Satureja hortensis L. and Calendula officinalis L., Two Romanian Plants, with In Vivo Antiparasitic Potential against Digestive Parasites of Swine
Abstract
:1. Introduction
2. Materials and Methods
2.1. Chemical Analysis of Satureja hortensis and Calendula officinalis
2.2. Experimental Design
2.3. Ontologies, Ethics Statement, and Assessment of Antiparasitic Efficacy
2.4. Statistical Analysis
- -
- Sphericity: The variances of the differences between all combinations of related groups (levels) are equal.
- -
- Normality: The distribution of the differences in the dependent variable between the two related groups should be approximately normally distributed for each level of the independent variable.
- -
- Lack of multivariate outliers.
- For the within-subjects factor (time) the Friedman test was used to compare the repeated measures (measurements at day 0, 14 and 28) for each group separately (control and experimental group). If the Friedman test returned significant differences, the Wilcoxon signed-rank test for pairwise comparisons was used to identify the groups with the significant differences. The Bonferroni correction for multiple comparisons was used to reduce the risk of false positives.
- For the between-subjects factor (treatment group) a Mann–Whitney U test was performed for each time point to compare the control and experimental groups.
3. Results
3.1. Chemical Analysis of S. hortensis and C. officinalis
3.2. Analysis of Antiparasitic Effects of Studied Plants
3.2.1. Descriptive Statistics
3.2.2. Inferential Statistics
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Wang, S.; Zhang, L.; Li, J.; Cong, J.; Gao, F.; Zhou, G. Effects of dietary marigold extract supplementation on growth performance, pigmentation, antioxidant capacity and meat quality in broiler chickens. Asian-Australas. J. Anim. Sci. 2017, 30, 71–77. [Google Scholar] [CrossRef] [PubMed]
- Jabbar, A.; Iqbal, Z.; Kerboeuf, D.; Muhammad, G.; Khan, M.N.; Afaq, M. Anthelmintic resistance: The state of play revisited. Life Sci. 2006, 79, 2413–2431. [Google Scholar] [CrossRef] [PubMed]
- Coles, G.C.; Jackson, F.; Pomroy, W.E.; Prichard, R.K.; von Samson-Himmelstjerna, G.; Silvestre, A.; Taylor, M.A.; Vercruysse, J. The detection of anthelmintic resistance in nematodes of veterinary importance. Vet. Parasitol. 2006, 136, 167–185. [Google Scholar] [CrossRef] [PubMed]
- Ayrle, H.; Mevissen, M.; Kaske, M.; Nathues, H.; Gruetzner, N.; Melzig, M.; Walkenhorst, M. Medicinal plants–prophylactic and therapeutic options for gastrointestinal and respiratory diseases in calves and piglets? A systematic review. BMC Vet. Res. 2016, 12, 89. [Google Scholar] [CrossRef] [PubMed]
- Blanco-Penedo, I.; Fernández González, C.; Tamminen, L.M.; Sundrum, A.; Emanuelson, U. Priorities and Future actions for an effective Use of Phytotherapy in livestock—Outputs from an expert Workshop. Front. Vet. Sci. 2018, 4, 248. [Google Scholar] [CrossRef] [PubMed]
- Castaño Osorio, J.C.; Giraldo García, A.M. Antiparasitic phytotherapy perspectives, scope and current development. Infectio 2019, 23, 189–204. [Google Scholar] [CrossRef]
- Ferreira, L.E.; Benincasa, B.I.; Fachin, A.L.; Franca, S.C.; Continia, S.S.H.T.; Chagas, A.C.S.; Beleboni, R.O. Thymus vulgaris L. Essential Oil and Its Main Component Thymol: Anthelmintic Effects against Haemonchus contortus from Sheep. Vet. Parasitol. 2016, 228, 70–76. [Google Scholar] [CrossRef] [PubMed]
- Yadav, P.; Singh, R. A review on anthelmintic drugs and their future scope. Int. J. Pharm. Pharm. Sci. 2011, 3, 17–21. [Google Scholar]
- Alban, L.; Petersen, J.V.; Busch, M.E. A comparison between lesions found during meat inspection of finishing pigs raised under organic/free-range conditions and conventional, indoor conditions. Porc. Health Manag. 2015, 1, 4. [Google Scholar] [CrossRef]
- Kongsted, H.; Sørensen, J.T. Lesions found at routine meat inspection on finishing pigs are associated with production system. Vet. J. 2017, 223, 21–26. [Google Scholar] [CrossRef]
