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Changes on fecal microbiota in rats exposed to permethrin during postnatal development

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Abstract

Alteration of the gut microbiota through diet and environmental contaminants may disturb the mammalian digestive system, leading to various diseases. Because most exposure to environmentally pyrethroid pesticides such as permethrin (PERM) occurs through the diet, the commensal gut microbiota is likely to be exposed to PERM. The study aimed at evaluating the effect of low-dose exposure to PERM in early life on the composition of fecal microbiota in rats. Over a 4-month follow-up period, fecal microbiota and short-chain fatty acids were measured in order to identify possible differences between PERM-treated rats and controls. Further in vitro antimicrobial experiments were conducted to establish the antibacterial activity of PERM against different strains to obtain Minimal Inhibitory Concentrations. The main finding focused on the reduced abundance of Bacteroides-Prevotella-Porphyromonas species, increased Enterobacteriaceae and Lactobacillus in PERM-treated rats compared to controls. Changes of acetic and propionic acid levels were registered in PERM-treated group. From in vitro studies, PERM showed higher antibacterial activity against beneficial bacteria such as Bifidobacterium and Lactobacillus paracasei, while to inhibit potential pathogens as Staphylococcus aureus and Escherichia coli PERM concentration needed to be increased. In summary, exposure to PERM could affect the fecal microbiota and could be a crucial factor contributing to the development of diseases.

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References

  • Avella MA, Olivotto I, Silvi S, Place AL, Carnevali O (2010) Effect of dietary probiotics on clownfish: a molecular approach to define how lactic acid bacteria modulate development in a marine fish. Am J Physiol Regul Integr Comp Physiol 298:R359–R371

    Article  CAS  Google Scholar 

  • Barr DB, Wong OA, Unubka S, Baker SE, Whitehead RD, Magsumbol MS, Williams BL, Needham LL (2010) Urinary concentration of metabolites of pyrethroid insecticides in the general U.S. population: National Health and Nutrition Examination Survey 1999–2002. Environ Health Perspect 118:742–748

    Article  CAS  Google Scholar 

  • Bartosch S, Fite A, Macfarlane GT, McMurdo ME (2004) Characterization of bacterial communities in feces from healthy elderly volunteers and hospitalized elderly patients by using real-time PCR and effects of antibiotic treatment on the fecal microbiota. Appl Environ Microbiol 70:3575–3581

    Article  CAS  Google Scholar 

  • Byun R, Nadkarni MA, Chhour KL, Martin FE, Jacques NA, Hunter N (2004) Quantitative analysis of diverse Lactobacillus species present in advanced dental caries. J Clin Microbiol 42:3128–3136

    Article  CAS  Google Scholar 

  • Carloni M, Nasuti C, Fedeli D, Montani M, Amici A, Vadhana MS, Gabbianelli R (2012) The impact of early life permethrin exposure on development of neurodegeneration in adulthood. Exp Gerontol 47:60–66

    Article  CAS  Google Scholar 

  • Casida JE, Durkin KA (2013) Neuroactive insecticides: targets, selectivity, resistance, and secondary effects. Annu Rev Entomol 58:99–117

    Article  CAS  Google Scholar 

  • Den Besten G, van Eunen K, Groen AK, Venema K, Reijngoud DJ, Bakker BM (2013) The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res 54(9):2325–2340

    Article  Google Scholar 

  • Fang H, Hedin G (2003) Rapid screening and identification of methicillin-resistant Staphylococcus aureus from clinical samples by selective-broth and real-time PCR assay. J Clin Microbiol 41:2894–2899

    Article  CAS  Google Scholar 

  • Fiorini D, Pacetti D, Gabbianelli R, Gabrielli S, Ballini R (2015) A salting out system for improving the efficiency of the headspace solid-phase microextraction of short and medium chain free fatty acids. J Chromatogr A 1409:282–287

    Article  CAS  Google Scholar 

  • Gabbianelli R, Nasuti C, Falcioni G, Cantalamessa F (2004) Lymphocyte DNA damage in rats exposed to pyrethroids: effect of supplementation with Vitamins E and C. Toxicology 203:17–26

    Article  CAS  Google Scholar 

  • Gabbianelli R, Martínez JA, De Caterina R (2014) European Summer School on Nutrigenomics: Camerino, Italy, September 1–5, 2014. J Nutrigenet Nutrigenomics 7:1–19

    Article  Google Scholar 

  • Heudorf U, Angerer J (2001) Metabolites of pyrethroid insecticides in urine specimens: current exposure in an urban population in Germany. Environ Health Perspect 109:213–217

    Article  CAS  Google Scholar 

  • Joly Condette C, Bach V, Mayeur C, Gay-Quéheillard J, Khorsi-Cauet H (2015) Chlorpyrifos exposure during perinatal period affects intestinal microbiota associated with delay of maturation of digestive tract in rats. J Pediatr Gastroenterol Nutr 61(1):30–40

    CAS  Google Scholar 

  • Joly C, Gay-Quéheillard J, Léké A, Chardon K, Delanaud S, Bach V, Khorsi-Cauet H (2013) Impact of chronic exposure to low doses of chlorpyrifos on the intestinal microbiota in the Simulator of the Human Intestinal Microbial Ecosystem (SHIME) and in the rat. Environ Sci Pollut Res Int 20(5):2726–2734

    Article  CAS  Google Scholar 

  • Kaufman, DD (1977) Permethrin degradation in soil and microbial cultures. In: Elliot Michael (ed) Synthetic Pyrethroids, reprinted from ACS Symposium series No. 42, American Chemical Society, chapter 14, pp 147–161

  • Clinical and Laboratory Standards Institute (2007) Performance standards for antimicrobial susceptibility testing. Seventeenth informational supplement, CLSI document M100-S17 [ISBN 1-56238-625-5]. Clinical and Laboratory Standards Institute, Wayne, Pennsylvania, 19087-1898 USA.

