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Early Access

Health impact of heavy metals stressed hydroponically grown garden lettuce (Lactuca sativa L.) on rat models

DOI
https://doi.org/10.14719/pst.5664
Submitted
9 October 2024
Published
01-07-2025
Versions

Abstract

In this study, in vivo pharmacological effects of plant extracts of hydroponically grown lettuce (HyL), compared with heavy metals (HMs) stressed hydroponically grown plants (HyCd, HyCr and HyPb) were studied. Lactuca sativa L. (lettuce) was grown hydroponically. The highest salt tolerance was estimated against 0.256 mM of Cd, Cr and Pb, respectively. So, we selected plants from 0.256 mM salt stress and extracts were prepared for in vivo pharmacological studies and data was analyzed statistically using ANOVA. Heavy metal stressed plants of HyCd, HyCr and HyPb showed elevated levels of glucose on the 21st day of the experiment, being as low as 355 mg/dl, 364 mg/dl and 210 mg/dl, respectively. In the instance of the liver, kidney and serum biomarkers; it was seen that the levels were restored to normal in HyL, in comparison to heavy metal stress groups (p<0.05). The histopathological studies showed normal distribution and morphology of cells, while in metal-induced plan extracts deformed, submerged and distorted morphology was noted, representing toxicity of heavy metals. We evaluated the antioxidant markers of different organs, which showed variation from normal control values, indicating a less protective effect of metal on antioxidant profiles. The administration of HyL treatment resulted in increased levels of serotonin (0.127 µg/mg of tissue) and dopamine (0.089 µg/mg of tissue) in HPLC quantification. Among heavy metals, HyPb showed minor levels of neurotransmitters (Dopamine; 0.024 and Serotonin; 0.236 µg/mg of tissue) while these neurotransmitters were not detected in the case of HyCd, HyCr. Overall, HyPb showed comparatively higher activity than HyCd and HyCr (p < 0.05). Lactuca sativa possesses good HMs accumulation potential; still, HMs had significant effects on the histology and antioxidant profiles in rat models.