- Bonnefous, C.; Collin, A.; Guilloteau, L.A.; Guesdon, V.; Filliat, C.; Réhault-Godbert, S.; Rodenburg, T.B.; Tuyttens, F.A.M.; Warin, L.; Steenfeldt, S.; et al. Welfare issues and potential solutions for laying hens in free range and organic production systems: A review based on literature and interviews. Front. Vet. Sci. 2022, 9, 1148. [Google Scholar] [CrossRef] [PubMed]
- Sowemimo, O.A.; Asaolu, S.O.; Adegoke, F.O.; Ayanniyi, O.O. Epidemiological survey of gastrointestinal parasites of pigs in Ibadan, Southwest Nigeria. J. Public Health Epidemiol. 2012, 4, 294–298. [Google Scholar] [CrossRef]
- Eijck, I.A.J.M.; Borgsteede, F.H.M. A survey of gastrointestinal pig parasites on free-range, organic and conventional pig farms in The Netherlands. Vet. Res. Commun. 2005, 29, 407–414. [Google Scholar] [CrossRef]
- Kaur, M.; Singh, B.B.; Sharma, R.; Gill, J.P.S. Prevalence of gastro intestinal parasites in pigs in Punjab, India. J. Parasit. Dis. 2017, 41, 483–486. [Google Scholar] [CrossRef] [PubMed]
- Tumusiime, M.; Ntampaka, P.; Niragire, F.; Sindikubwabo, T.; Habineza, F. Prevalence of Swine Gastrointestinal Parasites in Nyagatare District, Rwanda. J. Parasitol. Res. 2020, 2020, 8814136. [Google Scholar] [CrossRef] [PubMed]
- Băieş, M.H.; Boros, Z.; Gherman, C.M.; Spînu, M.; Mathe, A.; Pataky, S.; Lefkaditis, M.; Cozma, V. Prevalence of swine gastrointestinal parasites in two free-range farms from nord-west region of Romania. Pathogens 2022, 11, 954. [Google Scholar] [CrossRef] [PubMed]
- Uddin Khan, S.; Atanasova, K.R.; Krueger, W.S.; Ramirez, A.; Gray, G.C. Epidemiology, geographical distribution, and economic consequences of swine zoonoses: A narrative review. Emerg. Microbes Infect. 2013, 2, e92. [Google Scholar] [CrossRef] [PubMed]
- Thapaliya, D.; Hanson, B.M.; Kates, A.; Klostermann, C.A.; Nair, R.; Wardyn, S.E.; Smith, T.C. Zoonotic Diseases of Swine: Food-borne and Occupational Aspects of Infection. In Zoonoses: Infections Affecting Humans and Animals; Sing, A., Ed.; Springer: Cham, Switzerland, 2023; pp. 113–162. [Google Scholar] [CrossRef]
- Solaymani-Mohammadi, S.; Petri, W.A., Jr. Zoonotic implications of the swine-transmitted protozoal infections. Vet. Parasitol. 2006, 140, 189–203. [Google Scholar] [CrossRef]
- Ziemer, C.J.; Bonner, J.M.; Cole, D.; Vinjé, J.; Constantini, V.; Goyal, S.; Gramer, M.; Mackie, R.; Meng, X.J.; Myers, G.; et al. Fate and transport of zoonotic, bacterial, viral, and parasitic pathogens during swine manure treatment, storage, and land application. J. Anim. Sci. 2010, 88, E84–E94. [Google Scholar] [CrossRef]
- Pinilla, J.C.; Morales, E.; Muñoz, A.A.F. A survey for potentially zoonotic parasites in backyard pigs in the Bucaramanga metropolitan area, Northeast Colombia. Vet. World 2021, 14, 372–379. [Google Scholar] [CrossRef]
- Muley, B.P.; Khadabadi, S.S.; Banarase, N.B. Phytochemical constituents and pharmacological activities of Calendula officinalis Linn (Asteraceae): A review. Trop. J. Pharm. Res. 2009, 8, 455–465. [Google Scholar] [CrossRef]
- Jan, N.; Andrabi, K.I.; John, R. Calendula officinalis—An important medicinal plant with potential biological properties. Proc. Indian Natl. Sci. Acad. 2017, 83, 769–787. [Google Scholar] [CrossRef]
- Singh, M.K.; Sahu, P.; Nagori, K.; Dewangan, D.; Kumar, T.; Alexander, A.; Badwaik, H.; Tripathi, D.K. Organoleptic properties in-vitro and in-vivo pharmacological activities of Calendula officinalis Linn: An over review. J. Chem. Pharm. Res. 2011, 3, 655–663. [Google Scholar]
- Khalid, K.A.; Da Silva, J.T. Biology of Calendula officinalis Linn.: Focus on pharmacology, biological activities and agronomic practices. Med. Aromat. Plant Sci. Biotechnol. 2012, 6, 12–27. [Google Scholar]
- Ashwlayanvd, K.A.; Verma, M. Therapeutic potential of Calendula officinalis. Pharm. Pharmacol. Int. J. 2018, 6, 149–155. [Google Scholar]
- Lipi, P.; Vivek, S.; Makode, K.K.; Jain, U.K. Anthelmintic activity of aqueous extracts of some saponin containing medicinal plants. Pharm. Lett. 2010, 2, 476–481. [Google Scholar]
- Verma, P.K.; Raina, R.; Agarwal, S.; Kaur, H. Phytochemical ingredients and Pharmacological potential of Calendula officinalis Linn. Pharm. Biomed. Res. 2018, 4, 1–17. [Google Scholar] [CrossRef]
