The Effects of In Ovo Administered Monosodium Glutamate on the Embryonic Development of Skeletal Muscle in Chickens

Year 2023, Volume: 16 Issue: 1, 47 - 56, 31.03.2023

Ferhan Bölükbaş

https://doi.org/10.30607/kvj.1223940

Abstract

The aim of this study was to investigate the effects of monosodium glutamate (MSG) in ovo administration on
embryonic skeletal muscle development in chicken embryos, using histological, histopathological, and
immunohistochemical methods. In this study, a total of 410 fertilized chicken eggs were used and were divided
into five group as control, vehicle control, low-dose group (0.12 mg/g egg MSG), medium-dose group (0.6 mg/g
egg MSG), and high-dose group (1.2 mg/g egg MSG). At incubation days 18 and 21, eggs from each group were
opened and six live embryos were obtained. The embryos were sacrificed by decapitation, and skeletal muscle
tissue samples (musculus fibularis longus and musculus sternocoracoideus pectoralis) were obtained. Sections
were stained with hematoxylin-eosin. Moreover, caspase-3 reactivity was determined using the
immunohistochemical method. Muscle development was delayed in the MSG groups and the number of caspase3-positive cells was higher (p < 0.05) than in the controls. Histopathological examinations revealed degenerative
and necrotic changes in the skeletal muscle. Muscle degeneration (edema, muscle fiber degeneration, Zenker’s
necrosis, and mononuclear cell infiltrations) were observed in all groups, except for the control groups. It was
concluded that MSG could adversely affect the development of the skeletal muscle.

Keywords

Caspase-3, Embryotoxicity, Monosodium glutamate, Skeletal muscle

Yumurtaya Verilen Monosodyum Glutamat’ın Tavuklard

Abstract

Bu çalışmanın amacı yumurtaya verilen monosodyum glutamat (MSG)’ın civcivlerde iskelet kasının embriyonik
gelişimi üzerindeki etkilerinin histolojik, histopatolojik ve immunohistokimyasal yöntemlerle araştırmaktı. Bu
çalışmada 410 adet döllü tavuk yumurtası kullanıldı ve kontrol, taşıyıcı kontrol, düşük doz grup (0.12 mg/g MSG),
orta doz grup (0.6 mg/g MSG) ve yüksek doz grup (1.2 mg/g MSG) olarak 5 gruba ayrıldı. Kuluçkanın 18 ve 21.
günlerinde, her bir gruptan yumurtalar açıldı ve 6 canlı embriyo elde edildi. Embriyolar dekapitasyon ile sakrifiye
edildi ve iskelet kası (musculus sternocoracoideus pectoralis, musculus fibularis longus) doku örnekleri alındı.
Kesitler Hematoksilen-Eozin boyama yöntemi ile boyandı. Caspase-3 reaktivitesi ise immünohistokimyasal
yöntemle belirlendi. Kas gelişiminin MSG uygulanan gruplarda geri kaldığı ve caspase-3 immunpozitif hücrelerin
kontrol grupları ile karşılaştırıldığında daha fazla olduğu dikkati çekti (p<0.05). Histopatolojik incelemelerde
iskelet kasında dejeneratif ve nekrotik değişiklikler saptandı. Kontrol ve distile su grubu hariç tüm gruplarda
kaslarda dejenerasyon (ödem, kas fibrillerinde dejenerasyon, Zenker nekrozu ve mononükleer hücre infiltrasyonu)
gözlendi. MSG'nin iskelet kası gelişimi üzerine olumsuz etkilerinin olabileceği sonucuna varılmıştır.

