Skip to main content
SpringerLink
Log in

Wild Garlic Allium triquetrum L. Alleviates Lead Acetate-Induced Testicular Injuries in Rats

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

The current study investigates the potential alleviating activity of bulbs (B) and leaves (L) of Allium triquetrum aqueous extract (ATE) on repro-toxicity induced by lead acetate (Pb) in male Wistar rats administrated orally for 3 consecutive weeks. Eighteen groups of rats were divided into the control, Pb (500 mg/kg body weight/day), positive controls of B and L (2 g, 3 g, 4 g, 6 g/kg body weight/day), in addition to four mixtures of each of Pb-B (Pb-B1, Pb-B2, Pb-B3, Pb-B4) and Pb-L (Pb-L1, Pb-L2, Pb-L3, Pb-L4). The two extracts were subjected to phytochemical screening and HPLC analysis. Sperm characteristics were evaluated by CASA system, as well as the serum testosterone, testicular and epididymal levels of glutathione (GSH), glutathione peroxidase (GPx), and malondialdehyde (MDA). The phytochemical screening proved that bulbs’ and leaves’ extracts were rich in various compounds and the HPLC showed that leaves contain more tannins. Results revealed a significant decrease in the testicular and in the epididymal weights, sperm concentration, motility, testosterone, velocity, vitality, round cells, GSH, and GPx levels in the Pb-intoxicated rats compared to the control, with the exception of MDA concentration that was significantly increased. However, the co-administration of garlic extracts (Pb-B and Pb-L) exhibited a significant increase in all mentioned markers, except for the MDA level which was reduced. Likewise, Pb caused histological injuries in the testicular seminiferous of rats, while the co-administration of wild garlic has reduced such effect, especially in the higher doses. Both extracts of Pb-B and Pb-L have attenuated Pb toxicity in a dose-dependent manner. In conclusion, aqueous extracts of A. triquetrum have the potential to reduce Pb testicular injuries by boosting sperm characteristics and ameliorating oxidative stress markers.

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
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  1. Otmani I, Abdennour C, Dridi A, Kahalerras L, Halima-Salem A (2019) Characteristics of the bitter and sweet honey from Algeria Mediterranean coast. Vet World 12(4):551–557. https://doi.org/10.14202/vetworld.2019.551-557

    Article  PubMed  PubMed Central  Google Scholar 

  2. Lanzotti V, Romano A, Lanzuise S, Bonanomi S, Scala F (2012) Antifungal saponins from bulbs of white onion, Allium cepa L. Phytochemistry 74:133–139. https://doi.org/10.1016/j.phytochem.2011.11.008

    Article  CAS  PubMed  Google Scholar 

  3. Chowdhury R, Dutta A, Chaudhuri SR, Sharma N, Giri AK, Chaudhuri K (2008) In vitro and in vivo reduction of sodium arsenite induced toxicity by aqueous garlic extract. Food Chem Toxicol 46:740–751. https://doi.org/10.1016/j.fct.2007.09.108

    Article  CAS  PubMed  Google Scholar 

  4. Weiss N, Papatheodorou L, Morihara N, Hilge R, Ide N (2013) Aged garlic extract restores nitric oxide bioavailability in cultured human endothelial cells even under conditions of homocysteine elevation. J Ethnopharmacol 145:162–167. https://doi.org/10.1016/j.jep.2012.10.045

    Article  CAS  PubMed  Google Scholar 

  5. Rivlin RS (2001) Historical perspective on the use of garlic. J Nutr 131:951S-954S. https://doi.org/10.1093/jn/131.3.951S

    Article  CAS  PubMed  Google Scholar 

  6. Vijayakumar S, Malaikozhundan B, Saravanakumar K, Durán-Lara EF, Wang MH, Vaseeharan B (2019) Garlic clove extract assisted silver nanoparticle - antibacterial, antibiofilm, antihelminthic, anti-inflammatory, anticancer and ecotoxicity assessment. J PhotochemPhotobiol B 198:111558. https://doi.org/10.1016/j.jphotobiol.2019.111558

    Article  CAS  Google Scholar 

  7. Amagase H (2006) Clarifying the real bioactive constituents of garlic. In: Rivlin R, Budoff M, Amagase H (eds) Symposium of significance of garlic and its constituents in cancer and cardiovascular disease; 9–11 April 2005. Georgetown University, Washington, DC. J Nutr 136:716S–725S

  8. Morakinyo AO, Oloyo AK, Raji Y, Adegoke OA (2008) Effects of aqueous extract of garlic (Allium sativum) on testicular functions in the rats. Niger J Health Biomed Sci 7:26–30. https://doi.org/10.4314/njhbs.v7i2.11672

