Beta vulgaris Betalains Mitigate Parasitemia and Brain Oxidative Stress Induced by Plasmodium berghei in Mice
Abstract
:1. Introduction
2. Results
2.1. Therapeutic Protocol (Curative Screening)
2.1.1. The Changes in the Parasitemia Level Percentage and Suppression Level
2.1.2. Histopathological Observations of Ions in Brain
2.2. Protective Protocol (Prophylactic Screenings)
2.2.1. The Changes in Parasitemia Level
2.2.2. The Changes in Hematological Parameters
2.2.3. The Changes in Biochemical Assays in Brain Tissues
3. Discussion
4. Materials and Methods
4.1. Experimental Mice
4.2. Chemical Compounds Used
4.3. Antimalarial Activity
4.3.1. Therapeutic Protocol (Curative Screening)
4.3.2. Prophylactic Protocol (Protective Screening)
4.4. Statistical Analysis
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Sabina, K. Prevalence and epidemiology of malaria in Nigeria: A review. Int. J. Res. Pharm. Biosci. 2017, 4, 10–12. [Google Scholar]
- WHO. World Malaria Report; WHO: Geneva, Switzerland, 2021. [Google Scholar]
- Schiess, N.; Villabona-Rueda, A.; Cottier, K.E.; Huether, K.; Chipeta, J.; Stins, M.F. Pathophysiology and neurologic sequelae of cerebral malaria. Malar. J. 2020, 19, 266. [Google Scholar] [CrossRef] [PubMed]
- Garrido-Cardenas, J.A.; Gonzalez-Ceron, L.; Manzano-Agugliaro, F.; Mesa-Valle, C. Plasmodium genomics: An approach for learning about and ending human malaria. Parasitol. Res. 2019, 118, 1–27. [Google Scholar] [CrossRef] [PubMed]
- Sato, S. Plasmodium—A brief introduction to the parasites causing human malaria and their basic biology. J. Physiol. Anthropol. 2021, 40, 1. [Google Scholar] [CrossRef] [PubMed]
- Luzolo, A.L.; Ngoyi, D.M. Cerebral malaria. Brain Res. Bull. 2019, 145, 53–58. [Google Scholar] [CrossRef] [PubMed]
- Ayogu, E.E. Evaluation of Malaria Diagnostic Methods, Efficacy of Artemether-Lumefantrine Therapy and Genetic Determinants of Plasmodium Falciparum Resistance. Ph.D. Thesis, University of Nigeria, Enugu, Nigeria, 2017. [Google Scholar]
- Grau, G.E.; Craig, A.G. Cerebral malaria pathogenesis: Revisiting parasite and host contributions. Future Microbiol. 2012, 7, 291–302. [Google Scholar] [CrossRef]
- Shikani, H.J.; Freeman, B.D.; Lisanti, M.P.; Weiss, L.M.; Tanowitz, H.B.; Desruisseaux, M.S. Cerebral malaria: We have come a long way. Am. J. Pathol. 2012, 181, 1484–1492. [Google Scholar] [CrossRef] [PubMed]
- Hora, R.; Kapoor, P.; Thind, K.K.; Mishra, P.C. Cerebral malaria—Clinical manifestations and pathogenesis. Metab. Brain Dis. 2016, 31, 225–237. [Google Scholar] [CrossRef]
- Dunst, J.; Kamena, F.; Matuschewski, K. Cytokines and Chemokines in Cerebral Malaria Pathogenesis. Front. Cell Infect. Microbiol. 2017, 7, 324. [Google Scholar] [CrossRef]
- Plewes, K.; Turner, G.D.H.; Dondorp, A.M. Pathophysiology, clinical presentation, and treatment of coma and acute kidney injury complicating falciparum malaria. Curr. Opin. Infect. Dis. 2018, 31, 69–77. [Google Scholar] [CrossRef]
- Bruneel, F. Human cerebral malaria: 2019 mini review. Rev. Neurol. 2019, 175, 445–450. [Google Scholar] [CrossRef] [PubMed]
- Milner, D.A., Jr.; Whitten, R.O.; Kamiza, S.; Carr, R.; Liomba, G.; Dzamalala, C.; Seydel, K.B.; Molyneux, M.E.; Taylor, T.E. The systemic pathology of cerebral malaria in African children. Front. Cell. Infect. Microbiol. 2014, 4, 104. [Google Scholar] [CrossRef] [PubMed]
- Isah, M.B.; Ibrahim, M.A. The role of antioxidants treatment on the pathogenesis of malarial infections: A review. Parasitol. Res. 2014, 113, 801–809. [Google Scholar] [CrossRef] [PubMed]
- Ty, M.C.; Zuniga, M.; Gotz, A.; Kayal, S.; Sahu, P.K.; Mohanty, A.; Mohanty, S.; Wassmer, S.C.; Rodriguez, A. Malaria inflammation by xanthine oxidase-produced reactive oxygen species. EMBO Mol. Med. 2019, 11, e9903. [Google Scholar] [CrossRef] [PubMed]
- Ashok, G.R.; Samruddhi, M.; Shreewardhan, R.; Mira, R.; Abhay, C.; Ranjana, D. Influence of MDA and pro-inflammatory cytokine levels in the pathogenesis of severe malaria in experimental murine model. Sch. Acad. J. Biosci. 2016, 4, 617–626. [Google Scholar]
- Srivastava, P.; Puri, S.K.; Dutta, G.P.; Pandey, V.C. Status of oxidative stress and antioxidant defences during Plasmodium knowlesi infection and chloroquine treatment in Macaca mulatta. Int. J. Parasitol. 1992, 22, 243–245. [Google Scholar] [CrossRef] [PubMed]