Keywords

Embriyotoksisite, İskelet kası, Kaspaz-3, Monosodyum glutamate

References

• Abdel Moneim WM, Yassa HA, Makboul RA, Mohamed NA. Monosodium glutamate affects cognitive functions in male albino rats. Egyptian Journal of Forensic Sciences, 2018; 8, 9.
• Adeyemo OA, Farinmade AE. Genotoxic and cytotoxic effects of food flavor enhancer, monosodium glutamate (MSG) using Allium cepa assay. African Journal of Biotechnology, 2013; 12.
• Baky NA, Mohamed AM, Faddah LM. Protective effect of N-acetyl cysteine and/or pro vitamin A against monosodium glutamate-induced cardiopathy in rats. Journal of Pharmacology and Toxicology, 2009; 4(5), 178–193.
• Banerjee A, Mukherjee S, Maji BK. Worldwide flavor enhancer monosodium glutamate combined with high lipid diet provokes metabolic alterations and systemic anomalies: An overview. Toxicology Reports, 2021; 8, 938-961.
• Bauer R, Plieschnig JA, Finkes T, Riegler B, et al. The developing chicken yolk sac acquires nutrient transport competence by an orchestrated differentiation process of its endodermal epithelial cells. J Biol Chem, 2013; 288(2), 1088- 98.
• Berg C, Halldin K, Fridolfsson AK, Brandt I, et al. The avian egg as a test system for endocrine disrupters: effects of diethyl stilbestrol and ethynylestradiol on sex organ develop. Sci Total Environ,1999; 233(1-3), 57-6
• Berg C. Environmental pollutants and there productive system in birds. PHD Thesis, Acta Universitatis Upsaliensis Faculty of Science and Technology, 2000; Uppsala.
• Bölükbaş F, Öznurlu, Y. Yumurtaya verilen monosodyum glutamat’ın tavuk embriyolarında medulla spinalisin servikal bölgesinin embriyonik gelişimi üzerindeki etkilerinin belirlenmesi. J. Adv. VetBio Sci. Tech., 2021; 6, 298–311. https://doi.org/10.31797/vetbio.%201015200.
• Bölükbaş F, Öznurlu Y. The determination of the effect of in ovo administered monosodium glutamate on the embryonic development of thymus and bursa of Fabricius and percentages of alpha-naphthyl acetate esterase positive lymphocyte in chicken. Environmental Science and Pollution Research, 2022; 29, 45338-45348.
• Bölükbaş F, Öznurlu Y. Determining the effects of in ovo administration of monosodium glutamate on the embryonic development of brain in chickens. NeuroToxicology, 2023a; 94, 87–97.
• Bölükbaş F, Öznurlu, Y. Investigation of the Effects of Monosodium Glutamate on the Embryonic Development of the Eye in Chickens. Veterinary Sciences, 2023b; 10(2):99. https://doi.org/10.3390/vetsci10020099.
• Cairns BE, Dong X, Mann MK, Svensson P, Sessle BJ, Arendt-Nielsen L, & McErlane KM. Systemic administration ofmonosodium glutamate elevates intramuscular glutamate levels and sensitizesrat masseter muscle afferent fibers.Pain, 2007; 132(1-2), 33–41.
• Campos-Sepúlveda AE, Martínez Enríquez ME, Rodríguez Arellanes R, Peláez LE, Rodríguez Amézquita AL, Cadena Razo A. Neonatal monosodium glutamate administration increases aminooxyacetic acid (AOA) susceptibility effects in adult mice. Proc West Pharmacol Soc., 2009; 52, 72-4.
• Chakraborty SP. Patho-physiological and toxicological aspects of monosodium glutamate. Toxicology mechanisms and methods, 2019; 29, 389-396. https://doi.org/10.1080/15376516.2018.1528649 .
• El Kotb SM, El-ghazouly DE, Ameen O. The potential cytoprotective effect of Vitamin C and Vitamin E on monosodium glutamate-induced testicular toxicity in rats. Alexandria Journal of Medicine, 2020; 56(1), 134-147.