    Article  Google Scholar 

  9. Josling P (2005) ALLICIN: The heart of garlic nature’s aid to healing the human body. Chicago

  10. Yang JS, Kok LF, Lin YH, Kuo TC, Yang JL, Lin CC, Chen GW, Huang WW, Ho HC, Chung JG (2006) Diallyl disulfide inhibits WEHI-3 leukemia cells in vivo. Anticancer Res 26:219–225 (PMID: 16475702)

    CAS  PubMed  Google Scholar 

  11. Lanzotti V, Scala F, Bonanomi G (2014) Compounds from Allium species with cytotoxic and antimicrobial activity. Phytochem Rev 13:769–791. https://doi.org/10.1007/s11101-014-9366-0

    Article  CAS  Google Scholar 

  12. Drif F, Abdennour C, Ciğerci İH, Muddassir AM, Mansouri O, Messarah M (2019) Preliminary assessment of stress and genotoxicity biomarkers in bivalve molluscs from the Gulf of Annaba, Algeria. Bull Environ ContamToxicol 102:555–559. https://doi.org/10.1007/s00128-019-02583-4

    Article  CAS  Google Scholar 

  13. Senapati SK, Dey S, Dwived SK, Swarup D (2001) Effect of garlic (Allium sativum L.) extract on tissue lead level in rats. J Ethnopharmacol 76:229–232. https://doi.org/10.1016/s0378-8741(01)00237-9

    Article  CAS  PubMed  Google Scholar 

  14. Andjelkovic M, Djordjevic AB, Antonijevic E, Antonijevic B, Stanic M, Kotur-Stevuljevic J, Spasojevic-Kalimanovska V, Jovanovic M, Boricic N, Wallace D, Bulat Z (2019) Toxic effect of acute cadmium and lead exposure in rat blood, liver, and kidney. Int J Environ Res Public Health 16:274. https://doi.org/10.3390/ijerph16020274

    Article  CAS  PubMed Central  Google Scholar 

  15. El-Magd MA, Kahilo KA, Nasr NE, Kamal T, Shukry M, Saleh AA (2016) A potential mechanism associated with lead-induced testicular toxicity in rats. Andrologia 49:e12750. https://doi.org/10.1111/and.12750

    Article  CAS  Google Scholar 

  16. Allouche L, Hamadouche M, Touabti A (2009) Chronic effects of low lead levels on sperm quality, gonadotropins and testosterone in albino rats. Exp Toxicol Pathol 61:503–510. https://doi.org/10.1016/j.etp.2008.12.003

    Article  CAS  PubMed  Google Scholar 

  17. Berredjem R, Mansouri O, Abdennour C, Boulakoud MK, Khelili K (2014) What is the benefit of garlic supplementation to Pb intoxicated rats? Adv Environ Biol 8:268–275

    Google Scholar 

  18. Chowdhury AR (2009) Recent advances in heavy metals induced effect on male reproductive function-a retrospective. Al Ameen J Med Sci 2:37–42

    CAS  Google Scholar 

  19. Sainath SB, Meena R, Supriya C, Reddy KP, Reddy PS (2011) Protective role of Centella asiatica on lead-induced oxidative stress and suppressed reproductive health in male rats. Environ Toxicol Pharmacol 32:146–154. https://doi.org/10.1016/j.etap.2011.04.005

    Article  CAS  PubMed  Google Scholar 

  20. Iavicoli I, Fontana L, Bergamaschi A (2009) The effects of metals as endocrine disruptors. J Toxicol Environ Health Part B 12:206–223. https://doi.org/10.1080/10937400902902062

    Article  CAS  Google Scholar 

  21. Liguori G, Pelagalli A, Assisi L, Squillacioti C, Costagliola A, Mirabella N (2018) Effects of orexins on 17β-estradiol synthesis and P450 aromatase modulation in the testis of alpaca (Vicugna pacos). Anim Reprod Sci 192:313–320. https://doi.org/10.1016/j.anireprosci.2018.03.032

    Article  CAS  PubMed  Google Scholar 

  22. Elgawish RAR, Abdelrazek HMA (2014) Effects of lead acetate on testicular function and caspase-3 expression with respect to the protective effect of cinnamon in albino rats. Toxicol Rep 1:795–801. https://doi.org/10.1016/j.toxrep.2014.10.010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Limón-Pacheco J, Gonsebatt ME (2009) The role of antioxidants and antioxidant-related enzymes in protective responses to environmentally induced oxidative stress. Mutat Res 674:137–147. https://doi.org/10.1016/j.mrgentox.2008.09.015

