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Jornal de Pediatria

Print version ISSN 0021-7557On-line version ISSN 1678-4782

J. Pediatr. (Rio J.) vol.94 no.6 Porto Alegre Nov./Dec. 2018

http://dx.doi.org/10.1016/j.jped.2017.08.009 

Original articles

Tongue development in stillborns autopsied at different gestational ages, ☆☆

Laura S. Aguiara 

Guilherme R. Julianoa 

Luciano A.M. Silveirab  * 

Mariana S. Oliveiraa 

Bianca G.S. Torquatoa 

Gabriela R. Julianoa 

Márcia F. Araújoa 

Sanivia Aparecida L. Pereiraa 

Vicente de Paula A. Teixeirac 

Mara Lúcia F. Ferraza 

aUniversidade Federal do Triângulo Mineiro (UFTM), Uberaba, MG, Brazil

bUniversidade Federal do Triângulo Mineiro (UFTM), Departamento de Cirurgia, Programa de Pós-Graduação em Ciências da Saúde, Uberaba, MG, Brazil

cUniversidade Federal do Triângulo Mineiro (UFTM), Instituto de Ciências Biológicas e Naturais, Uberaba, MG, Brazil

Abstract

Objectives:

This study aimed to analyze, through the morphometric method, the perimeter and length of the tongue, the collagen fibers, and the perimeter of blood vessels at different gestational ages and fetal weights.

Material and methods:

Tongues (n = 55) of stillborns autopsied at 23-40 weeks of gestational age were macroscopically analyzed, and their length and perimeter were measured. Fifty-five tongue fragments were collected through a longitudinal section in the region that accompanies the median lingual sulcus and histologically processed. Slides were stained with picrosirius and immunolabeled with CD31 antibody. Quantification was performed on collagen fibers under polarized light, and on the perimeter of vessels with the CD31.

Results:

A positive and significant correlation of gestational age with tongue perimeter and length was found. There was a positive and significant correlation between collagen fibers and gestational age, as well as between gestational age and the perimeter of blood vessels. Between collagen fibers and fetal weight, a positive and significant increase was observed. Regarding the correlation between the perimeter of blood vessels and the fetal weight, an increase was observed.

Conclusion:

As gestational age advances, there is an increase in tongue perimeter and length, in the percentage of collagen fibers, and in vascular perimeter, demonstrating that tongue formation is directly related to tongue growth and development.

KEYWORDS Gestational age; Stillborn; Autopsy

Introduction

Pediatric autopsy is an important study of the structural and functional differences of the organs according to the time of fetal development. In the autopsy, the estimation of the gestational age (GA) is important to identify whether fetal development was occurring normally, to determine the death time in relation to the birth, to ascertain the diagnosis of the diseases that are specific to that developmental stage, and to detect those children classified as risk in the neonatal period.1

During examination, the evaluation of the tongue provides a variety of information, as it is a special organ of reception, chewing, swallowing, speaking, and tasting. Evidences from mammalian studies suggests that it is composed of muscle cells that have different arrangements in origin and insertion, and different histochemical properties in comparison with other skeletal muscles.2,3

The development of the tongue is described as a relatively rapid process, which begins between the fourth and fifth week of intrauterine life. This process has a remarkable effect on the oral cavity4; therefore, it is extremely important for the development of the stomatognathic system that the tongue develops correctly.5 There appears to be a synchrony in the formation of the orofacial complex since, from the 14th week onwards, the muscles of the oropharyngeal region are sufficiently advanced to move the tongue, coinciding with peaks in the growth of the head circumference that occur between the 15th and 17th week.6,7

Collagen is expressed in the tongue in the early stages of development, and is detectable in the mesenchyme derived from cranial neural crest cells (CNCC), adjacent to the tongue epithelium8 and in tendons of the extrinsic muscles, which connect the tongue to the mandible.9 The connective tissue and the vascular system of the tongue are derived from the CNCC, while most of its muscles originate from myoblasts that migrated from the occipital somites.10

Endothelial cells play a key role in the control of coagulation, thrombosis, vascular tone, permeability, inflammation, tissue repair, and angiogenesis.11 They constitute a heterogeneous population of cells in the human body. Functions and molecular characteristics of endothelial cells vary along the vascular tree and in the same organ between different vessels, as for example, phenotypic variations can occur in the expression of the CD31 molecule in these cells.12-14

