salumets A, et al. The influence of different maternal microbial communities on the development of infant gut and oral microbiota. Sci Rep. 2017;7(1):9940. doi:10.1038/s41598-017-09278-y.
  • Browne HP, Shao Y, Lawley TD. Mother-infant transmission of human microbiota. Curr Opin Microbiol. 2022;69:102173. doi:10.1016/j.mib.2022.102173.
  • Ferretti P, Pasolli E, Tett A, Asnicar F, Gorfer V, Fedi S, Armanini F, Truong DT, Manara S, Zolfo M, et al. Mother-to-infant microbial transmission from different body sites shapes the developing infant gut microbiome. Cell Host & Microbe. 2018;24(1):133–145.e5. doi:10.1016/j.chom.2018.06.005.
  • Bastiaanssen T, Gururajan A, van de Wouw M, Moloney GM, Ritz N, Long-Smith CM, Wiley NC, Murphy AB, Lyte JM, Fouhy F, et al. Volatility as a concept to understand the impact of stress on the microbiome. Psychoneuroendocrinology. 2021;124:105047. doi:10.1016/j.psyneuen.2020.105047.
  • Cappellato M, Baruzzo G, Di Camillo B, Coelho LP. Investigating differential abundance methods in microbiome data: a benchmark study. PLoS Comput Biol. 2022;18(9):e1010467. doi:10.1371/journal.pcbi.1010467.
  • Nearing JT, Douglas GM, Hayes MG, MacDonald J, Desai DK, Allward N, Jones CMA, Wright RJ, Dhanani AS, Comeau AM, et al. Microbiome differential abundance methods produce different results across 38 datasets. Nat Commun. 2022;13(1):342. doi:10.1038/s41467-022-28034-z.
  • Bastiaanssen TFS, Quinn TP, Loughman A Treating bugs as features: a compositional guide to the statistical analysis of the microbiome-gut-brain axis [internet]. 2022 [accessed 2022 Sep 6]. https://arxiv.org/abs/2207.12475.
  • Subramanian S, Huq S, Yatsunenko T, Haque R, Mahfuz M, Alam MA, Benezra A, DeStefano J, Meier MF, Muegge BD, et al. Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature. 2014;510(7505):417–421. doi:10.1038/nature13421.
  • Valles-Colomer M, Falony G, Darzi Y, Tigchelaar EF, Wang J, Tito RY, Schiweck C, Kurilshikov A, Joossens M, Wijmenga C, et al. The neuroactive potential of the human gut microbiota in quality of life and depression. Nat microbiol. 2019;4:623–632.
  • Clooney AG, Eckenberger J, Laserna-Mendieta E, Sexton KA, Bernstein MT, Vagianos K, Sargent M, Ryan FJ, Moran C, Sheehan D, et al. Ranking microbiome variance in inflammatory bowel disease: A large longitudinal intercontinental study. Gut. 2021;70(3):499–510. doi:10.1136/gutjnl-2020-321106.
  • de Weerth C, Fuentes S, Puylaert P, de Vos WM. Intestinal microbiota of infants with colic: development and specific signatures. PEDIATRICS. 2013;131:e550–8.
  • Depner M, Taft DH, Kirjavainen PV, Kalanetra KM, Karvonen AM, Peschel S, Schmausser-Hechfellner E, Roduit C, Frei R, Lauener R, et al. Maturation of the gut microbiome during the first year of life contributes to the protective farm effect on childhood asthma. Nat Med. 2020;26(11):1766–1775. doi:10.1038/s41591-020-1095-x.
  • Bokulich NA, Chung J, Battaglia T, Henderson N, Jay M, Li HD, Lieber A, Wu F, Perez-Perez GI, Chen Y, et al. Antibiotics, birth mode, and diet shape microbiome maturation during early life. Sci Transl Med. 2016;8(343). doi:10.1126/scitranslmed.aad7121.
  • Baniel A, Petrullo L, Mercer A, Reitsema L, Sams S, Beehner JC, Bergman TJ, Snyder-Mackler N, Lu A. Maternal effects on early-life gut microbiota maturation in a wild nonhuman primate. Curr Biol. 2022;32:4508–4520.e6.
  • Laursen MF, Laursen RP, Larnkjær A, Mølgaard C, Michaelsen KF, Frøkiær H, Bahl MI, Licht TR, Suen G. Faecalibacterium gut colonization is Accelerated by presence of older siblings. mSphere. 2017;2(6):e00448–17. doi:10.1128/mSphere.00448-17.
