Skip to main content

Advertisement

Log in

Black coffee mitigates diethyl phthalate disrupted folliculogenesis, reduced gonadotropins, and ovarian lesions in female albino mice

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

Abstract

Phthalates are multifunctional compounds with extensive applications and emerging environmental pollutants. Due to their ubiquity in the environment and unavoidable exposure to humans, concerns have been voiced about public health dangers. This study was aimed to explore the diethyl phthalate (DEP) toxicity and the potential protective effect of black coffee in female Swiss albino mice. Four-week-old mice, weighing 12 ± 1 g were segregated into five groups (n = 10), designated as G-I (without any treatment), G-II (treated with corn oil), G-III (exposed to 1.5 mg/g body wt. (B.W.) DEP), G-IV (received 2 μg/g B.W coffee), and G-V (co-administrated with 1.5 mg/g DEP and 2 μg/g B.W coffee). Before dose administration, the coffee extract was assessed for its antioxidant potential through FRAP, TPC, and GC–MS analyses. Respective phthalates/coffee doses were administrated orally, once a day for 8 weeks consecutively starting from the prepubescent stage. After 56 days, mice were acclimated for 4 days then dissected. Morphological assessments showed an irregular shape of the ovaries in DEP-treated mice as compared to the control. The average bodyweight of DEP-intoxicated mice (p ≤ 0.05) increased notably against control, while DEP plus coffee group showed a regular gain in the average weight of mice. The gonado-somatic index showed non-significant variations among all groups. Micrometric studies showed that the diameter of secondary follicles (115 µm) in the ovaries of DEP-exposed mice (p ≤ 0.001) decreased significantly as compared to control (204 µm); conversely, follicular diameter in the coffee control group (248) increased significantly. Serum FSH and LH levels were significantly increased in DEP-exposed mice with a noteworthy decrease in estrogen level while hormonal levels of all other groups were comparable to control. Histological sections of DEP-exposed mice ovaries showed anatomical disruptions contrary to other groups, which were comparable with control. Antioxidant potential was checked in ovaries homogenates; FRAP values showed a notable decrease in DEP group in comparison with the control group, in contrast to G-V, when DEP was co-administrated with coffee. This study concluded that black coffee has protective effect, against DEP-instigated reproductive toxicity in Swiss albino female mice.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

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

Similar content being viewed by others

Data availability

Most of the data generated during this study are included in this article. However, raw data sheets and histopathological figures are available from the corresponding as well as co-authors upon reasonable request.

References

  • Abdeltaif SA, Elkhatim KA, Hassan AB (2018) Estimation of phenolic and flavonoid compounds and antioxidant activity of spent coffee and black tea (processing) waste for potential recovery and reuse in Sudan. Recycling 3(2):27

    Article  Google Scholar 

  • Ali S, Hussain S, Khan R, Mumtaz S, Ashraf Nasra, Andleeb S, Shakir HA, Tahir HM, Khan MKA, Ulhaq M (2019) Renal toxicity of heavy metals (cadmium and mercury) and their amelioration with ascorbic acid in rabbits. Environ Sci  Pollut Res 26(4):3909–3920. https://doi.org/10.1007/s11356-018-3819-8

    Article  CAS  Google Scholar 

  • Ali S, Awan Z, Mumtaz S, Shakir HA, Ahmad F, Ulhaq M, Tahir HM, Awan MS, Sharif S, Irfan M, Khan MA (2020) Cardiac toxicity of heavy metals (cadmium and mercury) and pharmacological intervention by vitamin C in rabbits. Environ Sci Pollut Res 27(23):29266–29279

    Article  CAS  Google Scholar 

  • Ara C, Asmatullah NB, Ali S, Batool F, Shakir HA, Arshad A (2020) Abnormal steroidogenesis, oxidative stress, and reprotoxicity following prepubertal exposure to butylparaben in mice and protective effect of Curcuma longa. Environ Sci Pollut Res 28(9):1–11

    Google Scholar 

  • Ara C, Asmatullah, Butt N et al (2021) Abnormal steroidogenesis, oxidative stress, and reprotoxicity following prepubertal exposure to butylparaben in mice and protective effect of Curcuma longa. Environ Sci Pollut Res 28:6111–6121. https://doi.org/10.1007/s11356-020-10819-8

