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In vivo anthelmintic effect of Artemisia annua L. on oxyurid nematodes of laboratory mice

Year 2024, Volume: 35 Issue: 1, 34 - 43, 04.07.2024
https://doi.org/10.35864/evmd.1374233

Abstract

Oxyurids are common intestinal parasites of mammals, and they are the cause of recurrent helminthic infections, especially in children Hence natural herbal compounds are necessary for a repeatable cure. This study aimed to investigate the antinematodal effect of Artemisia annua L. n-hexane extract on oxyurids in vivo. In this study, A. annua L. n-hexane extract was applied to mice naturally infected with Syphacia obvelata and Aspiculuris tetraptera species orally at 300, 600, and 1200 mg/kg doses for seven days and the change occurring in the number of oxyurid eggs was investigated by the fecal flotation method. The nematodes in the necropsy were compared on the 8th day in all groups in terms of number, gender, and species. Albendazole (ABZ) was applied at a 5 mg/kg dose for three days as positive drug control, and corn oil was used as solvent control. The arithmetic mean of oxyurid eggs counted in fecal flotation 43.51% decrease in the drug control ABZ group and showed a 21.12% increase in the A. annua 1200 mg/kg group on the last day of application. When compared with the corn oil group, a 34.08%, 34.76% and 36.91% decrease in ABZ 5 mg/kg, A. annua 300 mg/kg and A. annua 1200 mg/kg group respectively were found in their necropsies in terms of nematode number. Non-polar compounds of A. annua L., very low concentration of ABZ and as a dilution solvent corn oil are probably responsible for this result.

