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Topografia y morfologia del estomago de llama (Lama glama).

TOPOGRAPHY AND MORPHOLOGY OF THE LLAMA (LAMA GLAMA) STOMACH

RESUMEN: El estomago de los camelidos sudamericanos presenta una estructura morfologica diferente al de rumiantes verdaderos. El objetivo del presente trabajo fue describir las caracteristicas anatomicas e histologicas del estomago de la llama y sus relaciones con las estructuras adyacentes.

Se utilizaron cuatro llamas machos. Las muestras para estudios anatomicos fueron fijadas por perfusion con formol al 10%. Para histologia, las muestras fueron fijadas en Bouin y procesadas rutinariamente. Los estudios anatomicos mostraron que el compartimiento proximal esta localizado totalmente en la pared abdominal izquierda. Un labio derecho simple, el pliegue ventricular, resulta notorio. El compartimiento intermedio presenta forma arrinonada con paredes gruesas. El compartimiento distal es elongado y tubular hacia la zona ventral derecha de la cavidad abdominal. Histologicamente, los compartimientos proximal e intermedio presentan areas con y sin glandulas. La region no glandular esta cubierta por epitelio plano estratificado con pliegues y sin papilas. El area glandular presenta pliegues cuyos recesos originan profundos sacos, ocupados por glandulas tubulares simples, tapizadas por epitelio cilindrico simple. El compartimiento distal es completamente glandular.

PALABRAS CLAVE: 1. Cavidad abdominal; 2. Compartimiento gastrico; 3. Camelidos sudamericanos; 4. Estomago.

SUMMARY: The stomach of the new world camelids presents a morphologic structure different from those of the true ruminants. The aim of the present work was to describe the anatomical and histologic features of the stomach of the llama and their relationship with the adjacent structures.

Four males llamas were used. Specimens for anatomical studies were fixed by perfusion with 10% formaldehyde. For histology, samples were fixed in Bouin and routinely processed. The anatomical studies showed the proximal compartment located totally in the left abdominal wall. A single right lip, the ventricular furrow, results notorious. The intermediate compartment is kidney-like in shape, with thick walls. The distal compartment is elongated and tubular, located toward ventral-right of the abdominal cavity. Histologicaly, the proximal and the intermediate compartments present areas with and without glands. The nonglandular region is covered by stratified plane epithelium with pleats and without papillae. The glandular area presents pleats whose recesses originate deep pouches, occupied by simple tubular glands, the lining epithelium is cylindrical simple. The distal compartment is completely glandular.

KEY WORDS: 1. Abdominal cavity; 2. Gastric compartment; 3. New World Camelids; 4. Ruminant stomach.

INTRODUCTION

The New World Camelids (NWC) have great importance for countries like Argentina, Bolivia, Chile and Peru. They provide meaningful economic resources due to the exploitation of fibers, meat, skins and transport (Nuevo Freire, 1994). They have acquired particular interest as an alternative animal production at the present time among other causes because they do not degrade the soil.

The morphology of the NWC is one of the less studied fields, in spite that in the last 40 years investigations, have been intensified on the morphology and physiology, especially in the alpaca and the llama (Paolicchi, 1997). The references covering these aspects are dispersed. Many of the studies have been carried out by isolated researchers and they don't keep the necessary coherence to explain integrally many physiologic processes (Fernandez-Baca, 1991).

The camelids in general, like the better studied domestic ruminants (bovine, ovine, caprine), have a very large stomach, divided in compartments. However, the stomach of the camelids differs considerably from that of the mentioned ruminants. Vallenas (1971) studied the gross anatomy of the stomach of the llama and the guanaco using "in vivo" and "in vitro" techniques. He describe the stomach of these animals (applicable also to the alpaca and vicuna) as constituted by three compartments denominated one, two and three. However, at the present time, they are designated as proximal, intermediate and distal compartments (PC, IC and DC, respectively) (Galotta & Galotta, 1988).

The aim of the present studies is to characterise grossly and microscopically the stomach of the llama (Lama glama) and establish its relationship with adjacent structures.

MATERIAL AND METHOD

Animals. Four male llamas, approximately 2 years old, with an average weight of 100 kg, coming from a Natural Reservation called "Sierra del Tigre" (Tandil County, Buenos Aires Province) were anaesthetized and bleeding to death. They should be sacrificed by overpopulation.

Anatomy. Two llamas were used to carry out the gross morphological studies. They were fixed by means of vascular perfusion through the carotid artery with 10% formaldehyde. The organs were observed "in situ" to describe their anatomical relationships. Each organ was isolated and dissected in order to define physical characteristics, conformation, fixation means and irrigation (Fig. 1 a, b, c).

