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Morphological Characterization of Diaphragm in Common Squirrel Monkey (Saimiri Sciureus)

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Morphological Characterization of Diaphragm in Common Squirrel Monkey (Saimiri Sciureus) Anais da Academia Brasileira de Ciências (2018) 90(1): 169-178 (Annals of the Brazilian Academy of Sciences) Printed version ISSN 0001-3765 / Online version ISSN 1678-2690 http://dx.doi.org/10.1590/0001-3765201820170167 www.scielo.br/aabc | www.fb.com/aabcjournal Morphological Characterization of Diaphragm in Common Squirrel Monkey (Saimiri sciureus) JOSÉ RICARDO N. DE SOUZA NETO1, ÉRIKA BRANCO1, ELANE G. GIESE2 and ANA RITA DE LIMA2 1Laboratório de Pesquisa Morfológica Animal/LaPMA, Faculdade de Medicina Veterinária, Universidade Federal Rural da Amazônia/UFRA, Avenida Presidente Tancredo Neves, 2501, Montese, 66077-530 Belém, PA, Brazil 2Laboratório de Histologia e Embriologia Animal/LHEA, Faculdade de Medicina Veterinária, Universidade Federal Rural da Amazônia/UFRA, Avenida Presidente Tancredo Neves, 2501, Montese, 66077-530 Belém, PA, Brazil Manuscript received on March 8, 2017; accepted for publication on September 11, 2017 ABSTRACT The wall of the diaphragm can be affected by congenital or acquired alterations which allow the passage of viscera between the abdominal and chest cavities, allowing the formation of a diaphragmatic hernia. We characterized morphology and performed biometrics of the diaphragm in the common squirrel monkey Saimiri sciureus. After fixation, muscle fragments were collected and processed for optical microscopy. In this species the diaphragm muscle is attached to the lung by phrenopericardial ligament. It is also connected to the liver via the coronary and falciform ligaments. The muscle is composed of three segments in total: 1) sternal; 2) costal, and 3) a segment consisting of right and left diaphragmatic pillars. The anatomical structures analyzed were similar to those reported for other mammals. Histological analysis revealed stable, organized muscle fibers with alternation of light and dark streaks, indicating transverse striation. Key words: diaphragmatic hernia, morphology, Saimiri sciureus. INTRODUCTION control of respiratory centers in the medullary region of the brainstem, and in mammals, inspiration is Knowledge of surface anatomy is essential for the crucial phase of the respiratory cycle (Feldman understanding basic topographical anatomy, and is and Del Negro 2006, Feldman 2011). The muscles needed for various tasks such as patient examination, involved in respiratory process are the diaphragm, interpretation of diagnostic images, and performance scalenes, and intercostals (Druz and Sharp 1981). of surgery or other medical procedures (Sayeed and Among these, the diaphragm is the most important, Darling 2007, Elliott et al. 2010). contributing between 60% and 80% of the body’s The respiratory system is complex because respiratory force (Wilson and Hayes 1986, Supinski continuous respiratory muscle contraction is requires et al. 1996, Shindoh et al. 2009). for lung ventilation. It is usually under automatic Morphological studies of the diaphragm Correspondence to: Ana Rita de Lima are important because irregularities may cause E-mail: [email protected] diaphragmatic hernias, which are classified in An Acad Bras Cienc (2018) 90 (1) 170 JOSÉ RICARDO N. DE SOUZA NETO et al. two major categories: congenital and acquired. Non-human primates are among the most Congenital diaphragmatic hernia (CDH) is a studies groups of mammals in the wild and in partial protrusion of abdominal organs through captivity (Cubas et al. 2007); however, data on the a defect in the diaphragm. CDH is caused by a morphology of many species is scarce. This study failure in the fusion of the pleuroperitoneal folds investigates morphological features of the squirrel that manifests as a defect during fetal development monkey respiratory system from a functional point (Friedenwald and Feldman 1925, Adeleman and of view, including location and histology of the Benson 1976, Gerszten et al. 1976, Munizaga et al. diaphragm. We hope to generate further discussion 1978). Three types of CDH have been described in on which to base future research with other species. humans: Bochdalek-type CDH, which presents as a protrusion through the posterolateral part of the MATERIALS AND METHODS diaphragm (Haller 1986, Salaçin et al. 1994, Colvin Six, male Saimiri sciureus specimens were et al. 2005, Gaxiola et al. 2009); Morgagni CDH, evaluated in the study, including 5 adults and 1 an exremely rare pathology caused by defects in juvenile. Specimens died of natural causes and were the development of the sternal fixation (Rodríguez donated by the National Primate Center (CENP) in Hermosa et al. 2003); and hiatal hernia, which is Ananindeua, Pará, Brasil. The study took place at caused by trauma (Skandalakis 2004, Bastos