Special Issue:

Emerging and Re-emerging Animal Health Challenges in Low and Middle-Income Countries

Prenatal and Histomorphological Development of Fungiform and Circumvallate Papillae in Local Awassi Sheep (Ovis aris)

Rusul Thamer Ali*, Jafar Ghazi Abbas Al-Jebori

College of Veterinary Medicine, Al-Qassim Green University, Iraq.

Received | June 25, 2024; Accepted | October 01, 2024; Published | December 04, 2024

*Correspondence | Rusul Thamer Ali, College of Veterinary Medicine, Al-Qassim Green University, Iraq; Email: [email protected]

Citation | Ali RT, Al-Jebori JGA (2024). Prenatal and histomorphological development of fungiform and circumvallate papillae in local Awassi sheep (Ovis aris). J. Anim. Health Prod. 12(s1): 187-195.

DOI | https://dx.doi.org/10.17582/journal.jahp/2024/12.s1.187.195

ISSN (Online) | 2308-2801

Copyright: 2024 by the authors. Licensee ResearchersLinks Ltd, England, UK.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

Introduction

Embryology, the tongue development begins from fourth week of embryo. the tongue is formed as five ridges originating from the pharyngeal arches (Sadler, 2022). The tongue is an extensible and muscular organ whose primary role is feeding, namely, in the stages of prehension, chewing and the swallowing of food. Although, they differ in characteristics, existence and distribution among animal species, lingual papillae are classified as gustatory and mechanical papillae, Gustatory papillae with taste buds are fungiform papillae, circumvallate papillae while mechanical papillae include lenticular papillae, conical papillae and filiform papillae (Emura et al., 2008). The surface of tongue was distinguished by great numbers of elevations named the lingual papillae which changed in size and shape according to the species of animals which distributed on the dorsum and divided into six types such as (filiform, fungiform and circumvallate) which presented in all domestic animal, while the lenticular papillae can be seen in the ruminants only, the tongue of sheep has five kinds of lingual papillae which were distribution on the dorsal surface of tongue which are conical, filiform, fungiform, circumvallate and lenticular papillae (Hassan and Abid, 2010). The tongue epithelial tissue is of non-keratinized stratified squamous; however, the tongue mucosal papillae have the keratinized mechanical form and seen as stratified squamous kind (Hejazi and Baroughi, 2013).

Currently, there are insufficient studies on the embryonic formation and development of papillae in sheep’s fetuses. Hence, this study attempts to analyze histomorphological description and the timing of first anlage of the circumvallate and fungiform papillae at prenatal periods.

MATERIALS AND METHODS

Experimental animals

The purpose of this work was to describe the histomorphological developmental of fungiform and circumvallate papillae in prenatal periods of local awassi sheep’s fetuses (Ovis aris) where experimental samples are gathered from September to November. The study is conducted on sheep fetuses from pregnant ewes that are slaughtered in Najaf’s and Babylon abattoirs for prenatal research. The sheep fetuses at prenatal stages distributed into three groups: First, second and third trimester of gestation according to the gestational age which determined depending on the crown rump length (CRL) by using of following formula (Y=2.74X+30.15) (Hejazi et al., 2013; Al-Jebori and Salih, 2022; Veeresh et al., 2022).

Sample collection and Light microscope technique

The sheep fetus’s tongue was preserved in buffered formalin (10%), dried out using a sequence of increasing alcohol concentrations, cleaned in xylene, and then embedded in paraffin wax. Using a rotary microtome, the blocks were sectioned at 5-6 μm thickness of slice According to (Al-Khakani et al., 2019; Al-Janabi et al., 2022), histological sections were stained with trichrome masons stain, periodic acid schiff (PAS), and Haematoxylin and Eosin (H and E). Olympus light microscope with USB digital camera attached to computer slides and various magnification settings was used to study the sections (Al-Jebori, 2014).

Statistical analysis

A computerized program (SPSS) version 21 was used to the statistical analysis of data had done by descriptive statistics.

