PLANT BIOLOGY
ANIMAL BIOLOGY
SUBSCRIPTION
E-SUBSCRIPTION
 
MAP
MAIN PAGE

 

 

 

 

Semenova A.A., Kuznetsova T.G., Pchelkina V.A.. Nasonova V.V, Loskutov S.I., Bogolyubova N.V., Nekraso R.V. Effect of adaptogens on muscle tissue microstructure of hybrid pigs (Sus scrofa domesticus L.) during intensive fattening Sel'skokhozyaistvennaya Biologiya [Agricultural Biology], 2023, Vol. 58, № 2, p. 355-372.
(how to cite this article)

doi: 10.15389/agrobiology.2023.2.355eng

UDC: 636.4:591.473.31:59.086

Acknowledgements:
Supported financially by Russian Science Foundation, project No. 19-16-00068-П

 

EFFECT OF ADAPTOGENS ON MUSCLE TISSUE MICROSTRUCTURE OF HYBRID PIGS (Sus scrofa domesticus L.) DURING INTENSIVE FATTENING

A.A. Semenova1, T.G. Kuznetsova1, V.A. Pchelkina1, V.V. Nasonova1,
S.I. Loskutov1, N.V. Bogolyubova2, R.V. Nekrasov2 ✉
1Gorbatov Federal Research Center for Food Systems, 26, ul. Talalikhina, Moscow,109316 Russia, e-mail a.semenova@fncps.ru, labsens@mail.ru, v.pchelkina@fncps.ru, v.nasonova@fncps.ru, spbsl21@gmail.com;
2Ernst Federal Research Center for Animal Husbandry, 60, pos. Dubrovitsy, Podolsk District, Moscow Province, 142132 Russia, e-mail nek_roman@mail.ru (✉ corresponding author), 652202@mail.ru

ORCID:
Semenova A.A. orcid.org/0000-0002-4372-6448
Loskutov S.I.orcid.org/0000-0002-8102-2900
Kuznetsova T.G. orcid.org/0000-0002-5164-1807
Bogolyubova N.V. orcid.org/0000-0002-0520-7022
Phelkina V.A. orcid.org/0000-0001-8923-8661
Nekrasov R.V. orcid.org/0000-0003-4242-2239
Nasonova V.V. orcid.org/0000-0001-7625-3838