- Scaccabarozzi, D.; Deroost, K.; Corbett, Y.; Lays, N.; Corsetto, P.; Sale, F.O.; Van den Steen, P.E.; Taramelli, D. Differential induction of malaria liver pathology in mice infected with Plasmodium chabaudi AS or Plasmodium berghei NK65. Malar. J. 2018, 17, 18. [Google Scholar] [CrossRef]
- Martins, Y.C.; Freeman, B.D.; Akide Ndunge, O.B.; Weiss, L.M.; Tanowitz, H.B.; Desruisseaux, M.S. Endothelin-1 Treatment Induces an Experimental Cerebral Malaria-Like Syndrome in C57BL/6 Mice Infected with Plasmodium berghei NK65. Am. J. Pathol. 2016, 186, 2957–2969. [Google Scholar] [CrossRef]
- Albohiri, H.H.; Al-Zanbagi, N.A.; Albohairi, S.H. In vivo trials of potential antimalarial from Beta vulgaris extracts in Jeddah, Saudi Arabia. World J. Zool. 2016, 11, 86–96. [Google Scholar]
- De Niz, M.; Meibalan, E.; Mejia, P.; Ma, S.; Brancucci, N.M.B.; Agop-Nersesian, C.; Mandt, R.; Ngotho, P.; Hughes, K.R.; Waters, A.P. Plasmodium gametocytes display homing and vascular transmigration in the host bone marrow. Sci. Adv. 2018, 4, eaat3775. [Google Scholar] [CrossRef]
- Chin, E.T.; Leidner, D.; Zhang, Y.; Long, E.; Prince, L.; Schrag, S.J.; Verani, J.R.; Wiegand, R.E.; Alarid-Escudero, F.; Goldhaber-Fiebert, J.D. Effectiveness of COVID-19 vaccines among incarcerated people in California state prisons: A retrospective cohort study. medRxiv 2021, 75, e838–e845. [Google Scholar] [CrossRef]
- Ghazanfari, N.; Mueller, S.N.; Heath, W.R. Cerebral Malaria in Mouse and Man. Front. Immunol. 2018, 9, 2016. [Google Scholar] [CrossRef] [PubMed]
- Basir, R.; Rahiman, S.S.F.; Hasballah, K.; Chong, W.C.; Talib, H.; Yam, M.F.; Jabbarzare, M.; Tie, T.H.; Othman, F.; Moklas, M.A.M. Plasmodium berghei ANKA infection in ICR mice as a model of cerebral malaria. Iran. J. Parasitol. 2012, 7, 62. [Google Scholar] [PubMed]
- White, N.J. Antimalarial drug resistance. J. Clin. Investig. 2004, 113, 1084–1092. [Google Scholar] [CrossRef] [PubMed]
- Ouji, M.; Augereau, J.M.; Paloque, L.; Benoit-Vical, F. Plasmodium falciparum resistance to artemisinin-based combination therapies: A sword of Damocles in the path toward malaria elimination. Parasite 2018, 25, 12. [Google Scholar] [CrossRef] [PubMed]
- Akoma, O.N.; Ezeonu, I.M.; Amadi, A.T. Antimalarial Drug Resistance: An Existential Burden for the Developing World. Microbiol. Res. J. Int. 2019, 27, 1–16. [Google Scholar] [CrossRef]
- Adetunji, C.O.; Inobeme, A.; Olaniyan, O.T.; Anani, O.A.; Oloke, J.K.; Palnam, W.D.; Ali, S. Application of biosurfactant for the management of Plasmodium parasites. In Green Sustainable Process for Chemical and Environmental Engineering and Science; Academic Press: Cambridge, MA, USA, 2022; pp. 159–173. [Google Scholar] [CrossRef]
- Manikandan, S.; Mathivanan, A.; Bora, B.; Hemaladkshmi, P.; Abhisubesh, V.; Poopathi, S. A Review on Vector Borne Disease Transmission: Current Strategies of Mosquito Vector Control. Indian J. Entomol. 2022, 85, 503–513. [Google Scholar] [CrossRef]
- Ahmed, N.; Alam, M.; Saeed, M.; Ullah, H.; Iqbal, T.; Awadh Al-Mutairi, K.; Shahjeer, K.; Ullah, R.; Ahmed, S.; Abd Aleem Hassan Ahmed, N.; et al. Botanical Insecticides Are a Non-Toxic Alternative to Conventional Pesticides in the Control of Insects and Pests. In Global Decline of Insects; IntechOpen: Rijeka, Croatia, 2022. [Google Scholar] [CrossRef]
- Gomes, A.R.Q.; Cunha, N.; Varela, E.L.P.; Brigido, H.P.C.; Vale, V.V.; Dolabela, M.F.; De Carvalho, E.P.; Percario, S. Oxidative Stress in Malaria: Potential Benefits of Antioxidant Therapy. Int. J. Mol. Sci. 2022, 23, 5949. [Google Scholar] [CrossRef] [PubMed]
- Jain, N.K.; Singhai, A.K. Protective effects of Chenopodium album (L.) on ethanol—Mediated hepatotoxicity and oxidative stress. Planta Medica 2012, 78, PI445. [Google Scholar] [CrossRef]
- Clifford, T.; Howatson, G.; West, D.J.; Stevenson, E.J. The potential benefits of red beetroot supplementation in health and disease. Nutrients 2015, 7, 2801–2822. [Google Scholar] [CrossRef]
- Lechner, J.F.; Stoner, G.D. Red Beetroot and Betalains as Cancer Chemopreventative Agents. Molecules 2019, 24, 1602. [Google Scholar] [CrossRef] [PubMed]
- Chhikara, N.; Kushwaha, K.; Sharma, P.; Gat, Y.; Panghal, A. Bioactive compounds of beetroot and utilization in food processing industry: A critical review. Food Chem. 2019, 272, 192–200. [Google Scholar] [CrossRef] [PubMed]
- USDA. USDA National Nutrient Database for Standard Reference. 2019. Available online: https://ndb.nal.usda.gov/ndb/foods/show/2849?fg=&man=&lfacet=&format=&count=&max=25&offset=&sort=&qlookup=beet. (accessed on 7 August 2024).