    Article  CAS  Google Scholar 

  • Asmatullah CA, Andleeb S, Tahir M, Zahid B, Arshad M (2018) Therapeutic effect of guava fruit extract on cadmium induced toxicity in developing Mus musculus. Pak J Zool 50(3):929–939

    Article  CAS  Google Scholar 

  • Beausoleil C, Ormsby JN, Gies A, Hass U, Heindel JJ, Holmer ML, …, Schoenfelder G (2013) Low dose effects and non-monotonic dose responses for endocrine active chemicals: science to practice workshop: workshop summary. Chemosphere 93(6):847-856

  • Benzie IF, Strain JJ (1999) Ferric reducing/antioxidant power assay: direct measure of total antioxidant activity of biological fluids and modified version for simultaneous measurement of total antioxidant power and ascorbic acid concentration. Methods Enzymol 29:15–27

    Article  Google Scholar 

  • Bouhlal F, Aqil Y, Chamkhi I, Belmaghraoui W, Labjar N, Hajjaji SE, Benabdellah GA, Aurag J, Lotfi EM, Mahi ME (2020) GC-MS analysis, phenolic compounds quantification, antioxidant, and antibacterial activities of the hydro-alcoholic extract of spent coffee grounds. J Biol Active Prod Nat 10(4):325–337

    CAS  Google Scholar 

  • Buckley JP, Engel SM, Braun JM, Whyatt RM, Daniels JL, Mendez MA, Richardson DB, Xu Y, Calafat AM, Wolff MS et al (2016) Prenatal phthalate exposures and body mass index among 4 to 7-year-old children: a pooled analysis. Epidemiology 27(3):449

    Article  Google Scholar 

  • Campos MS, Mello IF, Delgado AP, Favareto A, Lopes CMT, Batista MM, Kempinas WD-G, Paumgartten FJR (2015) Sexual maturation and fertility of mice exposed to triphenyltin during prepubertal and pubertal periods. Toxicology Reports 2:405–414

    Article  Google Scholar 

  • Chang HC, Nfor ON, Ho CC, Chen PH, Kung YY, Hsu SY, Liaw YP (2020) Changes in high-density lipoprotein cholesterol levels about coffee consumption among Taiwanese adults. J Multidiscip Healthc 13:1427

    Article  Google Scholar 

  • Chen S, Teoh NC, Chitturi S, Farrell GC (2014) Coffee and non-alcoholic fatty liver disease: brewing evidence for hepatoprotection? J Gastroenterol Hepatol 29(3):435–441

    Article  Google Scholar 

  • Dar KK, Ali S, Ejaz M, Nasreen S, Ashraf N, Gillani SF, Shafi N, Safeer S, Khan MA, Andleeb S, Mughal TA (2019) In vivo induction of hepatocellular carcinoma by diethylnitrosoamine and pharmacological intervention in Balb C mice using Bergenia ciliata extracts. Brazilian Journal of Biology 79(4):629–638. https://doi.org/10.1590/1519-6984.186565

    Article  CAS  Google Scholar 

  • Dórea JG, da Costa THM (2005) Is coffee a functional food? Br J Nutr. 93(6):773-782

  • El-Nabi SH, Dawoud G, El-Garawani I, El-Shafey S (2018) HPLC analysis of phenolic acids, antioxidant activity and in vitro effectiveness of green and roasted Caffea arabica bean extracts: a comparative study. Anticancer Agents Med Chem 18(9):1281–1288

    Article  CAS  Google Scholar 

  • Hafsah H, Iriawati I, Syamsudin TS (2020) Dataset of volatile compounds from flowers and secondary metabolites from the skin pulp, green beans, and peaberry green beans of robusta coffee. Data Brief 29:105219

    Article  Google Scholar 

  • Haile M, Bae HM, Kang WH (2020) Comparison of the antioxidant activities and volatile compounds of coffee beans obtained using digestive bio-processing (elephant dung coffee) and commonly known processing methods. Antioxidants 9(5):408

    Article  CAS  Google Scholar 

  • Hannon PR, Flaws JA (2015) The effects of phthalates on the ovary. Front Endocrinol 6:8

    Article  Google Scholar 

  • Hannon PR, Peretz J, Flaws JA (2014) Daily exposure to Di (2-ethylhexyl) phthalate alters estrous cyclicity and accelerates primordial follicle recruitment potentially via dysregulation of the phosphatidylinositol 3-kinase signaling pathway in adult mice. Biol Reprod 90(6):136–141