Final revision received August 25, 2022
Accepted October 10, 2022

At present, improving the quality of pork while increasing the production of pork is of generally recognized economic importance. Diets have been shown to affect the characteristics of muscle fibers. Adaptogens (vitamins and bioflavonoids) that animals need during active growth period can prevent myopathic transformation in meat. This paper for the first time reports on the improved microstructure of the musculus longissimus dorsi in crossbred pigs fed a complex of adaptogens (dihydroquercetin and vitamins E, C) during the fattening period. Our aim was to evaluate the effect of the complex of dihydroquercetin + vitamins E, C on the microstructure of meat muscle tissue in hybrid pigs. The experiments were carried out in 2021-2022 at Gorbatov Federal Research Center of Food Systems, Ernst Federal Research Center for Animal Husbandry and BMPK (Bryansk Province). Crossbred piglets (n = 108) (Sus scrofa domesticus) F2 [(Large White × Landrace) × Duroc] were randomly selected and assigned to two groups, n = 54 each, for a 58-day fattening. The control group were fed only a complex feed (SK-6, Russia), The test group was additionally fed an experimental dietary complex of adaptogens (DEC) that contains dihydroquercetin (DHQ, Ecostimul-2, JSC Ametis, Russia; 72-73 % DHQ, 32 mg/kg of feed), vitamin E (INNOVIT E60, GC MEGAMIX, Russia; 10 mg/kg feed) and vitamin C (Tiger C 35, Anhui Tiger Biotech Co. Ltd., China; 35 mg/kg feed). Young animals were weighed twice (on day 0 and day 58) by group weighing and individual weighing of 10 animals from each group. After slaughter, the paired carcass weight and the slaughter yield were assessed. To study the microstructure of muscle tissue, 45 min after slaughter, samples (3×3×3 cm) of the longest back muscle (musculus longissimus dorsi) were collected and fixed in 10 % neutral buffered formalin solution for 72 h at room temperature. For further study, two fragments (1.5×1.5×0.5 cm) of each sample with longitudinal and transverse orientations were washed with cold running water for 4 h, then compacted at 37 °C in gelatin (AppliChem GmbH, Germany) of ascending concentrations (12.5 and 25 %, for 8 h in each). Serial 16 µm sections were prepared using a MIKROM-HM525 cryostat (Thermo Scientific, USA), mounted on Menzel-Glaser glasses (Thermo Scientific, USA) and stained with Ehrlich’s hematoxylin and 1 % eosin water-alcohol solution (BioVitrum, Russia). The histological preparations were examined and photographed using an AxioImaiger A1 light microscope (Carl Zeiss, Germany) with a connected AxioCam MRc 5 video camera (Carl Zeiss, Germany). Morphometric studies were performed using the AxioVision 4.7.1.0 image analysis program (Carl Zeiss, Germany). Muscle fiber diameter, sarcomere length, and giant fiber cross-sectional area were measured online. On cross sections, the shape of muscle fibers, their density, the state of the nuclei, the thickness and state of the connective tissue layers were investigated, and giant fibers were identified. On longitudinal sections, the state and shape of muscle fibers, the state of the sarcolemma, the presence of striation (transverse, longitudinal) and destructive changes (ruptures, cracks, fragmentation), hypercontraction nodes were identified. Despite the absence of statistically significant differences in live weight and slaughter traits between groups during fattening, histological studies revealed significant differences in average values of muscle fiber density (p = 0.02) and sarcomere length (p = 0.000007). Almost a 2-fold decrease in the number of giant fibers in test group (11.60 vs. 21.30 pcs/cm2) indicates a significant improvement in the tissue microstructure compared to the control animals that did not receive DEC. The less pronounced destructive changes in the sarcolemma in the test animals also indicate an increase in the animal stress resistance. Given a significant variability of morphometric parameters in both groups, we applied a scoring procedure which allows us to classify carcasses according to the severity of myopathic changes in muscle tissues based on the results of the muscle fiber microstructure study. In control, there was only one carcass that had no signs of myopathy; four carcasses showed signs of moderate myopathy and five carcasses showed signs of severe myopathy. On the contrary, in the test group, there were four carcasses without signs of myopathy and six carcasses with signs of moderate myopathy.There were no cases of severe myopathy in the study group. The groups differed statistically significantly (p = 0.004) in scores characterizing the severity of myopathic changes in muscle tissue. Our findings show that the dietary adaptogen complex DEC can provide the improvement of the microstructure of the muscle tissue and, therefore, has a positive effect on animal stress resistance and the degree of glycolysis in meat.

Keywords: adaptogen, dihydroquercetin, stress, young pigs, muscle tissue, giant fibers, contractile nodes, microstructure, histology.

 