    Article  CAS  PubMed  Google Scholar 

  24. He Y, Zou Q, Chen H, Weng S, Luo T, Zeng W (2016) Lead inhibits human sperm functions by reducing the levels of intracellular calcium, cAMP, and tyrosine phosphorylation. Tohoku J Exp Med 238:295–303. https://doi.org/10.1620/tjem.238.295

    Article  CAS  PubMed  Google Scholar 

  25. Dorostghoal M, Seyyednejad SM, Jabari A (2013) Protective effects of Fumaria parviflora L on lead-induced testicular toxicity in male rats. Andrologia 46:437–446. https://doi.org/10.1111/and.12100

    Article  PubMed  Google Scholar 

  26. Corea G, Fattorusso E, Lanzotti V (2003) Saponins and flavonoids of Allium triquetrum. J Nat Prod 66:1405–1411. https://doi.org/10.1021/np030226q

    Article  CAS  PubMed  Google Scholar 

  27. Drevius LO, Eriksson H (1966) Osmotic swelling of mammalian spermatozoa. Exp Cell Res 42:136–156. https://doi.org/10.1016/0014-4827(66)90327-2

    Article  CAS  PubMed  Google Scholar 

  28. Jayendran RS, Van Der Ven HH, Zaneveld LJ (1992) The hypo-osmotic swelling test: an update. Arch Androl 29:105–116. https://doi.org/10.3109/01485019208987714

    Article  Google Scholar 

  29. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1006/abio.1976.9999

    Article  CAS  PubMed  Google Scholar 

  30. Weckbecker G, Cory JG (1988) Ribonucleotide reductase activity and growth of glutathione-depleted mouse leukemia L1210 cells in vitro. Cancer Lett 40:257–264. https://doi.org/10.1016/0304-3835(88)90084-5

    Article  CAS  PubMed  Google Scholar 

  31. Flohé L, Günzler WA (1984) [12] Assays of glutathione peroxidase. Methods Enzymol 105:114–120. Academic Press. https://doi.org/10.1016/S0076-6879(84)05015-1

  32. Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358. https://doi.org/10.1016/0003-2697(79)90738-3

    Article  CAS  PubMed  Google Scholar 

  33. Godínez-Solís Y, Solís-Heredia MJ, Roa-Espitia A, Parra-Forero Y, Hernández-González EO, Hernández-Ochoa I, Quintanilla-Vega B (2019) Low concentrations of lead decrease the sperm fertilization ability by altering the acrosome reaction in mice. Toxicol Appl Pharmacol 380:114694. https://doi.org/10.1016/j.taap.2019.114694

    Article  CAS  PubMed  Google Scholar 

  34. Fihri AF, Al-Waili NS, El-Haskoury R, Bakour M, Amarti A, Ansari MJ, Lyoussi B (2016) Protective effect of Morocco carob honey against lead-induced anemia and hepato-renal toxicity. Cell PhysiolBiochem 39:115–122. https://doi.org/10.1159/000445610

    Article  CAS  Google Scholar 

  35. Hamadouche NA, Sadi N, Kharoubi O, Slimani M, Aoues A (2013) The protective effect of vitamin E against genotoxicity of lead acetate intraperitoneal administration in male rat. Not Sci Biol 5: 412–419. https://doi.org/10.15835/nsb549125

  36. Wang L, Xun P, Zhao Y, Wang X, Qian L, Chen F (2008) Effects of lead exposure on sperm concentrations and testes weight in male rats: a meta-regression analysis. J Toxicol Environ Health A 71:454–463. https://doi.org/10.1080/15287390701839331

  37. Flora SJS, Agrawal S (2017) Arsenic, cadmium, and lead. In: Gupta RC (ed) Reproductive and developmental toxicology. Academic Press, Elsevier, USA, pp 537–566. https://doi.org/10.1016/B978-0-12-804239-7.00031-7

  38. Ouarda M (2011) Abdennour C (2016) Evaluation of the therapeutic efficiency of raw garlic on reproduction of domestic rabbits under lead induced toxicity. Ann Biol Res 2:389–393

    Google Scholar 

  39. Shubina OS, Dudenkova NA (2016) The effect of lead on the process of spermatogenesis in sex glands of male albino rats. Vet World 9:1129–1134. https://doi.org/10.14202/vetworld.2016.1129-1134

