Skip to main content
SpringerLink
Log in

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

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Monosodium glutamate (MSG) is a flavor enhancer commonly used in modern nutrition. In this study, it was aimed to determine the effect of in ovo administered MSG on the embryonic development of thymus, bursa of Fabricius, and percentages of alpha-naphthyl acetate esterase (ANAE) positive lymphocyte by using histological, histometrical, and enzyme histochemical methods in chickens. For this purpose, 410 fertile eggs were used. The eggs were then divided into five groups: group 1 (control group, n = 40 eggs), group 2 (distilled water-injected group, n = 62 eggs), group 3 (0.12 mg/g egg MSG-injected group, n = 80 eggs), group 4 (0.6 mg/g egg MSG-injected group, n = 90 eggs), and group 5 (1.2 mg/g egg MSG-injected group, n = 138 eggs), and injections were performed via the egg yolk. On the 18th and 21st days of the incubation, the eggs were randomly opened from each group until six live embryos were obtained. The embryos of each group were sacrificed by decapitation, and blood, thymus, and bursa of Fabricius tissue samples were taken from the obtained embryos. The MSG-treated groups were found to be retarded embryonic development of thymus and bursa of Fabricius tissue compared to the control and distilled water groups. MSG treatment also resulted in reduced lymphoid follicles count and follicle diameters in bursa of Fabricius (P < 0.05). The percentage of peripheral blood ANAE positive lymphocytes was significantly lower in the MSG-treated groups than in the control and distilled water groups (P < 0.05). In conclusion, it has been found that in ovo administered MSG can adversely affect the embryonic development of thymus and bursa of Fabricius and decrease percentage of ANAE positive lymphocyte.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Availability of data and materials

The data sets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Abu Elnaga NA, Sarhan M, Mansour H (2019) Teratogenicity of monosodium glutamate on the pregnant rats and their fetuses. The Egyptian Journal of Hospital Medicine 74, 1737–1747. https://doi.org/10.21608/ejhm.2019.28580

  • Akataobi U (2020) Key enzymes of glutamate metabolisms in the brain of neonatal and adult rats exposed to monosodium glutamate. Asia Pacific Journal of Clinical Trials: Nervous System Diseases 5:51–57. https://doi.org/10.4103/2542-3932.304946

    Article  Google Scholar 

  • Akbulut B, Sur E, Okur DN (2015) Determination of the agnor parameters, MN frequency, ANAE and ACP-ase positivity of PBL in pregnants. Selcuk Medical Journal 31:144–150

    Google Scholar 

  • Al-Gamdi F, Al-Harbi N (2020) Effect of grape seed extract in minimizing the harmful effects of monosodium glutamate on the chicken embryonic retina to show scientific miracles in the Holy Quran. Journal of Pharmaceutical Research International 32(25):7–18. https://doi.org/10.9734/jpri/2020/v32i2530819

    Article  CAS  Google Scholar 

  • Al-Qudsi F, Al-Jahdali A (2012) Effect of monosodium glutamate on chick embryo development. J Am Sci 8:499–509

    Google Scholar 

  • AL-Sharkawy AN, Gab-Allah MS, El-Mashad A-BI, Khater DF (2017) Pathological study on the effect of some food additives in male albino rats. Benha Veterinary Medical Journal 33, 75–87. https://doi.org/10.21608/BVMJ.2017.29996

  • Alsalmi F, Hamza R, El-Shenawy N (2019) Effect of green tea and zinc oxide nanoparticles complex on histopathology of spleen of male rats induced by monosodium glutamate. Instant Journal of Hematology and Oncology 2, 04–11. https://doi.org/10.36811/ijho.2019.110002

  • Ataseven N, Yuzbasioglu D, Keskin AC, Unal F (2016) Genotoxicity of monosodium glutamate. Food Chem Toxicol 91:8–18. https://doi.org/10.1016/j.fct.2016.02.021