Ultrasound examinations have indicated a highly significant correlation between fetal tongue circumference and gestational age (14 to 26 weeks).15 This data may be useful in the prenatal diagnosis of suspected congenital syndromes that include, among its manifestations, tongue growth disorders and GA estimation.12

The autopsy material is very rich for research, since through macro- and microscopic analyses it is possible to make feasible research studies with clinical diagnoses and detection of structural abnormalities. The autopsy is considered an important diagnostic method for the physician, since it allows documenting and comparing clinical and pathological cases.1 In pediatric autopsies, the hallux-calcaneus length (HCL) is a reliable parameter to establish GA in fetuses and stillbirths. The GA obtained by HCL is taken by measuring the length of the foot, from the heel to the tip of the hallux.16

The aim of this study was to analyze, through the morphometric method, the perimeter and length of the tongue, the collagen fibers, the perimeter of the blood vessels, at different GAs and in relation to the fetal weight. It can contribute as a new method to estimate GA through the tongue development.

Material and methods

This was a retrospective study, approved by the Ethics Committee of the Federal University of Triângulo Mineiro, under protocol No. 1158.

Of the 152 pediatric autopsy reports analyzed, those of 55 stillborns autopsied by the General Pathology Discipline at the Clinical Hospital of the Federal University of Triângulo Mineiro (HC/UFTM), Uberaba, State of Minas Gerais, from 1994 to 2015 were selected. The anatomopathological examination was performed by two pathologists, and the information obtained from the autopsy reports was GA, determined using the HCL method (hallux-calcaneus length), and fetal weight.

Inclusion criteria were GA between 23 and 40 weeks, those with data of gender and fetal weight, and those in which the tongue was in good preservation condition. The exclusion criteria were stillborn infants with malformations and lack of data in reports such as GA, fetal weight and gender. Moreover, any cases with intrauterine growth restriction or another alteration were excluded.

Measurement of tongue length and perimeter

The 55 tongues analyzed were arranged on the macroscopy laboratory bench and identified individually, with the respective autopsy number, along with a ruler for later calibration in the ImageJ® Software (National Institutes of Health, USA). All photographs were taken from the same distance (30 cm) using a Canon Rebel® camera (Canon, Tokyo, Japan). Morphometric analyses were performed measuring the length from the glossoepiglottic fold to the apex of the tongue; to obtain the perimeter of the tongue, the contour was measured throughout the macroscopic extension.

Sample collection and histopathological processing

Fifty-five tongue fragments from autopsied stillborns recovered in the archive of biological material of the discipline of General Pathology (UFTM) were used. Fragments were removed through a longitudinal section in the region that accompanies the median lingual sulcus, with a thickness of approximately 0.5 cm. Serial cuts of 4 µm in thickness were then performed. Slides were stained with Picrosirius (PS; saturated aqueous solution of picric acid added with 0.1 g% Sirius red F3B) (Bayer, Leverkusen, Germany) with counterstaining by hematoxylin, and a slide was used for immunohistochemistry.

Morphometric analysis of collagen fibers

The PS-stained slide was analyzed for quantification of collagen fibers. The number of fields for evaluation and quantification of collagen fibers of the longitudinal section of the tongue, at different GAs, was defined as four quadrants and ten fields per quadrant of the histological section were analyzed. The area of collagen fibers under polarized light presented a birefringent appearance, ranging from orange to red (Fig. 1). Collagen fibers were marked by the observer to obtain the percentage of collagen per field analyzed. Thus, the field image was digitized using a camera coupled to a microscope with a Leica Qwin Plus® image analyzer (Leica Microsystems Inc, IL, USA). Morphometry was performed with Leica Qwin Plus® software image analyzer system (Leica Microsystems Inc, IL, USA), with a 10× objective lens (final magnification of 320×).

Figure 1 Micrographs of stillborn tongue fragments examined under polarized light, showing the birefringent collagen fibers (arrows) (Picrosirius - 10×-320× final magnification) at different gestational ages (GA). (A) GA: 23 weeks; (B) GA: 28 weeks; (C) GA: 34 weeks; (D) GA: 37 weeks; (E) GA: 39 weeks, and (F) GA: 40 weeks. 