- Munekata, P.E.S.; Pateiro, M.; Dominguez, R.; Pollonio, M.A.R.; Sepulveda, N.; Andres, S.C.; Reyes, J.; Santos, E.M.; Lorenzo, J.M. Beta vulgaris as a Natural Nitrate Source for Meat Products: A Review. Foods 2021, 10, 2094. [Google Scholar] [CrossRef] [PubMed]
- Sadowska-Bartosz, I.; Bartosz, G. Biological Properties and Applications of Betalains. Molecules 2021, 26, 2520. [Google Scholar] [CrossRef] [PubMed]
- Miguel, M.G. Betalains in Some Species of the Amaranthaceae Family: A Review. Antioxidants 2018, 7, 53. [Google Scholar] [CrossRef]
- Vidal, P.J.; Lopez-Nicolas, J.M.; Gandia-Herrero, F.; Garcia-Carmona, F. Inactivation of lipoxygenase and cyclooxygenase by natural betalains and semi-synthetic analogues. Food Chem. 2014, 154, 246–254. [Google Scholar] [CrossRef] [PubMed]
- Vulić, J.J.; Ćebović, T.N.; Čanadanović-Brunet, J.M.; Ćetković, G.S.; Čanadanović, V.M.; Djilas, S.M.; Tumbas Šaponjac, V.T. In vivo and in vitro antioxidant effects of beetroot pomace extracts. J. Funct. Foods 2014, 6, 168–175. [Google Scholar] [CrossRef]
- Chen, C. Pigments in Fruits and Vegetables: Genomics and Dietetics; Springer: Berlin/Heidelberg, Germany, 2015. [Google Scholar]
- Belhadj Slimen, I.; Najar, T.; Abderrabba, M. Chemical and Antioxidant Properties of Betalains. J. Agric. Food Chem. 2017, 65, 675–689. [Google Scholar] [CrossRef] [PubMed]
- Choo, W.S. Betalains: Application in Functional Foods. In Bioactive Molecules in Food; Springer: Berlin/Heidelberg, Germany, 2019; pp. 1471–1498. [Google Scholar] [CrossRef]
- Gengatharan, A.; Dykes, G.A.; Choo, W.S. Fermentation of red pitahaya extracts using Lactobacillus spp. and Saccharomyces cerevisiae for reduction of sugar content and concentration of betacyanin content. J. Food Sci. Technol. 2021, 58, 3611–3621. [Google Scholar] [CrossRef]
- Yong, Y.Y.; Dykes, G.; Lee, S.M.; Choo, W.S. Effect of refrigerated storage on betacyanin composition, antibacterial activity of red pitahaya (Hylocereus polyrhizus) and cytotoxicity evaluation of betacyanin rich extract on normal human cell lines. LWT 2018, 91, 491–497. [Google Scholar] [CrossRef]
- Madadi, E.; Mazloum-Ravasan, S.; Yu, J.S.; Ha, J.W.; Hamishehkar, H.; Kim, K.H. Therapeutic Application of Betalains: A Review. Plants 2020, 9, 1219. [Google Scholar] [CrossRef]
- Hilou, A.; Nacoulma, O.G.; Guiguemde, T.R. In vivo antimalarial activities of extracts from Amaranthus spinosus L. and Boerhaavia erecta L. in mice. J. Ethnopharmacol. 2006, 103, 236–240. [Google Scholar] [CrossRef]
- Nirmal, N.P.; Medhe, S.; Dahal, M.; Koirala, P.; Nirmal, S.; Al-Asmari, F.; Xu, B. Betalains protect various body organs through antioxidant and anti-inflammatory pathways. Food Sci. Hum. Wellness 2024, 13, 1109–1117. [Google Scholar] [CrossRef]
- Rahimi, P.; Abedimanesh, S.; Mesbah-Namin, S.A.; Ostadrahimi, A. Betalains, the nature-inspired pigments, in health and diseases. Crit. Rev. Food Sci. Nutr. 2019, 59, 2949–2978. [Google Scholar] [CrossRef]
- Chang, Y.J.; Pong, L.Y.; Hassan, S.S.; Choo, W.S. Antiviral activity of betacyanins from red pitahaya (Hylocereus polyrhizus) and red spinach (Amaranthus dubius) against dengue virus type 2 (GenBank accession no. MH488959). Access Microbiol. 2020, 2, acmi000073. [Google Scholar] [CrossRef]
- Tenore, G.C.; Novellino, E.; Basile, A. Nutraceutical potential and antioxidant benefits of red pitaya (Hylocereus polyrhizus) extracts. J. Funct. Foods 2012, 4, 129–136. [Google Scholar] [CrossRef]
- Vulić, J.; Čanadanović-Brunet, J.; Ćetković, G.; Tumbas, V.; Djilas, S.; Četojević-Simin, D.; Čanadanović, V. Antioxidant and cell growth activities of beet root pomace extracts. J. Funct. Foods 2012, 4, 670–678. [Google Scholar] [CrossRef]
- Fordjour, P.A.; Adjimani, J.P.; Asare, B.; Duah-Quashie, N.O.; Quashie, N.B. Anti-malarial Activity of Phenolic Acids Is Structurally Related. Res. Square. 2020. [Google Scholar] [CrossRef]