    Article  CAS  Google Scholar 

  • Atay E, Ertekin A, Bozkurt E, Aslan E (2020) Impact of Bisphenol A on neural tube development in 48-hr chicken embryos. Birth Defects Research 112:1386–1396. https://doi.org/10.1002/bdr2.1791

    Article  CAS  Google Scholar 

  • Baad-Hansen L, Cairns B, Ernberg M, Svensson P (2010) Effect of systemic monosodium glutamate (MSG) on headache and pericranial muscle sensitivity. Cephalalgia : an International Journal of Headache 30:68–76. https://doi.org/10.1111/j.1468-2982.2009.01881.x

    Article  CAS  Google Scholar 

  • Banerjee A, Mukherjee S, Maji BK (2021) Worldwide flavor enhancer monosodium glutamate combined with high lipid diet provokes metabolic alterations and systemic anomalies: an overview. Toxicol Rep 8:938–961. https://doi.org/10.1016/j.toxrep.2021.04.009

    Article  CAS  Google Scholar 

  • Beas-Zárate C, Pérez-Vega M, González-Burgos I (2002) Neonatal exposure to monosodium L-glutamate induces loss of neurons and cytoarchitectural alterations in hippocampal CA1 pyramidal neurons of adult rats. Brain Res 952:275–281. https://doi.org/10.1016/s0006-8993(02)03252-3

    Article  Google Scholar 

  • Berktay EA (2014) Determination of the effects of sunset yellow FCF (E110) on the embryonic development of chicken thymus and bursa Fabricii by means of histological and enzyme histochemical methods., Master Thesis, Institute of Health Sciences, Konya

  • Bramardipa AAB, Adi AAAM, Putra I (2019) Effectiveness of Mangosteen peel extract (Garcinia Mangostana Linn) in minimizing the immunosuppressive effect of monosodium. Jurnal Veteriner 20, 211–218. https://doi.org/10.19087/jveteriner.2019.20.2.211

  • Chaudhry MS, Velardi E, Dudakov JA, van den Brink MR (2016) Thymus: the next (re) generation. Immunol Rev 271:56–71. https://doi.org/10.1111/imr.12418

    Article  CAS  Google Scholar 

  • Chen D, Hu G, Zhang S, Zhang H, Teng X (2020) Ammonia-triggered apoptosis via immune function and metabolic process in the thymuses of chickens by proteomics analysis. Ecotoxicol Environ Saf 198:110619. https://doi.org/10.1016/j.ecoenv.2020.110619

    Article  CAS  Google Scholar 

  • Çetin S, Özaydın T (2021) The effects of bisphenol A given in ovo on bursa of Fabricius development and percentage of acid phosphatase positive lymphocyte in chicken. Environ Sci Pollut Res, 1-10. https://doi.org/10.1007/s11356-021-13640-z

  • Emon ST, Orakdogen M, Uslu S, Somay H (2015) Effects of the popular food additive sodium benzoate on neural tube development in the chicken embryo. Turk Neurosurg 25:294–297. https://doi.org/10.5137/1019-5149.JTN.12551-14.2

    Article  Google Scholar 

  • Eweka A, Igbigbi P, Ucheya R (2011) Histochemical studies of the effects of monosodium glutamate on the liver of adult Wistar rats. Ann Med Health Sci Res 1:21–30

    Google Scholar 

  • Gad El-Hak HN, Abdelrazek HMA, Zeidan DW, Almallah AA, Khaled HE (2021) Assessment of changes in the liver of pregnant female rats and their fetuses following monosodium glutamate administration. Environ Sci Pollut Res 28(32):44432–44441. https://doi.org/10.1007/s11356-021-13557-7

    Article  CAS  Google Scholar 

  • Gad FA, Farouk SM, Emam MA (2021) Antiapoptotic and antioxidant capacity of phytochemicals from Roselle (Hibiscus sabdariffa) and their potential effects on monosodium glutamate-induced testicular damage in rat. Environ Sci Pollut Res Int 28:2379–2390. https://doi.org/10.1007/s11356-020-10674-7

