Effect of Chlorella on hematological parameters and nutrient bioavailability in the diet of rhesus monkeys (Macaca mulatta)

Chlorella shows a wide spectrum of biological activity, in particular, it exhibits a pronounced antioxidant activity and demonstrates anti-inflammatory, antitumor and antiviral properties. A number of research works have been devoted to studying feed advantages of this unicellular green algae when used in the diets of livestock animals, but the possibility of including different Chlorella species in the diet of primates has not been practically studied. The aim of this work was to assess the possibility of replacing high-protein animal and vegetable feeds with Chlorella, to calculate the digestibility coefficients for the diet nutrients and the effect of algal dry and suspension forms on hematological and serum biochemical parameters in male rhesus monkeys. The data obtained during the experiment indicate that the inclusion of Chlorella in the diet both in the dry form and cell suspension improves nutrient digestibility. Thus, the digestibility of crude protein in the animals receiving algae suspension increased by 4.18% (p < 0.05), that of crude fat – by 4.70% (p < 0.01), crude fiber – by 4.14% (p < 0.05) and crude ash – by 12.32% (p < 0.001). The digestibility coefficients of crude protein in the primates receiving compound feed supplemented with Chlorella powder were higher by 6.83% (p < 0.001), those of crude fiber – by 4.78% (p < 0.05) and crude ash – by 18.93% (p < 0.001) The hematological study results indicate the absence of side effects from long-term Chlorella consumption by primates. The introduction of dry Chlorella into the diet increased blood glucose levels to the upper limit of the control values, while Chlorella suspension did not produce this effect. Thus, Chlorella can be successfully used as a component of a balanced laboratory diet for primates or as a feed additive.

1. Liu J., Chen F. Biology and industrial applications of Chlorella: Advances and prospects. Adv. Biochem. Eng. Biotechnol. 2016; 153: 1–35. DOI: 10.1007/10_2014_286.

2. Safi C., Zebib B., Merah O., Pontalier P.-Y., Vaca-Garcia C. Morphology, composition, production, processing and applications of Chlorella vulgaris: A review. Renew. Sustain. Energy Rev. 2014; 35: 265–278. DOI: 10.1016/j.rser.2014.04.007.

3. Panahi Y., Darvishi B., Jowzi N., Beiraghdar F., Sahebkar A. Chlorella vulgaris: A multifunctional dietary supplement with diverse medicinal properties. Curr. Pharm. Des. 2016; 22 (2): 164–173. DOI: 10.2174/138161 2822666151112145226.

4. Dvoretsky D., Dvoretsky S., Peshkova E., Temnov M. Optimization of the process of cultivation of microalgae Chlorella vulgaris biomass with high lipid content for biofuel production. Chemical Engineering Transactions. 2015; 43: 361–366. DOI: 10.3303/CET1543061.

5. Yang B., Liu J., Jiang Y., Chen F. Chlorella species as hosts for genetic engineering and expression of heterologous proteins: Progress, challenge and perspective. Biotechnol. J. 2016; 11 (10): 1244–1261. DOI: 10.1002/biot.201500617.

6. Shalygo M. Microalgae and cyanobacteria as a bio-fertilizer. Science and Innovations. 2019; 3: 10–12. Available at: https://www.elibrary.ru/download/elibrary_37314804_36473977.pdf. (in Russ.)

7. Bogdanov N. I. Suspenziya khlorelly v ratsione sel’skokhozyaistvennykh zhivotnykh = Chlorella suspension in the diet of livestock animals. Penza: NITs PGU; 2006. 54 p. eLIBRARY ID: 28340038. (in Russ.)

8. Barkia I., Saari N., Manning S. R. Microalgae for high-value products towards human health and nutrition. Mar. Drugs. 2019; 17 (5):304. DOI: 10.3390/md17050304.

9. Lin C.-Y., Huang P.-J., Chao C.-Y. Chlorella protects against hydrogen peroxide-induced pancreatic β-cell damage. J. Med. Food. 2014; 17 (12): 1273–1280. DOI: 10.1089/jmf.2013.3002.

10. Kwak J. H., Baek S. H., Woo Y., Han J. K., Kim B. G., Kim O. Y., Lee J. H. Beneficial immunostimulatory effect of short-term Chlorella supplementation: enhancement of natural killer cell activity and early inflammatory response (randomized, double-blinded, placebo-controlled trial). Nutr. J. 2012; 11:53. DOI: 10.1186/1475-2891-11-53.

11. Azocar J., Diaz A. Efficacy and safety of Chlorella supplementation in adults with chronic hepatitis C virus infection. World J. Gastroenterol. 2013; 19 (7): 1085–1090. DOI: 10.3748/wjg.v19.i7.1085.