- Martins, Y.C.; Smith, M.J.; Pelajo-Machado, M.; Werneck, G.L.; Lenzi, H.L.; Daniel-Ribeiro, C.T.; Carvalho, L.J. Characterization of cerebral malaria in the outbred Swiss Webster mouse infected by Plasmodium berghei ANKA. Int. J. Exp. Pathol. 2009, 90, 119–130. [Google Scholar] [CrossRef]
- Farahna, M.; Bedri, S.; Khalid, S.; Idris, M.; Pillai, C.R.; Khalil, E.A. Anti-plasmodial effects of Azadirachta indica in experimental cerebral malaria: Apoptosis of cerebellar Purkinje cells of mice as a marker. North Am. J. Med. Sci. 2010, 2, 518. [Google Scholar] [CrossRef]
- Maslachah, L. Sequestration and Histopathological Changes of the Lung, Kidney and Brain of Mice Infected with Plasmodium berghei that Exposed to Repeated Artemisinin. Pak. Vet. J. 2019, 39, 499–504. [Google Scholar] [CrossRef]
- Ngo-Thanh, H.; Sasaki, T.; Suzue, K.; Yokoo, H.; Isoda, K.; Kamitani, W.; Shimokawa, C.; Hisaeda, H.; Imai, T. Blood-cerebrospinal fluid barrier: Another site disrupted during experimental cerebral malaria caused by Plasmodium berghei ANKA. Int. J. Parasitol. 2020, 50, 1167–1175. [Google Scholar] [CrossRef]
- Sarkar, S.; Keswani, T.; Sengupta, A.; Mitra, S.; Bhattacharyya, A. Differential modulation of glial cell mediated neuroinflammation in Plasmodium berghei ANKA infection by TGF beta and IL 6. Cytokine 2017, 99, 249–259. [Google Scholar] [CrossRef]
- Abdulazeez, M.; Adebisi, S.; Musa, S.; Abdullahi, M.; Mudassir, L. Histological Study of Ethanol Leaf Extract of Vernonia amgydalina in Cerebellum of Young Mice Malaria Model. Int. J. Res. Rep. Hematol. 2021, 4, 20–29. [Google Scholar]
- Damilola Asiru, F.; Dauda Shallie, P. Berghei model of gestational is associated with decreased locomotion and increased maternal anxiety. Int. J. Res. Ethics (IJRE) 2022, 5. [Google Scholar] [CrossRef]
- Bedri, S.; Khalil, E.A.; Khalid, S.A.; Alzohairy, M.A.; Mohieldein, A.; Aldebasi, Y.H.; Seke Etet, P.F.; Farahna, M. Azadirachta indica ethanolic extract protects neurons from apoptosis and mitigates brain swelling in experimental cerebral malaria. Malar. J. 2013, 12, 298. [Google Scholar] [CrossRef]
- Anand, K.S.; Dhikav, V. Hippocampus in health and disease: An overview. Ann. Indian Acad. Neurol. 2012, 15, 239–246. [Google Scholar] [CrossRef]
- Ding, Y.; Xu, W.; Zhou, T.; Liu, T.; Zheng, H.; Fu, Y. Establishment of a murine model of cerebral malaria in KunMing mice infected with Plasmodium berghei ANKA. Parasitology 2016, 143, 1672–1680. [Google Scholar] [CrossRef]
- Zhang, Y.P.; Cui, Q.Y.; Zhang, T.M.; Yi, Y.; Nie, J.J.; Xie, G.H.; Wu, J.H. Chloroquine pretreatment attenuates ischemia-reperfusion injury in the brain of ob/ob diabetic mice as well as wildtype mice. Brain Res. 2020, 1726, 146518. [Google Scholar] [CrossRef]
- Lee, C.H.; Wettasinghe, M.; Bolling, B.W.; Ji, L.L.; Parkin, K.L. Betalains, phase II enzyme-inducing components from red beetroot (Beta vulgaris L.) extracts. Nutr. Cancer 2005, 53, 91–103. [Google Scholar] [CrossRef]
- El Gamal, A.A.; AlSaid, M.S.; Raish, M.; Al-Sohaibani, M.; Al-Massarani, S.M.; Ahmad, A.; Hefnawy, M.; Al-Yahya, M.; Basoudan, O.A.; Rafatullah, S. Beetroot (Beta vulgaris L.) extract ameliorates gentamicin-induced nephrotoxicity associated oxidative stress, inflammation, and apoptosis in rodent model. Mediat. Inflamm. 2014, 2014, 983952. [Google Scholar] [CrossRef]
- Moreno-Ley, C.M.; Osorio-Revilla, G.; Hernández-Martínez, D.M.; Ramos-Monroy, O.A.; Gallardo-Velázquez, T. Anti-inflammatory activity of betalains: A comprehensive review. Hum. Nutr. Metab. 2021, 25, 200126. [Google Scholar] [CrossRef]
- Vali, L.; Stefanovits-Banyai, E.; Szentmihalyi, K.; Febel, H.; Sardi, E.; Lugasi, A.; Kocsis, I.; Blazovics, A. Liver-protecting effects of table beet (Beta vulgaris var. rubra) during ischemia-reperfusion. Nutrition 2007, 23, 172–178. [Google Scholar] [CrossRef]
- Wondafrash, D.Z.; Bhoumik, D.; Altaye, B.M.; Tareke, H.B.; Assefa, B.T. Antimalarial Activity of Cordia africana (Lam.) (Boraginaceae) Leaf Extracts and Solvent Fractions in Plasmodium berghei-Infected Mice. Evid. Based Complement. Altern. Med. 2019, 2019, 8324596. [Google Scholar] [CrossRef]
