Effect of Karas (Aquilaria malaccensis) on Male Reproductive Organs and Sperm Quality in Adult Sprague Dawley Rats

Main Article Content

Norahidah Zaidi
Mohd Nizam Haron
Connie Fay Komilus
Fathurrahman Lananan
Ha Hou Chew
Nadzifah Yaakub
Asmad Kari

Abstract

Reproductive health and male fertility are closely related to dietary practices. In recent years, Malaysia has shown a lot of interest in using herbal plants as dietary supplements or in the treatment of numerous diseases. Aquilaria malaccensis, commonly known as karas or gaharu, has recently gained attention for its potential to cure many diseases due to its pharmacological properties. However, studies on its effect on male fertility and reproductive organs are very scarce. This study was conducted to determine the effect of A. malaccensis on male reproductive organs’ weight (testis, epididymis, prostate gland and seminal vesicle) and sperm quality (sperm count, sperm morphology and sperm motility) in adult Sprague Dawley rats. Twenty-four male Sprague Dawley rats were allocated into four treatment groups; Control (C: 1 mL of distilled water, n = 6), Treatment 1 (T1: 1 g A. malaccensis/kg body weight, n = 6), Treatment 2 (T2: 2 g A. malaccensis/kg body weight, n = 6) and Treatment 3 (T3: 3 g A. malaccensis/kg body weight, n = 6), respectively. Distilled water and A. malaccensis were administered by oral gavage once daily for 28 days. The rats were euthanised on Day 29 for assessment of reproductive organs’ weight and sperm quality. Result shows that weight of testis, epididymis, prostate gland, seminal vesicle and sperm motility did not differ (p > 0.05) among control and treated groups. A significant increase (p < 0.05) of sperm number (1.36 × 10??) and a decrease (p < 0.05) in percentage of the abnormal sperm (8.17%) were observed in T1 group when compared to Control group. Incremental dosage of A. malaccensis seemed to decrease number of sperm (T3: 0.78 × 10?? < T1: 1.36 × 10?? with p < 0.05) and increase percentage of abnormal sperm (T3: 18.83% > T2: 12.17% > T1: 8.17% with p < 0.05). In conclusion, the administration of either 1, 2 or 3 grams of A. malaccensis did not alter the reproductive organs’ weight and sperm motility. However, the higher concentration of A. malaccensis consumed by the rats seemed to have detrimental effects on the number and morphology of sperm.

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Effect of Karas (Aquilaria malaccensis) on Male Reproductive Organs and Sperm Quality in Adult Sprague Dawley Rats. (2023). Tropical Life Sciences Research, 34(1), 241–259. https://doi.org/10.21315/tlsr2023.34.1.13
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References

Adam A Z, Tajuddin S N, Sudmoon R, Chaveerach A, Abdullah U H, Mahat M N and Mohamed R. (2018). Chemical constituents and toxicity effects of leaves from several agarwood tree species (Aquilaria). Journal of Tropical Forest Science 30(3): 342–353. https://doi.org/10.26525/jtfs2018.30.3.342353

Adhikari S R, Pokhrel K and Baral S D. (2021). Economic value of agarwood and its prospects of cultivation. International Journal of Applied Sciences and Biotechnology 9(1): 23–31. https://doi.org/10.3126/ijasbt.v9i1.35984

Afzan A, Kasim N, Ismail N H, Azmi N, Ali A M, Mat N and Wolfender J L. (2019). Differentiation of Ficus deltoidea varieties and chemical marker determination by UHPLC-TOFMS metabolomics for establishing quality control criteria of this popular Malaysian medicinal herb. Metabolomics 15(3): 1–11. https://doi.org/10.1007/s11306-019-1489-2

Agarwal A, Gupta S and Sikka S. (2006). The role of free radicals and antioxidants in reproduction. Current Opinion in Obstetrics and Gynecology 18(3): 325–332. https://doi.org/10.1097/01.gco.0000193003.58158.4e

Agarwal A, Leisegang K and Sengupta P. (2020). Oxidative stress in pathologies of male reproductive disorders. In Pathology. Academic Press, 15–27. https://doi.org/10.1016/B978-0-12-815972-9.00002-0

Ahmad Z Y. (2016). Growth and management of Aquilaria malaccensis for agarwood a new domestication perspective. International Journal of Agriculture, Forestry and Plantation 3: 55–60.

