ABSTRACT
Various studies have investigated the effects of olive oil on semen quality and sperm physiology. This review systematically discusses and summarises the link between olive oil and semen quality. To achieve this contribution, we searched the PubMed, Scopus, Web of Science, and Google scholar databases for articles and reports published in English (as full articles or abstract only) from September 1975 through February 2017 using the key words “olive oil” and “sperm”. Certain interrelated articles were also considered. In summary, olive oil appears to preserve semen quality in in vivo systems. This result seems to be applicable in humans, but requires additional confirmation in clinical trials. Meanwhile adding olive oil to seminal fluid in vitro seems not to be favorable to sperm parameters. The mechanisms by which olive oil preserves semen quality are through enhancing gonadal function, reducing the level of oxidative injury and lipid peroxidation, and improving nitric oxide signaling.
Introduction
Olive oil, the chief fat in the Mediterranean diet[Citation1], is used as a home remedy for serious diseases, such as cancers and cardiovascular diseases, via intentional modification of dietary habits.[Citation2–Citation4] Approximately 77% of olive oil is mono-unsaturated fatty acids such as oleic acid.[Citation5–Citation7] In addition, olive oil contains saturated fatty acids (~14%), polyunsaturated fatty acids (~9%), alpha-tocopherol, and vegetable mucilage.[Citation5,Citation6]
Moreover, olive oil contains several potent bioactive compounds such as antioxidant polyphenols (oleuropein[Citation8,Citation9], hydroxytyrosol[Citation10,Citation11], and tyrosol[Citation12,Citation13]), antioxidant flavonoids (luteolin[Citation14,Citation15] and apigenin[Citation16,Citation17]), and other bioactive organic molecules, including squalene.[Citation18,Citation19] These compounds have been directly and indirectly linked to various health problems such as cancer[Citation2,Citation20], coronary heart disease[Citation21,Citation22], and reproductive capability.[Citation5,Citation23,Citation24]
As it is the focus of many health investigations into olive oil, several scientists have explored the effects of olive oil or its above-mentioned bioactive compounds on semen quality and sperm physiology. Thus far, these studies have not been systematically summarised. Therefore, this review discusses and summarises the link between olive oil and semen quality (primarily sperm quality and quantity). To achieve this, we searched the PubMed, Scopus, Web of Science, and Google scholar databases for articles and reports published in English (as full articles or abstract only) from September 1975 through August 2016 using the key words “olive oil” and “sperm”. In addition, certain related articles were also considered to support the discussion and conclusion.
Effect of olive oil on sperm parameters
To-date, the majority of research studies that have directly interrelated olive oil with semen quality and sperm function have been nonclinical (i.e., animal studies). It has been shown that rabbits fed a high-fat diet (0.05% cholesterol) had significant decreases in their sperm parameters (volume, count, motility) associated with a marked increase in sperm cell abnormalities as well as abnormal acrosome reaction.[Citation6] Olive oil administration at 7% v/w for 16 weeks succeeded in recovering the loss in the above semen parameters and retaining sperm function[Citation6,Citation25] whereas, olive oil orally administered at 0.4 mL daily for 6 weeks did not alter sperm count, motility, or morphology in male rats.[Citation26]
A recent study by El-Kholy et al.[Citation27] showed that a genetically modified soya bean diet negatively affects sperm count, motility, and morphology.[Citation27] Furthermore, the addition of extra virgin olive oil to this diet restored these sperm parameters.[Citation27] Taken alone, extra virgin olive oil, when added to the normal diet of male rats at 15%, did not induce any change in semen quality.[Citation27] A newly published in vivo system study on the effect of olive oil compared to other toxicants showed that provision of olive oil (1 mL/kg/day) for 15 days did not affect sperm DNA fragmentation or the oxidative stress status (i.e., normal malondialdehyde).[Citation28]