    Article  Google Scholar 

  • Harley KG, Berger K, Rauch S, Kogut K, Henn BC, Calafat AM, Huen K, Eskenazi B, Holland N (2017) Association of prenatal urinary phthalate metabolite concentrations and childhood BMI and obesity. Pediatr Res 82(3):405

    Article  CAS  Google Scholar 

  • Hart R, Doherty DA, Frederiksen H, Keelan JA, Hickey M, Sloboda D, …, Main KM (2014) The influence of antenatal exposure to phthalates on subsequent female reproductive development in adolescence: a pilot study. Reproduction 147(4):379-390

  • Hayashi K, Nakae A, Fukushima Y et al (2010) Contamination of rice by etofenprox, diethyl phthalate and alkylphenols: effects on first delivery and sperm count in mice. J Toxicol Sci 35:49–55

    Article  CAS  Google Scholar 

  • Higdon JV, Frei B (2006) Coffee and health: a review of recent human research. Crit Rev Food Sci Nutr 46:101–123

    Article  CAS  Google Scholar 

  • Huber WW, Parzefall W (2005) Modification of N-acetyltransferases and glutathione S-transferases by coffee components: possible relevance for cancer risk. Methods Enzymol. 401:307–41

    Article  CAS  Google Scholar 

  • Hurst CH, Waxman DJ (2003) Activation of PPARα and PPARγ by environmental phthalate monoesters. Toxicol Sci 74(2):297–308

    Article  CAS  Google Scholar 

  • Hussain S, Ali S, Mumtaz S, Shakir HA, Ahmad F, Tahir HM, Ulhaq M, Khan MA, Zahid MT (2020) Dose and duration-dependent toxicological evaluation of lead acetate in chicks. Environ Sci Poll Res 27(13):15149–15164. https://doi.org/10.1007/s11356-020-08016-8

    Article  CAS  Google Scholar 

  • Khan R, Ali S, Mumtaz S, Andleeb S, Ulhaq M, Tahir HM, Khan MKA, Khan MA, Shakir HA (2019) Toxicological effects of toxic metals (cadmium and mercury) on blood and the thyroid gland and pharmacological intervention by vitamin C in rabbits. Environ Sci Poll Res 26(16):16727–16741. https://doi.org/10.1007/s11356-019-04886-9

    Article  CAS  Google Scholar 

  • Koch HM, Drexler H, Angerer J (2003) An estimation of the daily intake of di(2-ethylhexyl)phthalate (DEHP) and other phthalates in the general population. Int J Hyg Environ Health 206:1–7. https://doi.org/10.1078/1438-4639-00205

    Article  Google Scholar 

  • Kohn MC, Parham F, Masten SA, Portier CJ, Shelby MD, Brock JW, Needham LL (2000) Human exposure estimates for phthalates. Environ Health Perspect 108:A440–A442. https://doi.org/10.1289/ehp.108-a440b

    Article  CAS  Google Scholar 

  • Koniecki D, Wang R, Moody RP, Zhu J (2011) Phthalates in cosmetic and personal care products: concentrations and possible dermal exposure. Environ Res 111(3):329–336

    Article  CAS  Google Scholar 

  • Labunska I, Santillo D (2004) Environmental and human health concerns relating to diethyl phthalate (DEP), a common ingredient in cosmetics and other personal care products, Greenpeace Research Laboratories Technical Note 06

  • Lovekamp-Swan T, Davis BJ (2003) Mechanisms of phthalate ester toxicity in the female reproductive system. Environ Health Perspect 111(2):139–145

    Article  CAS  Google Scholar 

  • Martino-Andrade AJ, Chahoud I (2010) Reproductive toxicity of phthalate esters. Mol Nutr Food Res 54(1):148–157

    Article  CAS  Google Scholar 

  • Moura-Nunes N, Perrone D, Farah A, Donangelo CM (2009) The increase in human plasma antioxidant capacity after acute coffee intake is not associated with endogenous non-enzymatic antioxidant components. Int J Food Sci Nutr 60(sup6):173–181