  40. Castellini C, Mourvaki E, Sartini B, Cardinali R, Moretti E, Collodelb G, Fortanerc S, Sabbionic E, Renieri T (2009) In vitro toxic effects of metal compounds on kinetic traits and ultra structure of rabbit spermatozoa. ReprodToxicol 27:46–54. https://doi.org/10.1016/j.reprotox.2008.12.003

  41. Corpas I, Castillo M, Marquina D, Benito MJ (2002) Lead intoxication in gestational and lactation periods alters the development of male reproductive organs. Ecotox Environ Safe 53:259–266. https://doi.org/10.1006/eesa.2002.2230

    Article  CAS  Google Scholar 

  42. He X, Wu J, Yuan L, Lin F, Yi J, Li J, Yuan H, Shi J, Yuan T, Zhang S, Fan Y (2017) Lead induces apoptosis in mouse TM3 Leydig cells through the Fas/FasL death receptor pathway. Environ Toxicol Pharmacol 56:99–105. https://doi.org/10.1016/j.etap.2017.08.034

    Article  CAS  PubMed  Google Scholar 

  43. Fahim MA, Tariq S, Adeghate E (2013) Vitamin E modifies the ultrastructure of testis and epididymis in mice exposed to lead intoxication. Ann Anat 195:272–277. https://doi.org/10.1016/j.aanat.2012.11.001

    Article  CAS  PubMed  Google Scholar 

  44. Johanisson E, Campana A, Luthi R, de Agostini A (2000) Evaluation of ‘round cells’ in semen analysis: a comparative study. Hum Rep Update 6:404–412. https://doi.org/10.1093/humupd/6.4.404

    Article  CAS  Google Scholar 

  45. Palermo GD, Neri QV, Cozzubbo T, Cheung S, Pereira N, Rosenwaks Z (2016) Shedding light on the nature of seminal round cells. PLOS ONE 11:e0151640. https://doi.org/10.1371/journal.pone.0151640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Barraud-Lange V, Pont JC, Ziyyat A, Pocate KP, Sifer C, Cedrin-Durnerin I, Fechtali B, Ducot B, Wolf JP (2011) Seminal leukocytes are Good Samaritans for spermatozoa. FertilSteril 96:1315–1319. https://doi.org/10.1016/j.fertnstert.2011.09.035

    Article  Google Scholar 

  47. Batra N, Nehru B, Bansal MP (2011) Influence of lead and zinc on rat male reproduction at ‘biochemical and histopathological levels.’ J Appl Toxicol 21:507–512. https://doi.org/10.1002/jat.796

    Article  Google Scholar 

  48. Naha N, Chowdhury AR (2006) Inorganic lead exposure in battery and paint factory: effect on human sperm structure and functional activity. J UOEH 28:157–171. https://doi.org/10.7888/juoeh.28.157

    Article  CAS  PubMed  Google Scholar 

  49. Nasr NE, Elmadawy MA, Almadaly EA, Abdo W, Zamel MM (2017) Garlic powder attenuates apoptosis associated with lead acetate-induced testicular damage in adult male rats. Alex J Vet Sci 54:70–78. https://doi.org/10.5455/ajvs.268149

    Article  Google Scholar 

  50. Yang JM, Arnush M, Chen QY, Wu XD, Pang B, Jiang XZ (2003) Cadmium-induced damage to primary cultures of rat Leydig cells. ReprodToxicol 17:553–560. https://doi.org/10.1016/S0890-6238(03)00100-X

    Article  CAS  Google Scholar 

  51. Soleimanzadeh A, Kian M, Moradi S, Mahmoudi S (2020) Carob (Ceratonia siliqua L.) fruit hydro-alcoholic extract alleviates reproductive toxicity of lead in male mice: evidence on sperm parameters, sex hormones, oxidative stress biomarkers and expression of Nrf2 and iNOS. Avicenna J Phytomed 10:35–49. https://doi.org/10.22038/AJP.2019.13513

  52. Li N, Hou Y, Ma D, Jing W, Dahms HU, Wang L (2015) Lead accumulation, oxidative damage and histopathological alteration in testes and accessory glands of freshwater crab, Sinopotamonhenanense, induced by acute lead exposure. Ecotoxicol Environ Saf 117:20–27. https://doi.org/10.1016/j.ecoenv.2015.03.019

    Article  CAS  PubMed  Google Scholar 

  53. Bechara EJH (2004) Lead poisoning and oxidative stress. In: Institute of de Quimica, Universidade de Sao Paulo, Brazil. SFRR`s 12th biennial meeting progamme and abstracts; 5–9 May 2004; Crown Plaza PanamericanoHotel Buenos Aires Argentina. Free Radic Biol Med 36:S9–46. p S22