References

  1. 1. Javaid A, Junaid JA, Ayub B, Chattha WS, Khan AI, Saleem H. Biofortified lettuce (Lactuca sativa L.): a potential option to fight hunger. Biofort Grain Veg Crops: Elsevier; 2024. p. 291–305. https://doi.org/10.1016/B978-0-323-91735-3.00016-9
  2. 2. Ismail H, Mirza B. Evaluation of analgesic, anti-inflammatory, anti-depressant and anti-coagulant properties of Lactuca sativa (CV. Grand Rapids) plant tissues and cell suspension in rats. BMC Comp Alter Med. 2015;15(1):1–7. https://doi.org/10.1186/s12906-015-0742-0
  3. 3. Mie A Andersen HR, Gunnarsson S, Kahl J, Kesse-Guyot E, Rembiałkowska E, et al. Human health implications of organic food and organic agriculture: a comprehensive review. Env Health. 2017;16:1–22. https://doi.org/10.1186/s12940-017-0315-4
  4. 4. Durán-Lara EF, Valderrama A, Marican A. Natural organic compounds for application in organic farming. Agri. 2020;10(2):41. https://doi.org/10.3390/agriculture10020041
  5. 5. Shatilov M, Razin A, Ivanova M. Analysis of the world lettuce market. IOP Conference Series: Earth and Environmental Science, IOP Publishing; 2019. https://doi.org/10.1088/1755-1315/395/1/012053
  6. 6. Roy S, Sarkar T, Upadhye VJ, Chakraborty R. Comprehensive review on fruit seeds: nutritional, phytochemical, nanotechnology, toxicity, food biochemistry and biotechnology perspective. Appli Biochem Bioechnol. 2023:1–172. https://doi.org/10.1007/s12010-023-04674-9
  7. 7. Karande UB, Kadam A, Umrikar BN, Wagh V, Sankhua R, Pawar N. Environmental modelling of soil quality, heavy-metal enrichment and human health risk in sub-urbanized semiarid watershed of Western India. Model Earth Syst Environ. 2020;6:545–56. https://doi.org/10.1007/s40808-019-00701-z
  8. 8. Uddin MM, Zakeel MCM, Zavahir JS, Marikar FM, Jahan I. Heavy metal accumulation in rice and aquatic plants used as human food: A general review. Toxics. 2021;9(12):360. https://doi.org/10.3390/toxics9120360
  9. 9. Zhao D, Wang P, Zhao FJ. Dietary cadmium exposure, risks to human health and mitigation strategies. Critic Rev Environ Sci Technol. 2023;53(8):939–63. https://doi.org/10.1080/10643389.2022.2099192
  10. 10. Tariq Y, Ehsan N, Riaz U, Nasir R, Khan WA, Iqbal R, et al. Assessment of heavy metals (oid) accumulation in eggplant and soil under different irrigation systems. Water. 2023;15(6):1049. https://doi.org/10.3390/w15061049
  11. 11. Rehman MU, Khan R, Khan A, Qamar W, Arafah A, Ahmad A, et al. Fate of arsenic in living systems: Implications for sustainable and safe food chains. J Hazard Mat. 2021;417:126050. https://doi.org/10.1016/j.jhazmat.2021.126050
  12. 12. Sarker A, Kim JE, Islam ARMT, Bilal M, Rakib MRJ, Nandi R, et al. Heavy metals contamination and associated health risks in food webs-a review focuses on food safety and environmental sustainability in Bangladesh. Environ Sci Pollu Res. 2022;29(3):3230–45. https://doi.org/10.1007/s11356-021-17153-7
  13. 13. Vasilachi IC, Stoleru V, Gavrilescu M. Analysis of heavy metal impacts on cereal crop growth and development in contaminated soils. Agri. 2023;13(10):1983. https://doi.org/10.3390/agriculture13101983
  14. 14. Behtash F, Amini T, Mousavi SB, Seyed HH, Kaya O. Efficiency of zinc in alleviating cadmium toxicity in hydroponically grown lettuce (Lactuca sativa L. cv. Ferdos). BMC Plant Bio. 2024;24(1):648. https://doi.org/10.1186/s12870-024-05325-9
  15. 15. León-Cañedo JA, Alarcón-Silvas SG, Fierro-Sañudo JF, de Oca GAR-M, Partida-Ruvalcaba L, Díaz-Valdés T, et al. Mercury and other trace metals in lettuce (Lactuca sativa) grown with two low-salinity shrimp effluents: accumulation and human health risk assessment. Sci Total Environ. 2019;650:2535–44. https://doi.org/10.1016/j.scitotenv.2018.10.003
  16. 16. Mulyukin MA, Sutormin OS, Samoylenko ZA, Kravchenko IV, Bulatova EV, Gulakova NM, et al. Heavy metal content in medicinal plants grown in hydroponics and forest soil in the central part of Western Siberia. Forests. 2024;15(9):1606. https://doi.org/10.3390/f15091606
  17. 17. Helms KM, Dickson RW, Bertucci MB, Rojas AA, Gibson KE. Metal micronutrient and silicon concentration effects on growth and susceptibility to pythium root rot for hydroponic lettuce (Lactuca sativa). Horticult. 2023;9(6):670. https://doi.org/10.3390/horticulturae9060670
  18. 18. Naseem S, Ismail H. In vitro and In vivo valuations of antioxidative, anti-alzheimer, antidiabetic and anticancer potentials of hydroponically and soil grown Lactuca sativa. BMC Comp Med Therapies. 2022;22(1):30. https://doi.org/10.1186/s12906-022-03520-5