    Article  CAS  Google Scholar 

  • Moyer B, Hixon ML (2012) Reproductive effects in F1 adult females exposed in utero to moderate to high doses of mono-2-ethylhexylphthalate (MEHP). Reprod Toxicol 34(1):43–50

    Article  CAS  Google Scholar 

  • Mughal TA, Saleem MZ, Ali S, Anwar KK, Bashir MM, Babar M, Khan MA (2019) Evaluation of hepatotoxicity of carbon tetrachloride and pharmacological intervention by vitamin E in Balb c mice. Pak J Zool 51(2):755–761

    Article  CAS  Google Scholar 

  • Mumtaz S, Ali S, Khan R, Andleeb S, Ulhaq M, Khan MA, Shakir HA (2019) The protective role of ascorbic acid in the hepatotoxicity of cadmium and mercury in rabbits. Environ Sci Pollut Res 26(14):14087–14096. https://doi.org/10.1007/s11356-019-04620-5

    Article  CAS  Google Scholar 

  • National Research Council (US) (2011) Committee for the update of the guide for the care and use of laboratory animals. In: Guide for the care and use of laboratory animals. 8th edition. National Academies Press (US), Washington (DC)

  • Nawrot P, Jordan S, Eastwood J, Rotstein J, Hugenholtz A, Feeley M (2003) Effects of caffeine on human health. Food Addit Contam 20(1):1–30

    Article  CAS  Google Scholar 

  • Pan MH, Tung YC, Yang G, Li S, Ho CT (2016) Molecular mechanisms of the anti-obesity effect of bioactive compounds in tea and coffee. Food Funct 7(11):4481–4491

    Article  CAS  Google Scholar 

  • Pietrini F, Iannilli V, Passatore L, Carloni S, Sciacca G, Cerasa M, Zacchini M (2022) Ecotoxicological and genotoxic effects of dimethyl phthalate (DMP) on Lemna minor L. and Spirodela polyrhiza (L.) Schleid. plants under a short-term laboratory assay. Sci Total Environ. https://doi.org/10.1016/j.scitotenv.2021.150972

  • Rodríguez-Carmona Y, Cantoral A, Trejo-Valdivia B, Téllez-Rojo MM, Svensson K, Peterson KE, Meeker JD, Schnaas L, Solano M, Watkins DJ (2019) Phthalate exposure during pregnancy and long-term weight gain in women. Environ Res 169:26–32. https://doi.org/10.1016/j.envres.2018.10.014

    Article  CAS  Google Scholar 

  • Şanlialp SE, Erteki̇n A (2019) The effects of coffee consumption on cardiovascular heart diseases and other diseases. Van Sag Bil Derg. 12(2):25–31

    Google Scholar 

  • Schettler T (2006) Human exposure to phthalates via consumer products. Int J Androl 29(1):134–139

    Article  CAS  Google Scholar 

  • Sekiguchi S, Ito S, Honma T (2003) Experimental model to study reproductive toxicity of chemicals using induced ovulation in immature F344 rats. Ind Health 41(3):287–290

    Article  CAS  Google Scholar 

  • Sekizawa J, Dobson S, Touch RJ, Sekizawa J, Dobson S et al (‎2003)‎ Diethyl phthalate. World Health Organization. https://apps.who.int/iris/handle/10665/42637

  • Silva MJ, Barr DB, Reidy JA, Malek NA, Hodge CC, Caudill SP, Brock JW, Needham LL, Calafat AM (2004) Urinary levels of seven phthalate metabolites in the US population from the National Health and Nutrition Examination Survey (NHANES) 1999–2000. Environ Health Perspect 112(3):331–338

    Article  CAS  Google Scholar 

  • Sonde V, D’Souza A, Tarapore R, Pereira L, Khare MP, Sinkar P, Krishnan S, Rao CV (2000) Simultaneous administration of diethylphthalate and ethyl alcohol and its toxicity in male Sprague-Dawley rats. Toxicology 147(1):23–31

    Article  CAS  Google Scholar 

  • Staples CA, Parkerton TF, Peterson DR (2000) A risk assessment of selected phthalate esters in North American and Western European surface waters. Chemosphere 40(8):885–891

    Article  CAS  Google Scholar 

  • Su PH, Chen JY, Lin CY, Chen HY, Liao PC, Ying TH, Wang SL (2014) Sex steroid hormone levels and reproductive development of eight-year-old children following in utero and environmental exposure to phthalates. PLoS One 9(9):e102788