- Alehegn, A.A.; Yesuf, J.S.; Birru, E.M. Antimalarial Activity of Crude Extract and Solvent Fractions of the Leaves of Bersama abyssinica Fresen. (Melianthaceae) against Plasmodium berghei Infection in Swiss Albino Mice. Evid. Based Complement. Altern. Med. 2020, 2020, 9467359. [Google Scholar] [CrossRef]
- Koltas, I.S.; Demirhindi, H.; Hazar, S.; Ozcan, K. Supportive presumptive diagnosis of Plasmodium vivax malaria. Thrombocytopenia and red cell distribution width. Saudi. Med. J. 2007, 28, 535–539. [Google Scholar]
- Lathia, T.B.; Joshi, R. Can hematological parameters discriminate malaria from nonmalarious acute febrile illness in the tropics? Indian J. Med. Sci. 2004, 58, 239–244. [Google Scholar]
- George, I.O.; Ewelike-Ezeani, C.S. Haematological changes in children with malaria infection in Nigeria. J. Med. Sci. 2011, 2, 768–771. [Google Scholar]
- Jairajpuri, Z.S.; Rana, S.; Hassan, M.J.; Nabi, F.; Jetley, S. An Analysis of Hematological Parameters as a Diagnostic test for Malaria in Patients with Acute Febrile Illness: An Institutional Experience. Oman Med. J. 2014, 29, 12–17. [Google Scholar] [CrossRef]
- Onohuean, H.; Alagbonsi, A.I.; Usman, I.M.; Iceland Kasozi, K.; Alexiou, A.; Badr, R.H.; Batiha, G.E.-S.; Ezeonwumelu, J.O.C. Annona muricata linn and Khaya grandifoliola C. DC. Reduce oxidative stress in vitro and ameliorate Plasmodium berghei-induced parasitemia and cytokines in BALB/c mice. J. Evid.-Based Integr. Med. 2021, 26, 2515690–211036669. [Google Scholar] [CrossRef]
- Percario, S.; Moreira, D.R.; Gomes, B.A.; Ferreira, M.E.; Goncalves, A.C.; Laurindo, P.S.; Vilhena, T.C.; Dolabela, M.F.; Green, M.D. Oxidative stress in malaria. Int. J. Mol. Sci. 2012, 13, 16346–16372. [Google Scholar] [CrossRef]
- Reis, P.A.; Comim, C.M.; Hermani, F.; Silva, B.; Barichello, T.; Portella, A.C.; Gomes, F.C.; Sab, I.M.; Frutuoso, V.S.; Oliveira, M.F.; et al. Cognitive dysfunction is sustained after rescue therapy in experimental cerebral malaria, and is reduced by additive antioxidant therapy. PLoS Pathog. 2010, 6, e1000963. [Google Scholar] [CrossRef]
- Al-Shaebi, E.M.; Mohamed, W.F.; Al-Quraishy, S.; Dkhil, M.A. Susceptibility of mice strains to oxidative stress and neurotransmitter activity induced by Plasmodium berghei. Saudi J. Biol. Sci. 2018, 25, 167–170. [Google Scholar] [CrossRef]
- Padin-Irizarry, V.; Colon-Lorenzo, E.E.; Vega-Rodriguez, J.; del, R. Castro, M.; Gonzalez-Mendez, R.; Ayala-Pena, S.; Serrano, A.E. Glutathione-deficient Plasmodium berghei parasites exhibit growth delay and nuclear DNA damage. Free Radic. Biol. Med. 2016, 95, 43–54. [Google Scholar] [CrossRef]
- Khandare, A.V.; Bobade, D.; Deval, M.; Patil, T.; Saha, B.; Prakash, D. Expression of negative immune regulatory molecules, pro-inflammatory chemokine and cytokines in immunopathology of ECM developing mice. Acta Trop. 2017, 172, 58–63. [Google Scholar] [CrossRef]
- Lyke, K.E.; Burges, R.; Cissoko, Y.; Sangare, L.; Dao, M.; Diarra, I.; Kone, A.; Harley, R.; Plowe, C.V.; Doumbo, O.K.; et al. Serum levels of the proinflammatory cytokines interleukin-1 beta (IL-1beta), IL-6, IL-8, IL-10, tumor necrosis factor alpha, and IL-12(p70) in Malian children with severe Plasmodium falciparum malaria and matched uncomplicated malaria or healthy controls. Infect. Immun. 2004, 72, 5630–5637. [Google Scholar] [CrossRef]
- Dobano, C.; Nhabomba, A.J.; Manaca, M.N.; Berthoud, T.; Aguilar, R.; Quinto, L.; Barbosa, A.; Rodriguez, M.H.; Jimenez, A.; Groves, P.L.; et al. A Balanced Proinflammatory and Regulatory Cytokine Signature in Young African Children Is Associated with Lower Risk of Clinical Malaria. Clin. Infect. Dis. 2019, 69, 820–828. [Google Scholar] [CrossRef] [PubMed]
- Pino, P.; Vouldoukis, I.; Kolb, J.P.; Mahmoudi, N.; Desportes-Livage, I.; Bricaire, F.; Danis, M.; Dugas, B.; Mazier, D. Plasmodium falciparum--infected erythrocyte adhesion induces caspase activation and apoptosis in human endothelial cells. J. Infect. Dis. 2003, 187, 1283–1290. [Google Scholar] [CrossRef]