References

  • Arise RO, Malomo SO. (2009) Effects of ivermectin and albendazole on some liver and kidney function indices in rats. African Journal of Biochemistry Research. 3: 190-197. https://doi.org/10.5897/AJBR.9000102
  • Baytop T. (1999) Türkiye’de Bitkiler ile Tedavi. (In Turkish) Turkey: Nobel Tıp Kitabevleri.
  • Brisibe EA, Umoren UE, Brisibe F, Magalhäes PM, Ferreira JFS, Luthria D, Wu X, Prior RL. (2009) Nutritional characterisation and antioxidant capacity of different tissues of Artemisia annua L. Food Chemistry 115: 1240-1246. https://doi.org/10.1016/j.foodchem.2009.01.033.
  • Brown GD. (2010) The biosynthesis of artemisinin (Qinghaosu) and the phytochemistry of Artemisia annua L. (Qinghao). Molecules 15: 7603–7698. https://doi.org/10.3390/molecules15117603
  • Cala AC, Ferreira JFS, Chagas ASC, Gonzalez JM, Rodrigues RAF, Foglio MA, Oliveira CS, Sousa IMO, Magalhães PM, Júnior WB. (2014) Anthelmintic activity of Artemisia annua L. extracts in vitro and the effect of an aqueous extract and artemisinin in sheep naturally infected with gastrointestinal nematodes. Parasitol Res 113: 2345–2353. https://doi.org/10.1007/s00436-014-3891-z
  • Çetinkaya H, Taş T, Vuruşaner C. (2017) Determination of the parasitic stages in the faeces of some laboratory and pet animals by using flotation technique in Istanbul, Turkey. Journal of Istanbul Veterinary Sciences 1: 35-39. https://doi.org/10.30704/http-www-jivs-net.322964
  • Ferguson DL. (1981) Anthelmintic activity of albendazole against adult Metastrongylus apri in artificially infected swine. J Anim Sci 53: 1511-5. https://doi.org/10.2527/jas1982.5361511x.
  • Fox JG, Cohen BJ, Loew FW. (1984) Laboratory Animal Medicine. Orlando, Florida: Academic Press.
  • Gonzalez RH. (1996) Produccion de roedores dentro de un sistema de barreras. Experimental Animals 2: 26–27.
  • Harling et al. (1988) T104 Methyl Isothiocyanate: 1 Year Oral Toxicity Study in Beagle Dogs. US EPA Archive Document. Study No: Tox 87246 https://archive.epa.gov/pesticides/chemicalsearch/chemical/foia/web/pdf/068103/068103-1994-12-06a.pdf
  • Harvey CM. (1996) Anthelmintic macrocyclic lactone compositions. European Patent Office EP0873127A4: 1-9.
  • Hedrich HJ. (2012) The Laboratory Mouse Second Edition. London, UK: Academic Press Elsevier.
  • Kasım H. (1994) The spread of gastro-intestinal parasites in primary school children in Bursa region. MSc, Uludag University, Bursa, Turkey.
  • Keeling JE. (1961) Experimental trichuriasis I Antagonism between Trichuris muris and Aspiculuris tetraptera in the albino mouse. J Parasitol 47: 641–646. PMID: 13752160
  • Keiser J, Veneziano V, Rinaldi L, Mezzino L, Duthaler U, Cringoli G. (2010) Anthelmintic activity of artesunate against Fasciola hepatica in naturally infected sheep. Res Vet Sci 88: 107–110. https://doi.org/10.1016/j.rvsc.2009.05.007
  • Kozan E, Çankaya IT, Kahraman C, Akkol EK, Akdemir Z. (2011) The in vivo anthelmintic efficacy of some Verbascum species growing in Turkey. Exp Parasitol 129:211−214. doi:10.1016/j.exppara.2011.06.005
  • Mares MM, Murshed M, Aljawdah HMA, Al-Quraishy S. (2023) The Assessment of the Anthelmintic Activity of Laurus nobilis Extract in Mice Naturally Infected with Aspiculuris tetraptera. Indian Journal of Animal Research. https://doi.org/10.18805/IJAR.BF-1693.
  • Mc Govern PE, Christofidou-Solomidou M, Wang W, Dukes F, Davidson T, El-Deiry WS. (2010) Anticancer activity of botanical compounds in ancient fermented beverages (review). Int J Oncol; 37: 5-14. https://doi.org/10.3892/ijo_00000647
  • Memorial Sloan Kettering Cancer Center. (2010) MSKCC summary on Artemisia annua L. Memorial Sloan Kettering Cancer Center. http://www.mskcc.org/mskcc/html/69126.cfm, accessed July 2012.
  • Mohammed OB, Al-Shaebi EM, Omer SA, Abdel-Gaber RA. (2024) Morphological and molecular studies on a nematode parasite, Syphacia obvelata, infecting laboratory mice (Mus musculus) in Saudi Arabia. Arq. Bras. Med. Vet. Zootec.76: 84-92. https://doi.org/10.1590/1678-4162-13135