  • Roswall J, Olsson LM, Kovatcheva-Datchary P, Nilsson S, Tremaroli V, Simon M-C, Kiilerich P, Akrami R, Krämer M, Uhlén M, 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.
  • Adlerberth I, Strachan DP, Matricardi PM, Ahrné S, Orfei L, Åberg N, Perkin MR, Tripodi S, Hesselmar B, Saalman R, et al. Gut microbiota and development of atopic eczema in 3 European birth cohorts. J Allergy Clin Immunol. 2007;120(2):343–350. doi:10.1016/j.jaci.2007.05.018.
  • Azad MB, Konya T, Maughan H, Guttman DS, Field CJ, Sears MR, Becker AB, Scott JA, Kozyrskyj AL. CHILD study investigators. Infant gut microbiota and the hygiene hypothesis of allergic disease: impact of household pets and siblings on microbiota composition and diversity. Allergy, Asthma & Clinical Immunol. 2013;9:15.
  • Christensen ED, Hjelmsø MH, Thorsen J, Shah S, Redgwell T, Poulsen CE, Trivedi U, Russel J, Gupta S, Chawes BL, et al. The developing airway and gut microbiota in early life is influenced by age of older siblings. Microbiome. 2022;10(1):106. doi:10.1186/s40168-022-01305-z.
  • Laursen MF, Zachariassen G, Bahl MI, Bergström A, Høst A, Michaelsen KF, Licht TR. Having older siblings is associated with gut microbiota development during early childhood. BMC Microbiol. 2015;15:154.
  • Miquel S, Martín R, Rossi O, Bermúdez-Humarán L, Chatel J, Sokol H, Thomas M, Wells J, Langella P. Faecalibacterium prausnitzii and human intestinal health. Curr Opin Microbiol. 2013;16(3):255–261. doi:10.1016/j.mib.2013.06.003.
  • Tamana SK, Tun HM, Konya T, Chari RS, Field CJ, Guttman DS, Becker AB, Moraes TJ, Turvey SE, Subbarao P, et al. Bacteroides-dominant gut microbiome of late infancy is associated with enhanced neurodevelopment. Gut Microbes. 2021;13(1):1930875. doi:10.1080/19490976.2021.1930875.
  • Duncan SH, Louis P, Flint HJ. Cultivable bacterial diversity from the human colon. Lett Appl Microbiol. 2007;44(4):343–350. doi:10.1111/j.1472-765X.2007.02129.x.
  • Carey MA, Medlock GL, Alam M, Kabir M, Uddin MJ, Nayak U, Papin J, Faruque ASG, Haque R, Petri WA, et al. Megasphaera in the stool microbiota is negatively associated with diarrheal cryptosporidiosis. Clin Infect Dis. 2021;73(6):e1242–51. doi:10.1093/cid/ciab207.
  • Dutton CL, Maisha FM, Quinn EB, Morales KL, Moore JM, Mulligan CJ. Maternal psychosocial stress is associated with reduced diversity in the early infant gut microbiome. Microorganisms. 2023;11(4):975. doi:10.3390/microorganisms11040975.
  • Stokholm J, Blaser MJ, Thorsen J, Rasmussen MA, Waage J, Vinding RK, Schoos A-M, Kunøe A, Fink NR, Chawes BL, et al. Publisher correction: maturation of the gut microbiome and risk of asthma in childhood. Nat Commun. 2018;9(1). doi:10.1038/s41467-018-03150-x.
  • Ogita T, Yamamoto Y, Mikami A, Shigemori S, Sato T, Shimosato T. Oral administration of Flavonifractor plautii strongly suppresses Th2 immune responses in mice. Front Immunol. 2020;11:379. doi:10.3389/fimmu.2020.00379.
  • Wang Z, Neupane A, Vo R, White J, Wang X, Marzano SYL. Comparing gut microbiome in mothers’ own breast milk- and formula-fed moderate-late preterm infants. Front Microbiol. 2019;11. doi:10.3389/fmicb.2020.00891.
  • 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). doi:10.1126/scitranslmed.aab2271.
  • Shetty SA, Zuffa S, Bui TPN, Aalvink S, Smidt H, De Vos WM. Reclassification of Eubacterium hallii as Anaerobutyricum hallii gen. Nov., comb. Nov., and description of Anaerobutyricum soehngenii sp. Nov., a butyrate and propionate-producing bacterium from infant faeces. Int J Syst Evol Microbiol. 2018;68(12):3741–3746. doi:10.1099/ijsem.0.003041.