Effect of some olive oil bioactive compounds on sperm parameters
Boars fed on squalene at 20 or 40 mg/kg/day for 60 days had a higher semen volume and higher sperm motility, which increased their reproductive performance.[Citation29] A study by Mohamadi et al.[Citation30] showed that oleuropein intercalates with the DNA double helix of salmon sperm[Citation30], which increases the melting temperature of DNA and therefore stabilises its structure.[Citation30] Apigenin did not improve sperm count or motility in male mice.[Citation31]
In vitro studies
In their in vitro study to show the effects of vaginal lubricants on sperm motility, Goldenberg and White[Citation32] found that olive oil as a vaginal lubricant decreased sperm motility by approximately 50% and 25% after 15 min and 2 hours, respectively.[Citation32] A later in vitro study on human semen by Anderson et al.[Citation33] confirmed these findings by showing that the olive oil reduces sperm progressive motility.[Citation33]
Mechanistic studies
Olive oil enhances gonadal function
It has been found that a genetically modified soya bean diet (15%) reduced the weight of the testis, seminal vesicles, epididymis, and prostate in adult male albino rats.[Citation27] In addition, this diet decreased the serum testosterone, zinc, and alpha-tocopherol concentrations.[Citation27] Mixing extra virgin olive oil with the genetically modified soybean diet was found to increase all of these anatomical and biochemical markers.[Citation27]
In addition, squalene supplementation at 20–40 mg/kg/day for 60 days increased testosterone levels in boars, which improved their semen quality and thus reproductive outcomes.[Citation29] Rats fed a high-protein diet supplemented with oleuropein at 0.1 g/100 g had higher levels of luteinizing hormone and testicular testosterone, which positively affects spermatogenesis and hence semen quality.[Citation34]
In humans, administration of extra virgin olive oil was found to improve the androgen hormonal profiles (higher levels of testosterone and luteinizing hormone) in healthy male volunteers.[Citation35] In effect, these results have been found to be imperative for patients with poor semen quality, but not for normal individuals.[Citation35,Citation36] On the other hand, adult male Wistar rats orally administered olive oil at 0.4 mL/day for 6 weeks had an insignificant change in their gonadal hormones (testosterone, follicle stimulating hormone, and luteinizing hormone), or inhibin-B, a protein that inhibits follicle-stimulating hormone production, compared to the control group (without olive oil).[Citation26] In addition, in the same study, the authors showed that olive oil did not change the weight of the seminal vesicles, epididymis, prostate gland, Cowper glands, and testes.[Citation26]
Olive oil reduces oxidative injury to sperm
Oleic acid, the main component of olive oil, was found to be easily oxidised compared to other types of fat.[Citation37] This chemical property is favorable to sperm since it lowers the free radical level as a result of oxidation, which may damage the main cellular macromolecules (e.g., proteins, lipids, and nucleic acids).[Citation6,Citation38] Therefore, administration of olive oil may improve sperm integrity, and consequently, sperm function, by modifying the lipid composition of these dynamic cells. This modification is mimicked by lowering the cholesterol content, which lowers the cholesterol/phospholipids ratio, in the bilayer membrane of sperm.[Citation6]
Olive oil improves nitric oxide signaling in sperm
It has been shown that nitric oxide diffusion dynamics and signaling are inversely proportional to the cholesterol content in the bilayer membrane of the cell.[Citation39] The lower the phospholipid/cholesterol ratio in the bilayer membrane the higher the nitric oxide diffusion, and hence the signaling.[Citation39] Based on this evidence, given that administration of olive oil lowers the content of cholesterol in the bilayer membrane and that nitric oxide is crucial for adequate sperm motility, olive oil may improve sperm quality by improving nitric oxide signaling.