    Article  CAS  Google Scholar 

  • Hajihasani MM, Soheili V, Zirak MR, Sahebkar A, Shakeri A (2020) Natural products as safeguards against monosodium glutamate-induced toxicity. Iranian Journal of Basic Medical Sciences 23, 416. https://doi.org/10.22038/ijbms.2020.43060.10123

  • Harapko T, Mateshuk-Vatseba L (2021) Effects of MSG on the lymph nodes of the albino rat: ultrastructural and morphometric studies. Eur J Anat 25(1):75–81

    Google Scholar 

  • Hassan ZA, Arafa MH, Soliman WI, Atteia HH, Al-Saeed HF (2014) The effects of monosodium glutamate on thymic and splenic immune functions and role of recovery (biochemical and histological study). Journal of Cytology & Histology 5:1. https://doi.org/10.4172/2157-7099.1000283

    Article  CAS  Google Scholar 

  • Hegazy AA, Ibrahim IH, Sabry RM, Abass ES (2017) Effect of gestational exposure to monosodium glutamate on the structure of fetal rat lung. Anatomy Physiol Biochem Int J 3:1–6

    Google Scholar 

  • Henry-Unaeze HN (2017) Update on food safety of monosodium l-glutamate (MSG). Pathophysiology : the Official Journal of the International Society for Pathophysiology 24:243–249. https://doi.org/10.1016/j.pathophys.2017.08.001

    Article  CAS  Google Scholar 

  • Jelinek R (1977) Methods in prenatal toxicology. In: The chick embryotoxicity screening test (CHEST). Eds: Neubert D, Merker H, Kwasigrooh T. Stutgort: Georg Thieme, p. 381–6.

  • Jessl L, Lenz R, Massing FG, Scheider J, Oehlmann J (2018) Effects of estrogens and antiestrogens on gonadal sex differentiation and embryonic development in the domestic fowl (Gallus gallus domesticus). PeerJ 6:e5094. https://doi.org/10.7717/peerj.5094

    Article  CAS  Google Scholar 

  • Kandil B, Sur E (2018) The light microscopic investigation of the effects of in-ovo administered bisphenol A (BPA) on the development of testes. Ankara Üniversitesi Veteriner Fakültesi Dergisi 65(3):273–281. https://doi.org/10.1501/Vetfak_0000002857

    Article  Google Scholar 

  • Kaya S, Dönmez HH (2020) Effects of paclitaxel and resveratrol on blood characteristics in rabbits. Biotech Histochem 95:198–202. https://doi.org/10.1080/10520295.2019.1663557

    Article  CAS  Google Scholar 

  • Kazmi Z, Fatima I, Perveen S, Malik SS (2017) Monosodium glutamate: review on clinical reports. Int J Food Prop 20:1807–1815. https://doi.org/10.1080/10942912.2017.1295260

    Article  CAS  Google Scholar 

  • Kısadere İ, Aydın MF, Ündağ İ (2021) Partial protective effects of melatonin on cadmium-induced changes in hematological characteristics in rats. Biotech Histochem 17:1–7. https://doi.org/10.1080/10520295.2021.1925965

    Article  CAS  Google Scholar 

  • Miko AM, Shehu AM, Bello N, Allyu IA, Tasiu I, Abdussalam AO, Isa AS (2016) A morphometric study of the teratogenic effect of monosodium glutamate on the developing cerebral cortex of Wista Rat (Rattus norvegicus). Nigerian Journal of Scientific Research 15(3):240–244

    Google Scholar 

  • Nguyen L, Salanta L-C, Socaci S, Tofana M, Fărcaş A, Pop C (2020) A mini review about monosodium glutamate. Bulletin of University of Agricultural Sciences and Veterinary Medicine Cluj-Napoca. Food Science and Technology 77(1). https://doi.org/10.15835/buasvmcn-fst:2019.0029