  • National Toxicology Program. NTP Toxicology and Carcinogenesis Studies of 4-Hexylresorcinol (CAS No. 136-77-6) in F344/N Rats and B6C3F1 Mice (Gavage Studies). Natl Toxicol Program Tech Rep Ser. 1988 May;330:1-166. PMID: 12732906.
  • Omer SA, Alghamdi JM, Alrajeh AH, Aldamigh M, Mohammed OB. (2020) Morphological and molecular characterization of Aspiculuris tetraptera (nematoda: Heteroxynematidae) from Mus musculus (Rodentia: Muridae) in Saudi Arabia. Biosci. Rep. 40: 1-11. https://doi.org/10.1042/BSR20203265
  • Perec-Matysiak A, Okulewicz A, Hildebrand J, Zalesny G. (2006) Helminth parasites of laboratory mice and rats. Wiad. Parazytol. 52: 99-102.
  • Pinto RM, Vicente JJ, Noronha D, Gonçalves L, Gomes DC. (1994) Helminth parasites of conventionally maintained laboratory mice. Memórias do Instituto Oswaldo Cruz; 89: 33–40. https://doi.org/1010.1590/s0074-02761994000100007
  • Pritchett-Corning KR, Clifford CB. (2012) Parasitic infections of laboratory mice. The Laboratory Mouse. 503-518.
  • Singh NP, Lai H. (2001) Selective cytotoxicity of dihydroartemisinin and holotransferrin toward human breast cancer cells. Life Sci 70: 49-56. https://doi.org/10.1016/s0024-3205(01)01372-8
  • Singh NP, Lai H. (2005) Synergistic cytotoxicity of artemesinin and sodium butyrate on human cancer cells. Anticancer Res 25: 4325-4332.
  • Soulsby EJL. (1982) Helminths Arthropods and Protozoa of Domesticated Animals. 7th ed. Bailliere Tindal, London.
  • Stepek G, Lowe AE, Buttle DJ, Duce IR, Behnke JM. (2006) In vitro and in vivo anthelmintic efficacy of plant cysteine proteinases against the rodent gastrointestinal nematode, Trichuris muris. Parasitology. 132: 681-689. Stewart A, Lowe A, Smales L. et al. (2018) Parasitic nematodes of the genus Syphacia Seurat, 1916 infecting Muridae in the British Isles, and the peculiar case of Syphacia frederici. Parasitology. 145: 269-280.
  • Sueta T, Miyoshi I, Okamura T, Kasai N. (2002) Experimental eradication of pinworms Syphacia obvelata and Aspiculuris tetraptera from mice colonies using ivermectin. Experimental Animals 51: 367–373. https://doi.org/10.1538/expanim.51.367
  • Taljaard L, Probst A, Tornow R, Keiser J, Haynes RK, van der Kooy F. (2022) In vitro antischistosomal activity of Artemisia annua and Artemisia afra extracts, Phytomedicine Plus, 2: 100279. https://doi.org/10.1016/j.phyplu.2022.100279.
  • Tariq KA, Chishti MZ, Ahmad F, Shawl AS. (2009) Anthelmintic activity of extracts of Artemisia absinthium against ovine nematodes. Vet Parasitol 160: 83-88. https://file.scirp.org/pdf/CM20120200002_44197281.pdf
  • Theodorides VJ. (1976) Anthelmintic: from laboratory animals to target species. In: Gadebusch HH. (Ed.) Chemotherapy of Infections Disease. Cleveland: CRC Press.
  • Tritten L, Silbereisen A, Keiser J. (2011) In vitro and In vivo Efficacy of Monepantel (AAD 1566) against Laboratory Models of Human Intestinal Nematode Infections. PLoS Negl Trop Dis 5: 1457. https://doi.org/10.1371/journal.pntd.0001457
  • Turel I, Oto G, Ayaz E, Yilmaz O, Mercan U. (2008) Anthelmintic Activity of Urtica dioica L in Mice Naturally Infected with Aspiculuris tetraptera. Journal of Animal and Veterinary Advances 7: 1628-1630. https://doi.org/javaa.2008.1628.1630
  • Turel I, Ayaz E, Dinç H. (2013) Anthelmintic Effect of Plantago major L. in Mice Infected with Aspiculuris tetraptera. YYU Veteriner Fakultesi Dergisi 24: 15 – 17.
  • Wertheim G, Lengy J. (1965) Growth and Development of Strongyloides ratti Sandground 1925 in the Albino Rat. J Parasitol 51: 636–639. PMID: 14339380
  • Willcox M, Bodeker G, Geneviève B, Dhingra V, Falquet J, Ferreira JFS, Graz B, Hirt HM, Hsu E, de Magalhaes PM, Provendier D, Wright CW. (2004) Artemisia annua as a traditional herbal antimalarial. In : Willcox M. (ed.) Bodeker G. (ed.) Rasaoanaivo P. (ed.) Traditional medicine medicinal plants and malaria. Boca Raton: CRC Press. https://doi.org/10.1201/9780203502327.
  • Youn HJ, Noh JW. (2001) Screening of the anticoccidial effects of herb extracts against Eimeria tenella. Vet Parasitol 96: 257–263. https://doi.org/10.1016/s0304-4017(01)00385-5

