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Asian Pac J Trop Dis 2014; 4(Suppl 1): S250-S254 S250

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Document heading doi: 10.1016/S2222-1808(14)60449-7 2014 by the Asian Pacific Journal of Tropical Disease. All rights reserved. 襃 In vivo evaluation of antiparasitic effects of abrotanum and officinalis extracts on Syphacia obvelata, Aspiculoris tetrapetra and Hymenolepis nana parasites

1 2 3 4 5 Mahdi Amirmohammadi , Shole Khajoenia , Mahmoud Bahmani *, Mahmoud Rafieian-Kopaei , Zohre Eftekhari , Mostafa 6,7 Qorbani 1Jiroft Branch, Islamic Azad University, Jiroft, Iran 2Department of Clinical Science , Faculty of Medicine, Medical Science University Jiroft, Iran 3Food and Beverages Safety Research Center, Urmia University of Medical Sciences, Urmia, Iran 4Medical Research Center, Shahrekord University of Medical Sciences, Shahrekord, Iran 5Veterinary Medicine Faculty, Tehran University, Tehran, Iran 6Alborz University of Medical Sciences, Karaj, Iran 7Department of Epidemiology, Tehran University of Medical Sciences, Tehran, Iran

PEER REVIEW ABSTRACT

Peer reviewer Objective: To evaluate the effects of and extracts against Dr. Hassan hassanzadazar, PhD of food dMethods:igestive s ystem parasites of mice. hygiene, food control expert of food The ethanol extract was prepared and dissolved in distilled water. The mebendazole and drug deputy, Urmia university of was used as positive control and distilled water as negative control. After counting eggs Syphaciaper gram 16 medical science, Urmia, Iran. fobvelataeces, infeAspicoloriscted mice terepetrawith eggs Hymenolipisper gram fe cnanaes contained two to three parasites of +989144412026 4 Tel: , Artemisia and designated in Salvia groups. The first group was Fax: +984413455839 given extracts of (150 mg/kg), the second group was given extract (150 mg/kg), the E-mail: [email protected] third group was given mebendazole (10 mg/kg) and finally the fourth group was given distilled (2 ) Comments Results:water m L/kg . Artemisia Salvia The ethanol extracts of and plantPs reduced the number of parasite eggs ( 0 001) This is a good research in which the per gram of Hymenolepisfeces. Resul tnanas showAspiculurised signific tetrapteraant reductSyphaciaion -va obvelatalue< . in the number of eggs authors determined effects of two eConclusions:xcreted by , , Artemisia in mice. Salvia local extracts on three various These results revealed that antiparasitic effects of and are parasites in miceS.. Tofficinalishe results are reasonable and these two plants might be used as antiparasitic natural products. A.int eabrotanumresting that and extracts had good antiparasitic effects on three various KEYWORDS parasite. 253 Salvia officinalis Artemisia abrotanum Syphacia obvelata Aspicoloris terepetra Details on Page S , , Mice, Parasite, , , Hymenolipis nana

1. Introduction victims. Chemical drug against parasites is beneficial, but this method has some problems such as drug resistance, Parasitic infections cause major public health problems residue and unwanted side effects associated. Therefore, leading to morbidity and sometimes mortality of the study on alternative therapies are important[1]. For

