Histomorphometric changes during prenatal development of the spleen in different gestational phases of the dromedary camel (Camelus dromedarius): Prenatal spleen development in camel

Eiman Ahmed Elsayed Yousif; Haider Ibrahim Ismail Mohammed; Nawal Sirelkhatim Osman Omer; Lemiaa Eissa Saeed Harown; Mortada Mahjoub Osman Elhassan

doi:10.62310/liab.v6i2.352

Authors

Eiman Ahmed Elsayed Yousif Department of Anatomy, College of Veterinary Medicine, University of Bahri, Sudan https://orcid.org/0009-0004-9484-7188
Haider Ibrahim Ismail Mohammed Department of Anatomy, College of Veterinary Medicine, University of Bahri, Sudan
Nawal Sirelkhatim Osman Omer Department of Anatomy, College of Veterinary Medicine, University of Bahri, Sudan
Lemiaa Eissa Saeed Harown Department of Anatomy, College of Veterinary Medicine, University of Bahri, Sudan
Mortada Mahjoub Osman Elhassan Department of Anatomy, College of Veterinary Medicine, University of Bahri, Sudan

DOI:

https://doi.org/10.62310/liab.v6i2.352

Keywords:

Camel fetus, Spleen, Capsule, Lymphoid nodule

Abstract

The spleen functions as the principal secondary lymphoid organ and plays a critical role in filtering blood and initiating immune responses to antigens. The present study examined the prenatal histological and histometric development of the spleen across the three trimesters of gestation. Sixteen camel fetuses were collected and allocated to first, second, and third trimester groups by measuring the crown vertebral rump length (CVRL) of each fetus. Tissue samples were taken from the spleen and processed for histological investigations. In the first trimester, the spleen exhibited a thin capsule, small lymphoid nodules, and a network of developing blood sinuses. In the second trimester, the capsule differentiated into an outer collagenous layer and an inner smooth muscle layer with well-developed and branched trabeculae. The lymphoid nodules in the stroma increased both in number and size. During the third trimester, the trabeculae showed increased branching and contained smooth muscle layer. The white pulp structures appeared spherical, with prominent central arterioles. The thickness of the capsule increased significantly (p < 0.05) from 21.3 μm in the first trimester to 54.6 μ in the second trimester, whereas no significant increase was noted in the third trimester (55.2 μ). The diameter of the lymphoid nodules increased significantly (p < 0.05) from 133.0 μ to 161.6 μ in the second and third trimesters, respectively. These observations suggest a progressive increase in the size of these nodules during fetal development. It is concluded that the structural changes in the camel spleen during embryonic development were similar in trend to those of other domestic animals. This study provides novel baseline quantitative data on the morphometry of the splenic capsule and lymphoid nodules during prenatal development of the camel spleen, offering a reference for future studies on lymphoid organ maturation in camelids.

Metrics

Metrics Loading ...

References

Alex L, Rajan ML, Xavier B, Jacob P, Rani KD, Lakshmi GV. (2015). Microscopic study of human spleen in different age groups. International Journal of Research in Medical Sciences 3(7): 1701–1706. https://doi.org/10.18203/2320-6012.ijrms20150255

Alim A, Nurunnabi ASM, Ara S, Mahbub S, Mohanta LC. (2012). Comparative histological study on the spleen of human (Homo sapiens), cow (Bos indicus) and goat (Capra hircus). Nepal Journal of Medical Sciences 1(2): 64–67. https://doi.org/10.3126/njms.v1i2.6601

Alshamarry HA. (2010). Histological and histometric study on the spleen of Iraqi camel (Camelus dromedarius). Emirates Journal of Food and Agriculture 22(1): 65–70. https://doi.org/10.9755/ejfa.v22i1.4908

Arey LB. (1954). Developmental Anatomy: A Textbook and Laboratory Manual of Embryology. 6th edition, WB Saunders Company, Philadelphia, USA.