Laboratuvar farelerinin oksiyür nematodları üzerine Artemisia annua L.’nin in vivo antihelmintik etkisi

Year 2024, Volume: 35 Issue: 1, 34 - 43, 04.07.2024
https://doi.org/10.35864/evmd.1374233

Abstract

Oksiyürler, memelilerde yaygın olarak görülen bağırsak parazitleridir ve özellikle çocuklarda tekrarlayan helmintik enfeksiyonlara neden olurlar. Bu nedenle, tekrarlanabilir bir tedavi için doğal bitkisel bileşikler gereklidir. Bu çalışma, Artemisia annua L. n-hekzan ekstraktının oksiyürler üzerindeki antinematodal etkisini in vivo olarak araştırmayı amaçladı. Bu çalışmada, A. annua L. n-hekzan ekstraktı doğal olarak Syphacia obvelata ve Aspiculuris tetraptera türleri ile enfekte olmuş farelere uygulandı. 300, 600 ve 1200 mg/kg dozlarında 7 gün süreyle oral olarak verildi ve oksiyür yumurta sayısında meydana gelen değişim fekal flotasyon yöntemi ile araştırıldı. Nekropsideki nematodlar 8. günde tüm gruplarda sayı, cinsiyet ve tür açısından karşılaştırıldı. Pozitif ilaç kontrolü olarak Albendazol (ABZ) 5 mg/kg dozunda üç gün süreyle uygulandı ve çözücü kontrol olarak mısır yağı kullanıldı. Gaitada sayılan oksiyür yumurtaların aritmetik ortalaması flotasyon uygulamasının son gününde ilaç kontrol ABZ grubunda %43,51 azalma ve A. annua 1200 mg/kg grubunda %21,12 artış gösterdi. Mısır yağı grubu ile karşılaştırıldığında ABZ 5 mg/kg, A. annua 300 mg/kg ve A. annua 1200 mg/kg gruplarında nematod sayısı açısından sırasıyla %34,08, %34,76 ve %36,91 azalma saptandı. Polar olmayan A. annua L. bileşenleri, ABZ’nin çok düşük dozda olması ve çözücü solventi olarak mısır yağı kullanılması bu sonuçtan muhtemelen sorumludur.