- Keita Alassane, S.; Nicolau-Travers, M.L.; Menard, S.; Andreoletti, O.; Cambus, J.P.; Gaudre, N.; Wlodarczyk, M.; Blanchard, N.; Berry, A.; Abbes, S.; et al. Young Sprague Dawley rats infected by Plasmodium berghei: A relevant experimental model to study cerebral malaria. PLoS ONE 2017, 12, e0181300. [Google Scholar] [CrossRef]
- Schofield, L.; Hackett, F. Signal transduction in host cells by a glycosylphosphatidylinositol toxin of malaria parasites. J. Exp. Med. 1993, 177, 145–153. [Google Scholar] [CrossRef]
- Maitland, K.; Levin, M.; English, M.; Mithwani, S.; Peshu, N.; Marsh, K.; Newton, C.R. Severe, P. falciparum malaria in Kenyan children: Evidence for hypovolaemia. QJM 2003, 96, 427–434. [Google Scholar] [CrossRef] [PubMed]
- Amani, V.; Vigario, A.M.; Belnoue, E.; Marussig, M.; Fonseca, L.; Mazier, D.; Renia, L. Involvement of IFN-gamma receptor-medicated signaling in pathology and anti-malarial immunity induced by Plasmodium berghei infection. Eur. J. Immunol. 2000, 30, 1646–1655. [Google Scholar] [CrossRef]
- Kwiatkowski, D.; Hill, A.V.; Sambou, I.; Twumasi, P.; Castracane, J.; Manogue, K.R.; Cerami, A.; Brewster, D.R.; Greenwood, B.M. TNF concentration in fatal cerebral, non-fatal cerebral, and uncomplicated Plasmodium falciparum malaria. Lancet 1990, 336, 1201–1204. [Google Scholar] [CrossRef]
- Strle, K.; Zhou, J.-H.; Shen, W.-H.; Broussard, S.R.; Johnson, R.W.; Freund, G.G.; Dantzer, R.; Kelley, K.W. lnterleukin-10 in the Brain. Crit. Rev. Immunol. 2001, 21, 23. [Google Scholar] [CrossRef]
- Lopera-Mesa, T.M.; Mita-Mendoza, N.K.; van de Hoef, D.L.; Doumbia, S.; Konate, D.; Doumbouya, M.; Gu, W.; Traore, K.; Diakite, S.A.; Remaley, A.T.; et al. Plasma uric acid levels correlate with inflammation and disease severity in Malian children with Plasmodium falciparum malaria. PLoS ONE 2012, 7, e46424. [Google Scholar] [CrossRef] [PubMed]
- Martinez, R.M.; Hohmann, M.S.; Longhi-Balbinot, D.T.; Zarpelon, A.C.; Baracat, M.M.; Georgetti, S.R.; Vicentini, F.; Sassonia, R.C.; Verri, W.A., Jr.; Casagrande, R. Analgesic activity and mechanism of action of a Beta vulgaris dye enriched in betalains in inflammatory models in mice. Inflammopharmacology 2020, 28, 1663–1675. [Google Scholar] [CrossRef]
- Dai, R.; Wang, Y.; Wang, N. Betalain Alleviates Airway Inflammation in an Ovalbumin-Induced-Asthma Mouse Model via the TGF-beta1/Smad Signaling Pathway. J. Environ. Pathol. Toxicol. Oncol. 2021, 40, 11–21. [Google Scholar] [CrossRef]
- da Silva, D.V.T.; Pereira, A.D.; Boaventura, G.T.; Ribeiro, R.S.A.; Vericimo, M.A.; Carvalho-Pinto, C.E.; Baiao, D.D.S.; Del Aguila, E.M.; Paschoalin, V.M.F. Short-Term Betanin Intake Reduces Oxidative Stress in Wistar Rats. Nutrients 2019, 11, 1978. [Google Scholar] [CrossRef]
- Gao, Y.; Liang, X.; Tian, Z.; Ma, Y.; Sun, C. Betalain exerts cardioprotective and anti-inflammatory effects against the experimental model of heart failure. Hum. Exp. Toxicol. 2021, 40, S16–S28. [Google Scholar] [CrossRef]
- Macias-Ceja, D.C.; Cosin-Roger, J.; Ortiz-Masia, D.; Salvador, P.; Hernandez, C.; Esplugues, J.V.; Calatayud, S.; Barrachina, M.D. Stimulation of autophagy prevents intestinal mucosal inflammation and ameliorates murine colitis. Br. J. Pharmacol. 2017, 174, 2501–2511. [Google Scholar] [CrossRef]
- Albasher, G.; Almeer, R.; Alarifi, S.; Alkhtani, S.; Farhood, M.; Al-Otibi, F.O.; Alkubaisi, N.; Rizwana, H. Nephroprotective Role of Beta vulgaris L. Root Extract against Chlorpyrifos-Induced Renal Injury in Rats. Evid. Based Complement. Altern. Med. 2019, 2019, 3595761. [Google Scholar] [CrossRef]
- Albasher, G.; Albrahim, T.; Alsultan, N.; Alfaraj, S.; Alharthi, M.S.; Kassab, R.B.; Abdel Moneim, A.E. Red beetroot extract mitigates chlorpyrifos-induced reprotoxicity associated with oxidative stress, inflammation, and apoptosis in rats. Environ. Sci. Pollut. Res. Int. 2020, 27, 3979–3991. [Google Scholar] [CrossRef] [PubMed]