Results and Discussion

First trimester of gestation (50-55) days

The body weight of sheep embryos was about 39.4±1.02 grams, tongue weight about 0.154±0.0053 gram and crown rump length was about (10.6±0.509) cm (Table 1 and Figure 1).

 

Morphological

The tongue at this stage where appeared whitish or colorless and opaque in appearance with small in size relatively compare with the advanced stages with irregular and an uneven dorsal surface, The dorsal surface of the tongue is smooth and slop relatively and the shape of the tongue is a vertical bar stable in the floor of the mouth cavity between ram of mandible set in proper mouth cavity and lingual papillae could not be observed at this age (Figure 2).

 

vestibule (green arrow) of the mouth cavity.

 

Table 1: Crown rump length, weight of embryo and tongue weight of sheep embryo in different ages of embryonic life.

Tongue weight (gram)	Embryo weight (gram)	Embryo length (mm)	Parameter/ Time
0.154±0.0053A	39.4±1.02A	10.6±0.509 A	50-55 days of gestation
1.426±0.0353B	256±2.91B	19.2±0.583B	70-75 days of gestation
5.426±0.374C	849.2±3.26C	30.4±0.927C	100-105 days of gestation
12.80±1.281D	1360±3.53D	41.4±1.886D	130-140 days of gestation

 

Values represent mean ±S.E. Different capital letters mean significant differences (P≤0.05) between different age.

 

Histologically

Histological observations showed that the tongue at this age has three layers: tunica mucosa with primitive of lingual papillae, undeferential mesenchymal tissue (Pluripotiantial tissue) and tunica muscularis (Figure 3). Tunica mucosa covered by epithelial cells which was stratified cuboidal or stratified squamous cells (non-keratinized) about 7-8 cellular layer, the dorsal lining of the tongue apex epithelium was thicker than the lateral borders and ventral side and there were signs of forming domed papillae at several points of the tongue epithelium, where showed there are primordium of development of undifferential lingual papillae may be filiform or fungiform papillae with advancement of gestation. The primordium of lingual papillae appears clearly on dorsal epithelium of apex tongue and absent on lateral borders and ventral surface (Figure 4). The layer of mesenchymal tissue of tongue sheep fetuses at 50-55 days of gestation showed to be consisted of undifferentiated mesenchymal cells that will eventually differentiate into various types of connective tissue like fibroblast, collagen fiber and myoblast rich with blood vessels. The tunica muscularis at first stage of gestation

 

 

composed of primitive muscle fiber not fully developed or prominent in the tongue tissue where noticed firstly the long and short strands of immature muscle fibers appear among the undifferentiation of mesenchymal tissue (Figure 5).

 

At second trimester of gestation (70-75) days

The body weight of sheep embryos in current stage at (70-75) days of gestation about (256±2.91) gram, tongue weight about (1.426±0.0353) gram and crown rump length about (19.2±0.583) cm (Table 1).

Morphologically

The tongue appeared more elongated flat organ with a flat surface and almost uniform in thickness and width throughout its length whitish or creamy opaque in color and consisting from three parts: apex (Apex linguae), body (Corpus linguae) and root (Radix linguae) more development of the pervious stage and appear impression of hard palate, the dorsal surface of the tongue appeared rough showing beginning of formation of lingual papillae scattered mostly at the tip and on the dorsum-linguae (Figure 6).

 

While histologically, the epithelial layer was distinctly stratified and was divided into dark basal and light superficial zones; a basal layer of cuboidal cells which dark stain in color with Haematoxylin and eosin, middle layer of squamous cells or hexagonal cells lighter in color than the previous layer by different stains with irregular or rounded centrally nuclei light in color and finally, superficial layer including flattened cells may be keratinization or non-keratinize on the dorsum of tongue (Figure 7).