    Article  Google Scholar 

  • Thammarat P, Kulsing C, Wongravee K, Leepipatpiboon N, Nhujak T (2018) Identification of volatile compounds and selection of discriminant markers for elephant dung coffee using static headspace gas chromatography—Mass spectrometry and chemometrics. Molecules 23(8):1910

    Article  Google Scholar 

  • Tunnicliffe JM, Erdman KA, Reimer RA, Lun V, Shearer J (2008) Consumption of dietary caffeine and coffee in physically active populations: physiological interactions. Appl Physiol Nutr Metab 33(6):1301–1310

    Article  CAS  Google Scholar 

  • WHO (2003) Diethyl phthalate. Concise international chemical assessment document 52. World Health Organization, Geneva, Switzerland. http://www.inchem.org/documents/cicads/cicads/cicad52.htm

  • Wu AH, Arakawa K, Stanczyk FZ, Berg DVD, Koh WP, Yu MC (2005) Tea and circulating estrogen levels in postmenopausal Chinese women in Singapore. Carcinogenesis 26(5):976–980

    Article  CAS  Google Scholar 

  • Zhang T, Li L, Qin XS, Zhou Y, Zhang XF, Wang LQ, …, Shen W (2014) Di-(2-ethylhexyl) phthalate and bisphenol A exposure impairs mouse primordial follicle assembly in vitro. Environ Mol Mutagen 55(4):343-353

  • Zhou C, Flaws JA (2017) Effects of an environmentally relevant phthalate mixture on cultured mouse antral follicles. Toxicol Sci 156(1):217–229

    CAS  Google Scholar 

  • Zhou C, Gao L, Flaws JA (2017) Prenatal exposure to an environmentally relevant phthalate mixture disrupts reproduction in F1 female mice. Toxicol Appl Pharmacol 318:49–57

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors are highly obliged to the Institute of Zoology, University of the Punjab, Lahore, Pakistan, for providing research facilities.

Author information

Authors and Affiliations

Authors

Contributions

Conceptualization: Chaman Ara and Asmatullah; data curation: Chaman Ara, Asmatullah, Shaukat Ali, Nageena Ramzan, Hafiz Abdullah Shakir, and Faiza Yaseen; formal analysis: Chaman Ara, Asmatullah, Nida Shahzad, Shaukat Ali, and Asia Iqbal; investigation: Chaman Ara, Asmatullah, Shaukat Ali, and Hafiz Abdullah Shakir; Methodology: Chaman Ara, Asmatullah, Asia Iqbal, Shaukat Ali, Farrah Batool, Hafiz Abdullah Shakir, and Aqsa Arshad; histopathology: Naila Butt, Nageena Ramzan, and Faiza Yaseen; software: Shaukat Ali and Hafiz Abdullah Shakir; Supervision: Chaman Ara and Asmatullah; writing original draft: Faiza Yaseen, Iram Liaqat, and Faiza Yasee; review and editing: Chaman Ara, Asmatullah, Hafiz Abdullah Shakir, and Shaukat Ali; all authors have read and approved the manuscript.

Corresponding author

Correspondence to Shaukat Ali.

Ethics declarations

Ethics approval

All animal trials were executed according to local and worldwide procedures. The nearby way is the Wet op de dierproeven (article 9) of Dutch law (international) and an associated rule planned via the Bureau of Animal Research Licensing, Local University, as detailed in our earlier papers (Ali et al. 2019, 2020; Hussain et al. 2020; Ara et al. 2020; Khan et al. 2019; Mumtaz et al. 2019; Mughal et al. 2019; Dar et al. 2019). The rearing and use of mice were carried out using NIH Publication “Guide for the Care and Use of Laboratory Animals” (NRC 2004) and with the approval vide No. D/681/UZ dated 04–04-2019 by the local bioethical committee of the university on animal experimentation.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declared 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

Ara, C., Asmatullah, Ramzan, N. et al. Black coffee mitigates diethyl phthalate disrupted folliculogenesis, reduced gonadotropins, and ovarian lesions in female albino mice. Environ Sci Pollut Res 29, 47254–47266 (2022). https://doi.org/10.1007/s11356-022-19138-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-022-19138-6

Keywords

Navigation