Alterations in lipids and minerals in relation to larval trematode infections of Nerita polita marine snails

Hassan, A. H.; Alhazmi, N. S.; Filimban, A. AR.; Alsulami, M. N.

doi:10.2478/helm-2021-0039

Abstract

Marine snails provide an important source of vitamins, proteins, minerals, and essential fatty acids, and their mucus has a therapeutic significance. Parasitic infection of larval trematodes in these snails affects their nutritional value. The present study aimed to screen Nerita polita marine snails for the prevalence of cercarial infections and to evaluate the changes in lipids and some minerals in the infected as well as non-infected ones. Snails were collected randomly from February 2018 to January 2019 from the Red Sea Obhor bay, Jeddah city, Saudi Arabia. The amount of triglycerides, cholesterol, and phospholipids in the Digestive Gland Gonad Complex (DGG), hemolymph, and Snail Conditioned Water (SCW) of non-infected and infected Nerita polita snail was estimated using a spectrophotometer. Minerals content such as Ca, Zn, Pb, Na, Mn, Mg, K, Fe, Cu, and Cd, in the DGG and shell in the infected and non-infected snails were analyzed using an Inductively Coupled Plasma Optical Emission Spectrometer (ICP-OES). Two types of cercariae were detected, ocellate furcocercus cercaria (Trichobilharzia regent) and xiphidiocercaria (Litorina saxatilis VII). The study showed that there is a fl uctuation in the concentration of lipids and minerals between increase and decrease in DGG, hemolymph, shell, and SCW in infected snails. The nutritive value of the snails is affected with infection through the decrease of some lipids and minerals in infected snails. Further qualitative studies are needed.