  • Obayashi Y, Nagamura Y (2016) Does monosodium glutamate really cause headache? A systematic review of human studies. J Headache Pain 17:54. https://doi.org/10.1186/s10194-016-0639-4

    Article  CAS  Google Scholar 

  • Oladipo I, Adebayo E, Kuye O (2015) Effects of monosodium glutamate in ovaries of female Sprague-Dawley rats. Int J Curr Microbiol App Sci 4:737–745

    CAS  Google Scholar 

  • Onaolapo A, Onaolapo O (2011) Acute low dose monosodium glutamate retards novelty induced behaviours in male Swiss albino mice. J Journal of Neuroscience and Behavioural Health 3:51–56

    CAS  Google Scholar 

  • Özaydın T, Öznurlu Y, Sur E, Çelik İ, Uluışık D (2018) The effects of bisphenol A on some plasma cytokine levels and distribution of CD8+ and CD4+ T lymphocytes in spleen, ileal Peyer’s patch and bronchus associated lymphoid tissue in rats. Acta Histochem 120:728–733. https://doi.org/10.1016/j.acthis.2018.08.002

    Article  CAS  Google Scholar 

  • Öznurlu Y, Özaydın T, Sur E, Özparlak H (2021) The effects of in ovo administered bisphenol A on tibial growth plate histology in chicken. Birth Defects Research. https://doi.org/10.1002/bdr2.1925(inpress)

    Article  Google Scholar 

  • Park JH, Choi TS (2016) Subcutaneous administration of monosodium glutamate to pregnant mice reduces weight gain in pups during lactation. Lab Anim 50:94–99. https://doi.org/10.1177/0023677215590526

    Article  CAS  Google Scholar 

  • Paula Neto HA, Ausina P, Gomez LS, Leandro JGB, Zancan P, Sola-Penna M (2017) Effects of food additives on immune cells as contributors to body weight gain and immune-mediated metabolic dysregulation. Front Immunol 8:1478. https://doi.org/10.3389/fimmu.2017.01478

    Article  CAS  Google Scholar 

  • Pavlovic V, Pavlovic D, Kocic G, Sokolovic D, Sarac M, Jovic Z (2009) Ascorbic acid modulates monosodium glutamate induced cytotoxicity in rat thymus. Bratisl Lek Listy 110:205–209

    CAS  Google Scholar 

  • Pavlovic V, Cekić S, Kocić G, Sokolović D, Zivković V (2007) Effect of monosodium glutamate on apoptosis and Bcl-2/Bax protein level in rat thymocyte culture. Physiol Res 56:619–626. https://doi.org/10.1007/s11010-007-9469-7

    Article  CAS  Google Scholar 

  • Roongruangchai J, Viravud Y, Plakornkul V, Sripaoraya K, Boonmark W, Roongruangchai K (2018) The teratogenic effects of monosodium glutamate (MSG) on the development of chick embryos. Siriraj Medical Journal 70:514–522. https://doi.org/10.1080/10520295.2019.1571227

    Article  Google Scholar 

  • Shah SWA, Chen D, Zhang J, Liu Y, Ishfaq M, Tang Y, Teng X (2020a) The effect of ammonia exposure on energy metabolism and mitochondrial dynamic proteins in chicken thymus: through oxidative stress, apoptosis, and autophagy. Ecotoxicol Environ Saf 206:111413. https://doi.org/10.1016/j.ecoenv.2020.111413

    Article  CAS  Google Scholar 

  • Shah SWA, Ishfaq M, Nasrullah M, Qayum A, Akhtar MU, Jo H, Hussain M, Teng X (2020b) Ammonia inhalation-induced inflammation and structural impairment in the bursa of fabricius and thymus of broilers through NF-κB signaling pathway. Environ Sci Pollut Res 27(11):11596–11607. https://doi.org/10.1007/s11356-020-07743-2