 

At third trimester of gestation (100-105) and (130-140) days

The body weight of embryo at age (100-105 days) was 849.2 ± 3.26 grams, crown rump length was about 30.4±0.927cm. While at age (130-140 days). The body weight of sheep embryo in this study about (1360±3.53) grams and crown rump length in about (41.4 ±1.886) cm (Table 1).

Morphologically on the dorsal surface of the tongue sheep fetuses that appear rough due to presence of the lingual papillae and this papillae on the root area more developed than the filiform papillae in the apex area and also develop of conical and lenticular papillae, while the circumvallate papillae are not clearly defined. While n the age of (130-140 days) of gestation the fungiform and circumvallate papillae more development, the fungiform papillae they are flat mushroom shape present among the filiform of the anterior two-thirds of dorsum and are larger and more prominent than others types of papillae, such as filiform papillae. And the circumvallate papillae, are large in size and are arrangement an irregular double row on each side of caudal part of dorsum and about (18-24) on each side (Figure 8).

Histologically: The lingual papillae at (100-105 day) of tongue sheep fetuses continue to develop until they become more mature, visible with gestation advancement with the appearance of rudimentary or primitive of taste buds at fungiform papillae (Figure 10) and more clear on the lateral surface of circumvallate papillae (Figure 9).

 

 

The fungiform papilla observed are scattered among the filiform papillae on dorsal surface of body and apex to appear in different patterns and shapes of development and growth with advancement of gestation to be smaller than circumvallate and conical papillae and larger than filiform and lenticular have flask or rounded or oval like shape as evagination of unmesenchymal layer to epithelium with or without taste buds embedded within the epithelial layer and their connective tissue core surround by multiple layers of squamous epithelium cell tissue and The connective tissue core was continuous with lamina properia and there was no glands associated with these papillae and highly vascularized with blood capillaries may be including lymphocytes, fibroblasts and macrophages. Also seen bundle of collagen fibers appeared to run parallel to the longitudinal axis of the papillae and continued into secondary papillae (Figures 11 and 12).

 

 

The circum-vallate papillae were large flattened circumscribed papillae with minute elevation from the lingual surface which appear in various morphohistological developmental stages with many different shapes, patterns and sizes according to evolution periods and growth of these papillae surrounded by deep circular trenches or moats located on both sides of torus linguae or It was situated on the dorsolateral surface of the caudal part extended from the torus linguae to root of tongue relatively, arranged in two rows on each side of tongue. The papillae entirely covered by a moderately or delicate cornified stratified squamous epithelium layer which was thicker on the dorsal surface, and it is almost non-existent on lateral sides of papillae. The upper epithelium revealed several small secondary papillae. Some of the secondary papillae which located in the angles reached to the half of the epithelium and other special on the dorso-lateral sides of the papillae. The epithelium of this papillae is lined by stratified squamous epithelium tissue that covering the surface, with invagination known as taste buds embedded within the epithelium and also consider of this papillae houses for taste buds (Figure 13).

 

The connective tissue core was continuous with lamina properia and there were glands associated with these papillae and highly vascularized with blood capillaries may be including lymphocytes, fibroblasts and macrophages with bundle of collagen fibers appeared to run parallel to the longitudinal axis of the papillae and continued into secondary papillae (Figure 14).

 

Lingual gland: The current study appear two types of gland, the first associated with circumvallate papillae called von-abners gland (Figure 15) and the other called the weber gland associated with root of tongue in deep muscular tissue (Figure 16).

Von-Ebner’s gland: The von-Ebner’s gland is a serious compound tubuloalveolar gland, located beneath the circumvallate papillae in the lamina propria and extend deeply in the submucosa until reach to the muscular layers These glands consist of variable numbers of lobules in different size and their ducts open at the bottom of the groove surrounding the circumvallate papillae The lobules were seen separated from each other by muscles bundle, adipose tissue and little amount of loose connective tissue which rich in blood vessels and nerve fibers. The lobules consist of densely packed acini cells, lined by pyramidal cells. The serous acini cells have stained darkly with (H and E) stain from pink to purple. while appearing light with (PAS) stain due to secreted serous fluid and rich by enzyme and have round nuclei that lie toward the base of cell with relatively few serous demilunes (Figure 17).