Immunohistochemical analysis

Immunohistochemistry was performed to identify anti-CD31 positivity. The number of fields for evaluation and quantification of the CD31 marker in the longitudinal section of the tongue, at different GAs, was defined as four quadrants and tend fields per quadrant of the histological section were analyzed. Measurements were taken using a video camera coupled to a light microscope, and these to a computer with the image analyzer system Axiovision SE64 Rel. 4.9.1® software. The perimeter of blood vessels was measured using ImageJ® Software (National Institutes of Health, USA), with an objective lens 100× (final magnification 3250×; Fig. 2).

Figure 2 Micrographs of stillborn tongue fragments examined under light microscopy, showing the increase in anti-CD31 immunolabeled blood vessels (arrows) (objective 100×-3250× final magnification) at different gestational ages (GA). (A) GA: 23 weeks; (B) GA: 28 weeks; (C) GA: 34 weeks; (D) GA: 37 weeks; (E) GA: 39 weeks, and (F) GA: 40 weeks. 

Statistical analysis

For the statistical analysis, a spreadsheet of the program Microsoft Excel® was elaborated. The information was analyzed using the electronic program GraphPad Prism® version 5.0 (GraphPad Software, Inc, CA, USA). To verify the type of distribution of the variables the statistical test of Shapiro-Wilk was applied. For correlation, the Spearman correlation coefficient (rS) was used for non-normal distribution. The differences were considered statistically significant when p was less than 5% (p < 0.05).

Results

Of the 152 reports of pediatric autopsies analyzed, 55 were selected for evaluation, with a median GA of 33 weeks, ranging from 23 to 40 weeks. Regarding gender, 34 (60.71%) were male and 22 (39.28%) were female. The analyzed data were presented in Table 1.

Table 1 Constitutional and morphometric data of the 55 stillborns autopsied by the discipline of General Pathology at the Clinical Hospital of the Federal University of Triângulo Mineiro (HC/UFTM), Uberaba, State of Minas Gerais, Brazil, from 1994 to 2015. 

