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Age-Related Changes in the Myenteric Plexus of the Human Jejunum P

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Age-Related Changes in the Myenteric Plexus of the Human Jejunum P Folia Morphol. Vol. 75, No. 2, pp. 188–195 DOI: 10.5603/FM.a2015.0097 O R I G I N A L A R T I C L E Copyright © 2016 Via Medica ISSN 0015–5659 www.fm.viamedica.pl Age-related changes in the myenteric plexus of the human jejunum P. Mandic1, S. Lestarevic2, T. Filipovic1, S. Savic2, S. Stevic3, M. Kostic4 1Institute of Anatomy, Medical School Pristina, Kosovska Mitrovica, Serbia 2Institute of Histology, Medical School Pristina, Kosovska Mitrovica, Serbia 3Institute of Pharmacology, Medical School Pristina, Kosovska Mitrovica, Serbia 4Institute of Medical Statistics and Informatics, Medical School Pristina, Kosovska Mitrovica, Serbia [Received: 15 August 2015; Accepted: 21 October 2015] Background: Myenteric ganglia are an important regulator of peristaltic activity of the digestive tract. Getting to know its normal morphological changes during aging are of great importance for the interpretation of intestinal motility disorders. The aim of our histomorphometric study was to reveal detailed characteristics of myenteric plexus, cell number, orientation, properties of as well as age-related changes in the human jejunum. Materials and methods: We examined the myenteric ganglia in the proximal jejunum specimens obtained from 30 human cadavers aged from 20 to 84 years. Tissue samples were classified into three age groups: 20–44, 45–64 and 65–84 years. After standard histological preparation, specimens were stained with haematoxylin and eosin method, Cresyl-Violet and silver nitrate (AgNO3) by the method of Masson Fontana. In addition to standard staining methods we use and enzyme histochemical method for acetylcholinesterase. Morphometric analysis of all the specimens was performed, using a multipurpose test system M42. The data were subjected to the Tukey post hoc HSD significance test using one-way ANOVA. There is a significant decrease (p < 0.001) in the number of neurons in persons aged between 65 and 84 years. Results: It was found that the reduction in number of neurons is 25.93% in oldest compared to the youngest. It was also noted a significant increase (p < 0.05) of the surface profile of ganglion neurons. Conclusions: This increase in the size of neurons can be explained as compen- sation for the loss in the number of neurons in order to maintain the normal function of innervations of the jejunum. (Folia Morphol 2016; 75, 2: 188–195) Key words: myenteric plexus, jejunum, human, aging INTRODUCTION of the peripheral nervous system. Its complexity is Normal functioning of the gastrointestinal tract reflected in the phenotypic diversity of neurons and is dependent on the interaction of the enteric nerv- the existence of a wide range of neurotransmitters ous system (ENS), the smooth muscle layers and the [5, 6, 16] that are present and act in these neurons. submucosal and mucosal layer of wall of the diges- The nerve junctions of the intestinal wall are respon- tive tube. The ENS is also the most complex part sible for peristaltic contractions and coordination of Address for correspondence: Dr P. Mandic, Institute of Anatomy, Medical School Pristina, Kosovska Mitrovica, Ljube Davidovica 126, 11400 Mladenovac, Serbia, tel: +381116236174, e-mail: [email protected] 188 P. Mandic at al., Myenteric nervous plexus and aging the motor activity of smooth muscles, which does sought to determine the presence of individual dif- not disappear even in the complete absence of ex- ferences and verify certain changes in the structure of ternal innervations [10, 11]. Neurons of the enteric myenteric plexus that occur during the aging process. system play an important role in coordinating the In order to achieve this, we determined the number activities of other gastrointestinal cells and influ- of neurons of the myenteric plexus per unit area of ence the processes such as absorption, secretion, the jejunum, the surface area of the nerve structures, and microvasculature. Recent evidence shows that as well as the surface of the individual neurons and the enteric neurons also influence the function of their nuclei. the epithelial barrier [23]. Two basic plexuses of the ENS are interconnected and arranged in the form of MATERIALS AND METHODS concentric circles in the wall of the intestine [12, 18]. Tissue samples of the human jejunum were The first is the myenteric plexus, which lies between obtained from autopsy material at the Institute of the longitudinal and circular smooth muscle layers. Forensic Medicine in Belgrade from 30 cadavers The second is the submucosal plexus, which is lo- (17 men and 13 women), aged from 20 to 84 years, cated in the layer of connective tissue between the who were divided into three age groups (20–44 years, mucosal epithelium and the layers of circular smooth n = 10; 45–64 years, n = 10; 65–84 years, n = 10). muscle. However, there are recent views that the ENS The cause of death of each was