• Elwan H, Xie C, Miao L, Dong X, Zou Xt, Mohany M, Ahmed MM, Al-Rejaie SS, Elnesr S. Methionine alleviates aflatoxinb1-induced broiler chicks embryotoxicity through inhibition of caspase-dependent apoptosis and enhancement of cellular antioxidant status. Poultry Science, 2021; 100, 101103.
• Gündüz N, Oznurlu Y. Adverse effects of aflatoxin B1 on skeletal muscle development in broiler chickens. Br Poult Sci., 2014; 55, 684-92.
• Hamza RZ, Diab AE-AA. Testicular protective and antioxidant effects of selenium nanoparticles on Monosodium glutamate-induced testicular structure alterations in male mice. Toxicology Reports, 2020; 7, 254-260.
• Henry MH, Burke WH. Sexual dimorphism in broiler chick embryos and embryonic muscle development in late incubation. Poultry Science, 1998; 77, 728-736.
• Jubaidi FF, Mathialagan RD, Noor MM, Taib IS, Budin SB. Monosodium glutamate daily oral supplementation: Study of its effects on male reproductive system on rat model. Systems biology in reproductive medicine, 2019; 65, 194-204.
• Kemper F, Luepke N. Toxicity testing by the hen's egg test (HET). Food and chemical toxicology, 1986; 24 (6-7), 647–648.
• Kikuchi T. Studies on developmentanddifferentiation of muscle III. Especially on themode of increase in thenumber of musclecells. Tohoku J Agric Res, 1971; 22, 1–15.
• Kingsley OA, Jacks, TW, Amaza, DS, Peters TM, Otong, ES. The Effect of Monosodium Glutamate (MSG) on the Gross Weight of the Heart of Albino Rats Sch. J. App. Med. Sci., 2013; 1(2):44- 47.
• Kitamura A, Sato W, Uneyama H, Torii K, Niijima A. Effects of intra gastric infusion of inosine monophosphate and L-glutamate on vagal gastric afferent activity and subsequen tautonomicreflexes. The Journal of Physiological Sciences, 2010; 61(1), 65–71. https://doi.org/10.1007/s12576-010-0121-z
• Kumar P, Bhandari U. Protective effect of Trigonellafoenum-Graecum Linn. On monosodium glutamate-induced dyslipidemia and oxidative stress in rats, Indian J. Pharmacol. 2013; 45, 136–140, https://doi.org/10.4103/0253-7613.108288.
• Latshaw WK. Veterinary Developmental Anatomy. Toronto, Philadelphia, 1987; p.184-204.
• Liu Y, Zhou L, Xu HF, Yan L, Ding F, Hao W, Gao X. A. Preliminary experimental study on the cardiac toxicity of glutamate and the role of alphaamino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor in rats. Chinese Medical Journal, 2013; 126 (7), 1323–1332.
• Mohamed HA, Mohamed MA. Possible Ameliorative Role of Ethanolic Ginger Extract (Zingiber officinale) against Testicular Toxicity Induced By Monosodium Glutamate In Albino Rats. Egyptian Academic Journal of Biological Sciences, B. Zoology, 2021; 13(2), 285-300.
• Mokhtar HL, Sewelam AS. Impact of Monosodium Glutamate Intake on Heart Structure of Neonate Albino Rats and The Protective Role of Vitamin C. Egyptian Journal of Histology, 2021; 44, 787-804.
• Moore DT, Ferket PR, Mozdziak PE. Muscle Development in the late embryonic andearly post-hatchpoult. Int J Poult Sci, 2005; 4(3), 138-142.
• Mortensen A, Aguilar F, Crebelli R, Di Domenico A, Dusemund B, Frutos MJ, Galtier P, Gott D, Gundert-Remy U. Re-evaluation of glutamicacid (E 620), sodiumglutamate (E 621), potassiumglutamate (E 622), calciumglutamate (E 623), ammoniumglutamate (E 624) andmagnesiumglutamate (E 625) as foodadditives. EFSA Journal., 2017;15(7), 1-90.