Effect of some olive oil constituents on sperm health
Further, oleic acid was found to possess antioxidant behaviour.[Citation40] Oleic acid quenches free radicals, which may attack the sperm plasma membrane and reduces the lipid peroxidation, which improves sperm vitality. Furthermore, olive oil is rich in several potent antioxidant compounds such as polyphenols (e.g., oleuropein[Citation8,Citation9], hydroxytyrosol[Citation10,Citation11], tyrosol[Citation12,Citation13]), flavonoids (e.g., luteolin[Citation14,Citation15], apigenin[Citation16,Citation17]), and vitamin E (approximately 14 mg per 100 g of olive oil).[Citation41] These molecular defense mechanisms were found to counteract the damaging effect of pro-oxidants and enhance sperm quality. Moreover, it has been shown that semen centrifugation reduces the sperm quality (i.e., lower motility and viability).[Citation42,Citation43] Adding hydroxytyrosol to sperm incubating media improved sperm viability and reduced the levels of reactive oxygen species, a highly reactive chemical species that can cause oxidative damage to biomolecules[Citation44], and sperm DNA oxidation following centrifugation.[Citation43]
Conclusions and future perspectives
Olive oil appears to preserve semen quality in in vivo systems (~9 studies). This result seems to also be applicable in humans (~2 studies), but requires additional proof through clinical trials. However, direct addition of olive oil to seminal fluid in vitro is not favorable to sperm parameters. The mechanisms by which olive oil preserves semen quality in in vivo systems or humans include reduction of the level of oxidative damage and lipid peroxidation, enhancing gonadal function, and improving nitric oxide dynamics and signaling.
Acknowledgments
This study was supported by the deanship of research at Jordan University of Science and Technology. The author declares no conflict of interest.
Related Research Data
References
- Abdul, R.; Yaakob Bin, C. M.; Ismail, A.; Hashim, P. FTIR Spectroscopy Coupled with Chemometrics of Multivariate Calibration and Discriminant Analysis for Authentication of Extra Virgin Olive Oil. Int. J. Food Properties. 2017.
- Banks, L. D.; Amoah, P.; Niaz, M. S.; Washington, M. K.; Adunyah, S. E.; Ramesh, A. Olive Oil Prevents Benzo(A)Pyrene [B(A)P]-Induced Colon Carcinogenesis through Altered B(a)P Metabolism and Decreased Oxidative Damage in Apc(Min) Mouse Model. J. Nutr. Biochem. 2016, 28, 37–50. 10.1016/j.jnutbio.2015.09.023.
- Psaltopoulou, T.; Kosti, R. I.; Haidopoulos, D.; Dimopoulos, M.; Panagiotakos, D. B. Olive Oil Intake Is Inversely Related to Cancer Prevalence: A Systematic Review and a Meta-Analysis of 13,800 Patients and 23,340 Controls in 19 Observational Studies. Lipids Health Dis. 2011, 10, 127. 10.1186/1476-511X-10-127.
- Guasch-Ferre, M.; Hu, F. B.; Martinez-Gonzalez, M. A.; Fito, M.; Bullo, M.; Estruch, R.; Ros, E.; Corella, D.; Recondo, J.; Gomez-Gracia, E.; Fiol, M.; Lapetra, J.;, et al. . Olive Oil Intake and Risk of Cardiovascular Disease and Mortality in the PREDIMED Study. BMC Med. 2014, 12, 78. 10.1186/1741-7015-12-78.
- Waterman, E.; Lockwood, B. Active Components and Clinical Applications of Olive Oil. Altern. Med. Rev. 2007, 12, 331–342.
- Saez Lancellotti, T. E.; Boarelli, P. V.; Romero, A. A.; Funes, A. K.; Cid-Barria, M.; Cabrillana, M. E.; Monclus, M. A.; Simon, L.; Vicenti, A. E.; Fornes, M. W. Semen Quality and Sperm Function Loss by Hypercholesterolemic Diet Was Recovered by Addition of Olive Oil to Diet in Rabbit. PLoS One. 2013, 8, e52386. 10.1371/journal.pone.0052386.
- Al-Bachir, M.; Sahloul, H. Fatty Acid Profile of Olive Oil Extracted from Irradiated and Non-Irradiated Olive Fruits. Int. J. Food Properties. 2016, 1–9. 10.1080/10942912.2016.1243557.
- Briante, R.; La Cara, F.; Tonziello, M. P.; Febbraio, F.; Nucci, R. Antioxidant Activity of the Main Bioactive Derivatives from Oleuropein Hydrolysis by Hyperthermophilic Beta-Glycosidase. J. Agric. Food Chem. 2001, 49, 3198–3203. 10.1021/jf001342r.