References

AB LAH, R., SMITH, J., SAVINS, D., DOWELL, A. BUSHER, D., BENKENDROFF, K. (2017): Investigation of nutritional properties of three species of marine turban snails for human consumption. Food Sci Nutr, 5(1): 14–30. DOI: 10.1002/fsn3.360
Open DOI Search in Google Scholar Back to article
ADIKWU, M.U., ALOZIE, B.U. (2007): Application of snail mucin dispersed in detarium gum gel in wound healing. SRE, 2: 195–198. DOI: 10.5897/SRE.9000205
Open DOI Search in Google Scholar Back to article
ADIKWU, M.U., ENEBEKE, T.C. (2007): Evaluation of snail mucin dispersed in Brachystegia gum gel as a wound-healing agent. Anim. Res. Int, 4(2): 685–697. DOI: 10.4314/ari.v4i2.40818
Open DOI Search in Google Scholar Back to article
AL-SOLAMI, M., HASSAN, S., HASSAN, A. (2019): Molecular Method vs Traditional methods for Estimating the Prevalence of Larval Trematode Infections in Some Red Sea Snails. Int. J. Pharm. Res. Allied Sci., 8 (2): 1–13
Search in Google Scholar Back to article
ALVES, H., TUNHOLI-ALVES, V.M., TUNHOLI, V.M., GÔLO, P., BITTENCOURT, V.R.E.P., PINHEIRO, J. (2014): Changes in the lipid profile of Bradybaena similaris (Férussac, 1821) (Gastropoda, Xanthonychidae) during the development of Eurytrema coelomaticum (Giard and Billet, 1892) (Digenea, Dicrocoeliidae). Exp Parasitol, 144: 52–56. DOI: 10.1016/j.exppara.2014.06.010
Open DOI Search in Google Scholar Back to article
BAGNISKI, E., ZAK, B. (1960): Micro-determination of serum phosphate and phospholipids. Clin Chim Acta, 5(6): 834–838. DOI: 10.1016/0009-8981(60)90117-0
Open DOI Search in Google Scholar Back to article
BANDSTRA, S.R., FRIED, B., SHERMA, J. (2006): High-performance thin-layer chromatographic analysis of neutral lipids and phospholipids in Biomphalaria glabrata patently infected with Echinostoma caproni Parasitol Res, 99(4): 414–418. DOI: 10.1007/s00436007-0798-y
Open DOI Search in Google Scholar Back to article
BECKER, W. (1980): Metabolic interrelationship of parasitic trematodes and molluscs, especially Schistosoma mansoni in Biomphalaria glabrata Parasitol Res 63(2): 101–111. DOI: 10.1007/ bf00927526
Open DOI Search in Google Scholar Back to article
BUI, Q. H.D., FRIED, B., SHERMA, J. (2016): High-performance thin-layer chromatographic analysis of phospholipids in Biomphalaria glabrata snails infected with Schistosoma mansoni Trends Chromatogr,10: 7–12. DOI: 10.1007/s00436-006-0180-5
Open DOI Search in Google Scholar Back to article
CLINE, D.J., FRIED, B., SHERMA, S. (2000): High-performance thin-layer chromatographic analysis of neutral lipids and phospholipids in Cerithidia californica (Gastropoda) infected with three species of larval trematodes. Acta Chromatogr, 10: 183–189
Search in Google Scholar Back to article
EBEREMU, N. C. (2018): Impact of schistosoma haematobium infection and starvation on some neutral and polar lipids contect of Bulinus truncates FJS, 2(3): 224–232
Search in Google Scholar Back to article
ETIM, L., ALERUSHI, C., OBANDE, G.A. (2016): Antibacterial Properties of Snail Mucus on Bacteria Isolated from Patients with Wound Infection. Br Microbiol Res J, 11(2): 1–9. DOI: 10.9734/ BMRJ/2016/21731
Open DOI Search in Google Scholar Back to article
EVANS, D.W., IRWIN, S.W.B., FITZPATRICK, S. (2001): The effect of digenean (Platyhelminthes) infections on heavy metal concentrations in Littorina littorea J Mar Biol Assoc UK, 81: 349–350. DOI: 10.1017/S0025315401003873
Open DOI Search in Google Scholar Back to article
FRIED, B., REDY, A. (1999): Effects of snail-conditioned water from Biomphalaria glabrata on hatching of Echinostoma caproni miracidia. Parasitol Res, 85(2): 155–157. DOI: 10.1007/ s004360050526
Open DOI Search in Google Scholar Back to article
FRIED, B., LEWIS JR, P.D., BEERS, K. (1995): Thin-layer chromatographic and histochemical analyses of neutral lipids in the intramolluscan stages of Leucochloridium variae (Digenea, Leucochloridiidae) and the snail host, Succinea ovalis J Parasitol, 81(1): 112–114. DOI: 10.2307/3284019
