Skip to main content
SpringerLink
Log in

The impact of age-related sub-chronic exposure to chlorpyrifos on metabolic indexes in male rats

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Chlorpyrifos (CPF), an organophosphorus pesticide (OP), has been implicated in metabolic diseases; however, the data are controversial. Rising age has been found as a main risk factor for metabolic diseases, and it has been proposed that advanced age increases susceptibility to the toxic effects of OPs. Therefore, this investigation aimed to evaluate the impact of CPF on hyperglycemia, hypercholesterolemia, and inflammation in animals with different ages. CPF (5 mg/kg) for 45 consecutive days was administered orally to male Wistar rats with different ages including 2-, 10-, and 20-month-old. The results indicated an increase in glucose and inflammatory indices, and also lipid profile was changed in the serum of aged animals in comparison with the 2-month-old animals. CPF administration amplified these parameters in the 20-month-old rats in comparison with that of aged-matched controls. The histopathological examination also indicated that CPF caused slight to moderate changes in the liver of 2-, 10-, and 20-month-old animals. Cholestasis was also observed in the CPF-administrated 20-month-old rats. In conclusion, aging may increase the susceptibility to CPF-induced metabolic disturbances in the animal models. It is proposed that advancing in age elevates the susceptibility to the metabolic effects of CPF.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abdel-Daim MM, Dawood MA, Elbadawy M, Aleya L, Alkahtani S (2020) Spirulina platensis reduced oxidative damage induced by chlorpyrifos toxicity in Nile tilapia (Oreochromis niloticus). Animals 10(3):473

    Google Scholar 

  • Acker CI, Nogueira CW (2012) Chlorpyrifos acute exposure induces hyperglycemia and hyperlipidemia in rats. Chemosphere 89(5):602–608

    CAS  Google Scholar 

  • Adedara IA, Owoeye O, Awogbindin IO, Ajayi BO, Rocha JB, Farombi EO (2018) Diphenyl diselenide abrogates brain oxidative injury and neurobehavioural deficits associated with pesticide chlorpyrifos exposure in rats. Chem Biol Interact 296:105–116

    CAS  Google Scholar 

  • Akhtar N, Srivastava MK, Raizada RB (2009) Assessment of chlorpyrifos toxicity on certain organs in rat, Rattus norvegicus. J Environ Biol 30(6):1047–1053

    CAS  Google Scholar 

  • Albasher G, Almeer R, Al-Otibi FO, Al-Kubaisi N, Mahmoud AM (2019) Ameliorative effect of Beta vulgaris root extract on chlorpyrifos-induced oxidative stress, inflammation and liver injury in rats. Biomolecules 9(7):261

    CAS  Google Scholar 

  • AlKahtane AA, Ghanem E, Bungau SG, Alarifi S, Ali D, AlBasher G, Alkahtani S, Aleya L, Abdel-Daim MM (2020) Carnosic acid alleviates chlorpyrifos-induced oxidative stress and inflammation in mice cerebral and ocular tissues. Environ Sci Pollut Res 27(11):11663–11670

  • Ambali SF, Onukak C, Idris SB, Yaqub LS, Shittu MU, Aliyu H, Kawu MU (2010) Vitamin C attenuates short-term hematological and biochemical alterations induced by acute chlorpyrifos exposure in Wistar rats. J Med Med Sci 1(10):465–477

    Google Scholar 

  • Ambali SF, Abubakar AT, Kawu MU, Uchendu C, Shittu M, Salami SO (2011) Biochemical alterations induced by subchronic chlorpyrifos exposure in Wistar rats: ameliorative effect of zinc. J Am Sci 7(9):73–81

  • Atterberry TT, Burnett WT, Chambers JE (1997) Age-related differences in parathion and chlorpyrifos toxicity in male rats: target and nontarget esterase sensitivity and cytochrome P450-mediated metabolism. Toxicol Appl Pharmacol 147(2):411–418