- Achat, S.; Rakotomanomana, N.; Madani, K.; Dangles, O. Antioxidant Activity of Olive Phenols and Other Dietary Phenols in Model Gastric Conditions: Scavenging of the Free Radical DPPH and Inhibition of the Haem-Induced Peroxidation of Linoleic Acid. Food Chem. 2016, 213, 135–142. 10.1016/j.foodchem.2016.06.076.
- Deiana, M.; Incani, A.; Rosa, A.; Corona, G.; Atzeri, A.; Loru, D.; Paola Melis, M.; Assunta Dessi, M. Protective Effect of Hydroxytyrosol and Its Metabolite Homovanillic Alcohol on H(2)O(2) Induced Lipid Peroxidation in Renal Tubular Epithelial Cells. Food Chem. Toxicol. 2008, 46, 2984–2990. 10.1016/j.fct.2008.05.037.
- Gallardo, E.; Palma-Valdes, R.; Sarria, B.; Gallardo, I.; De La Cruz, J. P.; Bravo, L.; Mateos, R.; Espartero, J. L. Synthesis and Antioxidant Activity of Alkyl Nitroderivatives of Hydroxytyrosol. Molecules. 2016, 21, 656. 10.3390/molecules21050656.
- Paradiso, V. M.; Di Mattia, C.; Giarnetti, M.; Chiarini, M.; Andrich, L.; Caponio, F. Antioxidant Behavior of Olive Phenolics in Oil-In-Water Emulsions. J. Agric. Food Chem. 2016, 64, 5877–5886. 10.1021/acs.jafc.6b01963.
- Vlachogianni, I. C.; Fragopoulou, E.; Kostakis, I. K.; Antonopoulou, S. In Vitro Assessment of Antioxidant Activity of Tyrosol, Resveratrol and Their Acetylated Derivatives. Food Chem. 2015, 177, 165–173. 10.1016/j.foodchem.2014.12.092.
- Hani, S. B.; Bayachou, M. Salvia Fruticosa Reduces Intrinsic Cellular and H2O2-induced DNA Oxidation in HEK 293 Cells; Assessment Using Flow Cytometry. Asian Pac. J. Trop Biomed. 2014, 4, 399–403. 10.12980/APJTB.4.2014C1270.
- Franco, M. N.; Galeano-Diaz, T.; Lopez, O.; Fernandez-Bolanos, J. G.; Sanchez, J.; De Miguel, C.; Gil, M. V.; Martin-Vertedor, D. Phenolic Compounds and Antioxidant Capacity of Virgin Olive Oil. Food Chem. 2014, 163, 289–298. 10.1016/j.foodchem.2014.04.091.
- An, F.; Cao, X.; Qu, H.; Wang, S. Attenuation of Oxidative Stress of Erythrocytes by the Plant-Derived Flavonoids Vitexin and Apigenin. Pharmazie. 2015, 70, 724–732.
- Li, R.; Wang, X.; Qin, T.; Qu, R.; Ma, S. Apigenin Ameliorates Chronic Mild Stress-Induced Depressive Behavior by Inhibiting Interleukin-1beta Production and NLRP3 Inflammasome Activation in the Rat Brain. Behav. Brain Res. 2016, 296, 318–325. 10.1016/j.bbr.2015.09.031.
- Ravi Kumar, S.; Narayan, B.; Sawada, Y.; Hosokawa, M.; Miyashita, K. Combined Effect of Astaxanthin and Squalene on Oxidative Stress in Vivo. Mol. Cell. Biochem. 2016, 417, 57–65. 10.1007/s11010-016-2713-2.
- Warleta, F.; Campos, M.; Allouche, Y.; Sanchez-Quesada, C.; Ruiz-Mora, J.; Beltran, G.; Gaforio, J. J. Squalene Protects against Oxidative DNA Damage in MCF10A Human Mammary Epithelial Cells but Not in MCF7 and MDA-MB-231 Human Breast Cancer Cells. Food Chem. Toxicol. 2010, 48, 1092–1100. 10.1016/j.fct.2010.01.031.
- Rosignoli, P.; Fuccelli, R.; Sepporta, M. V.; Fabiani, R. In Vitro Chemo-Preventive Activities of Hydroxytyrosol: The Main Phenolic Compound Present in Extra-Virgin Olive Oil. Food Funct. 2016, 7, 301–307. 10.1039/C5FO00932D.