Asha A, Maya S, Harshan KR, Chungath JJ. (2008). Prenatal histological changes in the spleen of goat. In: Proceedings of the National Symposium and XXIII Annual Convention of the Indian Association of Veterinary Anatomists, HAU, Hisar, India. Pp. 42.

Bancroft JD, Gamble M. (2008). Theory and Practice of Histological Techniques. 6th edition, Churchill Livingstone Elsevier, Edinburgh, UK.

Belic O. (2015). Morphology of the spleen and its ligamentous apparatus. Curierul Medical 58(5): 37-47.

Bello A, Onu JE, Fawaz AM, Hena SA, Sonfada ML, Umaru MA, Shehu SA. (2016). Prenatal development of the spleen of one-humped camel (Camelus dromedarius): A comparative histological study. Scholarly Journal of Agricultural Science 6(8): 263–269.

Cesta MF. (2006). Normal structure, function, and histology of the spleen. Toxicologic Pathology 34(5): 455–465. https://doi.org/10.1080/01926230600867743

Colakoğlu A, Selcuk ML. (2020). Morphohistometric evaluation of embryonic development of spleen in chicken. Kocatepe Veterinary Journal 13(4): 368–374. https://doi.org/10.30607/kvj.765775

Elwishy AB, Hemeida NA, Omar MA, Mobarak AM, El Sayed MAI. (1981). Functional changes in the pregnant camel with special reference to foetal growth. British Veterinary Journal 137(5): 527–537. https://doi.org/10.1016/S0007-1935(17)31592-0

Ernst LM, Ruchelli ED, Carreon CK, Huff DS. (2019). Color atlas of human fetal and neonatal histology. Springer Nature, Cham, Switzerland, 261-268. https://doi.org/10.1007/978-3-030-11425-1

Eurell JAC, Frappier BL. (2006). Dellmann’s Textbook of Veterinary Histology. Blackwell Publishing, Ames, Iowa, USA.

Gautam AK, Mishra UK. (2015). Histochemical and transmission electron microscopic studies of spleen in prenatal stages of goat. Indian Journal of Animal Research 49(1): 59–62. https://doi.org/10.5958/0976-0555.2015.00013.8

Gupta V, Farooqui MM, Prakash A, Archana, Kumar P. (2017). Morphological and cytological differentiation of goat spleen (Capra hircus). Indian Journal of Animal Research 51(6): 1027–1032. https://doi.org/10.18805/ijar.v0iOF.7820

Halder A, Gaikwad M, Patra A, Chakraborty S. (2021). Cytological, histochemical, and ultrastructural study of the human fetal spleen of various gestational age with future implications in spleen transplantation: an anatomical perspective. Cureus 13(10): e18911. https://doi.org/10.7759/cureus.18911

Jaji A, Saidu AS, Mahre M, Yawulda MP, Girgiri IA, Tomar P, Dau F. (2019). Morphology, morphometry and histogenesis of the prenatal dromedary spleen. Macedonian Veterinary Review 42(2): 141–149. https://doi.org/10.2478/macvetrev-2019-0018

Khalel EM. (2010). Anatomical and histological study of the spleen in Iraqi sheep (Awasi sheep). Basrah Journal of Veterinary Research 9(2): 163–171. https://doi.org/10.33762/bvetr.2010.55061

Khalil M, Sultana SZ, Rahman M, Mannan S, Ahmed S, Ara ZG, Sultana ZR, Chowdhury AI. (2009). Study of prenatal and postnatal development of spleen of Gallus domesticus (Deshi chicken). Mymensingh Medical Journal 18(2): 169–174

Krause WJ, Cutts JH. (1986). Concise Text of Histology. 2nd edition. Williams & Wilkins, Baltimore, USA.