- Butnariu, M.; Coradini, C.Z. Evaluation of biologically active compounds from Calendula officinalis flowers using spectrophotometry. Chem. Cent. J. 2012, 6, 35. [Google Scholar] [CrossRef]
- Shehata, A.A.; Yalçın, S.; Latorre, J.D.; Basiouni, S.; Attia, Y.A.; El-Wahab, A.; Visscher, C.; El-Seedi, H.R.; Huber, C.; Hafez, H.M.; et al. Probiotics, prebiotics, and phytogenic substances for optimizing gut health in poultry. Microorganisms 2022, 10, 395. [Google Scholar] [CrossRef]
- Kostadinović, L.; Lević, J. Effects of phytoadditives in poultry and pigs diseases. J. Agron. 2018, 1, 1–7. [Google Scholar]
- Hamidpour, R.; Hamidpour, S.; Hamidpour, M.; Shahlari, M.; Sohraby, M. Summer savory: From the selection of traditional applications to the novel effect in relief, prevention, and treatment of a number of serious illnesses such as diabetes, cardiovascular disease, Alzheimer’s disease, and cancer. J. Tradit. Complement. Med. 2014, 4, 140–144. [Google Scholar] [CrossRef] [PubMed]
- Fierascu, I.; Dinu-Pirvu, C.E.; Fierascu, R.C.; Velescu, B.S.; Anuta, V.; Ortan, A.; Jinga, V. Phytochemical profile and biological activities of Satureja hortensis L.: A review of the last decade. Molecules 2018, 23, 2458. [Google Scholar] [CrossRef] [PubMed]
- Mohammadhosseini, M.; Beiranvand, M. Chemical composition of the essential oil from the aerial parts of Satureja hortensis as a potent medical plant using traditional hydrodistillation. J. Chem. Health Risks 2013, 3, 43–54. [Google Scholar]
- Mahboubi, M.; Kazempour, N. Chemical composition and antimicrobial activity of Satureja hortensis and Trachyspermum copticum essential oil. Iran. J. Microbiol. 2011, 3, 194–200. [Google Scholar] [PubMed]
- Bimbiraitė-Survilienė, K.; Stankevičius, M.; Šuštauskaitė, S.; Gęgotek, A.; Maruška, A.; Skrzydlewska, E.; Barsteigienė, Z.; Akuņeca, I.; Ragažinskienė, O.; Lukošius, A. Evaluation of chemical composition, radical scavenging and antitumor activities of Satureja hortensis L. herb extracts. Antioxidants 2021, 10, 53. [Google Scholar] [CrossRef] [PubMed]
- Jafari, F.; Ghavidel, F.; Zarshenas, M.M. A critical overview on the pharmacological and clinical aspects of popular Satureja species. J. Acupunct. Meridian Stud. 2016, 9, 118–127. [Google Scholar] [CrossRef] [PubMed]
- Tepe, B.; Cilkiz, M. A pharmacological and phytochemical overview on Satureja. Pharm. Biol. 2016, 54, 375–412. [Google Scholar] [CrossRef] [PubMed]
- Bǎieş, M.H.; Gherman, C.; Boros, Z.; Olah, D.; Vlase, A.M.; Cozma-Petrut, A.; Györke, A.; Miere, D.; Vlase, L.; Crişan, G.; et al. The Effects of Allium sativum L., Artemisia absinthium L., Cucurbita pepo L., Coriandrum sativum L., Satureja hortensis L. and Calendula officinalis L. on the Embryogenesis of Ascaris suum Eggs during an In Vitro Experimental Study. Pathogens 2022, 11, 1065. [Google Scholar] [CrossRef]
- Mircean, V.; Cozma, V.; Gyorke, A. Diagnostic Coproscopic in Bolile Parazitare la Animale, (Coproparasitological Diagnostic in Parasitic Diseases in Animals); Risoprint: Cluj-Napoca, Romania, 2011; pp. 23–35. [Google Scholar]
- Manser, M.M.; Saez, A.C.; Chiodini, P.L. Faecal Parasitology: Concentration Methodology Needs to be Better Standardised. PLoS Negl. Trop. Dis. 2016, 10, e0004579. [Google Scholar] [CrossRef]
- McKenna, P.B. 2006. Further comparison of faecal egg count reduction test procedures: Sensitivity and specificity. N. Z. Vet. J. 2006, 54, 365–366. [Google Scholar] [CrossRef]
- Băieş, M.H.; Cotuţiu, V.D.; Spînu, M.; Mathe, A.; Cozma-Petruț, A.; Miere, D.; Bolboacǎ, S.D.; Cozma, V. The Effects of Coriandrum sativum L. and Cucurbita pepo L. against Gastrointestinal Parasites in Swine: An In Vivo Study. Microorganisms 2023, 11, 1230. [Google Scholar] [CrossRef] [PubMed]
- SciPy. Available online: https://scipy.org/ (accessed on 1 October 2023).
- Seaborn: Statistical Data Visualization. Available online: https://seaborn.pydata.org/ (accessed on 1 October 2023).
- IBM SPSS Statistics. Available online: https://www.ibm.com/products/spss-statistics (accessed on 1 October 2023).