[FIGURA 1 OMITIR]

Histology. Samples collected in two animals were used for the microscopic study. Different regions of the three compartments (Fig. 2 a, b, c) were fixed in Bouin solution, during 12 hours. After dissection, the samples remained in the fixative for a total of 48 hours. Later on, they were dehydrated, cleared in butyl alcohol and embedded in paraplast. Five gm thick sections were stained with haematoxylin and eosin. The samples were selected according to the anatomical features of the different regions (Fig. 2).

[FIGURA 2 OMITIR]

RESULTS

The stomach is composed by three compartments (Fig. 1b).The PC, which has been frequently compared with the rumen (Fig. 1a, b, c). is the most voluminous; 83% of the whole gastric volume. The kidney-shaped IC is the smallest (Fig. 1b): 6% of the total gastric volume. The DC is elongated and tubular (Fig. 1a, b); it constitute around 11% of the gastric volume.

Proximal compartment. It is located toward the left abdominal wall in contact with the diaphragm, the whole costal wall to the left and part of the flank. The ventral portion presents a transverse furrow that divides it in a cranial and a caudal sacs (Fig. 1c). In the alive animal, the base of the cranial sack is ventral in comparison with the base of the caudal sack. The walls form ventrally an area of elevations formed by very thin walled saccules. Dorsally, the traverse furrow is absent. The oesophagus ends in the cranial sack on the right. The PC communicates with the IC through the ventricular furrow, conformed by a single lip to the right. Internally, it is divided by a transverse muscular pillar, the one that corresponds to the external transverse furrow; on the right, this pillar forks in two branches, cranial and caudal. The caudal continues in arch form over the cranial and dorsal areas at the entrance to the IC, and in whose journey is intercepted by the lip of the ventricular furrow (Fig. 2a). The cranial branch of the pillar continues like a thick band on the dorsal margin of the cranial sack that contains "the glandular bags or saccules" of this region. The ventricular furrow is defined dorsally by a simple lip, located to the right, the one that goes caudaly from the cardias toward the entrance of the IC.

Histologically, PC and IC presents two regions: one nonglandular and another glandular. The nonglandular is formed by a mucous membrane covered by plane stratified epithelium (Fig. 3 a), with folds, but non papillae. The folds are not permanent and their prominence varies with the state of contraction of the stomach. The epithelium is supported by dense connective tissue that constitutes the lamina propria (Fig. 3 b). It is mainly formed by collagen libres, being scarce the elastic and reticular elements.

[FIGURA 3 OMITIR]

The glandular region, presents a mucous membrane with a glandular epithelium that originate folds whose recesses produce deep pits (glandular bags), in its great majority occupied by simple or sometimes ramified tubular glands. The lining epithelium is cylindrical and simple. The glands, located in the lamina propria, are surrounded by a scarce quantity of loose connective tissue with support and nutrition functions (Fig. 3 c).

Intermediate eompartment. The IC, is the smallest of the gastric compartments. It is reniform with flat and thick walls (Fig. 1 b). It presents a dorsal smaller and a ventral mayor curvature (Fig. 2 b). The IC is located to the right of the PC although it is not reflected on the right abdominal wall since the liver contacts on the wall. The content of this compartment is liquid.

The IC communicates craneally to the DC through a thick walled strait tubular passage, the "channel of the isthmus".

Histologically, two regions can be distinguished. They showed the same characteristics that in the PC. Moderate amount of lymphoid tissue is present in the lamina propria of the glandular region (Fig. 3 d, e). The continuation of the ventricular furrow is covered by flat stratified epithelium. The only muscular lip of the furrow extends along the smallest curvature toward the hole that communicates with the DC. The superficial mucous membrane of the walls of the major curvature is divided in reticular pattern by means of crests that are intercepted, defining the holes of deep cells or cameras. That area is surfaced by glandular epithelium covered by abundant mucus.

The muscularis mucosae is absent in the nonglandular regions of both PC and IC (Fig. 3 f). It is present in the glandular areas, although this layer is incomplete (Fig. 3 e). The submucosa of the PC and IC is similar to both regions (glandular and nonglandular) and it is constituted by abundant elastic, reticular and collagen's fibres, besides a numerous cellular population. The muscularis contains an inner circular and an outer longitudinal layers. A serous membrane covers the muscular external layer of the two compartments.

The channel of the isthmus connects the IC with the DC. It is a small tubular continuation of the ventricular furrow, it is sheltered by a stratified epithelium (Fig. 3 f). The mucous membrane presents thick longitudinal folds and their walls contain a well developed muscular layer.

Distal eompartment. The DC is elongated and tubular (Fig. 1 a, b). The anatomical location allows to observe that initially it goes ventrally toward the right abdominal wall, then a tortuous course continues in dextro-caudal direction (Fig. 1 a). Distally, and on the right side, it presents a preterminal bending at the beginning of the fifth terminal of the DC, whit a thick walled area. This segment continues to the pylorus and with the initial portion of the duodenum. The DC presents a bigger ventral curvature and another smaller one dorsally.