REFERENCES

  1. Komlatskiy G.V. Industrializatsiya i intensifikatsiya otrasli svinovodstva na yuge Rossii. Doktorskaya dissertatsiya [Industrial and intensive technologies of pig ferming in the south of Russia. DSc Thesis]. Cherkessk, 2014 (in Russ.).
  2. Mörlein D., Link C., Werner C., Wicke M. Werner suitability of three commercially produced pig breeds in Germany for a meat quality program with emphasis on drip loss and eating quality. Meat Science, 2002, 77(4): 504-511 CrossRef
  3. Informatsionno-tekhnicheskiy spravochnik po nailuchshim dostupnym tekhnologiyam ITS 41-2017. Intensivnoe razvedenie sviney [Information and technical guide to the best available technologies ITS 41-2017. Intensive breeding of pigs]. Moscow, 2017 (in Russ.).
  4. Petracci M., Cavani S. Muscle growth and poultry meat quality issues. Nutrients, 2012, 4(1): 1-12 CrossRef
  5. Szulc K., Wojtysiak D., Migdał Ł., Migdał W. The muscle fibre characteristics and the meat quality of m. longissimus thoracis from polish native złotnicka spotted pigs and the crossbreed fatteners from the crossing of Duroc and Polish Large White boars. Appl. Sci.,2022, 12(6): 3051 CrossRef
  6. Listrat A., Lebret B., Louveau I., Astruc T., Bonnet M., Lefaucheur L., Bugeon J. Comment la structure et la composition du muscle déterminent la qualité des viands ou chairs. INRAE Productions Animales, 2015, 28(2): 125-136 CrossRef
  7. Vermeulen L., Van de Perre V., Permentier L., De Bie S., Verbeke G., Geers R. Pre-slaughter sound levels and pre-slaughter handling from loading at the farm till slaughter influence pork quality. Meat Science, 2016, 116: 86-90 CrossRef
  8. Scheffler T.L., Gerrard D.E. Mechanisms controlling pork quality development: The biochemistry controlling postmortem energy metabolism. Meat Science, 2007, 77(1): 7-16 CrossRef
  9. Fiedler I., Ender K., Wicke M., Maak S., von Lengerken G., Meyer W. Structural and functional characteristics of muscle fibres in pigs with different malignant hyperthermia susceptibility (MHS) and different meat quality. Meat Science, 1999, 53(1): 9-15 CrossRef
  10. Fiedler I., Dietl G., Rehfeldt C., Wegner J., Ender K. Muscle fibre traits as additional selection criteria for muscle growth and meat quality in pigs — results of a simulated selection. Journal of Animal Breeding and Genetics, 2004, 121(5): 331-344 CrossRef
  11. Brooke M.H., Kaiser K.K. Muscle fiber types: How manyand what kind? Arch. Neurol.,1970, 23: 369-379 CrossRef
  12. Greaser M.L., Okochi H., Sosnicki A.A. Role of fiber types in meat quality. Proc. 47th ICoMST. Cracow, Poland, 2001: 34-37.
  13. Karlsson A.H., Klont R.E., Fernadez X. Skeletal muscle fibres as factors for pork quality. Livestock Production Science, 1999, 60(2-3): 255-269 CrossRef
  14. Cameron N.D., Oksbjerg N., Henckel P. Muscle fibre characteristics of pigs selected for components of efficient lean growth rate. Proceedings of the British Society of Animal Science, 1997: 32 CrossRef
  15. Cameron N.D., Oksbjerg N., Henckel P., Nute G., Brown S., Wood J.D. Relationships between muscle fibre traits with meat and eating quality in pigs. Proceedings of the British Society of Animal Science, 1998: 123 CrossRef
  16. Wegner J., Ender K. Microstructural bases for the growth of muscle and fatty tissue and relation to meat deposit and meat quality. Fleischwirtschaft, 1990, 70: 337-340.
  17. Semenova A.A., Kuznetsova T.G., Nasonova V.V., Nekrasov R.V., Bogolyubova N.V. Myopathy as a destabilizing factor of meat quality formation. Theory and Practice of Meat Processing, 2019, 4(3): 24-31 CrossRef
  18. Ryu Y.C., Choi Y.M., Lee S.H., Shin H.G., Choe J.H., Kim J.M., Hong K.C., Kim B.C. Comparing the histochemical characteristics and meat quality traits of different pig breeds. Meat Science, 2008, 80(2): 363-369 CrossRef
