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Journal of the Anatomical Society of India

Histogenesis And Morphometric Study Of Human Foetal Submandibular Salivary Gland

Author(s): Sivakumar, M; Sud. M; Vathsala, V.

Vol. 52, No. 1 (2003-01 - 2003-12)

Department of Anatomy, Pondicherry Institute of Medical Sciences, Pondicherry, INDIA

Abstract

Histogenesis and morphometric study of submandibular salivary gland in 25 normal human foetuses at different stages of development was done. It was observed that the gland was undifferentiated at 10th week and active differentiation started at 12th week. The diameter of tubules reached the maximum between 18 - 22 weeks. By 28 weeks of gestation 90 - 95% of tubules were canalised. The number of lobes increased from 2 at 16th week to 13 by full term.

Key words: Submandibular salivary gland, ducts, ductules, terminal tubule, acini.

Introduction:

The submandibular salivary gland being one of the major salivary glands contributes to substantial amount of saliva secreted into the mouth. Various studies have been done on this gland in human foetuses and adults. Gibson (1983) studied the submandibular gland of six human foetuses using light and electron microscopes and observed lumen in the acini and ducts at the age of 13.5 to 16 weeks. The time of formation and number of acini, ducts and the functional maturity of the gland were studied by El - Mohandes et al (1987) in human foetuses ranging from 10 weeks to full term. In a study by Martinez et al (1991) in 8 foetuses, the submandibular gland was found to appear before the parotid gland. The morphogenetic events in submandibular gland were studied in 37 human foetuses and the gland was found to grow from the medial paralingual groove (Merida-Velasco et al, 1993). The location of orifice of human submandibular gland was observed to be in the medial paralingual sulcus. Apart from the above cited studies, many experiments were done on hamster and mice (Chaudry et al, 1986; Watanabe et al, 1997). Culter and Mooradian (1987) found canalisation and lumen formation at 17th day of gestation in rat submandibular gland.

As the above studies left some lapses and lacunae on the histogenesis of human prenatal submandibular gland, the present work was undertaken with an aim to highlight few of the ontogenetic events in morphogenesis and histogenesis of human foetal submandibular salivary gland.

Materials and Methods:

25 normal human foetuses ranging from 10 weeks to full term were chosen for the study. Age was assessed using crown-rump length (CRL) and correlated with available history. They were fixed in 10% formalin and after a week's time submandibular glands were dissected, their relations and duct patterns were noted and then they were removed. Their weight and dimensions like length, breadth and thickness were measured and tabulated.

The glands were subjected to routine histological processing. Sections of 5 m thickness were cut and stained with Haematoxylin and Eosin and Masson's trichrome stain. The number of lobes and lobules, the time of appearance of ducts, acini and their canalisation, the diameter and epithelial lining of tubules were observed and recorded. The foetuses ranging from 10 weeks of gestation to full term were divided into 3 groups viz., Group I [10-16 weeks], Group II [18-25 weeks], and Group III [28 weeks - full term].

Observations:

Group I [10 - 16 weeks]

The morphometric study of the submandibular gland showed that on average it measured 8.9 mm in length 5.7 mm in breadth, 4 mm in thickness and weighed 23 mg [Table - I].

At 10 weeks the gland was seen as a very small mass without any lobar and lobular subdivisions. The cells were clustered as cords or bunches located over a sheet of mesenchymal tissue. A linear cluster of cells was just forming a long duct and the rest were uncanalised tubules. About 15 to 18 tubules were found in the form of small round clusters of cells. So till 10th week, no lobulation, no organised duct pattern and no canalised acini were seen.

Table I: Dimensions and weight of human foetal submandibular salivary glands

  Length (mm) Breadth (mm) Thickness (mm) Weight (mg)
Group I (10-16 weeks)
Rt 9 5.8 4 24
Lt 8.8 5.5 4 22
Average 8.9 5.7 4 23
Group II (18 - 25 weeks)
Rt 15 9 6.5 57
Lt 14.8 9 6.5 53.5
Average 14.9 9 6.5 55.3
Group III (28 weeks full term)
Rt 17 12 8 111.5
Lt 16.5 11 8 109
Average 16.8 11.5 8 110.3

By 12 - 14 weeks, the lobulation started and the 16th week gland had lobar division also with 2 major lobes and many small lobules. The lobules increased from 7 in 12th week to 20 in 16th week. The number of tubules increased to a greater extent and they showed canalisation starting first at 12th week, in which 25% were canalised. This proportion of canalisation changed gradually from 60% in 14th week to 75% in 16th week.