ischaemic heart failure consists of three different ganglionated plexuses, or intracranial bleeding. None had undergone previ- myenteric plexus, outer submucosal plexus and inner ous surgery, and in their medical documents there submucosal plexus [2, 3]. In addition to the ganglion was no information about gastrointestinal diseases. plexuses, in the wall of alimentary tract, there are Fragments of the jejunum were taken during the a large number of aganglionated nervous plexuses [35, first 24 h from the moment of death. The collection 37]. Myenteric plexus mainly regulates motility, and of materials is satisfied ethical requirements of the submucosal plexus mainly regulates secretion and institutions from which is obtained (the Ethics Com- local blood flow. Researches on aging ENS are largely mittee of the Medical Faculty in Belgrade). Samples focused on the analysis of changes in the number of were taken always from the same topographic places neurons in the myenteric plexus. These studies were (antimesenteric wall of the jejunum, 80 cm from du- carried out in a number of animal species [27, 29, odenojejunal flexure) and sorted by age in groups. 31]. The literature that has been documented support Immediately after taken, tissue slices of preparations varying data from those which indicate the significant the size of 1 × 1 cm were fixed in 4% buffered para- reduction (30–50%) in the number of neurons [17, formaldehyde for 48 h. After the routine processing 33] to those where there is no significant loss of the in an increasing series of alcohol, samples were em- neurons [14, 24, 36] in the aging process. There are bedded in paraffin blocks, which were then cut in a number of studies [7, 34] which describe changes in two ways: sections perpendicular to the longitudinal ENS due to the introduction of certain dietary restric- axis of the jejunum (classical) and sections parallel tions in experimental animals. In addition to the loss to the longitudinal axis of the jejunum (from serosa of enteric neurons in the aging process, other signs until myenteric plexus and through it). Histological of neurodegeneration such as dystrophic nerve fibres, preparations were stained with the routine haematox- the accumulation of lipofuscin, a change in the size of ylin and eosin method (H&E), and to ensure reliable the neurons and their nuclei are occurring. It should identification of ganglion, cells and structures were also be noted that a large number of phenotypically stained with silver nitrate (AgNO3) by the method and functionally different subpopulations of enteric of Masson Fontana and Cresyl-Violet (CV) staining. neurons showed various levels of susceptibility to Enzyme histochemistry for acetylcholinesterase age-related changes. Some of the researchers [20] (AChE) was used to stain the myenteric plexus in one suggest that in terms of aging, myenteric neurons part of the samples of jejunum for the reason that this show age-related phenotypes. The aim of this study enzyme occurs non-specifically within intrinsic nerves is detailed examination of myenteric plexus in the and ganglia. The hyaluronidase-treated part of the tis- proximal part of the human jejunum using specific sue samples were incubated for 1–3 h at 4ºC in the histological, morphometric, and stereological meth- incubation medium (pH 5.6) containing the following: ods. Using methods that allow quantification, we sodium acetate, 60 mM; acetylthiocholine iodide 2 mM; 189 Folia Morphol., 2016, Vol. 75, No. 2 sodium citrate 15 mM; CuSO4, 3 mM; K3Fe(CN)6, 0.5 mM; Triton-X100 supplemented the incubation me- dium up to 1% and hyaluronidase (0.5 mg/100 mL). All fats from the surface of gut which are almost completely non-permeable for the incubation media were previous- ly removed. Following staining, the preparations were fixed in neutral 4% formalin in 0.1 M phosphate buffer. The preparations were stored in the same formalin. After that tissues were embedded in paraffin blocks, cut and mounted on glass slides. Silver nitrate staining by the method of Masson Fontana was performed as follows: the hydrated prepa- rations were put in a previously prepared solution of silver nitrate for 2 h at 56°C, rinsed in distilled water and tones with 0.2% gold chloride solution for 2–3 min, rinsed again with distilled water and 1 min down to 5% sodium thiosulfate. Preparations were again rinsed with distilled water and 5 min immersed in nuclear-fast Figure 1. Manner of using the multipurpose system M42 (arrows red and then mounted on glass slides and covered indicate “forbidden line”). the outer husks. The result of staining was following: argentaffin granules in neural cells were black, nuclei were pink-reddish, and cytoplasm pale-pink. myenteric nerve cells. In addition, it was counted Cresyl-Violet staining for nerve cells was per- the total number of neurons within each ganglion formed as follows: hydrated preparations were left structure. At Figure 1 is illustrated how to use the in the previously prepared 0.5% solution of CV stain test system M42.
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