Cases Tongue length (cm) Tongue perimeter (cm) Collagen (%)
X ± SD
Vessels perimeter (µm)
X ± SD
Gestational age (weeks) Fetal weight (kg)
N4210 3.314 8.227 2.084 ± 0.305 16.86 ± 1.343 23 0.54
N4156 3.287 9.065 13.231 ± 1.036 23.37 ± 2.147 23 0.7
N4301 3.295 8.161 2.881 ± 0.526 70.09 ± 7.397 23 0.545
N4051 3.901 10.182 2.572 ± 0.564 121.3 ± 15.25 24 1.3
N4162 3.542 8.861 4.987 ± 0.658 80.48 ± 10.23 24 0.64
N4238 3.891 10.172 20.588 ± 1.511 19.20 ± 1.555 24 1.08
N4279 3.622 9.572 2.319 ± 0.563 70.74 ± 6.36 24 0.620
N4149 4.135 11.021 1.493 ± 0.315 71.18 ± 15.62 25 0.57
N4313 4.378 11.46 2.527 ± 0.372 80.27 ± 9.780 26 1.04
N4265 2.951 7.354 7.383 ± 0.634 86.48 ± 12.30 26 0.985
N4269 3.994 10.333 11.299 ± 0.812 84.02 ± 12.44 26 0.8
N4090 3.344 9.422 2.833 ± 0.266 24.64 ± 2.078 27 0.85
N4199 3.237 8.339 3.737 ± 0.569 66.40 ± 4.911 27 0.9
N4159 4. 327 11.856 6.139 ± 0.791 15.62 ± 1.075 27 2.25
N3935 4.423 11.43 8.013 ± 1.430 18.38 ± 2.382 28 1.09
N4086 3.746 10.379 12.202 ± 0.747 25.90 ± 7.057 28 1.25
N4134 3.755 9.872 1.745 ± 0.218 89.27 ± 8.840 28 1.02
N4108 3.751 10.033 2.419 ± 0.638 54.88 ± 4.987 28 1.2
N4174 3.482 9.813 1.327 ± 0.199 70.18 ± 7.454 28 1.08
N4275 3.324 8.864 4.142 ± 0.401 105.1 ± 7.451 28 1
N4239 4.423 11.213 1.837 ± 0.305 21.89 ± 1.765 29 1.24
N3976 4.902 11.618 6.757 ± 1.049 20.22 ± 1.582 29 2.77
N4125 4.493 11.031 9.542 ± 0.941 96.22 ± 8.743 30 1.7
N4295 3.785 9.065 0.7795 ± 0.294 117.5 ± 10.20 30 0.780
N4325 4.134 11.322 4.25 ± 0.4896 73.24 ± 5.928 31 1.65
N4284 4.209 11.585 1.699 ± 0.1744 56.87 ± 4.441 31 1.85
N4145 4.026 11.131 0.993 ± 0.1784 124.0 ± 11.56 31 1.42
N3901 4.071 11.122 0.888 ± 0.139 28.68 ± 2.396 33 1.9
N4011 3.357 8.832 10.116 ± 0.551 47.02 ± 3.687 33 1.63
N4115 4.293 11.784 9.551 ± 1.126 75.32 ± 4.602 33 1.92
N4136 4.122 10.528 22.634 ± 1.795 22.12 ± 2.462 33 1.02
N4276 4.491 11.467 2.556 ± 0.448 65.22 ± 7.612 33 1.46
N4230 3.748 10.117 3.551 ± 0.322 59.95 ± 6.142 34 3.5
N3913 4.247 11.092 1.444 ± 0.233 30.04 ± 3.152 34 1.96
N3986 4.449 10.919 9.536 ± 1.255 50.56 ± 5.330 35 1.4
N4113 3.189 9.173 7.149 ± 1.022 75.35 ± 7.662 35 1.3
N4119 4.445 11.221 10.357 ± 1.056 22.57 ± 2.067 35 2.34
N4257 3.682 10.251 3.048 ± 0.472 51.36 ± 4.841 35 2.2
N4260 40.2 10.34 1.8 ± 0.305 47.83 ± 4.937 35 2.15
N4083A 4.848 11.893 2.255 ± 0.154 22.41 ± 1.893 35 2.25
N4232 4.138 11.905 16.117 ± 1.874 18.75 ± 1.413 36 2.66
N4147 4.07 10.951 2.863 ± 0.475 76.22 ± 6.190 36 3.88
N4111 3.914 11.641 20.782 ± 1.296 105.5 ± 8.113 37 4.23
N4150 3.986 10.208 11.147 ± 1.029 22.62 ± 3.218 37 2.16
N4297 4.313 11.555 5.233 ± 0.524 109.1 ± 9.913 37 1.4
N3989 4.879 13.47 12.774 ± 1.047 110.4 ± 9.032 38 3.55
N4019 5.865 14.985 10.028 ± 0.908 76.11 ± 10.24 38 3.44
N4204 4.851 11.971 6.958 ± 0.589 74.43 ± 8.284 39 2.8
N3894 3.623 11.214 3.701 ± 0.452 112.5 ± 9.923 40 3.56
N4100 3.353 8.512 1.889 ± 0.240 26.86 ± 2.116 40 0.9
N4107 3.592 11.174 12.609 ± 1.94 124.1 ± 9.532 40 0.9
N4126 5.13 13.431 17.911 ± 3.24 33.13 ± 2.671 40 1.7
N4140 4.5 11.866 8 ± 0.917 24.90 ± 2.074 40 1.35
N4158 4.535 12.504 10.003 ± 0.755 18.18 ± 1.370 40 2.93
N4176 3.395 9.463 4.078 ± 0.327 64.04 ± 6.370 40 1.28

The tongue perimeter presented a positive and significant correlation with GA (rS = 0.528; p < 0.001; Fig. 3).

Figure 3 Graphs showing the association of GA with tongue perimeter (A), tongue length (B), collagen fibers (C), and vessel perimeter (E). Fetal weight was associated with the collagen fibers (D) and the perimeter of the vessels (F). 

The correlation of GA and tongue length was also positive and significant (rS = 0.527; p < 0.001; Fig. 3).

A positive and significant increase was observed in the correlation of the GA with collagen fibers (rS = -0.071; p = 0.001; Fig. 3).

Considering the relationship between collagen fibers and fetal weight, a positive and significant correlation was observed (rS = 0.143; p < 0.001; Fig. 3).