    Article  CAS  Google Scholar 

  • Singh K, Pushpa A (2005) Alteration in some antioxidant enzymes in cardiac tissue upon monosodium glutamate [MSG] administration to adult male mice. Indian J Clin Biochem 20:43–46. https://doi.org/10.1007/bf02893040

    Article  CAS  Google Scholar 

  • Sur E, Öznurlu Y, Özaydın T, Çelik İ, Aydın İ, Kadıralieva N (2014) The proportion and the distribution of T-lymphocytes, null lymphocytes and acid phosphatase positive lymphocytes of the peripheral blood and endometrium in pregnant mice. Kafkas Üniversitesi Veteriner Fakültesi Dergisi 20:131–137

    Google Scholar 

  • Umukoro S, Oluwole GO, Olamijowon HE, Omogbiya AI, Eduviere AT (2015) Effect of monosodium glutamate on behavioral phenotypes, biomarkers of oxidative stress in brain tissues and liver enzymes in mice. World Journal of Neuroscience 5:339

    Article  CAS  Google Scholar 

  • Vucic M, Cojbasic I, Vucic J, Pavlovic V (2018) The effect of curcumin and PI3K/Akt inhibitor on monosodium glutamate-induced rat thymocytes toxicity. Gen Physiol Biophys 37:329–336. https://doi.org/10.1590/s0102-86502006000600013

    Article  CAS  Google Scholar 

  • Yener Y, Çelik İ, Sur E, Öznurlu Y, Özaydin T (2019) Effects of long term oral acrylamide administration on alpha naphthyl acetate esterase and acid phosphatase activities in the peripheral blood lymphocytes of rats. Biotech Histochem 94:352–359. https://doi.org/10.1080/10520295.2019.1571227

    Article  CAS  Google Scholar 

  • Yiğit F, Aktaş A, Dağlıoğlu S (2013) Effects of bisphenol A and diethylstilbestrol on the involution of bursa of Fabricius in the hens. İstanbul Üniversitesi Veteriner Fakültesi Dergisi 39:168–174

    Google Scholar 

  • Yılmaz D, Öznurlu Y (2019) Yumurtaya verilen bisfenol a nın, tavuklarda timusun gelişimi ve perifer kan alfa naftil asetat esteraz pozitif lenfosit oranı üzerindeki etkilerinin histolojik ve enzim histokimyasal yöntemlerle belirlenmesi. Eurasian Journal of Veterinary Sciences 35, 144–151. https://doi.org/10.15312/EurasianJVetSci.2019.23

  • Zanfirescu A, Ungurianu A, Tsatsakis AM, Nițulescu GM, Kouretas D, Veskoukis A, Tsoukalas D, Engin AB, Aschner M, Margină D (2019) A review of the alleged health hazards of monosodium glutamate. Comprehensive Reviews in Food Science and Food Safety 18:1111–1134. https://doi.org/10.1111/1541-4337.12448

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Histology and Embryology, Faculty of Medicine, Aksaray University, Aksaray, Turkey

    Ferhan Bölükbaş

  2. Department of Histology and Embryology, Faculty of Veterinary Medicine, University of Selcuk, Konya, Turkey

    Yasemin Öznurlu

Authors
  1. Ferhan Bölükbaş
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yasemin Öznurlu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

FB performed the experiments. FB prepared the tissue sections and the blood smears. FB and YÖ performed the histological examination of the thymus and bursa of Fabricii. The first draft of the manuscript was written by FB. YÖ commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Ferhan Bölükbaş.

Ethics declarations

Ethics approval and consent to participate

This study was conducted with the approval (31.05.2017 and 2017/48) of the Ethics Committee of Selcuk University Veterinary Faculty Experimental Animals Production and Research Center.

Consent for publication

Not applicable.

Competing of interests

The authors declare no competing interests.

Additional information

Responsible Editor: Mohamed M. Abdel-Daim

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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. Environ Sci Pollut Res 29, 45338–45348 (2022). https://doi.org/10.1007/s11356-022-19112-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-022-19112-2

Keywords

Search

Navigation