 

 

Weber’s glands (Posterior lingual gland): The Weber’s gland is a mucous compound branched acinar gland appear more development than von-abners gland consist of acini cluster of secretory cells that produce thick, clear mucous secretion, the secretion is released into ducts that empty into the oral cavity, and they founded in the root region and the cells which are cuboidal or columnar in shape (Figure 18).

 

 

Taste buds for the first time, taste buds of tongue sheep fetuses appear more clear and growth at third trimester of gestation in various shape, pattern and sizes to be oval, rounded or elongated bodies in lateral and dorsal surfaces of epithelial tissue of fungiform and un lateral sides of circumvallate papillae epithelium extending from basement membrane to surface, the apical free ends of these cells converge on small opening on the surface of the epithelium called taste pore, (Figures 11, 13, 14) and which has three cell types; such as sustentacular or supportive cells, neuroepithelial cells and basal or stem cells; Basal cells, these cells were similar in shape to those in the stratum basalis but gave darker appearance these cells usually located at periphery of taste buds near the basement membrane. Taste cells (gustatory cells), spindle-shape neuroepithelial or taste cells. Each taste cell exhibits an elongated deeply stained nucleus these cells located nearly in center of taste buds and the distal end present delicate processes extending to the outer taste pore which are taste hair. Supporting cells (Sustentacular cells), they rounded and wide cells which exhibit darker cytoplasm and slender, dark nucleus the sustentacular cells found in middle part of taste buds (Figure 19).

 

