Sequential morphohistological and scanning electron microscopic developmental study of thymus at prenatal stages in Iraqi Awassi sheep fetuses

Document Type : Research Paper

Authors

Department of Veterinary Anatomy, Veterinary College, Qasim Green University, Babylon 51013, Iraq.

10.22103/jab.2026.27058.1877

Abstract

Objective
One of the primary lymphoid organs is the thymus, which is of great importance during prenatal and early life. It is responsible for the growth, maturation, and selection of thymocytes and plays a role in the development of T-cell functional competence and central immune tolerance, which is closely related to its specialized histological architecture. This study investigates the prenatal morphological and histological development of the thymus gland in local Awassi sheep with scanning electron microscopy (SEM).
Materials and methods
Thirty thymus specimens were collected from healthy pregnant ewes at different stages of gestation. Fetal age was determined using the fetal crown rump length (CRL) equation and the specimens were classified into three groups: Group 1: 50–55 days, Group 2: 90–100 days, and Group 3: 130–140 days. scanning electron microscopy (SEM) was used to observe the thymic surface at multiple magnifications. Data analysis of histological and morphological parameters was performed using the Statistical Package for the social sciences (SPSS).
Results
In Group 1, thymus was small, underdeveloped organ with soft lobes and thin capsule without connection between cervical and thoracic part. Scanning electron microscopy and histologically revealed an immature surface structure, irregular thymic cells, an unclear connection between the cortex and the medulla, reflecting early thymic differentiation. While in Group 2, the thymus showed an increase in size and improved lobular organization to revealed a more clearly defined cortical-membrane boundary, the growth of tissue bundles extending from the capsule to the viscera, and a higher density of cortical thymus cells. The medullary region also showed reticular epithelial cells, indicating progressive structural maturation. In group 3, thymus was well-developed with prominent lobes separated by connective tissue septa. Histological and Scanning observations revealed highly organized visceral tissue, a clear cortical-membrane boundary, extensive reticular epithelial cells, and fully formed Hassall’s corpuscles within the medulla, demonstrating advanced prenatal microstructural maturation.
Conclusion
These findings highlight the progressive prenatal maturation of the thymus and underscore its pivotal role in immune system development. Deviations from these normal microstructural patterns may indicate pathological or immunological disorders.