Open DOI Search in Google Scholar Back to article
FRIED, B., SCHAFER, S., KIM, S. (1989): Effects of Echinostoma caproni infection on the lipid composition of Biomphalaria glabrata Int J Parasitol, 19(3): 353–354. DOI: 10.1016/0020-7519(89)90149-5 GIOKAS, S., PAFILIS, P., VALAKOS, E. (2005): Ecological and physiological adaptations of the land snail Albinaria caerulea (Pulmonata: Clausiliidae). J Molluscan Stud, 71(1): 15–23. DOI: 10.1093/ mollus/eyi001
Open DOI Search in Google Scholar Back to article
HASAN, A. (2008): Effects of digenean larval infection on the shells and soft parts of their intermediate host Lanistes carinatus J Egypt Soc Parasitol, 38 (3): 805–812
Search in Google Scholar Back to article
HASAN, A., AL-SOLAMI, M., HASAN, S. (2018a): Identification of some trematode cercariae collected from six marine snail species belonging to the genus Nerita J Egypt Soc Parasitol, 48(2): 251–258
Search in Google Scholar Back to article
HASAN, A., MOHARAM, S., AL-HELALI, H. (2018b): Role of parasitic helminthes in bioremediating some heavy metal accumulation in the tissues of Lethrinus mahsena Turk J Fish Aquat Sci, 18: 435–443. DOI: 10.4194/1303-2712-v18_3_09
Open DOI Search in Google Scholar Back to article
HELVICH, K. (1990): Official methods of analysis (No. 630.24 A88 1990). Association of official analytical chemists (AOAC), 7: 39–65. Retrieved from https://law.resource.org/pub/us/cfr/ibr/002/aoac.methods.1.1990.pdf
Search in Google Scholar Back to article
HUMICZEWSKA, M., RAJSKI, K. (2005): Lipids in the host-parasite system: digestive gland of Lymnaea truncatula infected with the developmental stages of Fasciola hepatica Acta Parasitol, 50(3): 235–239
Search in Google Scholar Back to article
HUNSBERGER, A., DEGRANDCHAMP, D., FRIED, B., SHERMA, J. (2014): Effects of high and low temperatures on the lipid content of the digestive gland-gonad complex of Biomphalaria glabrata as determined by high-performance thin layer chromatography. J Liq Chromatogr Relat Technol, 37(20): 2989–2999. DOI: 10.1080/10826076.2014.907106
Open DOI Search in Google Scholar Back to article
HUNSBERGER, A., FRIED, B., SHERMA, J. (2013): Effects of Echinostoma caproni miracidia dose on the neutral and polar lipids of Biomphalaria glabrata as determined by high-performance thin-layer chromatography. Acta Parasitol, 58(4): 615–618. DOI: 10.2478/ s11686-013-0180-4
Open DOI Search in Google Scholar Back to article
INOUYE, L.S., LOTUFO, G.R. (2006): Comparison of macro-gravimetric and micro-colorimetric lipid determination methods. Talanta, 70(3): 584–587. DOI: 10.1016/j.talanta.2006.01.024
Open DOI Search in Google Scholar Back to article
KANTAWONG, F., THAWEENAN, P., MUNGKALA, S., TAMANG, S., MANAPHAN, R., WANACHANTARARAK, P., CHUMNANPUEN, P. (2016): Mucus of Achatina fulica stimulates mineralization and inflammatory response in dental pulp cells. Turk J Biol, 40(2): 353–359. DOI: 10.3906/biy1505-29
Open DOI Search in Google Scholar Back to article
KAUFER, S.W., CHEJLAVA, M., FRIED, B., SHERMA, J. (2002): Effects of Euhaplorchis califorensis (Trematoda) infection on metallic ions in the host snail Cerithidea californica Parasitol Res, 88: 1080–1082. DOI: 10.1007/s00436-002-0718-0
Open DOI Search in Google Scholar Back to article
LUSTRINO, D., TUNHOLI-ALVES, V.M., TUNHOLI, V. M., MARASI, M. P., PINHEIRO, J. (2010): Lipids analysis in hemolymph of African giant Achatina fulica (Bowdich, 1822) exposed to different photoperiods. Braz J Biol, 70(1): 129–134. DOI: 10.1590/s151969842010000100018
Open DOI Search in Google Scholar Back to article