• Özgermen BB, Yavuz O, Haydardedeoğlu AE. Investigation of the effects of mesenchymal stem cell administration on liver recovery in experimental hepatotoxicity model. Journal of Advances in VetBio Science and Techniques, 2022, 7(2), 185-193.
• Öznurlu Y, Özaydın T, Sur E, Kuşat T. Yumurta sarısına enjekte edilen bisfenol A'nın tavuklarda iskelet kası gelişimi üzerindeki etkileri. Eurasian Journal of Veterinary Sciences, 2022; 38(2), 90-100.
• Öznurlu Y, Celik I, Sur E, Ozaydın T, Oğuz H, Altunbaş K. Determination of the effects of aflatoxin B1 given in ovo on the proximal tibial growth plate of broiler chickens: histological, histometric and immunohistochemical findings. Avian Pathol., 2012; 41(5), 469-77.
• Park E, Yu KH, Kim DK, Kim S, Sapkota K, Kim S-J, Kim CS, Chun HS. Protective effects of N-acetylcysteine against monosodium glutamate-induced astrocytic cell death. Food and chemical toxicology, 2014; 67, 1-9.
• Pavlović V, Cekić S, Kocić G, Sokolović D, Zivković V. Effect of monosodium glutamate on apoptosis and Bcl-2/Bax protein level in rat thymocyte culture. Physiol Res., 2007; 56, 619-26.
• Qureshi A, Pervez S. Allred scoring for ER reporting and it's impact in clearly distinguishing ER negative from ER positive breast cancers. Journal Pakistan Medical Association, 2010, 60, 350-353.
• Remignon H, Gardahaut MF, Marche G, Ricard FH. Selection for rapid growth increases the number and the size of muscle fibres with outchanging their typing in chickens. J Muscle Res Cell Motil,1995; 16 (2), 95-102.
• Rhodes J, Titherley AC, Norman JA, Wood R, Lord DW. A survey of the monosodium glutamate content of foods and an estimation of the dietary intake of monosodium glutamate, Food Addit. Contam, 1991; 8 (5), 663–672, https:// doi.org/10.1080/02652039109374021.
• Sadighara P, Khaniki GJ, Baseri E, Dehghani MH, et al. Effects of Bisphenol A on the quality charecteristics of meat in a chicken embryo model. Sci Int, 2013; 11(1), 375-8.
• Schaumburg HH, Byck R, Gerstl R, Mashman JH. Monosodium L-glutamate: Its pharmacology and role in the Chinese restaurant syndrome, Science, 1969; 163 (3869), 826–828, https://doi.org/10.1126/science .163.3869.826.
• Stoloff L, Verrett MJ, Dantzman J, Reynaldo EF. Toxicological study of aflatoxin P1 using the fertile chicken egg. Toxicology and applied pharmacology, 1972; 23, 528-531.
• Swamy AH, Patel NL, Gadad PC, Koti BC, Patel UM, Thippeswamy AH, Manjula DV. Neuroprotective activity of Pongamiapinnata in monosodium glutamate-induced neurotoxicity in rats. Indian Journal of Pharmaceutical Sciences, 2014; 75(6), 657–663.
• Toth L, Karcsu S, Feledi J, Kreutzberg G. Neurotoxicity of monosodium-L-glutamate in pregnant and fetal rats. Acta neuropathologica, 1987; 75, 16-22.
• Velleman SG. Muscle development in the embryo and hatchling. Poult Sci, 2007; 86(5),1050-4.
• Yang WH, Drouin MA, Herbert M, Mao Y, Karsh J. The monosodium glutamate symptom complex: assessment in a double-blind placebo-controlled randomized study, J. Allergy Clin. Immunol. 1997; 99 (6 Pt 1), 757–762, https:// doi.org/10.1016/s0091-6749(97)80008-5.
• Zanfirescu A, Ungurianu A, Tsatsakis AM, Nițulescu GM, Kouretas D, Veskoukis A, Tsoukalas D, Engin AB, Aschner M, Margină D. A Review of the Alleged Health Hazards of Monosodium Glutamate. Comprehensive Reviews in Food Science and Food Safety, 2019; 18, 1111-1134.