et al. the Research Laboratory of Animal Morphology 2008). (LaPMA) at the Federal Rural University of The diaphragm surface is concave facing the Amazonia with approval by the Committee for thoracic cavity and convex facing the abdominal Research with Animals (CEPAN /IEC/SVS/MS - cavity, resulting in a dome-like shape. It is covered N° 008/2010). by the peritoneum on the abdominal face and serves Specimens were fixed in 10% aqueous as a border between the thoracic and abdominal formaldehyde solution. After fixation, an incision cavities (Getty 1986, Dyce et al. 2010). In humans, was made along the ventral midline and skin and the diaphragm muscle is directly associated with subcutaneous tissue of the sternal manubrium was hiccups, which result from diaphragmatic spasm folded to the umbilical scar, allowing visualization at the moment of inspiration concomitant with the of the abdominal cavity. All organs were removed closure of the glottis. There are many causes, and to expose the caudal face of the diaphragm muscle. in severe cases hiccups are linked to diaphragmatic Photos were taken and morphometric data was hernias and gastrointestinal causes, such as the collected using a caliper. We measured the length hiatal hernia and gastroesophageal reflux (Cardoso and width of the muscle from equally spaced points. and Xavier 2011). Nomenclature for structures was in accordance Saimiri sciureus, known as a common squirrel with the Anatomical Veterinary Nomenclature monkey, inhabits tropical dry and temporarily (International Committee on Veterinary Gross flooded forests. This species is diurnal and Anatomical Nomenclature 2012). characterized by having short and thick greenish- Samples of diaphragm muscle tissue were yellow fur. They have rounded heads and markings fixed with 4% formaldehyde. Following overnight on the back, a black snout, rounded ears, well fixation, the tissues were embedded in paraffin, developed fingers, and a non-prehensile tail; they sectioned to 5µm thickness in a Zeiss Hyrax M25 are omnivorous, feeding on flowers, insects and microtome, and stained with hematoxylin and eosin small vertebrates (Auricchio 1995). and Gomori trichrome to observe the collagen An Acad Bras Cienc (2018) 90 (1) DIAPHRAGM MORPHOLOGY IN COMMON SQUIRREL MONKEY 171 Figure 1 - Fotomacrography of abdominal face of the diaphragm of the Saimiri sciureus. a - tendinous center (1), part of the costal diaphragm dome (2), sternal part of the diaphragm dome (3), esophageal hiatus (4), aortic hiatus (5), foramen of the caudal vena cava (6), diaphragmatic pillars right (7), diaphragmatic pillars left (8) and xiphoidal process (9). b - Esophagus (1) and phrenicopericardic ligament (2). Scale bar: 1cm. fibers. Images were taken using a Leica DM 2500 TABLE I Saimiri sciureus. microscope with camera attachment (Leica DFC Biometric values of diaphragm muscle in 310FX). Animal Length Width M1 64.6 mm 63.0 mm RESULTS M2 68.5 mm 58.1 mm M3 54.3 mm 51.0 mm The diaphragm muscle of S. sciureus is dome- M4 61.5 mm 74.6 mm shaped, convex facing the abdomen and concave M5 63.3 mm 69.7 mm facing the chest. It is connected to the lung by the M6 67.0 mm 81.0 mm phrenicopericardial ligament, located caudally Average 63.2 mm 66.2 mm from the lungs and heart. The diaphragm is Standard deviation 14.3 mm 30.2 mm connected to the liver by the coronary and the falciform ligaments. passes, and the second is the aortic hiatus, through The central region of the diaphragm is which the aorta, azygous vein and thoracic duct composed of fibrous connective tissue called the pass (Fig. 1a and b). central tendon, which contains and aperture called The muscle is subdivided into three regions. the vena cava foramen which transmits the inferior The sternal region is fixed cranially to the xiphoidal vena cava. This is a region anatomically fragile process of the sternum. The coastal region has bars of diaphragm. The peripheral region is formed by a muscle portion which contained two apertures. of cartilage that connect to the ribs called costal The first aperture is the esophageal hiatus, through cartilages. The third regions are formed by the right which the abdominal region of the esophagus and left diaphragmatic pillars, which lie opposite An Acad Bras Cienc (2018) 90 (1) 172 JOSÉ RICARDO N. DE SOUZA NETO et al. the central tendon. The insertion of the diaphragm enveloping the muscle. The endomysium is formed is at the level of the eighth rib. by basal lamina of the muscle fiber in association The average length of the diaphragm along with reticular fibers. the dorsoventral axis was 63.2 ± 14.3 mm (mean ± S.D.), and average width along the latero-lateral axis DISCUSSION was 66.26 ± 30.2 mm (Table I). Optical microscopy The zoology, comparative and experimental showed that skeletal muscle fiber of the diaphragm contained transverse striations, visualized by anatomy, physiology,
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