MARSIT, C.J., FRIED, B., SHERMA, J. (2000): Neutral lipids in cercariae, encysted metacercariae, and rediae of Echinostoma caproni J Helminthol, 74(4): 365–367. DOI: 10.1017/S0022149X00000548 MOMOSE, T., UEDA, Y., YAMAMOTO, K., MASUMURA, T., OHTA, K. (1963): Determination of Total Cholesterol in Blood Serum with Perchloric Acid-Phosphoric Acid-Ferric Chloride Reagent. Anal Chem, 35(11): 1751–1753. DOI: 10.1021/ac60204a062
Open DOI Search in Google Scholar Back to article
MOSTAFA, O.M.S. (2008): Effects of Fasciola gigantica experimental infection on some inorganic elements in the snail host. Lymnaea natalensis. Exp Parasitol, 118(4): 468–471. DOI: 10.1016/j.exppara.2007.10.009
Open DOI Search in Google Scholar Back to article
NARAYANAN, R., VENKATESWARARAO, P. (1980): Effect of xiphidiocercarial infection on oxidation of glycolytic and Krebs cycle intermediates in Lymnaea luteola (Mollusca). J Invertebr Pathol, 36(1): 21–24. DOI: 10.1016/0022-2011(80)90129-9
Open DOI Search in Google Scholar Back to article
ONG, J. H. L., CHEJLAVA, M., FRIED, B., KOEHNLEIN, K. M., BOSAVAGE, G. L., SHERMA, J. (2004): Effects of Schistosoma mansoni infection on inorganic elements in the snail Biomphalaria glabrata J Helminthol, 78(4): 343–346. DOI: 10.1079/JOH2004244
Open DOI Search in Google Scholar Back to article
PARK, J., JEONG, H.J., YOON, E.Y., MOON, S.J., PARK, J., JEONG, H.J., MOON, S.J. (2016): Easy and rapid quantification of lipid contents of marine dinoflagellates using the sulpho-phospho-vanillin method. Algae, 31(4): 391–401. DOI: 10.4490/algae.2016.31.12.7
Open DOI Search in Google Scholar Back to article
PINHEIRO, J., JÚNIOR, A.M., LANFREDI, R.M. (2009): Physiological changes in Lymnaea columella (Say, 1817) (Mollusca, Gastropoda) in response to Echinostoma paraensei Lie and Basch, 1967 (Trematoda: Echinostomatidae) infection. Parasitol Res, 106(1): 55–59. DOI: 10.1007/s00436-009-1630-7
Open DOI Search in Google Scholar Back to article
PINHEIRO, J., JUNIOR, A.M., ATTIAS, M., LANFREDI, R. M. (2004): Morphology of the rediae of Echinostoma paraensei (Trematoda: Echinostomatidae) from its intermediate host Lymnaea columella (Mollusca, Gastropoda). Parasitol Res, 93(3): 171–177. DOI: 10.1007/s00436-004-1110-z
Open DOI Search in Google Scholar Back to article
PINHEIRO, J., MALDONADO, A., ATTIAS, M., LANFREDI, R. M. (2005): Ultrastructure of the miracidium of Echinostoma paraensei Lie and Basch, 1967 (Trematoda, Echinostomatidae). Parasitol Res, 97(5): 367–372. DOI: 10.1007/s00436-005-1458-8
Open DOI Search in Google Scholar Back to article
SILVA, L.D., AMARAL, V.C.S., VINAUD, M.C., CASTRO, A.M., REZENDE, H.H. A., SANTOS, D.B., BEZERRA, J.C.B. (2017): Changes in energetic metabolism of Biomphalaria glabrata (Mollusca, Planorbidae) in response to exogenous calcium. Braz. J. Biol., 77(2): 304–311. DOI: 10.1590/1519-6984.13315
Open DOI Search in Google Scholar Back to article
SMITH, A.M., ROBINSON, T.M., SALT, M.D., HAMILTON, K.S., SILVIA, B.E., BLASIAK, R. (2009): Robust cross-links in molluscan adhesive gels: testing for contributions from hydrophobic and electrostatic interactions. Comp Biochem Physiol B Biochem Mol Biol, 152(2): 110–117. DOI: 10.1016/j.cbpb.2008.10.004
Open DOI Search in Google Scholar Back to article
STOREY, K.B. (2002): Life in the slow lane: molecular mechanisms of estivation. Comp Biochem Physiol A Mol Integr Physiol, 133(3): 733–754. DOI: 10.1016/s1095-6433(02)00206-4
Open DOI Search in Google Scholar Back to article
STUART, J.A., GILLIS, T.E., BALLANTYNE, J.S. (1998): Compositional correlates of metabolic depression in the mitochondrial membranes of estivating snails. Am J Physiol, 275(6): 1977–1982. DOI: 10.1152/ajpregu.1998.275.6.R1977
Open DOI Search in Google Scholar Back to article
THOMAS, S. (2013): Medicinal use of terrestrial molluscs (slugs and snails) with particular reference to their role in the treatment of wounds and other skin lesions. Retrieved from http://www.worldwidewounds.com/2013/July/Thomas/slug-steve-thomas.html
Search in Google Scholar Back to article