- Amirmohammadi, M.; Khajoenia, S.; Bahmani, M.; Rafieian-Kopaei, M.; Eftekhari, Z.; Qorbani, M. In vivo evaluation of antiparasitic effects of Artemisia abrotanum and Salvia officinalis extracts on Syphacia obvelata, Aspiculoris tetrapetra and Hymenolepis nana parasites. Asian Pac. J. Trop. Dis. 2014, 4, S250–S254. [Google Scholar] [CrossRef]
- Bakare, A.G.; Shah, S.; Bautista-Jimenez, V.; Bhat, J.A.; Dayal, S.R.; Madzimure, J. Potential of ethno-veterinary medicine in animal health care practices in the South Pacific Island countries: A review. Trop. Anim. Health Prod. 2020, 52, 2193–2203. [Google Scholar] [CrossRef] [PubMed]
- Hart, B.L. The evolution of herbal medicine: Behavioural perspectives. Anim. Behav. 2005, 70, 975–989. [Google Scholar] [CrossRef]
- Szakiel, A.; Ruszkowski, D.; Grudniak, A.; Kurek, A.; Wolska, K.I.; Doligalska, M.; Janiszowska, W. Antibacterial and antiparasitic activity of oleanolic acid and its glycosides isolated from marigold (Calendula officinalis). Planta Med. 2008, 74, 1709–1715. [Google Scholar] [CrossRef] [PubMed]
- Doligalska, M.; Jóźwicka, K.; Kiersnowska, M.; Mroczek, A.; Pączkowski, C.; Janiszowska, W. Triterpenoid saponins affect the function of P-glycoprotein and reduce the survival of the free-living stages of Heligmosomoides bakeri. Vet. Parasitol. 2011, 179, 144–151. [Google Scholar] [CrossRef] [PubMed]
- Kaplan, R.M.; Storey, B.E.; Vidyashankar, A.N.; Bissinger, B.W.; Mitchell, S.M.; Howell, S.B.; Mason, M.E.; Lee, M.D.; Pedroso, A.A.; Akashe, A.; et al. Antiparasitic efficacy of a novel plant-based functional food using an Ascaris suum model in pigs. Acta Trop. 2014, 139, 15–22. [Google Scholar] [CrossRef] [PubMed]
- Ferreira, T.S.; Moreira, C.Z.; Cária, N.Z.; Victoriano, G.; Silva, W.F., Jr.; Magalhães, J.C. Phytotherapy: An introduction to its history, use and application. Rev. Bras. Plantas Med. 2014, 16, 290–298. [Google Scholar] [CrossRef]
- Moghaddam, S.; Kermanshahi, H.; Vahed, R.; Nasiri Moghaddam, H. The protective effects of marigold (Calendula officinalis) extract in liver damage by CCl4 in broiler chicken. Vet. Res. Biol. Prod. 2015, 28, 60–69. [Google Scholar] [CrossRef]
- Lagarto, A.; Bueno, V.; Guerra, I.; Valdés, O.; Vega, Y.; Torres, L. Acute and subchronic oral toxicities of Calendula officinalis extract in Wistar rats. Exp. Toxicol. Pathol. 2011, 63, 387–391. [Google Scholar] [CrossRef]
- Strychalski, J.; Gugołek, A.; Antoszkiewicz, Z.; Fopp-Bayat, D.; Kaczorek-Łukowska, E.; Snarska, A.; Zwierzchowski, G.; Król-Grzymała, A.; Matusevičius, P. The Effect of the BCO2 Genotype on the Expression of Genes Related to Carotenoid, Retinol, and α-Tocopherol Metabolism in Rabbits Fed a Diet with Aztec Marigold Flower Extract. Int. J. Mol. Sci. 2022, 23, 10552. [Google Scholar] [CrossRef] [PubMed]
- Sagar, R.; Sahoo, H.B.; Kar, B.; Mishra, N.K.; Mohapatra, R.; Sarangi, S.P. Pharmacological evaluation of Calendula officinalis L. on bronchial asthma in various experimental animals. Int. J. Nutr. Pharmacol. Neurol. Dis. 2014, 4, 95–103. [Google Scholar] [CrossRef]
- Leffa, D.D.; da Rosa, R.; Munhoz, B.P.; Mello, A.D.A.M.; Mandelli, F.D.; Amaral, P.d.A.; Rossatto, Â.E.; de Andrade, V.M. Genotoxic and antigenotoxic properties of Calendula officinalis extracts in mice treated with methyl methanesulfonate. Adv. Life Sci. 2012, 2, 21–28. [Google Scholar] [CrossRef]
- Silva, E.J.; Gonçalves, E.S.; Aguiar, F.; Evêncio, L.B.; Lyra, M.M.; Coelho, M.C.O.C.; Fraga, M.d.C.C.A.; Wanderley, A.G. Toxicological studies on hydroalcohol extract of Calendula officinalis L. Phytother. Res. Int. J. Devoted Pharmacol. Toxicol. Eval. Nat. Prod. Deriv. 2007, 21, 332–336. [Google Scholar] [CrossRef] [PubMed]
- Gol’dman, I.I. Anaphylactic shock after gargling with an infusion of Calendula. Klin. Meditsina 1974, 52, 142–143. [Google Scholar]