    CAS  Google Scholar 

  • Benke GM, Murphy SD (1975) The influence of age on the toxicity and metabolism of methyl parathion and parathion in male and female rats. Toxicol Appl Pharmacol 31(2):254–269

    CAS  Google Scholar 

  • Blaya R, Blaya P, Rhoden L, Rhoden EL (2017) Low testosterone levels and metabolic syndrome in aging male. Curr Pharm Des 23(30):4470–4474

    CAS  Google Scholar 

  • Bozkurt A, Yardan T, Ciftcioglu E, Baydin A, Hakligor A, Bitigic M, Bilge S (2010) Time course of serum S100B protein and neuron-specific enolase levels of a single dose of chlorpyrifos in rats. Basic Clin Pharmacol Toxicol 107(5):893–898

    CAS  Google Scholar 

  • Cacciatore LC, Nemirovsky SI, Guerrero NRV, Cochón AC (2015) Azinphos-methyl and chlorpyrifos, alone or in a binary mixture, produce oxidative stress and lipid peroxidation in the freshwater gastropod Planorbarius corneus. Aquat Toxicol 167:12–19

    CAS  Google Scholar 

  • Catrysse L, van Loo G (2017) Inflammation and the metabolic syndrome: the tissue-specific functions of NF-κB. Trends Cell Biol 27(6):417–429

    CAS  Google Scholar 

  • Chávez-Talavera O, Tailleux A, Lefebvre P, Staels B (2017) Bile acid control of metabolism and inflammation in obesity, type 2 diabetes, dyslipidemia, and nonalcoholic fatty liver disease. Gastroenterology 152(7):1679–1694

    Google Scholar 

  • Cimini FA, D'Eliseo D, Barchetta I, Bertoccini L, Velotti F, Cavallo MG (2019) Increased circulating granzyme B in type 2 diabetes patients with low-grade systemic inflammation. Cytokine 115:104–108

    CAS  Google Scholar 

  • Dominguez LJ, Barbagallo M (2016) The biology of the metabolic syndrome and aging. Curr Opin Clin Nutr Metab Care 19(1):5–11

    CAS  Google Scholar 

  • El-Bassossy HM, Abo-Warda SM, Fahmy A (2014) Chrysin and luteolin alleviate vascular complications associated with insulin resistance mainly through PPAR-γ activation. Am J Chin Med 42(05):1153–1167

    CAS  Google Scholar 

  • Elgawish RA, El-Beltagy MA, El-Sayed RM, Gaber AA, Abdelrazek HM (2020) Protective role of lycopene against metabolic disorders induced by chronic bisphenol A exposure in rats. Environ Sci Pollut Res 27(9):9192–9201

  • Elsharkawy EE, Yahia D, El-Nisr NA (2013) Sub-chronic exposure to chlorpyrifos induces hematological, metabolic disorders and oxidative stress in rat: attenuation by glutathione. Environ Toxicol Pharmacol 35(2):218–227

    CAS  Google Scholar 

  • El-Tawil MF (2014) Toxicological effects of short-term feeding with chlorpyrifos and chlorpyrifos-methyl insecticides on adult albino rats. Middle East J Agric Res 3(2):208–220

    Google Scholar 

  • Fang B, Li JW, Zhang M, Ren FZ, Pang GF (2018) Chronic chlorpyrifos exposure elicits diet-specific effects on metabolism and the gut microbiome in rats. Food Chem Toxicol 111:144–152

    CAS  Google Scholar 

  • Feldman N, Rotter-Maskowitz A, Okun E (2015) DAMPs as mediators of sterile inflammation in aging-related pathologies. Ageing Res Rev 24:29–39

    CAS  Google Scholar 

  • Halajzadeh J, Milajerdi A, Reiner Ž, Amirani E, Kolahdooz F, Barekat M et al (2019) Effects of resistant starch on glycemic control, serum lipoproteins and systemic inflammation in patients with metabolic syndrome and related disorders: a systematic review and meta-analysis of randomized controlled clinical trials. Crit Rev Food Sci Nutr 1–13. https://doi.org/10.1080/10408398.2019.1680950