*Corresponding author: Mahmoud Bahmani, Food and Beverages Safety Research Article history: Center, Urmia University of Medical Sciences, Urmia, Iran. Received 28 Nov 2013 Tel: 984412772023 Received in revised form 5 Dec, 2nd revised form 11 Dec, 3rd revised form 16 Dec 2013 Fax: 984412787814 Accepted 20 Jan 2014 E-mail: [email protected] Available online 28 Jan 2014 Foundation Project: Supported by Jiroft Branch, Islamic Azad University of Jiroft, Iran (Grant No. 1713864). Mahdi Amirmohammadi et al./Asian Pac J Trop Dis 2014; 4(Suppl 1): S250-S254 S251 2. Materials and methods centuries, medicinal plants have been used to eliminate parasites in many parts of the world, and humans used A. abrotanum S. officinalis the plant to treat various diseases. Herbal medicines The methanolic extracts of and are used in recent years due to the high reliability and were prepared by adding a 1:3 ratio of garlic and methanol, effectiveness, and cost is also taken into consideration[2,3]. respectively, and this was subjected to Soxhlet extraction et al In ethnoveterinary medicine, which draws inspiration for 72 h according to the prescribed method of Eidi [5]. from traditional practice, there seems to be various plants After extraction, the solvent was filtered[5]. The information suitable for treating almost every parasitic disorder about the studied plants is presented in Table 1. Table 1 of livestock. Although the majority of the evidence on Scientific name, English name, part used, extract type, and traditional treatment antiparasitic activity of plants has been customarily based A. abrotanum S. officinalis. on anecdotal observations, there are currently an increasing of and Scientific name English name Part used Extract Traditional use[6] A. abrotanum number of controlled experimental studies aimed to verify, Wormwood Ethanolic extract Antiparasite S. officinalis validate and quantify such plant activity in a scientific Garden sage Leaf Ethanolic extract Antiparasite manner. Currently, there are 119 drugs composed of plants, S. officinalis and only 90 of the 250 000 known plant species, has been (garden sage, common sage) is a small, obtained[2,3]. In Chaharmahal va Bakhtiari and Kerman perennial, evergreen , with woody stems, grayish Artemisia abrotanum A. abrotanum provinces in Iran, ( ) and , and blue to purplish flowers. It is a family member Salvia officinalis S. officinalis ( ) are used as medicinal plants of and is native to the Mediterranean region, against parasites. and it has been naturalized in many places throughout the S. officinalis of are quite variable in size, leaf world. It has a long history of medicinal and culinary use, and flower color and foliage pattern with many variegated and in modern times as an ornamental garden plant. A. abrotanum leaf types. The Old World type grows approximately 0.61 m Wormwood or southernwood ( ) is a flowering tall and wide with lavender flowers, the most common color. plant. Southernwood is antiseptic and kills intestinal And the flower can also be white, pink, or purple. The plant worms. flowers bloom in late spring or summer. The leaves are First, a few infected mice were randomly divided into four oblong, ranging in size up to 6.4 cm long by 2.5 cm wide. groups. The mice were treated with doses of 20, 50, 100 and Leaves are grey-green, rugose on the upper side, and nearly 150 mg kg body weight of ethanol extracts or normal saline white underneath due to many short soft hairs. Modern (2 mL/kg), orally. All animals were tested during 48 h for cultivars include leaves with purple, rose, cream, and symptoms of poisoning and death. After that, 16 mice with H. nana yellow in many variegated combinations. Sage leaf contains equal weight, nutritional conditions, infected with , A. tetraptera S. obvelata tannic acid, oleic acid, ursonic