THOMPSON, S. N., MEJIA-SCALES, V. (1993): Effects of restricted food intake on hemolymph glucose concentration and digestive gland-gonad lipid level in the schistosome vector Biomphalaria glabrata (Say) (Gastropoda: Planorbidae). Veliger, 36(4); 425–427
Search in Google Scholar Back to article
THOMPSON, S.N. (1987): Effect of Schistosoma mansoni on the gross lipid composition of its vector Biomphalaria glabrata Comp Biochem Physiol B, 87(2): 357–360. DOI: 10.1016/03050491(87)90152-0
Open DOI Search in Google Scholar Back to article
THOMSON C.D., ROBINSON M.F. (1980): Selenium in human health and disease with emphasis on those aspects peculiar to New Zealand. Am J Clin Nutr, 33(2, 1): 303–323. DOI: 10.1093/ ajcn/33.2.303
Open DOI Search in Google Scholar Back to article
TOLEDO, R., MUNOZ-ANTOLI, C., ESTEBAN, J.G. (2014): Intestinal trematode infections. In: TOLEDO R., FRIED B. (Eds) Digenetic Trematodes. Advances in Experimental Medicine and Biology, vol 766. Springer, New York, NY. DOI: 10.1007/978-1-4939-0915-5_7
Open DOI Search in Google Scholar Back to article
TRIPATHI, P.K., SINGH, A. (2002): Toxic effects of dimethoate and carbaryl pesticides on carbohydrate metabolism of freshwater snail Lymnaea acuminata Bull Environ Contam Toxicol, 68(4): 606–611. DOI: 10.1007/s001280297
Open DOI Search in Google Scholar Back to article
TUNHOLI, V.M., LUSTRINO, D., TUNHOLI-ALVES, V.M., MELLO-SILVA, C.C., MALDONADO, A., PINHEIRO, J., RODRIGUES, M.D.L.D.A. (2011): Biochemical profile of Biomphalaria glabrata (Mollusca: Gastropoda) after infection by Echinostoma paraensei (Trematoda: Echinostomatidae). Parasitol Res, 109(3): 885–891. DOI: 10.1007/s00436-011-2330-7
Open DOI Search in Google Scholar Back to article
TUNHOLI-ALVES, V.M., TUNHOLI, V.M., GARCIA, J.S., COSTA-NETO, S.F., MALDONADO, A., SANTOS, M. A. J., PINHEIRO, J. (2014): Changes in the calcium metabolism of Biomphalaria glabrata experimentally infected with Angiostrongylus cantonensis J Helminthol, 88(2): 160–165. DOI: 10.1017/S0022149X12000867
Open DOI Search in Google Scholar Back to article
TUNHOLI-ALVES, V.M., TUNHOLI, V.M., GÔLO, P., LIMA, M., GARCIA, J., JÚNIOR, A.M., PINHEIRO, J. (2013): Effects of infection by larvae of Angiostrongylus cantonensis (Nematoda, Metastrongylidae) on the lipid metabolism of the experimental intermediate host Biomphalaria glabrata (Mollusca: Gastropoda). Parasitol Res, 112(5): 2111–2116. DOI: 10.1007/s00436-013-3308-4
Open DOI Search in Google Scholar Back to article
TUNHOLI-ALVES, V.M., TUNHOLI, V.M., GÔLO, P., LUSTRINO, D., MALDONADO JR, A., BITTENCOURT, V. R. E. P., PINHEIRO, J. (2011): Lipid levels in Biomphalaria glabrata infected with different doses of Echinostoma paraensei miracidia. Exp Parasitol, 128(3): 212–216. DOI: 10.1016/j.exppara.2011.03.009
Open DOI Search in Google Scholar Back to article
TUNHOLI-ALVES, V.M., TUNHOLI, V.M., PINHEIRO, J., THIENGO, S.C. (2012): Effects of infection by larvae of Angiostrongylus cantonensis (Nematoda, Metastrongylidae) on the metabolism of the experimental intermediate host Biomphalaria glabrata Exp Parasitol, 131(2): 143–147. DOI: 10.1016/j.exppara.2012.03.003
Open DOI Search in Google Scholar Back to article
TURKSTANI. A., HASSAN, A., RABAH, S. (2021): Effect of Larval Trematode Infection on the Nutritional Value of Nerita orbignyana Marine Snails. Int. J. Pharm. Phytopharm. Res., 11(2): In press. DOI: 10.51847/D2CHtkWEbS
Open DOI Search in Google Scholar Back to article
ZBIKOWSKA, E. (2003): The effect of digenea larvae on calcium content in the shells of Lymnaea stagnalis (L.) individuals. J Parasitol, 89(1): 76–79. DOI: 10.1645/0022-3395(2003)089[0076:TEODLO]2.0.CO;2
Open DOI Search in Google Scholar Back to article

Alterations in lipids and minerals in relation to larval trematode infections of Nerita polita marine snails

Abstract

Paradigm

My account