Alipieva K, Petreska J, Gil-Izquierdo A, Stefova M, Evstatieva L and Bankova V. (2010). Influence of the extraction method on the yield of flavonoids and phenolics from Sideritis spp. (Pirin Mountain tea). Natural Product Communications 5(1): 51–54. https://doi.org/10.1177/1934578X1000500113

Azah M A, Chang Y S, Mailina J, Saidatul H S, Nor H H and Nik Y Y. (2008). Comparison of chemical profiles of selected gaharu oils from Peninsular Malaysia. Malaysian Journal of Analytical Sciences 12(2): 338–340.

Azahari N, Khattak M M A K, Taher M and Ichwan S J A. (2015). Herbal extracts exhibit anti- diabetic activities in 3T3-L1 adipocytes model. Progress in Nutrition 17: 301–310.

Batubara R, Wirjosentono B, Siregar A H, Harahap U and Tamrin T. (2021). Bioactive compounds of ethanol extract from agarwood leaves (Aquilaria malaccensis) and antimicrobial activity against bacteria and fungi growing on the skin. Biodiversitas Journal of Biological Diversity 22(5): 2884–2890. https://doi.org/10.13057/biodiv/d220553

Bode A M and Dong Z. (2015). Toxic phytochemicals and their potential risks for human cancer. Cancer Prevention Research 8(1): 1–8. https://doi.org/10.1158/1940-6207.CAPR-14-0160

Cariati F, D’Uonno N, Borrillo F, Iervolino S, Galdiero G and Tomaiuolo R. (2019). Bisphenol a: An emerging threat to male fertility. Reproductive Biology and Endocrinology 17(1): 1–8. https://doi.org/10.1186/s12958-018-0447-6

Cock I E. (2015). The safe usage of herbal medicines: Counter-indications, cross-reactivity and toxicity. Pharmacognosy Communications 5(1): 2–38. https://doi.org/10.5530/pc.2015.1.2

Creasy D M and Chapin R E. (2013). Male reproductive system. In Haschek W M, Rousseaux C G and Wallig M A (eds.), Haschek and Rousseaux’s handbook of toxicologic pathology, volume 3. Academic Press, 2493–2598. https://doi.org/10.1016/B978-0-12-415759-0.00059-5

Derouiche S, Zeghib K, Gherbi S and Khelef Y. (2019). Protective effects of Aristolochia longa and Aquilaria malaccensis against lead-induced oxidative stress in rat cerebrum. Asian Journal of Research in Pharmaceutical Sciences 9(1): 57–63. https://doi.org/10.5958/2231-5659.2019.00010.9

Desa A P, Lee S Y, Mustapa M Z, Mohamed R and Emang D. (2021). Trends in the agarwood industry of Peninsular Malaysia. The Malaysian Forester 84: 152–168.

Desjardins C. (1978). Endocrine regulation of reproductive development and function in the male. Journal of Animal Science 47(2): 56–79.

Durairajanayagam D. (2018). Lifestyle causes of male infertility. Arab Journal of Urology 16(1): 10–20. https://doi.org/10.1016/j.aju.2017.12.004

Dutta S and Sengupta P. (2018). Medicinal herbs in the management of male infertility. Journal of Pregnancy and Reproduction 2(1): 1–6. https://doi.org/10.15761/JPR.1000128

Dym M, Raj H G, Lin Y C, Chemes H E, Kotite N J, Nayfeh S N and French F S. (1979). Is FSH required for maintenance of spermatogenesis in adult rats? Journal of Reproduction and Fertility. Supplement (26): 175–181.

Eissa M A, Hashim Y Z H, El-Kersh D M, Abd-Azziz S S, Salleh H M, Isa M L M and Abd-Warif N M. (2020). Metabolite profiling of Aquilaria malaccensis leaf extract using liquid Chromatography-Q-TOF-Mass spectrometry and investigation of its potential antilipoxygenase activity in-vitro. Processes 8(2): 202. https://doi.org/10.3390/pr8020202

Elangovan N, Chiou T J, Tzeng W F and Chu S T. (2006). Cyclophosphamide treatment causes impairment of sperm and its fertilising ability in mice. Toxicology 222(1–2): 60–70. https://doi.org/10.1016/j.tox.2006.01.027

Forestry Department of Peninsular Malaysia. (2012). Karas planting guidelines. Malaysia: Forestry Department of Peninsular Malaysia.