  19. 19. Minaiyan M, Asghari G, Taheri D, Saeidi M, Nasr-Esfahani S. Anti-inflammatory effect of Moringa oleifera Lam. seeds on acetic acid-induced acute colitis in rats. Avicenna J Phytomed. 2014;4(2):127. https://doi.org/10.22038/ajp.2014.1072
  20. 20. Singh Y, Gautam DS. Neuroprotective effect of Ashtanga Ghrita on spatial learning and memory in scopolamine-induced amnesia in at model. J Ayur. 2024;18(3):167–72. https://doi.org/10.4103/joa.joa_33_22
  21. 21. Yassa HD, Tohamy AF. Extract of Moringa oleifera leaves ameliorates streptozotocin-induced diabetes mellitus in adult rats. Acta Histochemica. 2014;116(5):844–54. https://doi.org/10.1016/j.acthis.2014.02.002
  22. 22. Akinola OB, Biliaminu SA, Adediran RA, Adeniye KA, Abdulquadir FC. Characterization of prefrontal cortex microstructure and antioxidant status in a rat model of neurodegeneration induced by aluminium chloride and multiple low-dose streptozotocin. Metabolic Brain Disease. 2015;30(6):1531–36. https://doi.org/10.1007/s11011-015-9719-4
  23. 23. OECD. Test No. 420: Rcute oral toxicity - Fixed dose procedure; 2002. https://doi.org/10.1787/9789264070943-en
  24. 24. Walf AA, Frye CA. The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nature Protocols. 2007;2(2):322–28. https://doi.org/10.1038/nprot.2007.44
  25. 25. Du LL, Chai DM, Zhao LN, Li XH, Zhang FC, Zhang HB, et al. AMPK activation ameliorates Alzheimer's disease-like pathology and spatial memory impairment in a streptozotocin-induced Alzheimer's disease model in rats. J Alzheimer's Disease. 2015;43(3):775–84. https://doi.org/10.3233/JAD-140564
  26. 26. Kumar R, Arora V, Ram V, Bhandari A, Vyas P. Hypoglycemic and hypolipidemic effect of Allopolyherbal formulations in streptozotocin induced diabetes mellitus in rats. Int J Diabetes Mellitus. 2015;3(1):45–50. https://doi.org/10.1016/j.ijdm.2011.01.005
  27. 27. Mughal I, Shah Y, Tahir S, Haider W, Fayyaz M, Yasmin T, et al. Protein quantification and enzyme activity estimation of Pakistani wheat landraces. PloS One. 2020;15(9):0239375. https://doi.org/10.1371/journal.pone.0239375
  28. 28. Tahir I, Khan MR, Shah NA, Aftab M. Evaluation of phytochemicals, antioxidant activity and amelioration of pulmonary fibrosis with Phyllanthus emblica leaves. BMC comp Alter Med. 2016;16:1–12. https://doi.org/10.1186/s12906-016-1387-3
  29. 29. Ghani MA, Barril C, Bedgood DR, Prenzler PD. Development of a method suitable for high-throughput screening to measure antioxidant activity in a linoleic acid emulsion. Antioxidants. 2019;8(9):366. https://doi.org/10.3390/antiox8090366
  30. 30. Kakkar P, Das B, Viswanathan P. A modified spectrophotometric assay of superoxide dismutase. Indian J Biochem Biophy. 1984;21:130–32.
  31. 31. Hashmi WJ, Ismail H, Mehmood F, Mirza B. Neuroprotective, antidiabetic and antioxidant effect of Hedera nepalensis and lupeol against STZ+ AlCl 3 induced rats model. DARU J Pharma Sci. 2018;26:179–90. https://doi.org/10.1007/s40199-018-0223-3
  32. 32. Ismail H, Khalid D, Ayub SB, Ijaz MU, Akram S, Bhatti MZ, et al. Effects of Phoenix dactylifera against streptozotocin-aluminium chloride induced Alzheimer’s rats and their In silico study. BioMed Res Int. 2023;2023(1):1725638. https://doi.org/10.1155/2023/1725638
  33. 33. Dong J, Xiao T, Xu Q, Liang F, Gu S, Wang F, et al. Anxious personality traits: Perspectives from basic emotions and neurotransmitters. Brain Sci. 2022;12(9):1141. https://doi.org/10.3390/brainsci12091141
  34. 34. Ostadkarampour M, Putnins EE. Monoamine oxidase inhibitors: a review of their anti-inflammatory therapeutic potential and mechanisms of action. Front Pharma. 2021;12:676239. https://doi.org/10.3389/fphar.2021.676239
  35. 35. Chatterjee M, Verma R, Lakshmi V, Sengupta S, Verma AK, Mahdi AA, et al. Anxiolytic effects of Plumeria rubra var. acutifolia (Poiret) L. flower extracts in the elevated plus-maze model of anxiety in mice. Asian J Psych. 2013;6(2):113–18. https://doi.org/10.1016/j.ajp.2012.09.005
  36. 36. Haider S, Tabassum S. Impact of 1-day and 4-day MWM training techniques on oxidative and neurochemical profile in rat brain: A comparative study on learning and memory functions. Neurobiol Learn Memory. 2018;155:390–402. https://doi.org/10.1016/j.nlm.2018.09.003
  37. 37. Rather MA, Thenmozhi AJ, Manivasagam T, Bharathi MD, Essa MM, Guillemin GJ. Neuroprotective role of Asiatic acid in aluminium chloride induced rat model of Alzheimer’s disease. Front Biosci. 2018;10:262–75. https://doi.org/10.2741/s514