Keywords


Abbas, A. K., Lichtman, A. H., & Pillai, S. (2019). Basic immunology: Functions and disorders of the immune system (6th ed.). Elsevier.
Amirteymoori, E., Khezri, A., Dayani, O., Mohammadabadi, M., Khorasani, S., Mousaie, A., & Kazemi-Bonchenari, M. (2021). Effects of linseed processing method (ground versus extruded) and dietary crude protein content on performance, digestibility, ruminal fermentation pattern, and rumen protozoa population in growing lambs. Italian Journal of Animal Science, 20(1), 1506–1517. https://doi.org/10.1080/1828051X.2021.1984324
Bancroft, J. D., Suvarna, K. S., & Layton, C. (2018). Bancroft’s theory and practice of histological techniques (8th ed.). Elsevier Health Sciences. https://doi.org/10.1016/C2015-0-00143-5
Barazandeh, A., Mohammadabadi, M. R., Ghaderi-Zefrehei, M., & Nezamabadipour, H. (2016). Predicting CpG islands and their relationship with genomic features in cattle by hidden Markov model algorithm. Iranian Journal of Applied Animal Science, 6(3), 571–579.
Berg, R., Taher, E.-S., & Moustafa, M. S. E. D. M. (1969). Comparative studies on the prenatal growth of the brain, thymus, stomach and oesophagus in the camel (Camelus dromedarius) and Egyptian water buffalo (Bos/Bubalus bubalis L.). Zentralblatt für Veterinärmedizin Reihe A, 16, 659–663. https://doi.org/10.1111/j.1439-0442.1969.tb00767.x
Bhagyalakshmi, J., Balasundaram, K., & Raju, N. K. B. (2023). Histological observations on prenatal development of thymus in sheep. The Haryana Veterinarian, 62(SI-2), 96–99. https://www.luvas.edu.in/haryana-veterinarian/archive-2023.php?AM19
Chaurasia, S. (2022). Gross and morphometrical studies on the thymus of prenatal Surti goat (Capra hircus). Indian Journal of Veterinary Anatomy, 33(2), 85–88. https://epubs.icar.org.in/index.php/IJVA/article/view/120488
Chaurasia, S., & Menaka, R. (2024). Histogenesis of thymus in prenatal Surti goats. Indian Journal of Veterinary Anatomy, 36(1), 60–64. https://epubs.icar.org.in/index.php/IJVA/article/view/162039
Chuluunbaatar, T., Ichii, O., Masum, M. A., Namba, T., & Kon, Y. (2023). Morphological characteristics of genital organ-associated lymphoid tissue in the vaginal vestibule of goats and pigs. Veterinary Sciences, 10(1), Article 51. https://doi.org/10.3390/vetsci10010051
Dalley, A. F., & Agur, A. M. R. (2022). Moore's clinically oriented anatomy (9th ed.). Wolters Kluwer.
Drenckhahn, D., von Gaudecker, B., Müller-Hermelink, H. K., Unsicker, K., & Gröschel-Stewart, U. (1979). Myosin and actin containing cells in the human postnatal thymus: Ultrastructural and immunohistochemical findings in normal thymus and in myasthenia gravis. Virchows Archiv B Cell Pathology Including Molecular Pathology, 32(1), 33–45. https://doi.org/10.1007/BF02889011
Fisher, D. A. (1991). Thyroid system ontogeny in the sheep: A model for precocial mammalian species. Advances in Experimental Medicine and Biology, 299, 11–26. https://doi.org/10.1007/978-1-4684-5973-9_2
Gulla, S., Reddy, M. C., Reddy, V. C., Chitta, S., Bhanoori, M., & Lomada, D. (2023). Role of thymus in health and disease. International Reviews of Immunology, 42(5), 347–363. https://doi.org/10.1080/08830185.2022.2064461
Hajalizadeh, Z., Dayani, O., Khezri, A., Tahmasbi, R., Mohammadabadi, M., Solodka, T., Kalashnyk, O., Afanasenko, V., & Babenko, O. (2021). Expression of calpastatin gene in Kermani sheep using real-time PCR. Journal of Livestock Science and Technology, 9(2), 51–57. https://doi.org/10.22103/jlst.2021.18165.1381
Kumar, V., Singh, S. P., Farooqui, M. M., Kumar, P., Prakash, A., & Archana. (2015). Gross and biometrical studies of placentome in goat (Capra hircus) during different stages of pregnancy. Journal of Animal Research, 5(2), 251–255. https://doi.org/10.5958/2277-940X.2015.00040.0 (Note: Semantic Scholar link retained if no DOI; adjust if needed.)