- Patil, K.; Sanjay, C.J.; Doggalli, N.; Devi, K.R.; Harshitha, N. A Review of Calendula officinalis—Magic in Science. J. Clin. Diagn. Res. 2022, 16, ZE23–ZE27. [Google Scholar] [CrossRef]
- Montazeri, S.; Jafari, M.; Khojasteh, S. The effect of powder and essential oil of savory medicinal plant me (Satureja hortensis) on performance and antioxidant status of broiler chicks under heat stress. Iran. J. Appl. Anim. Sci. 2014, 4, 573–577. [Google Scholar]
- Uslu, C.; Karasen, R.M.; Sahin, F.; Taysi, S.; Akcay, F. Effects of aqueous extracts of Satureja hortensis L. on rhinosinusitis treatment in rabbit. J. Ethnopharmacol. 2013, 88, 225–228. [Google Scholar] [CrossRef]
- Shanaida, M.I.; Oleshchuk, O.M. Acute toxicity determination of summer savory liquid extract. Ukr. Biopharm. J. 2017, 4, 22–26. [Google Scholar] [CrossRef]
- Movahhedkhah, S.; Rasouli, B.; Seidavi, A.; Mazzei, D.; Laudadio, V.; Tufarelli, V. Summer savory (Satureja hortensis L.) extract as natural feed additive in broilers: Effects on growth, plasma constituents, immune response, and ileal microflora. Animals 2019, 9, 87. [Google Scholar] [CrossRef]
- Rastegarpanah, M.; Omidzohour, N.; Vahedi, H.; Malekzadeh, R. Management of Human Ulcerative Colitis by Saturex”: A Randomized Controlled Trial. Int. J. Pharmacol. 2011, 37, 3. [Google Scholar]
- Liu, G.; Wu, C.; Song, H.; Wei, S.; Xu, M.; Lin, R.; Zhao, G.; Huang, S.; Zhu, X. Comparative analyses of the complete mitochondrial genomes of Ascaris lumbricoides and Ascaris suum from humans and pigs. Gene 2012, 492, 110–116. [Google Scholar] [CrossRef] [PubMed]
- Thamsborg, S.M.; Nejsum, P.; Mejer, H. Chapter 14. Impact of Ascaris suum in livestock. In Ascaris: The Neglected Parasite; Holland, C., Ed.; Elsevier: Amsterdam, The Netherlands, 2013; pp. 363–381. [Google Scholar] [CrossRef]
- Pettersson, E.; Halvarsson, P.; Sjölund, M.; Grandi, G.; Wallgren, P.; Höglund, J. First report on reduced efficacy of ivermectin on Oesophagostomum spp. on Swedish pig farms. Vet. Parasitol. Reg. Stud. Rep. 2021, 25, 100598. [Google Scholar] [CrossRef] [PubMed]
- Li, R.W.; Wu, S.; Li, W.; Navarro, K.; Couch, R.D.; Hill, D.; Urban, J.F., Jr. Alterations in the porcine colon microbiota induced by the gastrointestinal nematode Trichuris suis. Infect. Immun. 2012, 80, 2150–2157. [Google Scholar] [CrossRef]
- Symeonidou, I.; Tassis, P.; Gelasakis, A.Ι.; Tzika, E.D.; Papadopoulos, E. Prevalence and risk factors of intestinal parasite infections in Greek swine farrow-to-finish farms. Pathogens 2020, 9, 556. [Google Scholar] [CrossRef] [PubMed]
- Giarratana, F.; Nalbone, L.; Napoli, E.; Lanzo, V.; Panebianco, A. Prevalence of Balantidium coli (Malmsten, 1857) infection in swine reared in South Italy: A widespread neglected zoonosis. Vet. World 2021, 14, 1044. [Google Scholar] [CrossRef] [PubMed]
- Sharma, D.; Singh, N.K.; Singh, H.; Joachim, A.; Rath, S.S.; Blake, D.P. Discrimination, molecular characterisation and phylogenetic comparison of porcine Eimeria spp. in India. Vet. Parasitol. 2018, 255, 43–48. [Google Scholar] [CrossRef] [PubMed]
- Cernea, C.; Cernea, M.; Ognean, L.; Trîncă, S. The effect of certain essential oils on laboratory mice intestinal protozoa. Bull. Univ. Agric. Sci. Vet. Med. Cluj Napoca 2008, 65, 281–284. [Google Scholar]
- Doligalska, M.; Joźwicka, K.; Laskowska, M.; Donskow-Łysoniewska, K.; Pączkowski, C.; Janiszowska, W. Changes in Heligmosomoides polygyrus glycoprotein pattern by saponins impact the BALB/c mice immune response. Exp. Parasitol. 2013, 135, 524–531. [Google Scholar] [CrossRef]
- Nikmehr, B.; Ghaznavi, H.; Rahbar, A.; Sadr, S.; Mehrzadi, S. In vitro anti-leishmanial activity of methanolic extracts of Calendula officinalis flowers, Datura stramonium seeds, and Salvia officinalis leaves. Chin. J. Nat. Med. 2014, 12, 423–427. [Google Scholar] [CrossRef]