Gharagozloo P and Aitken R J. (2011). The role of sperm oxidative stress in male infertility and the significance of oral antioxidant therapy. Human Reproduction 26(7): 1628–1640. https://doi.org/10.1093/humrep/der132

Habibi P, Daniell H, Soccol C R and Grossidesa M F. (2019). The potential of plant systems to break the HIV?TB link. Plant Biotechnology Journal 17(10): 1868–1891. https://doi.org/10.1111/pbi.13110

Haron M N and Mohamed M. (2016). Effect of honey on the reproductive system of male rat offspring exposed to prenatal restraint stress. Andrologia 48(5): 525–531. https://doi.org/10.1111/and.12473

Haron M N, Souza U J, Jaafar H, Zakaria, R and Singh H J. (2010). Exogenous leptin administration decreases sperm count and increases the fraction of abnormal sperm in adult rats. Fertility and Sterility 93(1): 322–324. https://doi.org/10.1016/j.fertnstert.2009.07.995

Hashim Y Z H Y, Kerr P G, Abbas P and Salleh H M. (2016). Aquilaria spp. (agarwood) as source of health beneficial compounds: A review of traditional use, phytochemistry and pharmacology. Journal of Ethnopharmacology 189: 331–360. https://doi.org/10.1016/j.jep.2016.06.055

Hegde K, Jazeela F, Poojary V and Satish S. (2018). Anti-cancer potentials of the plant Aquilaria malaccensis leaves. Indian Journal of Pharmacy and Pharmacology 5(3): 135–140. https://doi.org/10.18231/2393-9087.2018.0029

Hendra H, Moeljopawiro S and Nuringtyas T R. (2016). Antioxidant and antibacterial activities of agarwood (Aquilaria malaccensis Lamk.) leaves. AIP Conference Proceedings 1755(1): 140004. https://doi.org/10.1063/1.4958565

Ilacqua A, Izzo G, Emerenziani G P, Baldari C and Aversa A. (2018). Lifestyle and fertility: The influence of stress and quality of life on male fertility. Reproductive Biology and Endocrinology 16(1): 1–11. https://doi.org/10.1186/s12958-018-0436-9

Indrisari M, Burhan A, Khairi N, Syahruni R, Samudra A G, Ismail A, Dayanti A and Wahyuni S. (2021). In vitro embryotoxicity assay of mulberry (Morus alba L.) and agarwood (Aquilaria malaccensis L.) leaves extracts in zebrafish (Danio rerio). Plant Cell Biotechnology and Molecular Biology 22(71–72): 683–690.

Ismail F, Wahab A Y A, Isac M L M, Muhammad H, Arif R, Ismail S R and Razak R N H A. (2019). The effects of Aquilaria malaccensis leaves aqueous extract on sperm of Sprague Dawley rats towards early embryogenesis. International Medical Journal Malaysia 18(2): 59–68. https://doi.org/10.31436/imjm.v18i2.96

Jegasothy R, Sengupta P, Dutta S and Jeganathan R. (2021). Climate change and declining fertility rate in Malaysia: The possible connexions. Journal of Basic and Clinical Physiology and Pharmacology 32(5): 911–924. https://doi.org/10.1515/jbcpp-2020-0236

Jimoh O A, Oyeyemi W A, Okin-Aminu, H O and Oyeyemi B F. (2021). Reproductive characteristics, semen quality, seminal oxidative status, steroid hormones, sperm production efficiency of rabbits fed herbal supplements. Theriogenology 168: 41–49. https://doi.org/10.1016/j.theriogenology.2021.03.020

Kakino M, Tazawa S, Maruyama H, Tsuruma K, Araki Y, Shimazawa M and Hara H. (2010). Laxative effects of agarwood on low-fiber diet-induced constipation in rats. BMC Complementary and Alternative Medicine 10(1): 1–8. https://doi.org/10.1186/1472-6882-10-68