  • Chia LW. Cross-feeding interactions of gut symbionts driven by human milk oligosaccharidesand mucins. 2018.
  • Dedon LR, Hilliard MA, Rani A, Daza-Merchan ZT, Story G, Briere C-E, Sela DA. Fucosylated human milk oligosaccharides drive structure-specific syntrophy between Bifidobacterium infantis and Eubacterium hallii within a modeled infant gut microbiome. Mol Nutr Food Res. 2023;67(11):2200851. doi:10.1002/mnfr.202200851.
  • Pham VT, Lacroix C, Braegger CP, Chassard C. Lactate-utilizing community is associated with gut microbiota dysbiosis in colicky infants. Sci Rep. 2017;7(1):11176. doi:10.1038/s41598-017-11509-1.
  • Gilijamse PW, Hartstra AV, Levin E, Wortelboer K, Serlie MJ, Ackermans MT, Herrema H, Nederveen AJ, Imangaliyev S, Aalvink S, et al. Treatment with Anaerobutyricum soehngenii: a pilot study of safety and dose–response effects on glucose metabolism in human subjects with metabolic syndrome. npj Biofilm Microbio. 2020;6(1):16. doi:10.1038/s41522-020-0127-0.
  • Hernán M, Hernández-Díaz S, Robins J. Randomized trials analyzed as observational studies. Ann Intern Med. 2013. doi:10.7326/0003-4819-159-8-201310150-00709.
  • Hernán M, Hernández-Díaz S. Beyond the intention-to-treat in comparative effectiveness research. Clin Trials. 2012;9(1):48–55. doi:10.1177/1740774511420743.
  • Ramiro-Garcia J, Hermes GDA, Giatsis C, Sipkema D, Zoetendal EG, Schaap PJ, Smidt H. NG-Tax, a highly accurate and validated pipeline for analysis of 16S rRNA amplicons from complex biomes. F1000Research. 2018;5:1791. doi:10.12688/f1000research.9227.2.
  • Huang R, Soneson C, Ernst FGM, Rue-Albrecht KC, Yu G, Hicks SC, Robinson MD. TreeSummarizedExperiment: a S4 class for data with hierarchical structure. F1000Research. 2021;9:1246. doi:10.12688/f1000research.26669.2.
  • R Core Team. R: a language and environment for statistical computing [internet]. Vienna, Austria: R Foundation for Statistical Computing; 2022. https://www.R-project.org/.
  • Kleinke K. Multiple imputation under violated distributional assumptions: a systematic evaluation of the assumed robustness of predictive Mean matching. J Educ Behav Stat. 2017;42(4):371–404. doi:10.3102/1076998616687084.
  • Van Buuren S, Groothuis-Oudshoorn K. Mice: multivariate imputation by chained equations in R. J Stat Soft. 2011;45(3). doi:10.18637/jss.v045.i03.
  • Bürkner P-C. Advanced Bayesian multilevel modeling with the R package brms. R J. 2018;10(1):18. doi:10.32614/RJ-2018-017.
  • Lin H, Peddada SD. Analysis of compositions of microbiomes with bias correction. Nat Commun. 2020;11(1):3514. doi:10.1038/s41467-020-17041-7.
  • Zhou H, He K, Chen J, Zhang X. LinDA: Linear models for differential abundance analysis of microbiome compositional data. Genome Biol. 2022;23(1):95. doi:10.1186/s13059-022-02655-5.
  • Mallick H, Rahnavard A, McIver LJ, Ma S, Zhang Y, Nguyen LH, Tickle TL, Weingart G, Ren B, Schwager EH, et al. Multivariable association discovery in population-scale meta-omics studies. PLoS Comput Biol. 2021;17(11):e1009442. doi:10.1371/journal.pcbi.1009442.
  • Oksanen J, Simpson GL, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Solymos P, Stevens MHH, Szoecs E, et al. Vegan: Community ecology package [Internet]. 2022. https://CRAN.R-project.org/package=vegan.
  • Ernst FGM, Shetty SA, Borman T, Lahti L. Mia: Microbiome analysis [Internet]. 2022. https://github.com/microbiome/mia.
  • Cinelli C, Forney A, Pearl J. A crash course in good and bad controls. SSRN Electron J. 2020. doi:10.2139/ssrn.3689437.
  • Vehtari A, Gelman A, Gabry J. Practical Bayesian model evaluation using leave-one-out cross-validation and WAIC. Stat Comput. 2017;27(5):1413–1432. doi:10.1007/s11222-016-9696-4.