- Ali Ahmad, N. The effect of Marigold flower extracts on growth of Leishmania. Kirkuk J. Sci. 2018, 13, 34–42. [Google Scholar] [CrossRef]
- Alexenizer, M.; Dorn, A. Screening of medicinal and ornamental plants for insecticidal and growth regulating activity. J. Pest. Sci. 2007, 80, 205–215. [Google Scholar] [CrossRef]
- Godara, R.; Katoch, R.; Yadav, A.; Ahanger, R.R.; Bhutyal, A.D.S.; Verma, P.K.; Katoch, M.; Dutta, S.; Nisa, F. In vitro acaricidal activity of ethanolic and aqueous floral extracts of Calendula officinalis against synthetic pyrethroid resistant Rhipicephalus (Boophilus) microplus. Exp. Appl. Acarol. 2015, 67, 147–157. [Google Scholar] [CrossRef] [PubMed]
- Singh, S.K.; Dimri, U. Amelioration of sarcoptic mange-induced oxidative stress and apoptosis in dogs by using Calendula officinalis flower extracts. Int. Sch. Res. Not. 2013, 2013, 657672. [Google Scholar] [CrossRef]
- Nogareda, C.; Moreno, J.A.; Angulo, E.; Sandmann, G.; Portero, M.; Capell, T.; Christou, P. Carotenoid-enriched transgenic corn delivers bioavailable carotenoids to poultry and protects them against coccidiosis. Plant Biotechnol. J. 2016, 14, 160–168. [Google Scholar] [CrossRef] [PubMed]
- Fabbri, J.; Maggiore, M.A.; Pensel, P.E.; Denegri, G.M.; Gende, L.B.; Elissondo, M.C. In vitro and in vivo efficacy of carvacrol against Echinococcus granulosus. Acta Trop. 2016, 164, 272–279. [Google Scholar] [CrossRef] [PubMed]
- Soosaraei, M.; Fakhar, M.; Teshnizi, S.H.; Hezarjaribi, H.Z.; Banimostafavi, E.S. Medicinal plants with promising antileishmanial activity in Iran: A systematic review and meta-analysis. Ann. Med. Surg. 2017, 21, 63–80. [Google Scholar] [CrossRef] [PubMed]
- Van Baren, C.; Anao, I.; Lira, P.D.L.; Debenedetti, S.; Houghton, P.; Croft, S.; Martino, V. Triterpenic acids and flavonoids from Satureja parvifolia. Evaluation of their antiprotozoal activity. Z. Naturforsch. C 2006, 61, 189–192. [Google Scholar] [CrossRef]
- Davoodi, J.; Abbasi Maleki, S. Comparison anti-giardia activity of Satureja hortensis alcoholic extract and metronidazole in vitro. Adv. Herb. Med. 2016, 2, 15–21. [Google Scholar]
- Tariku, Y.; Hymete, A.; Hailu, A.; Rohloff, J. Essential-oil composition, antileishmanial, and toxicity study of Artemisia abyssinica and Satureja punctata ssp. punctata from Ethiopia. Chem. Biodivers. 2010, 7, 1009–1018. [Google Scholar] [CrossRef]
- Arbabi, M.; Fakhrieh-Kashan, Z.; Delavari, M.; Taghizadeh, M.; Hooshyar, H. The effect of alcoholic extracts of Arctium lappa L. and Satureja hortensis L. against Trichomonas vaginalis in vitro. Feyz. Med. Sci. J. 2017, 21, 298–304. [Google Scholar]
- Sülsen, V.; Güida, C.; Coussio, J.; Paveto, C.; Muschietti, L.; Martino, V. In vitro evaluation of trypanocidal activity in plants used in Argentine traditional medicine. Parasitol. Res. 2006, 98, 370–374. [Google Scholar] [CrossRef] [PubMed]
- Malatyali, E.; Tepe, B.; Degerli, S.E.R.P.İ.L.; Berk, S. In vitro amoebicidal activities of Satureja cuneifolia and Melissa officinalis on Acanthamoeba castellanii cysts and trophozoites. Parasitol. Res. 2012, 110, 2175–2180. [Google Scholar] [CrossRef] [PubMed]
- Tepe, B. Inhibitory Effect of Satureja on Certain Types of Organisms. Rec. Nat. Prod. 2015, 9, 1–18. [Google Scholar]
- Urban, J.; Kokoska, L.; Langrova, I.; Matejkova, J. In vitro anthelmintic effects of medicinal plants used in Czech Republic. Pharm. Biol. 2008, 46, 808–813. [Google Scholar] [CrossRef]
- Trailović, S.M.; Marjanović, D.S.; Nedeljković Trailović, J.; Robertson, A.P.; Martin, R.J. Interaction of carvacrol with the Ascaris suum nicotinic acetylcholine receptors and gamma-aminobutyric acid receptors, potential mechanism of antinematodal action. Parasitol. Res. 2015, 114, 3059–3068. [Google Scholar] [CrossRef] [PubMed]