The lining epithelium also reduced from 3 - 4 layers to 2 layers in 16th week. The diameter of tubules ranged from 20 m in 12th week to 30.5 m in 16th week, which was the maximum in this foetal age group. The connective tissue partitions started forming incomplete septa in this group. The overall features in this group were increased lobulation, increased number and diameter of terminal tubules and redution in the eipthelial lining of tubules [Fig. 1].

Group II [18 - 25 weeks]:

The gland was 14.9 mm in length, 9 mm in breadth, 6.5 mm in thickness and weighed 55.3 mg. When compared to Group I, the dimensions of the gland increased 1.6 times and weight increased 2.4 times (Table - I).

The gland acquired a connective tissue capsule, more lobes and lobules were formed and lobules became well delineated by prominent septa. At 18th week the number of lobes were 3 and lobules were 22. At 22 weeks the lobules were 24 and by 25th week they were 30 - 35. The interlobular ducts started appearing from 22nd week. The number of canalised tubules showed a steep increase, 75% in 18th week, 80% in 22nd week, and 90% in 25th week. The diameter of the terminal tubules reached the maximum by 18 - 22 weeks. It was 40 m in 22nd week and 30.5 m in 25th week and the lining epithelium of the tubules was double layered till 25th week [Table. II] & [Fig. 2 & 3.].

Group III [28week - full term]

The gland measured 16.8 mm in length, 11.5 mm in breadth, 8mm in thickness and weighed 110.3 mg. The dimensions increased 2 times and the weight increased 5 times than that of Group I (Table - I).

Lobes and lobules increased much more and there were 10-13 lobes in 28th week and 13 in the full term group. The terminal tubules formed acini, which were still lined by double layered epithelium but some also had single layer of lining cells. By 28 weeks 90-95% of tubules were canalised and this continued to be the same till full term. The diameter showed an increase from 20 to 30.5 m.

Table II : Microscopic parameters of submandibular glands.

Age of foetus [weeks] No. of lobes Average No. of lobules Average No. of canalised tubules Average No. of uncanalised tubules Average diameter of terminal tubules [m]
10 - - - 16 20
12 - 7 45 135 20
14 - 11 26 17 30
16 2 20 36 12 30.5
18 3 22 30 10 30.5
22 4 24 34 8 40
25 6 32 42 5 30.5
28 11 40 45 5 20
36 13 110 120 4 30.5

In the full term group the connective tissue showed a further marked reduction and well demarcated lobes and lobules were found. The overall features of this group were increase in the number of acini, lobes and lobules and decreased diameter of the acini compared to the previous two groups. The connective tissue also formed encapsulations with single layer of lining cells around the terminal branching of all ductules and acini in all the age groups [Fig. 4].

Discussion:

In Group I [10 - 16 weeks], in the 10th week foetus the gland was in the undifferentiated stage and till then there was no lobulation, no organised duct system and no canalisation. But the proliferation was active from 12th week and it was more in 16th week as reflected by the first appearance of lobes in this group. The canalisation of the ducts also started in 12th week and reached the maximum in 16th week, where it became 75% from 25% in the 12th week. The epithelium of the ducts and terminal tubules changed from 3 - 4 layered to 2 layered in 16th week and so the lumen became prominent. The diameter of the terminal tubules increased from 20m to 30.5m. The main features of this group were inceased lobulation, increased number of terminal tubules or ductules and decrease in the number of lining epithelial cells. All the increased parameter in the first group were due to proliferation & canalisation of the terminal ductules. It was not complete till the end of 16 weeks. These terminal tubules even though stated as having secretory material, we feel should not be called as acini as reported by Gibson (1983) and El - Mohandes et al, (1987), as these are only branching terminal part of the duct system which coincides with the reports of Yaku (1983). The connective tissue elements were also prominent, which is an additional proof for the lack of glandular maturity in the first group.

In Group II [18 - 25 weeks], the connective tissue partitions created more number of lobes and lobules. This lobulation was stable till 25th week as the differentiation was not much in this period and the appearance of interlobular ducts only shows that there is further proliferation and differentiation of duct system. Increase in canalised tubules from 75% to 90% in this group, also proved the fact that the ductal proliferation was more. The increased diameter of the terminal tubules in this group was probably due to the functional activity of these as evidenced by El - Mohandes et al (1987), who state that these are secretory for a short period in the 2nd trimester and disappear in 3rd trimester. So the increased lobulation and increase in the size of the gland in this group were mainly due to the ductal proliferation.