acid, ursolic acid, cornsole, and were tested for four groups that cornsolic acid, fumaric acid, chlorogenic acid, caffeic each group consisted of four mice. The Lynn Clayton test acid, niacin, nicotinamide, flavones, flavonoid glycosides, was employed for detecting parasite eggs per gram feces. and estrogenic substance[3]. Its leaves contain essential These groups were treated as following: Salvia oils and tannins that can help to facilitate digestion with Group 1: treated with 150 mg/kg extract for 5 d. Artemisia anticonvulsant, anti-fever, antiseptic and anti-diabetic Group 2: treated with 150 mg/kg extract for 5 d. effect. Modern evidence shows possible uses as an anti- Group 3: treated with 10 mg /kg mebendazole for 5 d as sweating, antibiotic, antifungal, astringent, antispasmodic, positive control . estrogenic, hypoglycemic and tonic agent. This plant is Group 4: treated with 2 mL/kg normal saline as negative also used for the treatment of gout, chronic rheumatism, control. dizziness and headache. Investigations have be performed The parasite eggs were counted on the first, second, third ’ to use sage as a medication for Alzheimer s disease. and fifth day. On the seventh day, one mouse from each Wormwood is used to treat liver, spleen and stomach group was killed and the intestine was checked regarding disorders. It is seldom used for medicinal purpose the presence of parasites. The differences between the today, except in Germany, where poultices are placed on control and treated groups were analyzed using M-stat wounds, splinters and skin conditions and it is employed program. occasionally to treat frostbite[4]. In the present study, the antiparasitic effects of Artemisia S. officinalis 3. Results and plants were investigated on the most common gastrointestinal tract parasites such Hymenolepis nana H. nana Aspiculuris tetraptera A. as ( ), ( In the present study, the ethanol extracts of wormwood, tetraptera Syphacia obvelata S. obvelata ) and ( ). and garden sage, and mebendazole was examined for the effect on digestive tract parasites of mice. The results Mahdi Amirmohammadi et al./Asian Pac J Trop Dis 2014; 4(Suppl 1): S250-S254 S252 showed that in all groups which received drug or herbal 1000.00 extracts, but not in control group, the number of eggs excreted in per gram of feces was reduced one day after treatment. P Results showed significant differences ( -value<0.001) in 800.00 H. nana A. tetraptera the number of eggs excreted by the , S. obvelata and in mice, among the groups which had used 600.00 the wormwood or garden sage and control group. T his study showed a noticeable effect for wormwood and u m b e r o f g s 400.00 garden sage over time against parasites. So that on the N seventh day, the number of parasite eggs in feces was at the P 200 00 lowest amount ( <0.001). The garden sage and mebendazole . H. nana A. tetraptera revealed better effects on and in comparison to Wormwood. Wormwood, however, had better 0.00 S. obvelata effect on in comparison to garden sage. Average 0 1 3 5 7 S. obvelata, Day number of eggs in per gram of feces excreted by Wormwood Garden sage Mebendazol Distilled water A. tetrapetra H. nana Figure 3. S. and on Day 0, 1, 3, 5 and 7 after Average number of eggs in per gram of feces excreted by obvelata treatment in four groups is specified in Figure 1, 2 and 3. on Day 0, 1, 3, 5 and 7 after treatment in four groups. The mean and standard deviation of the different treatment 800 744 groups is shown in Figure 4. 663 699 700 627 635 600 572 800.00 500 400 305 300 272 211 214 195 200 600 00 107 . 51 47 55 100 16 0 0 0 0 0 -100 Zero day First day Third day Fifth day Seventh day 400.00 -200 u m b e r o f g s N Wormwood Garden sage Mebendazole Distilled water Figure 4. The mean and standard deviation of the different treatment 200.00 groups.