  • Hancock S, Ehrich M, Hinckley J, Pung T, Jortner BS (2007) The effect of stress on the acute neurotoxicity of the organophosphate insecticide chlorpyrifos. Toxicol Appl Pharmacol 219(2–3):136–141

    CAS  Google Scholar 

  • Ibrahim KA, Khwanes SA, El-Desouky MA, Elhakim HK (2019) Propolis relieves the cardiotoxicity of chlorpyrifos in diabetic rats via alleviations of paraoxonase-1 and xanthine oxidase genes expression. Pestic Biochem Physiol 159:127–135

    CAS  Google Scholar 

  • Jaiswal C, Verma Y (2012) Effect of α-tocopherol on haematological alteration induced by chlorpyrifos in albino rats. Haryana Veterinarian 51:108–110

    Google Scholar 

  • Jayaraj R, Megha P, Sreedev P (2016) Organochlorine pesticides, their toxic effects on living organisms and their fate in the environment. Interdiscip Toxicol 9(3–4):90–100

    CAS  Google Scholar 

  • Johnson FO, Chambers JE, Nail CA, Givaruangsawat S, Carr RL (2009) Developmental chlorpyrifos and methyl parathion exposure alters radial-arm maze performance in juvenile and adult rats. Toxicol Sci 109(1):132–142

    CAS  Google Scholar 

  • Kacem I, Maoua M, Hasni Y, Kalboussi H, Hafsia M, Souguir S et al (2019) Evaluation of the risk of metabolic syndrome among shift workers in Tunisia. East Mediterr Health J 25(10):677–685

    Google Scholar 

  • Kain V, Prabhu SD, Halade GV (2014) Inflammation revisited: inflammation versus resolution of inflammation following myocardial infarction. Basic Res Cardiol 109(6):444

    Google Scholar 

  • Kalender S, Ogutcu A, Uzunhisarcikli M, Açikgoz F, Durak D, Ulusoy Y, Kalender Y (2005) Diazinon-induced hepatotoxicity and protective effect of vitamin E on some biochemical indices and ultrastructural changes. Toxicology 211(3):197–206

    CAS  Google Scholar 

  • Karanth S, Pope C (2000) Carboxylesterase and A-esterase activities during maturation and aging: relationship to the toxicity of chlorpyrifos and parathion in rats. Toxicol Sci 58(2):282–289

    CAS  Google Scholar 

  • Li J, Ren F, Li Y, Luo J, Pang G (2019) Chlorpyrifos induces metabolic disruption by altering levels of reproductive hormones. J Agric Food Chem 67(38):10553–10562

    CAS  Google Scholar 

  • Mahlangu T, Dludla PV, Nyambuya TM, Mxinwa V, Mazibuko-Mbeje SE, Cirilli I et al (2020) A systematic review on the functional role of Th1/Th2 cytokines in type 2 diabetes and related metabolic complications. Cytokine 126:154892

    CAS  Google Scholar 

  • Mansour SA, Mossa ATH (2010) Oxidative damage, biochemical and histopathological alterations in rats exposed to chlorpyrifos and the antioxidant role of zinc. Pestic Biochem Physiol 96(1):14–23

    CAS  Google Scholar 

  • Mendoza CE, Shields JB, Phillips WEJ (1971) Distribution of carboxylesterase activities in different tissues of albino rats. Comp Biochem Physiol B: Comp Biochem 40(4):841–854

    CAS  Google Scholar 

  • Moon JM, Chun BJ, Cho YS (2016) Hyperglycemia at presentation is associated with in hospital mortality in non-diabetic patient with organophosphate poisoning. Clin Toxicol 54(3):252–258

    CAS  Google Scholar 

  • Overstreet DH (2000) Organophosphate pesticides, cholinergic function and cognitive performance in advanced age. Neurotoxicology 21(1–2):75–81