  19. Wojtysiak D., Połtowicz K. Carcass quality, physico-chemical parameters, muscle fibre traits and myosin heavy chain composition of m. longissimus lumborum from Pulawska and Polish Large White pigs. Meat Science, 2014, 97(4): 395-403 CrossRef
  20. Damez J.-L., Clerjon S. Meat quality assessment using biophysical methods related to meat structure. Meat Science, 2008, 80(1): 132-149 CrossRef
  21. Dutson T.R., Merkel R.A., Pearson A.M., Gann G.L. Structural characteristics of porcine skeletal-muscle giant myofibers as observed by light and electron microscopy. Journal of Animal Science, 1978, 46(5): 1212-1220 CrossRef
  22. Sink J.D., Mann O.M., Turgut H. Characterization of the giant myofiber in bovine skeletal muscle. Experimental Cell Biology, 1986, 54(1): 1-7 CrossRef
  23. Sosnicki A. Histopathological observation of stress myopathy in M. longissimus in the pig and relationships with meat quality. fattening and slaughter traits. Journal of Animal Science, 1987, 65(2): 584-596 CrossRef
  24. Schubert-Schoppmeyer A., Fiedler I., Nurnberg G., Jonas L., Ender K., Maak S., Rehfeldt C. Simulation of giant fibre development in biopsy samples from pig longissimus muscle. Meat Science, 2008, 80(4), 1297-1303 CrossRef
  25. Dalle Zotte A., Remignon H., Ouhayoun J. Effect of some biological and zootechnical factors on appearance of giant fibres in the rabbit. Consequences on muscle fibre type, morphology and meat quality. World Rabbit Science, 2001, 9: 1-7 CrossRef
  26. Remignon H., Zanusso J., Albert G., Babilé R. Occurrence of giant myofibres according to muscle type, pre- or post-rigor state and genetic background in turkeys. Meat Science, 2002, 56(4): 337-343 CrossRef
  27. Dalle Zotte A., Tasoniero G., Puolanne E., Remignon H., Cecchinato M., Catelli E., Cullere M. Effect of “Wooden Breast” appearance on poultry meat quality, histological traits, and lesions characterization. Czech J. Anim. Sci., 2017, 62: 51-57 CrossRef
  28. Wojtysiak D., Poltowicz K., Migdal W. Effect of breed and age on histopathological changes in pig m. semimembranosus. Annals of Animal Science, 2012, 12(3): 311-321 CrossRef
  29. Bee G., Biolley C., Guex G., Herzog W., Lonergan S.M., Huff-Lonergan E. Effects of available dietary carbohydrate and preslaughter treatment on glycolytic potential, protein degradation, and quality traits of pig muscles. Journal of Animal Science, 2006, 84(1): 191-203 CrossRef
  30. Küchenmeister U., Nürnberg K., Fiedler I., Kuhn G., Nürnberg G., Ender K. Cell injury and meat quality of Pig in the time period post mortem from two genotypes susceptible or resistant to malignant hyperthermia. European Food Research and Technology, 1999, 209: 97-103 CrossRef
  31. Wojtysiak D., Górska M., Wojciechowska J. Muscle fibre characteristics and physico-chemical parameters of m. semimembranosus from pulawska, Polish Large White and Pietrain pigs. Folia Biologica (Kraków), 2016, 64(3): 197-204 CrossRef
  32. Rey-Salgueiro, L., Martinez-Carballo E., Fajardo P., Chapela M.J., Espiñeira M., Simal-Gandara J. Meat quality in relation to swine well-being after transport and during lairage at the slaughterhouse. Meat Science, 2018, 142: 38-43 CrossRef
  33. Sobczak M., Lachowicz K., Żochowska-Kujawska J. The influence of giant fibres on utility for production of massaged products of porcine muscle longissimus dorsi. Meat Science, 2010, 84: 638-644 CrossRef
  34. Ostrenko K.S., Lemeshevsky V.O., Ovcharova A.N., Galochkina V.P., Sofronova O.V. Effect of adaptogens on the quality of pig meat. Ukrainian Journal of Ecology, 2020, 10(1): 344-348 CrossRef
  35. Kasprzyk A., Bogucka J. Meat quality of Pulawska breed pigs and image of longissimus lumborum muscle microstructure compared to commercial DanBred and Naima hybrids. Arch. Anim. Breed., 2020, 63(2): 293-301 CrossRef