- Massaro, M.; De Caterina, R. Vasculoprotective Effects of Oleic Acid: Epidemiological Background and Direct Vascular Antiatherogenic Properties. Nutr. Metab. Cardiovasc. Dis. 2002, 12, 42–51.
- Bulotta, S.; Celano, M.; Lepore, S. M.; Montalcini, T.; Pujia, A.; Russo, D. Beneficial Effects of the Olive Oil Phenolic Components Oleuropein and Hydroxytyrosol: Focus on Protection against Cardiovascular and Metabolic Diseases. J. Transl. Med. 2014, 12, 219. 10.1186/s12967-014-0219-9.
- Mateos, R.; Dominguez, M. M.; Espartero, J. L.; Cert, A. Antioxidant Effect of Phenolic Compounds, Alpha-Tocopherol, and Other Minor Components in Virgin Olive Oil. J. Agric. Food Chem. 2003, 51, 7170–7175. 10.1021/jf034415q.
- Owen, R. W.; Giacosa, A.; Hull, W. E.; Haubner, R.; Wurtele, G.; Spiegelhalder, B.; Bartsch, H. Olive-Oil Consumption and Health: The Possible Role of Antioxidants. Lancet Oncol. 2000, 1, 107–112. 10.1016/S1470-2045(00)00015-2.
- Bataineh, H. N.; Nusier, M. K. Effect of Cholesterol Diet on Reproductive Function in Male Albino Rats. Saudi Med. J. 2005, 26, 398–404.
- Mansour, S. W.; Sangi, S.; Harsha, S.; Khaleel, M. A.; Ibrahim, A. R. Sensibility of Male Rats Fertility against Olive Oil, Nigella Sativa Oil and Pomegranate Extract. Asian Pac. J. Trop Biomed. 2013, 3, 563–568. 10.1016/S2221-1691(13)60114-8.
- El-Kholy, T. A.; Al-Abbadi, H. A.; Qahwaji, D.; Al-Ghamdi, A. K.; Shelat, V. G.; Sobhy, H. M.; Abu Hilal, M. Ameliorating Effect of Olive Oil on Fertility of Male Rats Fed on Genetically Modified Soya Bean. Food Nutr. Res. 2015, 59, 27758. 10.3402/fnr.v59.27758.
- Oluwakemi, O.; Olufeyisipe, A. DNA Fragmentation and Oxidative Stress Compromise Sperm Motility and Survival in Late Pregnancy Exposure to Omega-9 Fatty Acid in Rats. Iran J. Basic Med. Sci. 2016, 19, 511–520.
- Zhang, W.; Zhang, X.; Bi, D.; Wang, X.; Cai, Y.; Dai, H.; Chen, S. Feeding with Supplemental Squalene Enhances the Productive Performance in Boars. Anim. Reprod. Sci. 2008, 104, 445–449. 10.1016/j.anireprosci.2007.08.003.
- Mohamadi, M.; Afzali, D.; Esmaeili-Mahani, S.; Mostafavi, A.; Torkzadeh-Mahani, M. Spectroscopic and Electrochemical Studies of the Interaction between Oleuropein, the Major Bio-Phenol in Olives, and Salmon Sperm DNA. Spectrochim Acta A Mol. Biomol. Spectrosc. 2015, 148, 260–265. 10.1016/j.saa.2015.03.123.
- Shi, X. R.; Liu, S. Y.; Chen, Y.; Li, F. L.; Xue, H. L.; Dang, Y. H.; Li, Z. L. [Apigenin Affects Semen Parameters in Male Mice]. Zhonghua Nan Ke Xue. 2010, 16, 778–782.
- Goldenberg, R. L.; White, R. The Effect of Vaginal Lubricants on Sperm Motility in Vitro. Fertil. Steril. 1975, 26, 872–873. 10.1016/S0015-0282(16)41350-6.
- Anderson, L.; Lewis, S. E.; McClure, N. The Effects of Coital Lubricants on Sperm Motility in Vitro. Hum. Reprod. 1998, 13, 3351–3356. 10.1093/humrep/13.12.3351.