The tongue at first trimester (50-55) days of gestation where appeared whitish or colorless and opaque in appearance with small in size relatively compare with the advanced stages with irregular and an uneven dorsal surface, the surface of tongue was smooth and lingual papillae could not be observed neither by naked eye. The pervious result agrees (Bello et al., 2015) in camel who mentioned that the tongue at first trimester, were seen as smooth muscle mass, with almost uniform width and thickness throughout the length. They were uniformly pinkish, no pigmentation and no visual evidence of lingual papillae. While histologically observations showed that the tongue at first trimester has three layers: Tunica mucosa with primitive of lingual papillae, undifferential mesenchymal tissue (Pluripotiantial tissue) and tunica muscularis. Tunica mucosa covered by epithelial cells which was stratified cuboidal or stratified squamous cells (non-keratinized) about 7-8 cellular layer. This current study agreement with a previous study (Hejazi and Baroughi, 2013) who have mentioned that the epithelial lining of the tongue is cubic in this age of gestation without indication of differentiation of the tongue mucosa epithelium. The dorsal lining of the tongue apex epithelium was thicker than the lateral borders and ventral side and there were signs of forming domed papillae at several points of the tongue epithelium, where showed there are primordium of development of undifferential lingual papillae may be filiform or fungiform papillae with advancement of gestation. The primordium of lingual papillae appears clearly on dorsal epithelium of apex tongue and absent on lateral borders and ventral surface, The pervious results agreement with (Mistretta and Haus, 1996) in sheep fetuses who mentioned that the early fetal tongue at 49-51 days of gestation has a relatively homogeneous epithelium with occasional undulations without obvious fungiform or circumvallate papilla development. The layer of mesenchymal tissue of tongue sheep fetuses at 50-55 days of gestation showed be consists of undifferentiated mesenchymal cells that will eventually differentiate into various types of connective tissue like fibroblast, collagen fiber and myoblast rich with blood vessels, This result is agreement with (Uppal et al., 2006) buffalo who mention that the connective tissue underneath the epithelium was composed of mesenchymal tissue differentiating into different types of cells and fibers. The tunica muscularis at first stage of gestation composed of primitive muscle fiber not fully developed or prominent in the tongue tissue where noticed firstly the long and short strands of immature muscle fibers appear among the undifferentiation of mesenchymal tissue. While at age (70-75) days of gestation the tongue appeared more elongated flat organ with a flat surface and almost uniform in thickness and width throughout its length whitish or creamy opaque in color and consisting from three parts: apex (apex linguae), body (corpus linguae) and root (radix linguae) more development of the pervious stage, dorsal surface of the tongue appeared rough showing beginning of formation of lingual papillae scattered mostly at the tip and on the dorsum-linguae agreement with result (Abou-Elhamd et al, 2015) in camel who mentioned that the first sign of lingual papillae was demonstrated on the surface of the lingual root at 4.7cm CVRL (78 days) and then after became visualized on the body and apex of the tongue at 8.2cm CVRL (88 days). Histologically, the epithelial layer of the tongue was distinctly stratified and was divided into dark basal and light superficial zones; a basal layer of cuboidal cells which dark stain in color with Haematoxylin and eosin, middle layer of squamous cells or hexagonal cells lighter in color than the previous layer by different stains with irregular or rounded centrally nuclei light in color and finally, superficial layer including flattened cells may be keratinization or non-keratinize on the dorsum of tongue, in contrast to (Chudasama, 2016) in goat who mention that the tongue goat fetuses at the same age relatively (67) days gestation, the lamina epithelialis was distinctly stratified and divided into dark basal (cuboidal or columnar type of cells), light middle and superficial flattened cells layer without keratinization, while at this age (119 days) onwards epithelium of dorsal surface revealed a slight degree of keratinization. While n the age of (130-140 days) of gestation the fungiform and circumvallate papillae more development, the fungiform papillae they are flat mushroom shape present among the filiform of the anterior two-thirds of dorsum and are larger and more prominent than other types of papillae, such as filiform papillae. this result is agree with the (Kumar et al., 2015) in goat that mentioned the fungiform papillae mushroom like were distributed at the tip on dorsal as well as on lateral edges. Body was well developed with but ton like fungiform papillae. Those papillae at the lateral edges were larger as compared to those on dorsum of the tongue. while in pre-pubertal (Al-Bazii et al., 2020) sheep who reported that the Fungiform papillae, which were dome-shaped and had multiple taste buds in the apex and lateral papillae epithelium. And the circumvallate papillae, are large in size and are arrangement an irregular double row on each side of caudal part of dorsum and about (18-24) on each side. This finding is in agreement with the previous studies (Bello et al., 2015) in camel, there were numerous large circumvallate papillae arranged on each side closer to one another forming two lines almost parallel to the rim of lingual torus. The shape and size of the papillae revealed remarkable differences with advancement in gestation; they were not identical or symmetrical in the two lines in the same specimen. The lingual papillae at (100-105 day) of tongue sheep fetuses continue to develop until they become more mature, visible with gestation advancement with the appearance of rudimentary or primitive of taste buds at fungiform papillae and more clear on the lateral surface of circumvallate papillae. this study agree with (Igbokwe and Okolie, 2009) in goat who reported that the goat fetuses at 90-day, looked the lingual papilla continued to mature with some rudiments of taste buds apparent on the fungiform papillae with presence and formed of filiform papillae. Result of description of fungiform and circumvallate papillae is agreement with agreement with (Bello et al, 2015) in camel who mention that observed of taste buds on both sides of the secondary groove and within the epithelial lining of deep sinuses in the lateral papillary wall at third trimester of gestation while, (Abou-Elhamd et al., 2015) reported in camel that the fungiform papillae, up to (110 days) of gestation, developed in the form of epithelial placodes or (epithelial thickening) which became invaded later on from below by mesenchymal cores and the vallate papillae were first demonstrated in the form of a circular groove resulting from sloughing of superficial epithelial cells and differential growth in the deep ones along the above mentioned groove The papilla appears as small prominence surrounded by circular groove and an annular pad of the surrounding lingual mucosa.