0.00 4. Discussion 0 1 3 5 7 Day The number of eggs among different groups in different days Wormwood Garden sage Mebendazol Distilled water In the present study, the ethanol extracts of wormwood, Figure 1. H. nana Average number of eggs in per gram of feces excreted by garden sage and mebendazole for treatment of the on Day 0, 1, 3, 5 and 7 after treatment in four groups. digestive tract parasites of mice was examined. The P results showed significant differences ( -value<0.001) in H. nana A. tetraptera the number of eggs excreted by the , S. obvelata and in mice among the groups which had used 600.00 the wormwood or garden sage and control group. This study found a noticeable effect of wormwood and garden

g s sage over time, so that the number of parasite eggs in the E 400.00 feces was at the lowest amount on the seventh day. In Iranian traditional medicine, one species of u m b e r o f Artemisia Artemisia aucheri N , namely Bioss, is known 200.00 as antiparasitic plant. Ghasemi pirbalouti showed that Artemisia salina had antiparasite and anti-pesticide Artemisia inculata effect, had anti-parasite and laxative 0.00 Saliva verbeneca effects, and L. had good effect for skin 0 1 3 5 7 [6] Day disorders . Wormwood Garden sage Mebendazol Distilled water S. officinalis Figure 2. A. The essence of can help to repair cell, Average number of eggs in per gram of feces excreted by tetraptera stimulate, and strengthen the skin and hair, and decrease on Day 0, 1, 3, 5 and 7 after treatment in four groups. et al depression. Sharifi . revealed that the extraction of Mahdi Amirmohammadi et al./Asian Pac J Trop Dis 2014; 4(Suppl 1): S250-S254 S253 Artemisia aucheri Bioss has an antiparasitic effect on the that traditional effects of antiparasitic on intestinal worms Leishmania major Artemisia herba-alba [7]. are introduced for [22,23]. Mahrami Poor and Neghahban in 2007 showed that This study and other studies revealed appropriate Artemisia sieberi Artemisia S. officinalis essential oils of and antiparasite effect of and which dependently reduced spawning, hatching eggs, and indicate that they might be used instead of chemical drugs mortality of first instars larvae of the beetle (parasite of in parasites control programs. et al grains)[8]. Jalali . revealed the insecticide effect of the L[9]. S. officinalis Conflict of interest statement contains compounds such as α thujine, cis humulen- , 1,8-cineole, (E)-Caryophylene, borneole, monoterpenes, diterpenes and diterpenes. The We declare that we have no conflict of interest. is one of the most important components of Artemisia [9]. Acknowledgements Results of study by Mirza showed that 32 compound has been identified on sage. Among the compounds identified, using gas chromatograph coupled with mass spectrometer, This work was supported by Jiroft Branch, Islamic Azad β -caryophyllene (16.3%), sclareol (13.3%), hexyl octanoate University of Jiroft, Iran. Grant number of this study is (12.2%) and bicyclogermacrene (10%) had the highest share, 1713864. respectively[10]. et al The results of Bahmani . showed that high doses of Comments the plant extract on antiparasitic effect against leeches Limnatis nilotica ( ) was found[11]. is antiparasitic Artemisia Background drug that is produced from the plant and its active ingredient is artemisian (artemisinin)[6]. Perhaps Parasitic infections in animals and humans are one of the powerful antiparasitic effects of garden sage and the medical problems. In recent decades the use of local wormwood plants are due to these compounds. medicinal and non-chemical remedies instead Artemisia Eimeria The antiparasitic effect of on has been of chemical drugs to treat diseases has been regarded. previously shown and it has been introduced as an anti- Herbal plants in different areas based on species and coccidian drug[12-14]. Bruce had demonstrated the effects amount of active ingredient have different therapeutic of Artemisia extract on malarial protozoa[13]. effects. et al Esfandiari . has shown effect of different Artemisia Syphacia Research frontiers concentrations of extract on nematode et al [15]. Khosravierad and Allen . showed that the Studies are performed in order to determine effects of Artemisia artemisinin, a component of (different species) two local plant extracts on three various parasites in mice. has appropriate antiparasite effect on Coccidia[16,17]. Certain dose of two plant extracts were fed to ternary test Linn. is used traditionally by groups of infected mice. people as a vermifuge in addition to its other livestock et al Related reports uses. The results of the study of Tariq . showed that Artemisia absinthium extracts are a promising alternative The data about the effects of two plant extracts on three to the commercially available anthelmintics for the parasites are different. This difference is probably due to ’ treatment of GI nematodes of sheep[18]. Study of Ezzat- extracts main ingredients and drug resistance of parasites et al. Artemisia kulbadica zadeh showed that the plant that cause various results during one week consuming of had antimicrobials and antioxidants effects[19]. Studies of plant extracts. Artemisia nilagirica Arokiyaraj showed that showed good Innovations & breakthroughs antibacterial effects[20]. In studies of Suresh it was found Artemisia parviflora that phytochemical contents of Roxb Data regarding effects of different plant extracts on were alkaloids, sterols/terpenoids, flavonoids, tannins, various parasites are scarce. This study showed that S. officinalis A. abrotanum phenols and coumarins[21]. Results of two studies showed and extracts can be use for Mahdi Amirmohammadi et al./Asian Pac J Trop Dis 2014; 4(Suppl 1): S250-S254 S254 progressive study on human and domestic animals. [10] M irza M, Ahmadi L. Identification of essential oil and extraction Salvia sclareae Iran J Med Aromat Plants Res 216 of . 1999; : Applications 115-136. S. officinalis A. The results of this study showed that and [11] B ahmani M, Avijgan M, Gholami-Ahangaran M, Rafieian abrotanum Limnatis nilotica extracts had good antiparasitic effects on three M. The comparison of the anti effets of Iran various parasite, one of which is common in human. So we albendazole and some of the Iranian medicinal plants. South Med J 15 can test those extracts on other parasites in human and 2012; : 25-34. domestic animals. [12] A rab HA, Rahbari S, Rassouli A, Moslemi MH, Khosravirad Artemisia sieberi F. Determination of artemisinin in and Peer review anticoccidial effects of the plant extract in broiler chickens. Trop Anim Health Prod 38 This is a good research in which the authors determined 2006; (6): 497-503. Br Med J effects of two local plant extracts on three various parasites [13] B ruce-Chwatt LJ. Qinghaosu: a new antimalarial. S. officinalis 284 in mice. The results are interesting, and and 1982; : 767-768. A. abrotanum extracts had good antiparasitic effects on [14] Y oun HJ, Noh JW. Screening of the anticoccidal effects of herb Eimeria tenella Vet parasitol 96 three various parasite. extract against . 2001; (4): 257- 263. In [15] E sfandiari B, Youssefi M, Keighobadi M, Nahrevanian H. 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