  36. Golovakha V.I., Piddubnyak O.V., Shulyak V.V., Petrenko A.S., Patsenko D.A., Patsenko E.V. Uchenye zapiski uchrezhdeniya obrazovaniya Vitebskaya ordena Znak pocheta gosudarstvennaya akademiya veterinarnoy meditsiny, 2015, 51(1-1): 21-25 (in Russ.).
  37. Bogolyubova N.V., Kuznetsova T.G., Nasonova V.V. i dr. Sposob otsenki kachestva svininy. A.s. 2770804 (RF) S1 MPK G01N 33/12. Federal’noe issledovatel’skiy tsentr zhivotnovodstva -VIZh imeni akademika L.K. Еrnsta" (RF), № 2021123212. Zayavl. 04.08.2021. Opubl. 21.04.2022. Byul. № 12 [Method for assessing the quality of pork. A.s. 2770804 (RF) C1 IPC G01N 33/12. Ernst Federal Research Center for Animal Husbandry (Russian Federation), №. 2021123212. Appl. 08/04/2021. Publ.  04/21/2022. Bull. № 12] (in Russ.).
  38. Joo S.T., Kim G.D., Hwang Y.H., Ryu Y.C. Control of fresh meat quality through manipulation of muscle fiber characteristics. Meat Science, 2013, 95(4): 828-836 CrossRef
  39. Rice D.A. Kennedy S. Vitamin E, selenium, and polyunsaturated fatty acid concentrations and glutathione peroxidase activity in tissues from pigs with dietetic microangiopathy (mulberry heart disease). American Journal of Veterinary Research, 1989, 50(12): 2101-2104.
  40. Li W.J., Zhao G.P., Chen J.L., Zheng M.Q., Wen J. Influence of dietary vitamin E supplementation on meat quality traits and gene expression related to lipid metabolism in the Beijing-you chicken. British Poultry Science, 2009, 50(2): 188-98.1 CrossRef
  41. Semenova A.A., Nasonova V.V., Kuznetsova T.G., Tunieva E.K., Bogolyubova N.V., Nekrasov R.V. Psiii-17 program chair poster pick: a study on the effect of dihydroquercetin added into a diet of growing pigs on meat quality. Journal of Animal Science, 2020, 98(S4): 364 CrossRef
  42. Semenova A.A., Kuznetsova T.G., Nasonova V.V., Nekrasov R.V., Bogolyubova N.V., Tsis E.Yu. Use of antioxidants as adaptogens fed to pigs (Sus scrofa domesticus Erxleben, 1777) (meta-analysis). Sel'skokhozyaistvennayabiologiya[AgriculturalBiology], 2020, 55(6): 1107-1125 CrossRef
  43. Direktiva 2010/63/EC Evropeyskogo parlamenta i Soveta Evropeyskogo soyuza po okhrane zhivotnykh, ispol’zuemykh v nauchnykh tselyakh. St. Petersburg, 2012. Available: https://ruslasa.ru/wp-content/uploads/2017/06/Directive_201063_rus.pdf. No date.
  44. European Convention for the Protection of Vertebrate Animals used for Experimental and other Scientific Purposes (ETS № 123) (Strasburg, 18.03.1986). Available: https://norecopa.no/legislation/council-of-europe-convention-ets-123. Accessed: 20.07.2022.
  45. GOST 33215-2014. Rukovodstvo po soderzhaniyu i ukhodu za laboratornymi zhivotnymi. Pravila oborudovaniya pomeshcheniy i organizatsii protsedur [GOST 33215-2014. Guidelines for the maintenance and care of laboratory animals. Rules for equipping premises and organizing procedures]. Moscow, 2016 (in Russ.).
  46. GOST 33647-2015. Printsipy nadlezhashchey laboratornoy praktiki (GLP). Terminy i opredeleniya [GOST 33647-2015. Principles of good laboratory practice (GLP). Terms and definitions]. Moscow, 2019 (in Russ.).
  47. GOST 33044-2014. Printsipy nadlezhashchey laboratornoy praktiki [GOST 33044-2014. Principles of good laboratory practice]. Moscow, 2019 (in Russ.).
  48. Metodologiya nauchnykh issledovaniy v zhivotnovodstve /Pod redaktsiey V.S. Antonovoy, G.M. Topurii, V.I. Kosilova [Methodology of research in animal husbandry. V.S. Antonova, G.M. Topurii, V.I. Kosilov (eds.)]. Orenburg, 2011 (in Russ.).
  49. Nekrasov R.V., Golovin A.V., Makhaev E.A., Anikin A.S., Pervov N.G., Strekozov N.I., Mysik A.T., Duborezov V.M., Chabaev M.G., Fomichev Yu.P., Gusev I.V. Normy potrebnostey molochnogo skota i sviney v pitatel’nykh veshchestvakh /Pod redaktsiey R.V. Nekrasova, A.V. Golovina, E.A. Makhaeva [Nutrient requirements for dairy cattle and pigs. R.V. Nekrasov, A.V. Golovin, E.A. Makhaev (eds.)]. Moscow, 2018 (in Russ.).