- Dimah, A.S. Egg Hatching Protocol and an In Vitro Scoring System in Parascaris univalens Larvae after Exposure to Anthelmintic Drugs. Master’s Thesis, Uppsala University, Uppsala, Sweden, 2020. [Google Scholar]
- Trailovic, S.M.; Rajkovic, M.; Marjanovic, D.S.; Neveu, C.; Charvet, C.L. Action of carvacrol on Parascaris sp. and antagonistic effect on nicotinic acetylcholine receptors. Pharmaceuticals 2021, 14, 505. [Google Scholar] [CrossRef]
- Mirza, Z.; Soto, E.R.; Hu, Y.; Nguyen, T.T.; Koch, D.; Aroian, R.V.; Ostroff, G.R. Anthelmintic activity of yeast particle-encapsulated terpenes. Molecules 2020, 25, 2958. [Google Scholar] [CrossRef]
- Felici, M.; Tugnoli, B.; Ghiselli, F.; Massi, P.; Tosi, G.; Fiorentini, L.; Grilli, E. In vitro anticoccidial activity of thymol, carvacrol, and saponins. Poult. Sci. 2020, 99, 5350–5355. [Google Scholar] [CrossRef]
- Remmal, A.; Achahbar, S.; Bouddine, L.; Chami, F.; Chami, N. Oocysticidal effect of essential oil components against chicken Eimeria oocysts. Int. J. Vet. Med. 2013, 2, 133–139. [Google Scholar] [CrossRef]
- Teichmann, K.; Kostelbauer, A.; Steiner, T.; Giannenas, I.; Tontis, D.; Papadopoulos, E.; Schatzmayr, G. Phytogenics to Prevent Chicken Coccidiosis. Planta Med. 2012, 78, PF72. [Google Scholar] [CrossRef]
- Gaur, S.; Kuhlenschmidt, T.B.; Kuhlenschmidt, M.S.; Andrade, J.E. Effect of oregano essential oil and carvacrol on Cryptosporidium parvum infectivity in HCT-8 cells. Parasitol. Int. 2018, 67, 170–175. [Google Scholar] [CrossRef] [PubMed]
- Dominguez-Uscanga, A.; Aycart, D.F.; Li, K.; Witola, W.H.; Laborde, J.E.A. Anti-protozoal activity of Thymol and a Thymol ester against Cryptosporidium parvum in cell culture. Int. J. Parasitol. Drugs Drug Resist. 2021, 15, 126–133. [Google Scholar] [CrossRef] [PubMed]
- Sennouni, C.I.; Oukouia, M.; Jabeur, I.; Hamdani, H.; Chami, F.; Remmal, A. In vitro and in vivo study of the antiparasitic effect of thymol on poultry drinking water. Acta Sci. Biol. Sci. 2022, 44, e58571. [Google Scholar] [CrossRef]
- Tanghort, M.; Chefchaou, H.; Mzabi, A.; Moussa, H.; Chami, N.; Chami, F.; Remmal, A. Oocysticidal Effect of Essential Oils (EOs) and Their Major Components on Cryptosporidium baileyi and Cryptosporidium galli. Int. J. Poult. Sci. 2019, 18, 475–482. [Google Scholar] [CrossRef]
- Andre, W.P.P.; Cavalcante, G.S.; Ribeiro, W.L.C.; Dos Santos, J.M.L.; Macedo, I.T.F.; De Paula, H.C.B.; De Morais, S.M.; De Melo, J.V.; Bevilaqua, C.M.L. Anthelmintic Effect of Thymol and Thymol Acetate on Sheep Gastrointestinal Nematodes and Their Toxicity in Mice. Rev. Bras. Parasitol. Vet. 2017, 26, 323–330. [Google Scholar] [CrossRef]
- Štrbac, F.; Bosco, A.; Maurelli, M.P.; Ratajac, R.; Stojanović, D.; Simin, N.; Orčić, D.; Pušić, I.; Krnjajić, S.; Sotiraki, S.; et al. Anthelmintic properties of essential oils to control gastrointestinal nematodes in sheep—In vitro and in vivo studies. Vet. Sci. 2022, 9, 93. [Google Scholar] [CrossRef]
Feed | Summer Savory Group | Marigold Group | ||||
---|---|---|---|---|---|---|
Sows | Fatteners | Weaners | Sows | Fatteners | Weaners | |
Calcium carbonate % | 1.4 | 1.4 | 1.4 | 1.4 | 1.4 | 1.4 |
Peas % | 15 | 15 | 10 | 15 | 15 | 10 |
Wheat % | 25 | 25 | 20 | 25 | 25 | 20 |
Barley % | 20 | 12 | 30 | 20 | 12 | 30 |
Corn % | 38.20 | 46.36 | 38.43 | 38.04 | 46.27 | 38.36 |
Aerial parts of S. hortensis % | 0.40 | 0.24 | 0.17 | - | - | - |
Aerial parts of C. officinalis % | - | - | - | 0.56 | 0.33 | 0.24 |
Parasite | C. officinalis (14) | C. officinalis (28) | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
Weaners | Fatteners | Sows | Weaners | Fatteners | Sows | |||||||
F1 | F2 | F1 | F2 | F1 | F2 | F1 | F2 | F1 | F2 | F1 | F2 | |
A. suum | - | - | 15.2 | 10.3 | - | 49.9 | - | - | 54.2 | 34.9 | - | 79.9 |