Kamonwannasit S, Nantapong N, Kumkrai P, Luecha P, Kupittayanant S and Chudapongse N. (2013). Antibacterial activity of Aquilaria crassna leaf extract against Staphylococcus epidermidis by disruption of cell wall. Annals of Clinical Microbiology and Anti-microbial 12(1): 1–7. https://doi.org/10.1186/1476-0711-12-20

Khaki A, Fathiazad F, Nouri M, Afshin-Khaki A, Ozanci C C, Ghafari-Novin M and Hamadeh M. (2009). The effects of ginger on spermatogenesis and sperm parameters of rat. International Journal of Reproductive BioMedicine 7(1): 7–12.

Kharnaior S and Thomas S C. (2021). A review of Aquilaria malaccensis propagation and production of the secondary metabolite from callus. Journal of Natural Resources 4(4): 85–94. https://doi.org/10.33002/nr2581.6853.040407

Liu P, Zhang X, Yang Y, Sui C, Xu Y and Wei J. (2019). Interxylary phloem and xylem rays are the structural foundation of agarwood resin formation in the stems of Aquilaria sinensis. Trees 33(2): 533-542. https://doi.org/10.1007/s00468-018-1799-4

Makler A. (1980). The improved ten-micrometre chamber for rapid sperm count and motility evaluation. Fertility and Sterility 33(3): 337–338. https://doi.org/10.1016/S0015-0282(16)44606-6

Mann U, Shiff B and Patel P. (2020). Reasons for worldwide decline in male fertility. Current Opinion in Urology 30(3): 296–301. https://doi.org/10.1097/MOU.0000000000000745

Modaresi M, Mesripour M, Asadi M M and Hamedanian M. (2008). The effect of saffron extract on testis tissue. Iranian Journal of Medicinal and Aromatic Plants 24(2): 237–243.

Mohajeri D, Mesgari A M, Delazar A, Doustar Y, Mousavi G and Amouoghli T B. (2009). Histopathological study of subacute toxicity of Crocus sativus L. (Saffron) stigma total extract on liver and kidney tissues in the rat. Pharmaceutical Sciences 15(2): 115–124.

Mohamad T A S T, Islahudin F, Jasamai M and Jamal J A. (2019). Preference, perception and predictors of herbal medicine use among Malay women in Malaysia. Patient Preference and Adherence 13: 1829–1837. https://doi.org/10.2147/PPA.S227780

Mohamed M, Sulaiman S A, Jaafar H and Sirajudeen K N S. (2012). Effect of different doses of Malaysian honey on reproductive parameters in adult male rats. Andrologia 44: 182–186. https://doi.org/10.1111/j.1439-0272.2010.01159.x

Mohammadi F, Nikzad H, Taherian A, Amini M J and Salehi M. (2013). Effects of herbal medicine on male infertility. Anatomical Sciences Journal 10(4): 3–16.

Mohanty S K and Singh R. (2017). Overview of the male reproductive system. In Singh R and Singh K, eds., Male infertility: Understanding, causes and treatment. Singapore: Springer, 3–12. https://doi.org/10.1007/978-981-10-4017-7_1

Mokhtar A M A, Zain H H M and Ta M M. (2021). Overview of medicinal properties and toxicities of agarwood species. Educatum Journal of Science, Mathematics and Technology 8(2): 1–16.

Musa N H C, Zain H H M and Ibrahim H. (2019). Aphrodisiac properties of Aquilaria malaccensis leaves aqueous extract in ICR mice. Marmara Pharmaceutical Journal 23(1): 130–140. https://doi.org/10.12991/jrp.2018.117

Narayana K D, Souza U J and Rao K S. (2002). Effect of ribavirin on epididymal sperm count in rat. Indian Journal of Physiology and Pharmacology 46(1): 97–101.

Norraidah R and Mahanem M N. (2015). Enhancement of fertility and libido in male Sprague Dawley rats following the administration of aqueous extract of Lunasia amara. Malaysian Applied Biology 44(1): 125–131.