  54. Manna P, Sinha M, Sil PC (2009) Taurine plays a beneficial role against cadmium-induced oxidative renal dysfunction. Amino Acids 36:417–428. https://doi.org/10.1007/s00726-008-0094-x

    Article  CAS  PubMed  Google Scholar 

  55. Moskaug JØ, Carlsen H, Myhrstad MC, Blomhoff R (2005) Polyphenols and glutathione synthesis regulation. Am J Clin Nutr 81:277S-283S. https://doi.org/10.1093/ajcn/81.1.277S

  56. Menacer A, Boukhatem MN, Benhelal A, Saïdi F (2017) In vitro antioxidant activity of different extracts of Algerian Allium plant (Allium triquetrum L.). Rev des Bio-Resources 7:80–91. https://doi.org/10.12816/0045885

  57. Abdelhamid FM, Mahgoub HA, Ateya AI (2020) Ameliorative effect of curcumin against lead acetate–induced hemato-biochemical alterations, hepatotoxicity, and testicular oxidative damage in rats. Environ Sci Pollut Res Int 27(10):10950–10965. https://doi.org/10.1007/s11356-020-07718-3

  58. Offor SJ, Mbagwu HOC, Orisakwe OE (2019) Improvement of lead acetate-induced testicular injury and sperm quality deterioration by Solanum anomalum Thonn. Ex. Schumach Fruit Extracts in Albino Rats. J Fam Reprod Health 13(2):98–108

    Google Scholar 

  59. Sharma P, Khan IA, Singh R (2018) Curcumin and quercetin ameliorated cypermethrin and deltamethrin-induced reproductive system impairment in male Wistar rats by upregulating the activity of pituitary gonadal hormones and steroidogenic enzymes. Int J Fertil Steril 12:72. https://doi.org/10.22074/ijfs.2018.5160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Odumosu FM, Olokodana O, Huthman IO, Akinyemi RA, Adesanya OA, Adefule AK (2013) Effect of onion, garlic and Aridan aqueous extract on hormone influenced testis weight of adult Wistar rats. Int J Chem Pharm Res 2:9

    Google Scholar 

  61. Kasuga S, Uda N, Kyo E, Ushijima M, Morihara N, Itakura Y (2001) Pharmacologic activities of aged garlic extract in comparison with other garlic preparations. J Nutr 131:1080S-S1084. https://doi.org/10.1093/jn/131.3.1080S

    Article  CAS  PubMed  Google Scholar 

  62. Nasr AY (2017) The impact of aged garlic extract on adriamycin-induced testicular changes in adult male Wistar rats. Acta Histochem 119(6):648–662. https://doi.org/10.1016/j.acthis.2017.07.006

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to thank the General Directorate of Scientific Research and Technological Development (DGRSDT) for supporting this project (award number 04/2016). Special thanks are given to Dr. T. Hamel (plant identification), Dr. M. Zebour, Dr. Z. Gouasmi, and Pr. Y. Hadef (HPLC analysis), University of Badji Mokhtar-Annaba. Thanks are also given to the Laboratory of Pathological Anatomy, EL-Hadjar, Annaba Hospital, for histological studies.

Funding

The author(s) received financial support for bench fees, but not for authorship, and/or for publication of this article.

Author information

Authors and Affiliations

  1. Laboratory of Animal Ecophysiology, Department of Biology, Faculty of Sciences, University of Badji Mokhtar-Annaba, 23000, Annaba, Algeria

    Labiba Kahalerras, Ines Otmani & Cherif Abdennour

Authors
  1. Labiba Kahalerras
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ines Otmani
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cherif Abdennour
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

L Kahalerras drafted the manuscript, managed the experimental work, and contributed to the analysis and interpretation of results; I Otmani participated in the experimental work; C Abdennour corrected and revised the manuscript. All authors read and gave the final approval of manuscript.

Corresponding author

Correspondence to Labiba Kahalerras.

Ethics declarations

Ethics Approval

Experiments were carried out according to the international animal handling of Helsinki Declaration of 2008 and to the National Ethical Committee of Animal Sciences.

Conflict of Interest

The authors declare no competing interests.

Additional information

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

Kahalerras, L., Otmani, I. & Abdennour, C. Wild Garlic Allium triquetrum L. Alleviates Lead Acetate-Induced Testicular Injuries in Rats. Biol Trace Elem Res 200, 2205–2222 (2022). https://doi.org/10.1007/s12011-021-02818-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-021-02818-8

Keywords

Search

Navigation