  38. 38. Lu C, Wang Y, Xu T, Li Q, Wang D, Zhang L, et al. Genistein ameliorates scopolamine-induced amnesia in mice through the regulation of the cholinergic neurotransmission, antioxidant system and the ERK/CREB/BDNF signaling. Frontiers in Pharma. 2018;9:1153. https://doi.org/10.3389/fphar.2018.01153
  39. 39. Rajput MS, Sarkar PD. Modulation of neuro-inflammatory condition, acetylcholinesterase and antioxidant levels by genistein attenuates diabetes associated cognitive decline in mice. Chem- Biol Int. 2017;268:93–102. https://doi.org/10.1016/j.cbi.2017.02.021
  40. 40. Rahman MS, Hossain KS, Das S, Kundu S, Adegoke EO, Rahman MA, et al. Role of insulin in health and disease: an update. Int J Mol Sci. 2021;22(12):6403. https://doi.org/10.3390/ijms22126403
  41. 41. Siedlecka D, Micał W, Krzewicka RE. Streptozotocin-an antibiotic used to induce diabetes on experimental animals. J Edu Health Sport. 2020;10(9):906–09. https://doi.org/10.12775/JEHS.2020.10.09.110
  42. 42. Huang Z, Chen Y, Zhang Y. Mitochondrial reactive oxygen species cause major oxidative mitochondrial DNA damages and repair pathways. J Biosci. 2020;45(1):84. https://doi.org/10.1007/s12038-020-00055-0
  43. 43. Ye J, Medzhitov R. Control strategies in systemic metabolism. Nature Metabolism. 2019;1(10):947–57. https://doi.org/10.1038/s42255-019-0118-8
  44. 44. Ragab AR, Elkablawy MA, Sheik BY, Baraka HN. Antioxidant and tissue-protective studies on ajwa extract: dates from Al Madinah Almonwarah, Saudia Arabia. Egyptian J Forensic Sci Appli Toxi. 2012;220(1245):1–22. https://doi.org/10.12816/0005068
  45. 45. Nandi A, Yan LJ, Jana CK, Das N. Role of catalase in oxidative stress-and age-associated degenerative diseases. Oxidat Med Cell Longe. 2019;2019(1):9613090. https://doi.org/10.1155/2019/9613090
  46. 46. Moghaddam AH, Zare M. Neuroprotective effect of hesperetin and nano-hesperetin on recognition memory impairment and the elevated oxygen stress in rat model of Alzheimer’s disease. Biomed Pharma. 2018;97:1096–101. https://doi.org/10.1016/j.biopha.2017.11.047
  47. 47. Arshad FK, Haroon R, Jelani S, Masood HB. A relative in vitro evaluation of antioxidant potential profile of extracts from pits of Phoenix dactylifera L. (ajwa and zahedi dates). Int J Adv Info Sci Technol. 2015;35(35):28–37.
  48. 48. Zhang M, ShiYang X, Zhang Y, Miao Y, Chen Y, Cui Z, et al. Coenzyme Q10 ameliorates the quality of postovulatory aged oocytes by suppressing DNA damage and apoptosis. Free Radical Biol Med. 2019;143:84–94. https://doi.org/10.1016/j.freeradbiomed.2019.08.002
  49. 49. Lakshmi B, Sudhakar M, Prakash KS. Protective effect of selenium against aluminum chloride-induced Alzheimer’s disease: behavioral and biochemical alterations in rats. Biol Trace Element Res. 2015;165(1):67–74. https://doi.org/10.1007/s12011-015-0229-3
  50. 50. Klein MO, Battagello DS, Cardoso AR, Hauser DN, Bittencourt JC, Correa RG. Dopamine: functions, signaling and association with neurological diseases. Cell Mol Neurobiol. 2019;39(1):31–59. https://doi.org/10.1007/s10571-018-0632-3
  51. 51. Kotagal V, Spino C, Bohnen NI, Koeppe R, Albin RL. Serotonin, β-amyloid and cognition in Parkinson disease. Annals Neuro. 2018;83(5):994–1002. https://doi.org/10.1002/ana.25236
  52. 52. Xu H, Wang Z, Zhu L, Sui Z, Bi W, Liu R, et al. Targeted neurotransmitters profiling identifies metabolic signatures in rat brain by LC-MS/MS: application in insomnia, depression and Alzheimer’s disease. Molecules. 2018;23(9):2375. https://doi.org/10.3390/molecules23092375
  53. 53. Hashmi WJ, Ismail H, Mehmood F, Mirza B. Neuroprotective, antidiabetic and antioxidant effect of Hedera nepalensis and lupeol against STZ+ AlCl 3 induced rats model. DARU J Pharma Sci. 2018;26(2):179–90. https://doi.org/10.1007/s40199-018-0223-3
  54. 54. El Rasafi T, Oukarroum A, Haddioui A, Song H, Kwon EE, Bolan N, et al. Cadmium stress in plants: A critical review of the effects, mechanisms and tolerance strategies. Critical Rev Environ Sci Technol. 2022;52(5):675–726. https://doi.org/10.1080/10643389.2020.1835435
  55. 55. Mitra S, Chakraborty AJ, Tareq AM, Emran TB, Nainu F, Khusro A, et al. Impact of heavy metals on the environment and human health: Novel therapeutic insights to counter the toxicity. J King Saud Uni-Sci. 2022;34(3):101865. https://doi.org/10.1016/j.jksus.2022.101865

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