12. Takekoshi H., Mizoguchi T., Komasa Y., Chubachi H., Inoue Y., Imanishi H., Nakano M. Suppression of glutathione S-transferase placental form-positive foci development in rat hepatocarcinogenesis by Chlorella pyrenoidosa. Oncol. Rep. 2005; 14 (2): 409–414. DOI: 10.3892/or.14.2.409.

13. Reyna-Martinez R., Gomez-Flores R., López-Chuken U., QuintanillaLicea R., Caballero-Hernandez D., Rodríguez-Padilla C., et al. Antitumor activity of Chlorella sorokiniana and Scenedesmus sp. microalgae native of Nuevo León State, México. Peer J. 2018; 6:e4358. DOI: 10.7717/peerj.4358.

14. Wang X., Zhang X. Separation, antitumor activities, and encapsulation of polypeptide from Chlorella pyrenoidosa. Biotechnol. Prog. 2013; 29 (3): 681–687. DOI: 10.1002/btpr.1725.

15. Nakano S., Takekoshi H., Nakano M. Chlorella (Chlorella pyrenoidosa) supplementation decreases dioxin and increases immunoglobulin a concentrations in breast milk. J. Med. Food. 2007; 10 (1): 134–142. DOI: 10.1089/ jmf.2006.023.

16. Gaponov N. V., Gamko L. N., Lenkova T. N. Determination of the level of bioconversion of nutrients in primates. Bulletin of NSAU (Novosibirsk State Agrarian University). 2020; 4: 65–72. DOI: 10.31677/2072-6724-2020-57-465-72. (in Russ.)

17. Shatskikh E. V., Gafarov Sh. S., Boyarintseva G. G., Safronov S. L. Use of feed additives in animal husbandry. Ekaterinburg: Urals State Agricultural University; 2006. 100 р. eLIBRARY ID: 21222020. (in Russ.)

18. Ovsyannikov A. I. Osnovy opytnogo dela v zhivotnovodstve = Fundamentals of animal experiments. Moscow: Kolos; 1976. 304 p. (in Russ.)

19. National Research Council. Guide for the Care and Use of Laboratory Animals. 8th ed. Washington: National Academies Press; 2011. 246 p. DOI: 10.17226/12910.

20. Rebrova O. Yu. Description of statistical analysis of data in original articles. Typical errors. Zhurnal Nevrologii i Psikhiatrii imeni S. S. Korsakova. 2010; 110 (11): 71–74. eLIBRARY ID: 16597037. (in Russ.)

21. Rukovodstvo dlya vrachei = A guide for doctors. Ed. by N. N. Mamaev. 3rd ed., revised and updated. Saint Petersburg: SpetsLit; 2019. 639 р. (in Russ.)

22. Koo B.-S., Lee D.-H., Kang P., Jeong K. J., Lee S., Kim K., et al. Reference values of hematological and biochemical parameters in young-adult cynomolgus monkey (Macaca fascicularis) and rhesus monkey (Macaca mulatta) anesthetized with ketamine hydrochloride. Lab. Anim. Res. 2019; 35:7. DOI: 10.1186/s42826-019-0006-0.

23. Jeong H., Kwon H. J., Kim M. K. Hypoglycemic effect of Chlorella vulgaris intake in type 2 diabetic Goto-Kakizaki and normal Wistar rats. Nutr. Res. Pract. 2009; 3 (1): 23–30. DOI: 10.4162/nrp.2009.3.1.23.

24. Noguchi N., Konishi F., Kumamoto S., Maruyama I., Ando Y., Yanagita T. Beneficial effects of Chlorella on glucose and lipid metabolism in obese rodents on a high-fat diet. Obes. Res. Clin. Pract. 2013; 7 (2):e95–e105. DOI: 10.1016/j.orcp.2013.01.002.

25. Kholif A. E., Hamdon H. A., Kassab A. Y., Farahat E. S. A., Azzaz H. H., Matloup O. H., et al. Chlorella vulgaris microalgae and/or copper supplementation enhanced feed intake, nutrient digestibility, ruminal fermentation, blood metabolites and lactational performance of Boer goat. J. Anim. Physiol. Anim. Nutr. (Berl.) 2020; 104 (6): 1595–1605. DOI: 10.1111/jpn.13378.

26. Gaponov N. V., Neverova O. P., Gorelik O. V., Stepanov A. V. Probiotics and animal feed in primates feeding. E3S Web of Conferences. International Scientific and Practical Conference “Development of the Agro-lndustrial Complex in the Context of Robotization and Digitalization of Production in Russia and Abroad” (DAIC 2020). 2020; 222:02006. DOI: 10.1051/e3sconf/202022202006.

27. Gaponov N. V., Lenkova T. N. Biotransformation of nutrients in the body of primates. Innovative Scientific Research. 2020; 12-1 (2): 5–14. DOI: 10.5281/zenodo.4444589.