References

  • Arise RO, Malomo SO. (2009) Effects of ivermectin and albendazole on some liver and kidney function indices in rats. African Journal of Biochemistry Research. 3: 190-197. https://doi.org/10.5897/AJBR.9000102
  • Baytop T. (1999) Türkiye’de Bitkiler ile Tedavi. (In Turkish) Turkey: Nobel Tıp Kitabevleri.
  • Brisibe EA, Umoren UE, Brisibe F, Magalhäes PM, Ferreira JFS, Luthria D, Wu X, Prior RL. (2009) Nutritional characterisation and antioxidant capacity of different tissues of Artemisia annua L. Food Chemistry 115: 1240-1246. https://doi.org/10.1016/j.foodchem.2009.01.033.
  • Brown GD. (2010) The biosynthesis of artemisinin (Qinghaosu) and the phytochemistry of Artemisia annua L. (Qinghao). Molecules 15: 7603–7698. https://doi.org/10.3390/molecules15117603
  • Cala AC, Ferreira JFS, Chagas ASC, Gonzalez JM, Rodrigues RAF, Foglio MA, Oliveira CS, Sousa IMO, Magalhães PM, Júnior WB. (2014) Anthelmintic activity of Artemisia annua L. extracts in vitro and the effect of an aqueous extract and artemisinin in sheep naturally infected with gastrointestinal nematodes. Parasitol Res 113: 2345–2353. https://doi.org/10.1007/s00436-014-3891-z
  • Çetinkaya H, Taş T, Vuruşaner C. (2017) Determination of the parasitic stages in the faeces of some laboratory and pet animals by using flotation technique in Istanbul, Turkey. Journal of Istanbul Veterinary Sciences 1: 35-39. https://doi.org/10.30704/http-www-jivs-net.322964
  • Ferguson DL. (1981) Anthelmintic activity of albendazole against adult Metastrongylus apri in artificially infected swine. J Anim Sci 53: 1511-5. https://doi.org/10.2527/jas1982.5361511x.
  • Fox JG, Cohen BJ, Loew FW. (1984) Laboratory Animal Medicine. Orlando, Florida: Academic Press.
  • Gonzalez RH. (1996) Produccion de roedores dentro de un sistema de barreras. Experimental Animals 2: 26–27.
  • Harling et al. (1988) T104 Methyl Isothiocyanate: 1 Year Oral Toxicity Study in Beagle Dogs. US EPA Archive Document. Study No: Tox 87246 https://archive.epa.gov/pesticides/chemicalsearch/chemical/foia/web/pdf/068103/068103-1994-12-06a.pdf
  • Harvey CM. (1996) Anthelmintic macrocyclic lactone compositions. European Patent Office EP0873127A4: 1-9.
  • Hedrich HJ. (2012) The Laboratory Mouse Second Edition. London, UK: Academic Press Elsevier.
  • Kasım H. (1994) The spread of gastro-intestinal parasites in primary school children in Bursa region. MSc, Uludag University, Bursa, Turkey.
  • Keeling JE. (1961) Experimental trichuriasis I Antagonism between Trichuris muris and Aspiculuris tetraptera in the albino mouse. J Parasitol 47: 641–646. PMID: 13752160
  • Keiser J, Veneziano V, Rinaldi L, Mezzino L, Duthaler U, Cringoli G. (2010) Anthelmintic activity of artesunate against Fasciola hepatica in naturally infected sheep. Res Vet Sci 88: 107–110. https://doi.org/10.1016/j.rvsc.2009.05.007
  • Kozan E, Çankaya IT, Kahraman C, Akkol EK, Akdemir Z. (2011) The in vivo anthelmintic efficacy of some Verbascum species growing in Turkey. Exp Parasitol 129:211−214. doi:10.1016/j.exppara.2011.06.005
  • Mares MM, Murshed M, Aljawdah HMA, Al-Quraishy S. (2023) The Assessment of the Anthelmintic Activity of Laurus nobilis Extract in Mice Naturally Infected with Aspiculuris tetraptera. Indian Journal of Animal Research. https://doi.org/10.18805/IJAR.BF-1693.
  • Mc Govern PE, Christofidou-Solomidou M, Wang W, Dukes F, Davidson T, El-Deiry WS. (2010) Anticancer activity of botanical compounds in ancient fermented beverages (review). Int J Oncol; 37: 5-14. https://doi.org/10.3892/ijo_00000647
  • Memorial Sloan Kettering Cancer Center. (2010) MSKCC summary on Artemisia annua L. Memorial Sloan Kettering Cancer Center. http://www.mskcc.org/mskcc/html/69126.cfm, accessed July 2012.
  • Mohammed OB, Al-Shaebi EM, Omer SA, Abdel-Gaber RA. (2024) Morphological and molecular studies on a nematode parasite, Syphacia obvelata, infecting laboratory mice (Mus musculus) in Saudi Arabia. Arq. Bras. Med. Vet. Zootec.76: 84-92. https://doi.org/10.1590/1678-4162-13135
  • National Toxicology Program. NTP Toxicology and Carcinogenesis Studies of 4-Hexylresorcinol (CAS No. 136-77-6) in F344/N Rats and B6C3F1 Mice (Gavage Studies). Natl Toxicol Program Tech Rep Ser. 1988 May;330:1-166. PMID: 12732906.
  • Omer SA, Alghamdi JM, Alrajeh AH, Aldamigh M, Mohammed OB. (2020) Morphological and molecular characterization of Aspiculuris tetraptera (nematoda: Heteroxynematidae) from Mus musculus (Rodentia: Muridae) in Saudi Arabia. Biosci. Rep. 40: 1-11. https://doi.org/10.1042/BSR20203265