    CAS  Google Scholar 

  • Park SK, Schwartz J, Weisskopf M, Sparrow D, Vokonas PS, Wright RO, Coull B, Nie H, Hu H (2006) Low-level lead exposure, metabolic syndrome, and heart rate variability: the VA Normative Aging Study. Environ Health Perspect 114(11):1718–1724

    CAS  Google Scholar 

  • Pawelec G, Goldeck D, Derhovanessian E (2014) Inflammation, ageing and chronic disease. Curr Opin Immunol 29:23–28

    CAS  Google Scholar 

  • Ramirez-Vargas MA, Flores-Alfaro E, Uriostegui-Acosta M, Alvarez-Fitz P, Parra-Rojas I, Moreno-Godinez ME (2018) Effects of exposure to malathion on blood glucose concentration: a meta-analysis. Environ Sci Pollut Res 25(4):3233–3242

    CAS  Google Scholar 

  • Rathod AL, Garg RK (2017) Chlorpyrifos poisoning and its implications in human fatal cases: a forensic perspective with reference to Indian scenario. J Forensic Legal Med 47:29–34

    Google Scholar 

  • Reygner J, Lichtenberger L, Elmhiri G, Dou S, Bahi-Jaber N, Rhazi L et al (2016) Inulin supplementation lowered the metabolic defects of prolonged exposure to chlorpyrifos from gestation to young adult stage in offspring rats. PLoS One 11(10):e0164614

  • Tang J, Cao Y, Rose RL, Hodgson E (2002) In vitro metabolism of carbaryl by human cytochrome P450 and its inhibition by chlorpyrifos. Chem Biol Interact 141(3):229–241

    CAS  Google Scholar 

  • Wang HP, Liang YJ, Long DX, Chen JX, Hou WY, Wu YJ (2009) Metabolic profiles of serum from rats after subchronic exposure to chlorpyrifos and carbaryl. Chem Res Toxicol 22(6):1026–1033

    CAS  Google Scholar 

  • Zimniak P (2008) Detoxification reactions: relevance to aging. Ageing Res Rev 7(4):281–300

    CAS  Google Scholar 

Download references

Acknowledgments

The authors want to convey an appreciation of Prof. Pamela J. Lein for her nice comments in editing the manuscript.

Funding

The authors received funding from the Research Affairs of Birjand University of Medical Sciences.

Author information

Authors and Affiliations

  1. Healthy Ageing Research Center, Neyshabur University of Medical Sciences, Neyshabur, Iran

    Saeed Samarghandian

  2. Cardiovascular Diseases Research Center, Birjand University of Medical Sciences, Birjand, Iran

    Moshen Foadoddin, Mahmoud Zardast & Tahereh Farkhondeh

  3. Medical Toxicology and Drug Abuse Research Center (MTDRC), Birjand University of Medical Sciences (BUMS), Birjand, Iran

    Omid Mehrpour

  4. Rocky Mountain Poison and Drug Safety, Denver Health, Denver, CO, USA

    Omid Mehrpour

  5. Department of Environmental Health Engineering, Food Safety Division, School of Public Health and Center for Environmental Research, Tehran University of Medical Sciences, Tehran, Iran

    Parisa Sadighara

  6. Student Research Committee, Birjand University of Medical Sciences, Birjand, Iran

    Babak Roshanravan

Authors
  1. Saeed Samarghandian
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Moshen Foadoddin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mahmoud Zardast
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Omid Mehrpour
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Parisa Sadighara
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Babak Roshanravan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Tahereh Farkhondeh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tahereh Farkhondeh.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Responsible Editor: Mohamed M. Abdel-Daim

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Samarghandian, S., Foadoddin, M., Zardast, M. et al. The impact of age-related sub-chronic exposure to chlorpyrifos on metabolic indexes in male rats. Environ Sci Pollut Res 27, 22390–22399 (2020). https://doi.org/10.1007/s11356-020-08814-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-020-08814-0

Keywords

Search

Navigation