Nusier M K, Bataineh H N and Daradkah H M. (2007). Adverse effects of rosemary (Rosmarinus officinalis L.) on reproductive function in adult male rats. Experimental Biology and Medicine 232(6): 809–813.

Nik W N N A, Nor A M O, Noorhuda A I and Saiful N T. (2014). In vitro antioxidant activity and phytochemical screening of Aquilaria malaccensis leaf extracts. Journal of Chemical and Pharmaceutical Research 6(12): 688–693.

OECD (2008). Test No. 407: Repeated dose 28-day oral toxicity study in rodents, OECD guidelines for the testing of chemicals, Section 4. Paris: OECD Publishing. https://doi.org/10.1787/20745788

Pauzi N A M, Cheema M S, Ismail A, Ghazali A R and Abdullah R. (2021). Safety assessment of natural products in Malaysia: current practices, challenges, and new strategies. Reviews on Environmental Health 37(2): 169–179. https://doi.org/10.1515/reveh-2021-0072

Priya G, Saravanan K and Renuka C. (2012). Medicinal plants with potential antifertility activity: A review of sixteen years of herbal medicine research (1994–2010). International Journal of PharmTech Research 4(1): 481–494.

Ramli A N M, Yusof S, Bhuyar P, Aminan A W, Tajuddin S N and Hamid H A. (2022). Production of volatile compounds by a variety of fungi in artificially inoculated and naturally infected Aquilaria malaccensis. Current Microbiology 79(5): 1–14. https://doi.org/10.1007/s00284-022-02840-6

Rasekh A, Jashni H K, Rahmanian K and Jahromi A S. (2015). Effect of palm pollen on sperm parameters of infertile man. Pakistan Journal of Biological Sciences 18(4): 196–199. https://doi.org/10.3923/pjbs.2015.196.199

Rashid Z M, Nasir N N M, Ahmad W N W and Mahmod N H. (2020). ?-glucosidase inhibition, DPPH scavenging and chemical analysis of polysaccharide extracts of Aquilaria sp. leaves. Journal of Agrobiotechnology 11(2): 59–69. https://doi.org/10.37231/jab.2020.11.2.225

Razak R N H A, Ismail F, Isa M L M, Wahab A Y A, Muhammad H, Ramli R and Ismail R A S R. (2019a). Ameliorative effects of Aquilaria malaccensis leaves aqueous extract on reproductive toxicity induced by cyclophosphamide in male rats. The Malaysian Journal of Medical Sciences 26(1): 44–57. https://doi.org/10.21315/mjms2019.26.1.4

Razak R N H A, Rahman S A, Hamdan A H, Ramli R, Isa M L M, Muhammad H and Nik N F. (2019b). Evaluation of acute and sub-acute oral toxicity of the aqueous extract of Aquilaria malaccensis leaves in Sprague Dawley rats. Journal of Molecular Biology and Biotechnology 27(1): 20–32. https://doi.org/10.35118/apjmbb.2019.027.1.03

Roy A, Jauhari N and Bharadvaja N. (2018). Medicinal plants as a potential source of chemopreventive agents. In Akhtar M S and Swamy M K, eds., Anticancer plants: Natural products and biotechnological implements, 2nd edition. Singapore: Springer Nature, 109–139. https://doi.org/10.1007/978-981-10-8064-7_6

Rozihawati Z, Wan M A W A, Sheriza M R, Hazandy A H, Mohd F A and Zaiton S. (2022). Formulation of alternative media for fungal growth and its application as agarwood- inducing agent in Aquilaria trees. Journal of Tropical Forest Science 34(1): 127–132. https://doi.org/10.26525/jtfs2022.34.1.127

Ruyani A and Sundaryono A. (2008). Pengembangan potensi kulit batang gaharu (Aquilaria malaccensis) sebagai perangsang seks (aphrodisiac) di Provinsi Bengkulu. In UNIB School Repository [online]. Available at http://repository.unib.ac.id/id/eprint/297 (accessed 10 August 2022).