The correlation between the GA and the perimeter of the blood vessels was positive and significant (rS = 0.093; p < 0.001; Fig. 3).

A correlation was observed between the perimeter of blood vessels and the fetal weight: there was an increase in the perimeter of the vessels, in tendency significant (rS = 0.028; p = 0.076; Fig. 3).

Discussion

The present study corroborates the literature, as a positive and significant increase in perimeter and length of the tongue was reported at different GAs.4,17 Fetal development is extremely important for the evaluation of the newborn, thus GA is an indispensable parameter for evaluation and survival after birth.18 Foot length is an important element for the structural assessment of the fetus at different GAs, because it is a body measurement that is closely related to GA, weight, and length.19

A positive and significant correlation was observed between collagen fibers in the tongue of stillborns and GA (23-40 weeks) and weight. This finding indicate that CNCC initiates and directly potentiates tongue development and gives rise to fibroblasts that promote the development of connective tissue.9,20

In addition, blood vessels perimeter was positively correlated with different GAs. The authors chose to use the perimeter for vessel morphometry using the CD31 marker, which has not yet been described in the literature. As observed in a study on stillborns with 20 to 40 weeks GA, anti-CD31 is a marker of vessels in relation to the development of GA.14,21

The present study corroborates the literature, in which 23 tongues of autopsied stillborns were analyzed, demonstrating that after the seventh week, the vessels (whose walls are beginning to develop) increase progressively. In the posterior region of the tongue, the blood vessels are small and form a very dense capillary network. The anterior vascularization of the tongue is greater, the vessels have smaller calibers, providing the conditions for a rapid supply of energy and nutrients to the myocytes. This capillary network of the tongue has been described in the literature as an important element against diseases.22-24

In turn, the increase of the perimeter of blood vessels correlated with the fetal weight was positive and tendency significant. There is a natural tendency for fetal growth during the different GAs, but some factors may cause changes in fetal weight, since this variable is different in each GA and depends on external factors, such as maternal nutrition. Intrauterine complications resulting in newborns with low birth weight (<2500 g) are recognized as risk factors that contribute to the development of vascular diseases in adulthood.25 Fetal weight and GA should be taken into account due to the influence of other characteristics (genetic and socioeconomic factors). The increase in fetal weight may be related to a severe fetal complication, which generates a fetal systemic response characterized by edema, inflammation, and alteration of chemical mediators.26

The precise evaluation for growth in the neonatal period is important to observe if the fetus was subjected to abnormal intrauterine conditions that resulted in delayed growth acceleration.27 However, antenatal ultrasound detection and estimated fetal weight are far from straightforward, because these well-defined parameters are estimated using complex calculations that may give varying results for the same fetus. To further complicate matters, then obtained results can then be plotted on a number of different antenatal reference charts generated from local, national, or international cohorts, some of which are customized for maternal factors, such as parity, height, weight, and ethnicity. These variations contribute to large differences in antenatal detection abnormalities.28,29

Therefore, with the advance of GA, there is an increase in the perimeter and length of the tongue, an increase in the percentage of collagen fibers and an increase in the vascular perimeter, demonstrating that tongue formation is directly linked to fetal growth and development. Therefore, tongue embryogenesis would be a valid parameter to estimate GA in the pediatric autopsy, in conjunction with traditional methods.

Please cite this article as: Aguiar LS, Juliano GR, Silveira LA, Oliveira MS, Torquato BG, Juliano GR, et al. Tongue development in stillborns autopsied at different gestational ages. J Pediatr (Rio J). 2018;94:616-23.

☆☆Study conducted at Universidade Federal do Triângulo Mineiro (UFTM), Instituto de Ciências Biológicas e Naturais, Disciplina de Patologia Geral, Uberaba, MG, Brazil.

Funding

Conselho Nacional de Desenvolvimento Cientifico e Tecnológico (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), and Fundação de Ensino e Pesquisa de Uberaba (FUNEPU).

Acknowledgments

The present study was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), and Fundação de Ensino e Pesquisa de Uberaba (FUNEPU).

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Received: May 2, 2017; Accepted: August 8, 2017; pub: November 4, 2017

* Corresponding author. E-mail:drluciano@hotmail.com (L.A. Silveira).

Conflicts of interest

The authors declare no conflicts of interest.

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