  • Perec-Matysiak A, Okulewicz A, Hildebrand J, Zalesny G. (2006) Helminth parasites of laboratory mice and rats. Wiad. Parazytol. 52: 99-102.
  • Pinto RM, Vicente JJ, Noronha D, Gonçalves L, Gomes DC. (1994) Helminth parasites of conventionally maintained laboratory mice. Memórias do Instituto Oswaldo Cruz; 89: 33–40. https://doi.org/1010.1590/s0074-02761994000100007
  • Pritchett-Corning KR, Clifford CB. (2012) Parasitic infections of laboratory mice. The Laboratory Mouse. 503-518.
  • Singh NP, Lai H. (2001) Selective cytotoxicity of dihydroartemisinin and holotransferrin toward human breast cancer cells. Life Sci 70: 49-56. https://doi.org/10.1016/s0024-3205(01)01372-8
  • Singh NP, Lai H. (2005) Synergistic cytotoxicity of artemesinin and sodium butyrate on human cancer cells. Anticancer Res 25: 4325-4332.
  • Soulsby EJL. (1982) Helminths Arthropods and Protozoa of Domesticated Animals. 7th ed. Bailliere Tindal, London.
  • Stepek G, Lowe AE, Buttle DJ, Duce IR, Behnke JM. (2006) In vitro and in vivo anthelmintic efficacy of plant cysteine proteinases against the rodent gastrointestinal nematode, Trichuris muris. Parasitology. 132: 681-689. Stewart A, Lowe A, Smales L. et al. (2018) Parasitic nematodes of the genus Syphacia Seurat, 1916 infecting Muridae in the British Isles, and the peculiar case of Syphacia frederici. Parasitology. 145: 269-280.
  • Sueta T, Miyoshi I, Okamura T, Kasai N. (2002) Experimental eradication of pinworms Syphacia obvelata and Aspiculuris tetraptera from mice colonies using ivermectin. Experimental Animals 51: 367–373. https://doi.org/10.1538/expanim.51.367
  • Taljaard L, Probst A, Tornow R, Keiser J, Haynes RK, van der Kooy F. (2022) In vitro antischistosomal activity of Artemisia annua and Artemisia afra extracts, Phytomedicine Plus, 2: 100279. https://doi.org/10.1016/j.phyplu.2022.100279.
  • Tariq KA, Chishti MZ, Ahmad F, Shawl AS. (2009) Anthelmintic activity of extracts of Artemisia absinthium against ovine nematodes. Vet Parasitol 160: 83-88. https://file.scirp.org/pdf/CM20120200002_44197281.pdf
  • Theodorides VJ. (1976) Anthelmintic: from laboratory animals to target species. In: Gadebusch HH. (Ed.) Chemotherapy of Infections Disease. Cleveland: CRC Press.
  • Tritten L, Silbereisen A, Keiser J. (2011) In vitro and In vivo Efficacy of Monepantel (AAD 1566) against Laboratory Models of Human Intestinal Nematode Infections. PLoS Negl Trop Dis 5: 1457. https://doi.org/10.1371/journal.pntd.0001457
  • Turel I, Oto G, Ayaz E, Yilmaz O, Mercan U. (2008) Anthelmintic Activity of Urtica dioica L in Mice Naturally Infected with Aspiculuris tetraptera. Journal of Animal and Veterinary Advances 7: 1628-1630. https://doi.org/javaa.2008.1628.1630
  • Turel I, Ayaz E, Dinç H. (2013) Anthelmintic Effect of Plantago major L. in Mice Infected with Aspiculuris tetraptera. YYU Veteriner Fakultesi Dergisi 24: 15 – 17.
  • Wertheim G, Lengy J. (1965) Growth and Development of Strongyloides ratti Sandground 1925 in the Albino Rat. J Parasitol 51: 636–639. PMID: 14339380
  • Willcox M, Bodeker G, Geneviève B, Dhingra V, Falquet J, Ferreira JFS, Graz B, Hirt HM, Hsu E, de Magalhaes PM, Provendier D, Wright CW. (2004) Artemisia annua as a traditional herbal antimalarial. In : Willcox M. (ed.) Bodeker G. (ed.) Rasaoanaivo P. (ed.) Traditional medicine medicinal plants and malaria. Boca Raton: CRC Press. https://doi.org/10.1201/9780203502327.
  • Youn HJ, Noh JW. (2001) Screening of the anticoccidial effects of herb extracts against Eimeria tenella. Vet Parasitol 96: 257–263. https://doi.org/10.1016/s0304-4017(01)00385-5
There are 39 citations in total.

Details

Primary Language English
Subjects Parasitology
Journal Section Original Article
Authors

Dilara Karaman 0000-0003-4386-8531

Ahmet Onur Girişgin 0000-0002-0020-2708

Oya Girişgin 0000-0001-9896-1093

Prof.dr.hulusi Malyer 0000-0002-6283-4540

Publication Date July 4, 2024
Submission Date October 11, 2023
Acceptance Date May 28, 2024
Published in Issue Year 2024 Volume: 35 Issue: 1

Cite

APA Karaman, D., Girişgin, A. O., Girişgin, O., Malyer, P. (2024). In vivo anthelmintic effect of Artemisia annua L. on oxyurid nematodes of laboratory mice. Etlik Veteriner Mikrobiyoloji Dergisi, 35(1), 34-43. https://doi.org/10.35864/evmd.1374233

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