Salleh N H, Zulkipli I N, Mohd Y H, Ja’afar F, Ahmad N, Wan A W A N and Ahmad S R. (2021). Systematic review of medicinal plants used for treatment of diabetes in human clinical trials: An ASEAN perspective. Evidence-Based Complementary and Alternative Medicine 2021: Article ID 5570939. https://doi.org/10.1155/2021/5570939

Samsulrizal N, Awang Z, Najib M L H M, Idzham M and Zarin A. (2011). Effect of Ficus deltoidea leaves extracts on sperm quality, LDH-C 4 activity and testosterone level in alloxan-induced male diabetic rats. Paper presented at Institute of Electrical and Electronics Engineers (IEEE) Colloquium on Humanities, Science and Engineering Research, Penang, Malaysia, 5–6 December. https://doi.org/10.1109/CHUSER.2011.6163864

Santos-Filho S D, Fonseca A D S D and Bernardo-Filho M. (2007). The male reproductive system and the effect of an extract of a medicinal plant (Hypericum perforatum) on the labeling process of blood constituents with technetium-99m. Brazilian Archives of Biology and Technology 50: 97–104. https://doi.org/10.1590/S1516-89132007000600011

Sekar M, Zulhilmi M, Hamdi A Y, Nabila N, Zahida Z and Shafiq M. (2014). Ten commonly available medicinal plants in Malaysia used for the treatment of diabetes: A review. Asian Journal of Pharmaceutical and Clinical Research 7(1): 1–5.

Semet M, Paci M, Saias?Magnan J, Metzler?Guillemain C, Boissier R, Lejeune H and Perrin J. (2017). The impact of drugs on male fertility: A review. Andrology 5(4): 640–663. https://doi.org/10.1111/andr.12366

Shrestha S, Jha C, Das B L and Yadav P. (2018). Effects of monosodium glutamate on liver tissue of Wistar albino rats - A histological and biochemical study. International Journal of Therapeutic Application 8(10): 68–73.

Uzbek U H and Shahidan W N. (2019). Tasty herb that heals: A review of Cosmos caudatus (Ulam raja) and its potential uses in dentistry. World Journal of Dentistry 10(4): 321–324. https://doi.org/10.5005/jp-journals-10015-1651

Van W A S and Prinsloo G. (2020). Health, safety and quality concerns of plant-based traditional medicines and herbal remedies. South African Journal of Botany 133: 54–62. https://doi.org/10.1016/j.sajb.2020.06.031

Walczak J R, Marchlewska K, Oszukowska E, Filipiak E, Bergier L and Slowikowska H J. (2013). Semen analysis standardization: Is there any problem in Polish laboratories? Asian Journal of Andrology 15(5): 616–621. https://doi.org/10.1038/aja.2013.48

Wan H W F F, Devita V D, Suriani I and Rosliza A M. (2017). The use of traditional Malay massage and traditional Malay herbs in Malaysia: A review. International Journal of Public Health and Clinical Sciences 4(5): 24–37.

Wang S, Wang C, Yu Z, Wu C, Peng D, Liu X, Liu Y, Yang Y, Guo P and Wei J. (2018). Agarwood essential oil ameliorates restrain stress-induced anxiety and depression by inhibiting HPA axis hyperactivity. International Journal of Molecular Sciences 19(11): 3468. https://doi.org/10.3390/ijms19113468

Woldemeskel M. (2017). Toxicologic pathology of the reproductive system. In Gupta R C, ed., Reproductive and developmental toxicology, 2nd edition. Cambridge, MA: Academic Press, 1209–1241. https://doi.org/10.1016/B978-0-12-804239-7.00064-0

Zakaria A A, Noor M H M, Ahmad H, Hassim H A, Mazlan M and Latip M Q A. (2021). A review on therapeutic effects of Labisia pumila on female reproductive diseases. BioMed Research International 2021. https://doi.org/10.1155/2021/9928199

Zakaria F H and Haron M N. (2020). Supplementation of bee bread decreases the abnormal sperm without affecting the sperm count of Sprague Dawley rats. Journal of Innovative Scientific Information & Services Network 17(1): 199–204.

Zulkifle N L, Sabri N A, Omar N A M, Shaari M R and Tajuddin S N. (2018). Acute and sub- chronic toxicity study of Aquilaria malaccensis leaves extract in Sprague Dawley rats. Chemistry of Advanced Materials 3(1): 8–15.