Lingual gland: The current study appears two types of gland, the first associated with circumvallate papillae called von-abners gland and the other called the weber gland associated with root of tongue in deep muscular tissue. This result agrees with previous finding (Mistretta and Bradley, 1983) who mention that the glands were appeared in the foetal tongue at 110 days of gestation in sheep. Also agree with (Dar et al., 2015) goat who reported that the gland were distributed in the submucosa as well as in between the skeletal muscle bundles. When I see the gland under the light microscope, I notice that there are two types of glands. Von-Ebner’s gland, was a serious compound tubuloalveolar gland, located beneath the circumvallate papillae in the lamina propria and extend deeply in the submucosa until reach to the muscular layers this result is agree with (Dar et al., 2015) in goat who mention that the first indication of appearance of Von Ebner’s glands was observed at 120 days in the tongue of goat foetal. These glandular acini appeared by 116 days (Uppal et al., 2006) and 122 days in the tongue of buffalo foetii which had characteristics of serous cells. Taste buds for the first time, taste buds of tongue sheep fetuses appear more clear and growth at third trimester of gestation in various shape, pattern and sizes to be oval, rounded or elongated bodies in lateral and dorsal surfaces of epithelial tissue of fungiform and un lateral sides of circumvallate papillae epithelium extending from basement membrane to surface, the apical free ends of these cells converge on small opening on the surface of the epithelium called taste pore, and which has three cell types; Basal cells, these cells were similar in shape to those in the stratum basalis but gave darker appearance. These cells usually located at periphery of taste buds near the basement membrane. Taste cells (gustatory cells), spindle-shape neuroepithelial or taste cells. Each taste cell exhibits an elongated deeply stained nucleus. These cells located nearly in centre of taste buds and the distal end present delicate processes extending to the outer taste pore which are taste hair. Supporting cells (Sustentacular cells), they rounded and wide cells which exhibit darker cytoplasm and slender, dark nucleus. The sustentacular cells found in middle part of taste buds. This result is similar to (Bello et al., 2015) in camel who mention that the taste buds were observed on both sides of the secondary groove and within the epithelial lining of deep sinuses in the lateral papillary wall. The taste buds comprised 3 cell types, viz. neuroepithelial cells, sustentacular cells and basal cells. The neuroepithelial or gustatory cells were having lightly stained elongated nuclei and their distinct processes extended towards taste pore while supporting cells had dark nuclei and variable shape. The basal cells were found at the base of taste bud. As the surface epithelium was invaded by the bud the taste pore became apparent at 80.0 cm CVR length (254 day).

Conclusions and Recommendations

In case of local awassi sheep fetuses at the first and second trimester the tongue occupies the greater part of proper oral cavity and extends into the oropharynx and whitish or colorless and opaque in appearance with small in size relatively compare with the advanced stages while at third trimester the tongue is relatively darkish. At second trimester, the transverse edges of hard palate became appear impression on the dorsal surface of the body and tip for tongue sheep fetuses. And primordium of lingual papillae on dorsal surface of the tongue. All the gross biometrical parameters prenatal (length, width and thickness) increased with the advanced in age of the fetus and there was significant variation in the gross biometry. The cornified layer is increases with advanced stage of ages fetuses. During second stage of gestation appear circumvallate papillae and more development during third stage of gestation and appear of taste buds.

The Weber’s gland that found in root region has appeared more development than von-abners gland.

Acknowledgements

Thank you very much to the chairman of the Department of Anatomy, Histology, and Embryology at AL- Qasim Green University

Novelty Statement

Presnt study can identifying breed- specific difference in anatomy and hostology of tongue for awassi sheep.

Author’s Contribution

RUSUL THAMER: Research proposal, design, experimental process and writing pf report.

JAFAR GHAZI AL- JEBORI Did reseach defining, timelining, experimental process and drafting manuscript.

Ethical approval

The experimental procedures were approved by the Institutional Animal Ethics Committee and conducted at Veterinary Medicine Collage, Al-Qasim Green University, Iraq.

Conflict of interest

The authors have declared no conflict of interest.

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