  • Langendijk PS, Schut F, Jansen GJ, Raangs GC, Kamphuis GR, Wilkinson MH, Welling GW (1995) Quantitative fluorescence in situ hybridization of Bifidobacterium spp. with genus-specific 16S rRNA-targeted probes and its application in fecal samples. Appl Environ Microbiol 61:3069–3075

    CAS  Google Scholar 

  • Morelli L (2008) Postnatal development of intestinal microflora as influenced by infant nutrition. J Nutr 138:1791S–1795S

    CAS  Google Scholar 

  • Morgan MK (2012) Children’s exposures to pyrethroid insecticides at home: a review of data collected in published exposure measurement studies conducted in the United States. Int J Environ Res Public Health 9(8):2964–2985

    Article  CAS  Google Scholar 

  • Nasuti C, Cantalamessa F, Falcioni G, Gabbianelli R (2003) Different effects of Type I and Type II pyrethroids on erythrocyte plasma membrane properties and enzymatic activity in rats. Toxicology 191(2-3):233–244

    Article  CAS  Google Scholar 

  • Nasuti C, Gabbianelli R, Falcioni ML, Di Stefano A, Sozio P, Cantalamessa F (2007) Dopaminergic system modulation, behavioural changes, and oxidative stress after neonatal administration of pyrethroids. Toxicology 229:194–205

    Article  CAS  Google Scholar 

  • Nasuti C, Falcioni ML, Nwankwo IE, Cantalamessa F, Gabbianelli R (2008) Effect of permethrin plus antioxidants on locomotor activity and striatum in adolescent rats. Toxicology 251:45–50

    Article  CAS  Google Scholar 

  • Nasuti C, Carloni M, Fedeli D, Gabbianelli R, Di Stefano A, Serafina CL, Silva I, Domingues V, Ciccocioppo R (2013) Effects of early life permethrin exposure on spatial working memory and on monoamine levels in different brain areas of pre-senescent rats. Toxicology 303:162–168

    Article  CAS  Google Scholar 

  • Nasuti C, Fattoretti P, Carloni M, Fedeli D, Ubaldi M, Ciccocioppo R, Gabbianelli R (2014) Neonatal exposure to permethrin pesticide causes lifelong fear and spatial learning deficits and alters hippocampal morphology of synapses. J Neurodev Disord 6:7

    Article  Google Scholar 

  • Rinttila T, Kassinen A, Malinen E, Krogius L, Palva A (2004) Development of an extensive set of 16S rDNA-targeted primers for quantification of pathogenic and indigenous bacteria in faecal samples by real-time PCR. J Appl Microbiol 97:1166–1177

    Article  CAS  Google Scholar 

  • Roberts JR, Karr CJ (2012) Council on Environmental Health: technical report: pesticide exposure in children. Pediatrics 130(6):e1765–e1788. doi:10.1542/peds.2012-2758

    Article  Google Scholar 

  • Scheperjans F, Aho V, Pereira PA, Koskinen K, Paulin L, Pekkonen E, Haapaniemi E, Kaakkola S, Eerola-Rautio J, Pohja M, Kinnunen E, Murros K, Auvinen P (2015) Gut microbiota are related to Parkinson’s disease and clinical phenotype. Mov Disord 30(3):350–358

    Article  Google Scholar 

  • Scheppach W, Weiler F (2004) The butyrate story: Old wine in new bottles? Curr Opin Clin Nutr Metab Care 7:563–567

    Article  Google Scholar 

  • Silvi S, Rumney CJ, Rowland IR (1996) An assessment of three selective media for bifidobacteria in faeces. J Appl Bacteriol 81:561–564

    CAS  Google Scholar 

  • Wagenet LP (1985) A review of physical-chemical parameters related to the soil and groundwater fate of selected pesticides in N.Y. State. Cornell University, Agricultural Experiment Station, N.Y. State College of Agriculture and Life Sciences, Ithaca, NY, #30. ISSN 0362-2754

    Google Scholar 

  • Williams MK, Rundle A, Holmes D, Reyes M, Hoepner LA, Barr DB, Camann DE, Perera FP, Whyatt RM (2008) Changes in pest infestation levels, self-reported pesticide use, and permethrin exposure during pregnancy after the 2000–2001 US Environmental Protection Agency restriction of organophosphates. Environ Health Perspect 116(12):1681–1688

    Article  CAS  Google Scholar 

  • Zampa A, Silvi S, Fabiani R, Morozzi G, Orpianesi C, Cresci A (2004) Effects of different digestible carbohydrates on bile acid metabolism and SCFA production by human gut micro-flora grown in an in vitro semi-continuous culture. Anaerobe 10:19–26

    Article  CAS  Google Scholar 

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Funding

This work was supported by a grant (FAR) from the University of Camerino (Italy).

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Correspondence to Cinzia Nasuti.

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The authors report no conflicts of interest relative to the research covered in this manuscript.

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Responsible editor: Philippe Garrigues

Cinzia Nasuti and Maria Magdalena Coman contributed equally to this work.

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Nasuti, C., Coman, M.M., Olek, R.A. et al. Changes on fecal microbiota in rats exposed to permethrin during postnatal development. Environ Sci Pollut Res 23, 10930–10937 (2016). https://doi.org/10.1007/s11356-016-6297-x

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  • DOI: https://doi.org/10.1007/s11356-016-6297-x

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