Mainde, U. P., Nandeshwar, N. C., Dalvi, R. S., Banubakode, S. B., Salankar, A. M., Sathapathy, S., & Rana, J. (2017). Histogenesis of thymus in different prenatal age groups of goat foetus. Indian Journal of Veterinary Anatomy, 29(1), 5–6. https://epubs.icar.org.in/index.php/IJVA/article/view/83058
McGeady, T. A., Quinn, P. J., FitzPatrick, E. S., & Ryan, M. T. (2006). Forms of implantation and placentation. In T. A. McGeady, P. J. Quinn, E. S. FitzPatrick, & M. T. Ryan, Veterinary embryology (pp. 87–104). Blackwell Publishing.
Mohammadabadi, M. R., Shaban Jorjandy, D., Arabpoor Raghabadi, Z., Abareghi, F., Sasan, H. A., & Bordbar, F. (2022). The role of fennel on DLK1 gene expression in sheep heart tissue. Agricultural Biotechnology Journal, 14(2), 155–170. https://doi.org/10.22103/jab.2022.19402.1399
Mohammadabadi, M. R. (2016). Inter-simple sequence repeat loci associations with predicted breeding values of body weight in Kermani sheep. Genetics in the Third Millennium, 14(4), 4386–4393.
Mohammadabadi, M., & Nanaei, H. A. (2021). Leptin gene expression in Raini Cashmere goat using real-time PCR. Agricultural Biotechnology Journal. https://doi.org/10.22103/JAB.2021.17334.1305
Mohammadabadi, M., Babenko, O., Borshch, O. O., Kalashnyk, O., Ievstafiieva, Y., & Buchkovska, V. (2024). Measurement of the relative expression pattern of the UCP2 gene in different tissues of the Raini Cashmere goat. Agricultural Biotechnology Journal, 16(3), 317–332. https://doi.org/10.22103/jab.2024.24337.1627
Mohammadabadi, M., Kheyrodin, H., Latifi, A., & Babenko, O. I. (2022). mRNA expression profile of DNAH1 gene in testis tissue of Raini Cashmere goat. Agricultural Biotechnology Journal. https://doi.org/10.22103/jab.2022.20199.1428
Mohammadinejad, F., Mohammadabadi, M., Roudbari, Z., & Sadkowski, T. (2022). Identification of key genes and biological pathways associated with skeletal muscle maturation and hypertrophy in Bos taurus, Ovis aries, and Sus scrofa. Animals, 12(24), Article 3471. https://doi.org/10.3390/ani12243471
Mohammadipour Saadatabadi, L. M., Mohammadabadi, M., Nanaei, H. A., Ghanatsaman, Z. A., Stavetska, R. V., Kalashnyk, O., Kochuk-Yashchenko, O. A., & Kucher, D. M. (2023). Unraveling candidate genes related to heat tolerance and immune response traits in some native sheep using whole genome sequencing data. Small Ruminant Research, 225, Article 107018. https://doi.org/10.1016/j.smallrumres.2023.107018
Mohassen, F. W., & Al-Jebori, J. G. A. (2020). Ontogenesis of thyroid gland in Awasi sheep foetuses: Prenatal study. Plant Archives, 20(Suppl. 1), 1096–1100. http://www.plantarchives.org/SPECIAL%20ISSUE%2020-1/1096-1100%20(64).pdf
Molaei Moghbeli, S., Barazandeh, A., Vatankhah, M., & Mohammadabadi, M. (2013). Genetics and non-genetics parameters of body weight for post-weaning traits in Raini Cashmere goats. Tropical Animal Health and Production, 45, 1519–1524. https://doi.org/10.1007/s11250-013-0393-4
Nejad, F. M., Mohammadabadi, M., Roudbari, Z., et al. (2024). Network visualization of genes involved in skeletal muscle myogenesis in livestock animals. BMC Genomics, 25, Article 294. https://doi.org/10.1186/s12864-024-10196-3
Niyf, A. M., & Al-Jebori, J. G. A. (2024). Ontogenesis of rectum in local Awassi sheep fetuses (Ovis aries) during prenatal periods. Journal of Animal Health and Production, 12(s1), 45–54. https://doi.org/10.17582/journal.jahp/2024/12.s1.45.54
Noakes, D. E., Parkinson, T. J., & England, G. C. W. (Eds.). (2019). Veterinary reproduction and obstetrics (10th ed.). Saunders Ltd. https://doi.org/10.1016/C2014-0-04782-X