Kulkarni SS, Falzarano D. (2021). Unique aspects of adaptive immunity in camelids and their applications. Molecular Immunology 134: 102–108. https://doi.org/10.1016/j.molimm.2021.03.001

Maddox JF, Mackay CR, Brandon MR. (1987). Ontogeny of ovine lymphocytes. II. An immunohistological study on the development of T lymphocytes in the sheep fetal spleen. Immunology 62(1): 107–112.

Maina MM, Usende IL, Igwenagu E, Onyiche TE, Yusuf ZM, Ntung NO. (2014). Gross, histological and histomorphometric studies on the spleen of one-humped camel (Camelus dromedarius) found in the semi-arid region of North Eastern Nigeria. Journal of Veterinary Advances 4(10): 703–711. https://doi.org/10.5455/jva.20141025045543

Marwa-Babiker AM, Alkhodair KM, Abdelhay AM, Elseory AMA, Zolain HB, Al-Ramadan SY, Althnaian TA. (2023). Morphology of the spleen in the camel's fetus (Camelus dromedarius): gross anatomy, histology and scanning electron microscopic studies. Journal of Applied Veterinary Sciences 8(4): 54-61. https://doi:10.21608/JAVS.2023.219602.1250

Marwa-Babiker AM, Althnaian TA, Ali AM. (2022). Histological study of prenatal development of the spleen in camel (Camelus dromedarius). Journal of Camel Practice and Research 29(2): 251–255. https://doi.org/10.5958/2277-8934.2022.00035.2

Mebius RE, Kraal G. (2005). Structure and function of the spleen. Nature Reviews Immunology 5(8): 606–616. https://doi.org/10.1038/nri1669

Mukhia R, Mukherjee A, Sabnis A, Mukhia MR. (2016). Histogenesis of human fetal spleen. International Journal of Anatomy and Research 4(1): 2119–2124. https://doi.org/10.16965/ijar.2016.159

Papenfuss TL, Cesta MF. (2017). Spleen. In: Parker GA, editor, Immunopathology in Toxicology and Drug Development: Volume 2 – Organ Systems. Springer Cham, Switzerland. 37–57. https://doi.org/10.1007/978-3-319-47385-7_2

Rahman N, Tandon R, Ghaus F, Moinuddin A, Akram W, Faruqi NA. (2016). Comparative anatomy of spleen: Histomorphometric study in human, goat, buffalo, rabbit and rat. Academia Anatomica International 2(1): 28–32. https://doi.org/10.21276/aanat.2016.2.1.6

Srivani D, Pillai JJ. (2019). A study of histology & histogenesis of fetal spleen at different gestational ages. International Journal of Medical and Biomedical Studies 3(12): 74–78. https://doi.org/10.32553/ijmbs.v3i12.798

Thomas S, Sinha DN, Singh AK, Deopa D, Niranjan R. (2017). Histogenesis of human fetal spleen. National Journal of Clinical Anatomy 6(1): 1-8. https://doi.org/10.4103/2277-4025.297651

Vap L, Bohn AA. (2015). Hematology of camelids. Veterinary Clinics of North America: Exotic Animal Practice 18(1): 41–49. https://doi.org/10.1016/j.cvex.2014.09.010

Verma R, Gupta SK, Karmore SK, Shukla S, Barhaiya RK. (2018). Histomorphological and histochemical studies on spleen of Kadaknath fowl. Indian Journal of Veterinary Anatomy 30(2): 121–123.

Vondenhoff MFR, Desanti GE, Cupedo T, Bertrand JY, Cumano A, Kraal G, Mebius RE, Golub R. (2008). Separation of splenic red and white pulp occurs before birth in a LTαβ-independent manner. Journal of Leukocyte Biology 84(1): 152–161. https://doi.org/10.1189/jlb.0907659

Zidan M, Kassem A, Dougbag A, El Ghazzawi E, Abd El Aziz M, Pabst R. (2000). The spleen of the one-humped camel (Camelus dromedarius) has a unique histological structure. The Journal of Anatomy 196(3): 425–432. https://doi.org/10.1046/j.1469-7580.2000.19630425.x