T. suis | - | - | - | 8.2 | - | - | - | - | - | 20.3 | - | - |
Oesophagostomum spp. | - | 60.5 | - | - | - | 28.6 | - | 32.9 | - | - | - | 45.8 |
Eimeria spp. | 91.8 | 42.5 | 95.5 | 75.9 | - | 74.9 | 72.5 | 57.1 | 88.9 | 30.0 | - | 76.5 |
B. coli | 72.0 | 90.9 | 73.1 | 53.6 | 84.9 | 69.8 | 74.7 | 69.2 | 58.3 | 61.1 | 76.1 | 58.2 |
Parasite | S. hortensis (14) | S. hortensis (28) | ||||||||||
Weaners | Fatteners | Sows | Weaners | Fatteners | Sows | |||||||
F1 | F2 | F1 | F2 | F1 | F2 | F1 | F2 | F1 | F2 | F1 | F2 | |
A. suum | - | - | 70.8 | 77.1 | 91.1 | 88.7 | - | - | 77.1 | 81.2 | 72.1 | 59.7 |
T. suis | - | - | 80.5 | 84.0 | - | - | - | - | 90.3 | 87.1 | - | - |
Oesophagostomum spp. | - | - | - | - | 80.2 | 69.2 | - | - | - | - | 100 | 83.7 |
Eimeria spp. | 78.2 | 68.7 | 76.3 | 89.7 | 25.1 | 70.3 | 66.8 | 80.3 | 46.8 | 83.8 | 80.9 | 94.1 |
B. coli | 80.1 | 88.4 | 63.5 | 74.7 | 70.2 | 70.5 | 83.6 | 86.5 | 72.2 | 71.2 | 70.7 | 74.6 |
Parasite | Bioactive Compound/ Extract | Evaluation | Antiparasitic Activity | References |
---|---|---|---|---|
A. suum | ethanolic extract | in vitro | ovicidal and development eggs inhibition | [91] |
A. suum | a-pinene/p-cymene/ thymol octanoate | in vivo | reduction of total worm counts, female worm counts, fecal egg counts, and worm volume | [52] |
A. suum | carvacrol | in vitro | inhibitory effect on the contractions induced by acetylcholine | [92] |
Parascaris univalens | carvacrol | in vitro | paralytic and lethal effects on L3 stage larvae | [93] |
Parascaris spp. | carvacrol | in vitro | fully and irreversibly abolished adult parasite muscle contractions | [94] |
Trichuris muris | thymol | in vitro | inhibition of the motility of the adult worms | [95] |
Eimeria spp. | thymol/carvacrol/ saponins | in vitro | decreasing the effectiveness of Eimeria sporozoites to invade bovine cells | [96] |
Eimeria spp. | carvacrol/thymol | in vitro | destruction of oocysts | [97] |
Eimeria spp | thymol | in vivo | reducing oocysts shedding and intestinal lesions | [98] |
Cryptosporidium parvum | carvacrol/thymol/thymol octanoate | in vitro | inhibition of parasitic invasion and infection of human cells | [99,100] |
Cryptosporidium | thymol | in vivo | reduces the pathogen parasitic load | [101] |
Cryptosporidium baileyi/Cryptosporidium galli | thymol | in vitro | destructive effect on oocysts at very low concentrations | [102] |
Haemonchus contortus/Trichostrongylus/Teladorsagia/Chabertia | thymol/carvacrol/p-cymene/terpinene | in vitro/in vivo | inhibition of egg hatching/larval development and larval motility/reduction of fecal eggs count | [7,103,104] |
Trichostrongylus colubriformis | ethanolic extract | in vitro | migration inhibition of the infective third-stage larvae | [91] |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Băieş, M.-H.; Cotuţiu, V.-D.; Spînu, M.; Mathe, A.; Cozma-Petruț, A.; Bocǎneţ, V.I.; Cozma, V. Satureja hortensis L. and Calendula officinalis L., Two Romanian Plants, with In Vivo Antiparasitic Potential against Digestive Parasites of Swine. Microorganisms 2023, 11, 2980. https://doi.org/10.3390/microorganisms11122980
Băieş M-H, Cotuţiu V-D, Spînu M, Mathe A, Cozma-Petruț A, Bocǎneţ VI, Cozma V. Satureja hortensis L. and Calendula officinalis L., Two Romanian Plants, with In Vivo Antiparasitic Potential against Digestive Parasites of Swine. Microorganisms. 2023; 11(12):2980. https://doi.org/10.3390/microorganisms11122980
Chicago/Turabian StyleBăieş, Mihai-Horia, Vlad-Dan Cotuţiu, Marina Spînu, Attila Mathe, Anamaria Cozma-Petruț, Vlad I. Bocǎneţ, and Vasile Cozma. 2023. "Satureja hortensis L. and Calendula officinalis L., Two Romanian Plants, with In Vivo Antiparasitic Potential against Digestive Parasites of Swine" Microorganisms 11, no. 12: 2980. https://doi.org/10.3390/microorganisms11122980