Noori, A. N., Behzadi, M. R. B., & Mohammadabadi, M. R. (2017). Expression pattern of Rheb gene in Jabal Barez Red goat. The Indian Journal of Animal Sciences, 87(11), 1375–1378. https://doi.org/10.56093/ijans.v87i11.75890
Owen, J. J., & Ritter, M. A. (1969). Tissue interaction in the development of thymus lymphocytes. Journal of Experimental Medicine, 129(2), 431–442. https://doi.org/10.1084/jem.129.2.431
Raghavan, D. (Ed.). (1964). Anatomy of the ox: With comparative notes on the horse, dog and fowl. Indian Council of Agricultural Research.
Ramayyai, P. J., Singh, O., & Roy, K. S. (2008). Gross anatomical studies on the thymus of pre- and post-natal buffalo (Bubalus bubalis). The Indian Journal of Animal Sciences, 78(5), 461–464. https://epubs.icar.org.in/index.php/IJAnS/article/view/4714
Rodewald, H. R. (2008). Thymus organogenesis. Annual Review of Immunology, 26, 355–388. https://doi.org/10.1146/annurev.immunol.26.021607.090408
Saadatabadi, L. M., Mohammadabadi, M., Ghanatsaman, Z. A., Babenko, O., Stavetska, R. V., Kalashnik, O. M., Afanasenko, V., Kochuk-Yashchenko, O. A., Kucher, D. M., & Nanaei, H. A. (2023). Data of whole-genome sequencing of Karakul, Zel, and Kermani sheep breeds. BMC Research Notes, 16(1), Article 353. https://doi.org/10.1186/s13104-023-06630-6
Safaei, S. M. H., Dadpasand, M., Mohammadabadi, M., Atashi, H., Stavetska, R., Klopenko, N., & Kalashnyk, O. (2022). An Origanum majorana leaf diet influences myogenin gene expression, performance, and carcass characteristics in lambs. Animals, 13(1), Article 14. https://doi.org/10.3390/ani13010014
Sarma, K., Kalita, A., Suri, S., & Zama, M. M. S. (2004). Gross anatomical observations on superficial lymph nodes of Bakarwali goat (Capra hircus). The Indian Journal of Animal Sciences, 74(7), 750–751. https://epubs.icar.org.in/index.php/IJAnS/article/view/39039
Schummer, A., Wilkens, H., Vollmerhaus, B., & Habermehl, K.-H. (1981). The circulatory system, the skin, and the cutaneous organs of the domestic mammals. Springer. https://doi.org/10.1007/978-1-4899-7102-9
Shokri, S., Khezri, A., Mohammadabadi, M., & Kheyrodin, H. (2023). The expression of MYH7 gene in femur, humeral muscle, and back muscle tissues of fattening lambs of the Kermani breed. Agricultural Biotechnology Journal, 15(2), 217–236. https://doi.org/10.22103/jab.2023.21524.1486
Šinkora, M., & Butler, J. E. (2009). The ontogeny of the porcine immune system. Developmental & Comparative Immunology, 33(3), 273–283. https://doi.org/10.1016/j.dci.2008.07.011
Uppal, V., Bansal, N., & Roy, K. S. (2007). Histoenzymic studies on the thymus of neonatal buffalo calves. The Indian Journal of Animal Sciences, 77(8), 723–726. https://epubs.icar.org.in/index.php/IJAnS/article/view/10382
Vahabzadeh, M., Chamani, M., Dayani, O., & Sadeghi, A. A. (2020). Effect of Origanum majorana leaf (sweet marjoram) feeding on lamb’s growth, carcass characteristics, and blood biochemical parameters. Small Ruminant Research, 192, Article 106233. https://doi.org/10.1016/j.smallrumres.2020.106233
van Ewijk, W., Holländer, G., Terhorst, C., & Wang, B. (2000). Stepwise development of thymic microenvironments in vivo is regulated by thymocyte subsets. Development, 127(8), 1583–1591. https://doi.org/10.1242/dev.127.8.1583
van Ewijk, W. (1984). Immunohistology of lymphoid and non-lymphoid cells in the thymus in relation to T lymphocyte differentiation. American Journal of Anatomy, 170(3), 311–330. https://doi.org/10.1002/aja.1001700307
Zamani, P., Akhondi, M., Mohammadabadi, M. R., Saki, A. A., Ershadi, A., Banabazi, M. H., & Abdolmohammadi, A. R. (2011). Genetic variation of Mehraban sheep using two inter simple sequence repeat (ISSR) markers. African Journal of Biotechnology, 10(10), 1812–1817. https://www.ajol.info/index.php/ajb/article/view/93089