- Shunan, D.; Yu, M.; Guan, H.; Zhou, Y. Neuroprotective effect of Betalain against AlCl3-induced Alzheimer’s disease in Sprague Dawley Rats via putative modulation of oxidative stress and nuclear factor kappa B (NF-κB) signaling pathway. Biomed. Pharmacother. 2021, 137, 111369. [Google Scholar] [CrossRef]
- Ahmadi, H.; Nayeri, Z.; Minuchehr, Z.; Sabouni, F.; Mohammadi, M. Betanin purification from red beetroots and evaluation of its anti-oxidant and anti-inflammatory activity on LPS-activated microglial cells. PLoS ONE 2020, 15, e0233088. [Google Scholar] [CrossRef] [PubMed]
- Imamura, T.; Isozumi, N.; Higashimura, Y.; Koga, H.; Segawa, T.; Desaka, N.; Takagi, H.; Matsumoto, K.; Ohki, S.; Mori, M. Red-Beet Betalain Pigments Inhibit Amyloid-beta Aggregation and Toxicity in Amyloid-beta Expressing Caenorhabditis elegans. Plant Foods Hum. Nutr. 2022, 77, 90–97. [Google Scholar] [CrossRef] [PubMed]
- Reddy, M.K.; Alexander-Lindo, R.L.; Nair, M.G. Relative inhibition of lipid peroxidation, cyclooxygenase enzymes, and human tumor cell proliferation by natural food colors. J. Agric. Food Chem. 2005, 53, 9268–9273. [Google Scholar] [CrossRef]
- Martinez, R.M.; Longhi-Balbinot, D.T.; Zarpelon, A.C.; Staurengo-Ferrari, L.; Baracat, M.M.; Georgetti, S.R.; Sassonia, R.C.; Verri, W.A., Jr.; Casagrande, R. Anti-inflammatory activity of betalain-rich dye of Beta vulgaris: Effect on edema, leukocyte recruitment, superoxide anion and cytokine production. Arch. Pharm. Res. 2015, 38, 494–504. [Google Scholar] [CrossRef]
- Rangel-Gomez, M.; Meeter, M. Neurotransmitters and Novelty: A Systematic Review. J. Psychopharmacol. 2016, 30, 3–12. [Google Scholar] [CrossRef] [PubMed]
- Gatkowska, J.; Wieczorek, M.; Dziadek, B.; Dzitko, K.; Dlugonska, H. Sex-dependent neurotransmitter level changes in brains of Toxoplasma gondii infected mice. Exp. Parasitol. 2013, 133, 1–7. [Google Scholar] [CrossRef]
- Bauomy, A. Neuronal activities of berberine in Schistosoma mansoni-infected mice. Afr. J. Pharm. Pharmacol. 2013, 7, 368–374. [Google Scholar] [CrossRef]
- Abdel Ghafar, A.E.; Elkowrany, S.; Salem, S.; Menaisy, A.; Fadel, W.; Awara, W. Effect of some parasitic infection on neurotransmitters in the brain of experimentally infected mice before and after treatment. J. Egypt. Soc. Parasitol. 1996, 26, 497–508. [Google Scholar]
- Clark, I.A.; Rockett, K.A.; Cowden, W.B. Possible central role of nitric oxide in conditions clinically similar to cerebral malaria. Lancet 1992, 340, 894–896. [Google Scholar] [CrossRef] [PubMed]
- Dascombe, M.J.; Sidara, J.Y. The Absence of Fever in Rat Malaria is Associated with Increased Turnover of 5-Hydroxytryptamine in the Brain. In Temperature Regulation; Springer: Berlin/Heidelberg, Germany, 1994; pp. 47–52. [Google Scholar] [CrossRef]
- Roy, S.; Chattopadhyay, R.N.; Maitra, S.K. Changes in brain neurotransmitters in rodent malaria. Indian J. Malariol. 1993, 30, 183–185. [Google Scholar] [PubMed]
- Taylor-Robinson, A.W. Validity of Modelling Cerebral Malaria in Mice: Argument and Counter Argument. J. Neuroparasitology 2010, 1, 45–49. [Google Scholar] [CrossRef]
- Motawi, T.K.; Ahmed, S.A.; El-Boghdady, N.A.; Metwally, N.S.; Nasr, N.N. Protective effects of betanin against paracetamol and diclofenac induced neurotoxicity and endocrine disruption in rats. Biomarkers 2019, 24, 645–651. [Google Scholar] [CrossRef] [PubMed]
- Salimi, A.; Sabur, M.; Dadkhah, M.; Shabani, M. Inhibition of scopolamine-induced memory and mitochondrial impairment by betanin. J. Biochem. Mol. Toxicol. 2022, 36, e23076. [Google Scholar] [CrossRef]
- Thong-Asa, W.; Prasartsri, S.; Klomkleaw, N.; Thongwan, N. The neuroprotective effect of betanin in trimethyltin-induced neurodegeneration in mice. Metab. Brain Dis. 2020, 35, 1395–1405. [Google Scholar] [CrossRef]
- WHO. Malaria Microscopy Quality Assurance Manual, Version 2. 2016. Available online: https://apps.who.int/iris/handle/10665/204266 (accessed on 7 August 2024).