In Group III [28 weeks - full term], the steep increase seen in the number of lobules was due to the formation of secretory acini and ductal branching. These, still showing double layered epithelium except for a few in the full term and the diameter of these end pieces showing a decline compared to the previous group, all prove that these were just forming acini and not fully mature even at full term. It was observed that these acini developed from the terminal tubules, which coincided with the observations of Chaudry et al (1986). They observed from their work on hamster submandibular gland that the acini developed from the periphery of terminal tubules, and that these terminal tubules also showed some secretory activity initially as these had precursors for both acinar and myoepithelial cells.

The connective tissue encapsulation seen around the terminal branches of ductules and acini, throughout the foetal period [Fig. 1] is not reported in any of the human study except for one by Watanabe et al (1997) on mouse submandibular gland. They stated that the ductal and acinar cells were enveloped by bundles of collagen fibrils disposed in several directions, in early stages of development. We observed that there were regularly arranged collagen fibrils, which remained till the full term period.

Increase in the size and weight of the gland from 12 weeks to full term [Table - I] was due to increased ductal proliferation, increased lobulation and connective tissue septa formation. Gibson (1983) reported that the human submandibular gland had the ability to become fully mature by birth as he could see secretory activity even in the 16th week. From our study we found that this could be due to the ductules which are secretory in that stage as we saw the acini formation only in the third group and the acini were lined by double layered epithelium even in the full term group except for a few. This shows that they were not mature and this finding is supported by El - Mohandes et al (1987), who also noticed the secretory activity in 16th week and found them to be disappearing in 28th week.

Henceforth we hypothetically categorise that the active differentiation starts at 12th week, the ductal proliferation is maximum by 18 - 25 weeks, the actual glandular acini start forming at 28th week [Group III] and the gland does not become fully mature even in the full term group.

References:

  1. Chaudry, A.P; Cutler, L.S; Schmutz, J.A; Yamane, G.M; Pierri, L.K; Sunderraj, M. [Jul 1986]: Development of the hamster submandibular gland. II. The ductal system. Journal of submicroscopic cytology. 18(3): 529-536.
  2. Cutler, LS; Mooradian, B.A. [Oct 1987]: Lumen formation during development of the rat Submandibular gland. Journal of Dental Research. 66(10): 1559-1562.
  3. El - Mohandes, E.A; Botros, K.G; Bondok A.A. (1987) : Prenatal development of the human submandibular gland. Acta Anatomica. 130(3): 213-218.
  4. Gibson, M.H. (1983): The prenatal human submandibular gland: a histological, histo-chemical and ultrastructural study. Anatomischer Anzeiger. 153(1): 91-105.
  5. Martinez, G; Caltabiano, C; Leonardi, R; Canterella, M.I. [1991]: Histo-ontogenetic study of the major salivary glands and Chievitz's organ. Stomatologia Mediterrania. 11(1): 33 37.
  6. Merida - Velasco, J.A. ; Sanchez - Montesinos, I; Espin - Ferra, J; Garcia - Garcia, J.D; Garcia-Gomez, S; Roldan- Schilling, V. [Aug. 1993]: Development of the human submandibular salivary gland. Journal of Dental Research 72(8): 1227-1232.
  7. Watanabe, I; Jin, C; Nagata, T. [Apr. 1997]: Field emission SEM, conventional TEM and HVTEM study of submandibular gland in prenatal and postnatal aging mouse. Histology and Histopathology. 12(2): 447-457.
  8. Watanabe, I; Nagata, T; Jin, C; Heyn, R; Motta, P.M. [Jan- Mar 1997]: Development of mouse submandibular gland studied by field emission scanning Electron microscopy. Italian Journal of Anatomy and Embryology. 102(1): 49-57.
  9. Yaku, Y. [Dec 1983] : Ultrastructural studies on the development of human fetal salivary glands. Archivum Histologicum Japonicum 46(5): 677-690.

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Fig. 1

Microphotograph of submandibular gland of 14 week foetus showing mesenchyme [MS], branching duct and ductule [Br], uncanalised tubule [UC] and connective tissue capsule [CC]. [Masson's trichrome stain x100]

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Fig. 2

Microphotograph of submandibular gland of 22 week foetus showing uncanalised tubule [UC], canalised tubule [CT] and interlobular duct [ID]. [Masson's trichrome stain x100].

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Fig. 3

Microphotograph of submandibular gland of 22 week foetus showing double layered tubule [DT] and uncanalised tubule [UC] [Masson's trichrome stain x400].

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Fig. 4

Microphotograph of submandibular gland of full term foetus showing canalised larger acinus [CA], canalised larger terminal ductule [CT], single layered acinus [SA and uncanalised tubule [UC} [Haematoxylin & Eosin x400]

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