- Oi-Kano, Y.; Kawada, T.; Watanabe, T.; Koyama, F.; Watanabe, K.; Senbongi, R.; Iwai, K. Oleuropein Supplementation Increases Urinary Noradrenaline and Testicular Testosterone Levels and Decreases Plasma Corticosterone Level in Rats Fed High-Protein Diet. J. Nutr. Biochem. 2013, 24, 887–893. 10.1016/j.jnutbio.2012.06.003.
- Derouiche, A.; Jafri, A.; Driouch, I.; El Khasmi, M.; Adlouni, A.; Benajiba, N.; Bamou, Y.; Saile, R.; Benouhoud, M. Effect of Argan and Olive Oil Consumption on the Hormonal Profile of Androgens among Healthy Adult Moroccan Men. Nat. Prod. Commun. 2013, 8, 51–53.
- Keskin, M. Z.; Budak, S.; Zeyrek, T.; Celik, O.; Mertoglu, O.; Yoldas, M.; Ilbey, Y. O. The Relationship between Serum Hormone Levels (Follicle-Stimulating Hormone, Luteinizing Hormone, Total Testosterone) and Semen Parameters. Arch. Ital Urol. Androl. 2015, 87, 194–197. 10.4081/aiua.2015.3.194.
- Sola, R.; La Ville, A. E.; Richard, J. L.; Motta, C.; Bargallo, M. T.; Girona, J.; Masana, L.; Jacotot, B. Oleic Acid Rich Diet Protects against the Oxidative Modification of High Density Lipoprotein. Free Radic. Biol. Med. 1997, 22, 1037–1045. 10.1016/S0891-5849(96)00490-X.
- Halliwell, B.;. The Role of Oxygen Radicals in Human Disease, with Particular Reference to the Vascular System. Haemostasis. 1993, 23(Suppl 1), 118–126.
- Miersch, S.; Espey, M. G.; Chaube, R.; Akarca, A.; Tweten, R.; Ananvoranich, S.; Mutus, B. Plasma Membrane Cholesterol Content Affects Nitric Oxide Diffusion Dynamics and Signaling. J. Biol. Chem. 2008, 283, 18513–18521. 10.1074/jbc.M800440200.
- Reaven, P.; Parthasarathy, S.; Grasse, B. J.; Miller, E.; Steinberg, D.; Witztum, J. L. Effects of Oleate-Rich and Linoleate-Rich Diets on the Susceptibility of Low Density Lipoprotein to Oxidative Modification in Mildly Hypercholesterolemic Subjects. J. Clin. Invest. 1993, 91, 668–676. 10.1172/JCI116247.
- Scaccini, C.; Nardini, M.; D’Aquino, M.; Gentili, V.; Di Felice, M.; Tomassi, G. Effect of Dietary Oils on Lipid Peroxidation and on Antioxidant Parameters of Rat Plasma and Lipoprotein Fractions. J. Lipid Res. 1992, 33, 627–633.
- Banihani, S.; Sharma, R.; Bayachou, M.; Sabanegh, E.; Agarwal, A. Human Sperm DNA Oxidation, Motility and Viability in the Presence of L-Carnitine during in Vitro Incubation and Centrifugation. Andrologia. 2012, 44(Suppl 1), 505–512. 10.1111/j.1439-0272.2011.01216.x.
- Kedechi, S.; Zribi, N.; Louati, N.; Menif, H.; Sellami, A.; Lassoued, S.; Ben Mansour, R.; Keskes, L.; Rebai, T.; Chakroun, N. Antioxidant Effect of Hydroxytyrosol on Human Sperm Quality during in Vitro Incubation. Andrologia. 2016, 49, 1-5.
- Mohamad Zakkirun, A.; Johari Mohd, A.; Mitra, A.; Puteri Shafinaz, A.-R.; Hashim, O. H. Anti-Proliferative, in Vitro Antioxidant and Cellular Antioxidant Activities of the Leaf Extracts from Polygonum Minus Huds: Effects of Solvent Polarity. Int. J. Food Properties. 2017.