- Rahayu, P.; Hernaningsih, Y.; Arwati, H. Antimalarial Activity of Ethanol Extract of Noni Leaves (Morinda citrifolia) towards Parasitemia, Splenomegaly, and Hepatomegaly in Plasmodium berghei ANKA Infected Mice. Biomol. Health Sci. J. 2021, 4, 5. [Google Scholar] [CrossRef]
- Lelliott, P.M.; Lampkin, S.; McMorran, B.J.; Foote, S.J.; Burgio, G. A flow cytometric assay to quantify invasion of red blood cells by rodent Plasmodium parasites in vivo. Malar J 2014, 13, 100. [Google Scholar] [CrossRef]
- Fu, Y.; Shi, J.; Xie, S.Y.; Zhang, T.Y.; Soladoye, O.P.; Aluko, R.E. Red Beetroot Betalains: Perspectives on Extraction, Processing, and Potential Health Benefits. J. Agric. Food Chem. 2020, 68, 11595–11611. [Google Scholar] [CrossRef]
- Fidock, D.A.; Rosenthal, P.J.; Croft, S.L.; Brun, R.; Nwaka, S. Antimalarial drug discovery: Efficacy models for compound screening. Nat. Rev. Drug Discov. 2004, 3, 509–520. [Google Scholar] [CrossRef] [PubMed]
- Enegide, C.; Akah, P.; Ofili, C.; Agatemor, U.; Ameh, S.; Dabum, J.; Onah, I. Evidence supporting the use of Combretum nigricans as an antimalarial agent in ethnomedicine. Int. J. Curr. Res. Physiol. Pharmacol. (IJCRPP) 2021, 5, 13–20. [Google Scholar] [CrossRef]
- Dunn, W.L. Handbook of Histopathological and Histochemical Techniques; Bun, Ltd.: Redwood, CA, USA, 1974. [Google Scholar]
- Raymond Bess, B.; Germain Sotoing, T.; David Denis Feugaing, S.; Orelien Sylvain Mtopi, B.; Hart Mann Alain Youbi, M.; Seraphin Nji Ombel, M.; Liliane Laure, T.; Helen Kuokuo, K. Prophylactic antimalarial effects of Cymbopogon citratus (DC.) Stapf (Poaceae) in a mouse model of Plasmodium berghei ANKA infection: Normalisation of haematological and serum biochemical status. GSC Biol. Pharm. Sci. 2021, 15, 05–017. [Google Scholar] [CrossRef]
Groups | Parasitemia % | |
---|---|---|
Pre-Treatment | Post-Treatment | |
Group 1 (Negative control group) | 35.40 ± 9.71 | 51.20 ± 12.27 a* |
Group 2 (Chloroquine 5 mg/kg) | 44.20 ± 8.58 | 19.40 ± 12.62 a**b**** |
Group 3 (Betalains 70 mg/kg) | 41.20 ± 15.61 | 17.00 ± 10.41 a**b**** |
Groups | Suppression % |
---|---|
Group 1 (Negative control group) | −47.46 ± 28.67 |
Group 2 (Chloroquine 5 mg/kg) | 59.27 ± 22.64 a**** |
Group 3 (Betalains 70 mg/kg) | 61.72 ± 16.23 a**** |
Groups | Parasitemia and Inhibition% | |||||
---|---|---|---|---|---|---|
Day 2 | In% | Day 4 | In% | Day 6 | In% | |
Group 2 (Negative control group) | 1.00 ± 0.81 | - | 26.00 ± 11.76 | - | 48.16 ± 8.37 | - |
Group 3 (Betalains 70 mg/kg) | 0.45 ± 0.32 | 55 | 18.33 ± 9.20 a* | 29.50 | 24.16 ± 6.11 a**** | 49.82 |
Group 4 (Chloroquine 5 mg/kg) | 0.23 ± 0.15 | 77 | 9.00 ± 5.32 a****b* | 65.38 | 20.00 ± 4.47 a**** | 58.47 |
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Khan, S.A.; Alsulami, M.N.; Alsehimi, A.A.; Alzahrani, M.S.; Mosule, D.A.; Albohiri, H.H. Beta vulgaris Betalains Mitigate Parasitemia and Brain Oxidative Stress Induced by Plasmodium berghei in Mice. Pharmaceuticals 2024, 17, 1064. https://doi.org/10.3390/ph17081064
Khan SA, Alsulami MN, Alsehimi AA, Alzahrani MS, Mosule DA, Albohiri HH. Beta vulgaris Betalains Mitigate Parasitemia and Brain Oxidative Stress Induced by Plasmodium berghei in Mice. Pharmaceuticals. 2024; 17(8):1064. https://doi.org/10.3390/ph17081064
Chicago/Turabian StyleKhan, Samar A., Muslimah N. Alsulami, Atif A. Alsehimi, Majed S. Alzahrani, Dina A. Mosule, and Haleema H. Albohiri. 2024. "Beta vulgaris Betalains Mitigate Parasitemia and Brain Oxidative Stress Induced by Plasmodium berghei in Mice" Pharmaceuticals 17, no. 8: 1064. https://doi.org/10.3390/ph17081064