  50. Romeis B. Mikroskopische technic. P. Böck (ed.). Urban und Schwarzenberg, Münche—Wien—Baltimore, 1989 CrossRef
  51. Matematicheskie metody v biologii i еkologii: vvedenie v еlementarnuyu biometriyu /Pod redaktsiey S.I. Sideleva [Mathematical methods in biology and ecology: an introduction to elementary biometrics. S.I. Sidelev (ed.)]. Yarostavl’, 2012 (in Russ.).
  52. Semenova A.A., Nasonova V.V., Kuznetsova T.G., Nekrasov R.V. Provedenie gistologicheskikh issledovaniy po vyyavleniyu miopatii. MR 001-00496254/00419779-2021 [Histological studies to identify myopathy. MP 001-00496254/00419779-2021]. Moscow, 2021 (in Russ.).
  53. Kuttappan V.A., Hargis B.M., Owens C.M. White striping and woody breast myopathies in the modern poultry industry: a review. Poultry Science, 2016, 95(11): 2724-2733 CrossRef
  54. Wojtysiak D. Pathological changes in the microstructure of longissimus lumborum muscle from five breeds of pigs. Folia Biologica, 2012, 60(1-2): 55-60 CrossRef
  55. Pirgozliev V.R., Mansbridge S.C., Westbrook C.A., Woods S.L., Rose S.P., Whiting I.M., Yovchev D.G., Atanasov A.G., Kljak K., Staykova G.P., Ivanova S.G., Karagecili M.R., Karadas F., Stringhini J.H. Feeding dihydroquercetin and vitamin E to broiler chickens reared at standard and high ambient temperatures. Archives of Animal Nutrition, 2020, 74(6): 496-451 CrossRef
  56. Zou Y., Wei H.K., Xiang Q.-H., Wang J., Zhou Y.-F., Peng J. Protective effect of quercetin on pig intestinal integrity after transport stress is associated with regulation oxidative status and inflammation. The Journal of Veterinary Medical Science, 2016, 78(6): 1487-1494 CrossRef
  57. Williamson G., Kay C.D., Crozier A. The bioavailability, transport, and bioactivity of dietary flavonoids: a review from a historical perspective. Comprehensive Reviews in Food Science and Food Safety, 2018, 17(5): 1054-1112 CrossRef
  58. Peeters E. Neyt A., Beckers F., De Smet S., Aubert A.E., Geers R. Influence of supplemental magnesium, tryptophan, vitamin C, and vitamin E on stress responses of pigs to vibration. Journal of Animal Science, 2005, 83(7): 1568-1580 CrossRef
  59. Gao K., Luo Z., Han S., Li Z., Choe H.M., Paek H., Quan B., Kang J., Yin X. Analysis of meat color, meat tenderness and fatty acid composition of meat in second filial hybrid offspring of MSTN mutant pigs. Meat Science, 2022, 193: 108929 CrossRef
  60. Lebedová N., Okrouhlá M., Zadinová K., Čítek J., Stupka R. Muscle fibre composition and meat quality in pigs with different nutrition level. IOP Conference Series: Materials Science and Engineering, 2018, 420: 012078 CrossRef
  61. Lebedová N., Stupka R., Čítek J., Okrouhlá M., Zadinová K. Effect of feed restriction on muscle fibre characteristics and meat quality traits in pigs. Agronomy Research, 2019, 17(1): 176-185 CrossRef
  62. Kim G.-D., Jeong J.-Y., Jung E.-Y., Yang H.-S., Lim H.-T., Joo S.-T. The influence of fiber size distribution of type IIB on carcass traits and meat quality in pigs. Meat Science, 2013, 94(2): 267-273 CrossRef
  63. Weng K., Huo W., Li Y., Zhang Y., Zhang Y., Chen G., Xu Q. Fiber characteristics and meat quality of different muscular tissues from slow- and fast-growing broilers. Poultry Science, 2021, 101(1): 101537 CrossRef
  64. Shen L., Luo J., Lei H., Jiang Y.Z., Bai L., Li M.Z., Tang G., Li X.W., Zhang S.H., Zhu L. Effects of muscle fiber type on glycolytic potential and meat quality traits in different Tibetan pig muscles and their association with glycolysis-related gene expression. Genetics and Molecular Research, 2015, 14(4): 14366-14378 CrossRef

 

back

 


CONTENTS

 

 

Full article PDF (Rus)

Full article PDF (Eng)