It left side touch on the PC and the glandular sacs. It is fixed in this position by means of the major omentum that continues through the major curvature until the beginning of the duodenum. In this place, it unites to the smallest omentum and continues as mesoduodenum.

Three regions can be characterised histologically:

1. The proximal region, where the IC ends, is characterised by the presence of abundant lymphoid tissue in the mucosa and submucosa (Fig. 3 g);

2. The wider central region, with simple tubular glands of mucous secretion (Fig. 3 h, 4 a, b);

[FIGURA 4 OMITIR]

3. The caudal region, extensive, where two different portions could be observed. The most ventral corresponded to the fundic glands (Fig. 4 c, d); the dorsal area, related with the "torus pyloricus", corresponds to the pyloric region (Fig. 4 e, h).

Internally, the DC is covered by a glandular mucosa, but its disposition varies according to the area (Fig. 2 c). In the smallest bend, in the fifth initial portion, the mucosa is reticular while in the major curvature it forms non permanent folds.

In the medial part, the mucosa is dispose in permanent longitudinal pleats. It finished at the preterminal bending, where the mucous membrane is thick and flat.

The mucosa covering most of the major curvature of the fifth terminal is very thick. It belongs to the area of the gastric glands (Fig. 4 c, d). The mucosa of the small bend is thinner. It contains the pyloric glands, and in their terminal part it is radiated to cover the pyloric circumference. On the small curvature a prominent "torus pyloricus" protects the entrance to the pylorus.

The superficial epithelium is cylindrical simple, the glands occupy the lamina propria surrounded by scarce soft connective tissue. In the region of the ventricular isthmus corresponding to the outlet of the IC the secretor epithelium is covering partially the glands. The whole area is infiltrated by an abundant diffuse lymphoid tissue that is observed as isolated lymphonodes surrounded by connective tissue. This tissue occupies the mucosa and great part of the submucosa of this region (Fig. 3 g).

The central region, is characterised by the presence of abundant simple tubular glands of mucous secretion (Figs. 3h, 4a, b).

In the caudal region, two different portions are observed, the ventral region occupied by the fundic glands with similar features to those described for other mammals (Fig. 4 c, d). The dorsal region is occupied by a mucous membrane that presents simple tubular glands (Figs. 4 e, f, g, h).

The muscularis mucosae is very well developed; from it come off fibres that ate distributed among the glands of the lamina propria (Figs. 4 a, f, g, h). The thin submucosa is constituted by semilaxe connective tissue having blood vessels and nerves (Fig. 4 a, c, e, f, h).

The muscular contains an inner circular and an outer longitudinal layers. The first one is prominent to the level of the pyloric sphincter. It defines the terminal portion of the DC and with the initial expanded part of the duodenum. Fat tissue is frequently dispose between both muscular layers (Fig. 4 a, b, e, g, h).

DISCUSSION

Formerly, the simple stomach of the animals with superior and inferior incisives were distinguished from the multiple stomach of the animals without superior incisives. Among these, camel, ox, goat and deer were mentioned (Aristote, 1957). By the middle of the XX century, the camelids were separated from the true ruminants in the main classifications (Simpson, 1945).

Cuvier (1805), in a description carried out on the stomach of camels and a non-born llama, make reference to four stomachs with a different structure to that of true ruminants. It described the sacks of the "paunch" one of those which him denominated reservoir or fifth stomach. The gastric furrow is formed by a lip and he observed the torus pyloricus. One century later, Chaveau et al. (1903) mentioned that the stomach of the camels and llama are formed by the "paunch", "reticulum" and "abomasum" and point out that those are not in comparable to those of other ruminants.

Other authors (Colin, 1886; Barone, 1976), sustain that the camels present four stomachs like the other ruminants, using the same names to designate them. Gusman Chaves (1970) in studies carried out in alpacas, points out that they have a single stomach with three proventricles similar to those of the camel and whose names would be "rumen, reticulum and omaso-abomasum." The three gastric compartments described in the llama seems to be equivalent to those described by Amasaki et al. (1988) for the bactrian camel (Camelus bactrianus).

According to Vallenas (1970a), a great part of the confusion was due to the application of the nomenclature primary established for the bovine.

Later on, several authors accepted the existence of three compartments which they denominated glandular sacks C1, C2 and C3 (Bustinza Cordero, 1970; Cummings et al., 1972; von Engelhardt & Sallman, 1972; Luciano et al. 1979; Gregory et al., 1985; Heller et al., 1986; Yarbrough et al. 1995; Dulphy et al., 1997; van Hoogmoed et al., 1998 (a); (b), Timm et al., 1999; Navarre et al., 1999; Wang et al., 2000). Galotta et al. (1994) follows the approaches of the V.A.N. (Veterinary Anatomical Nomina) and denominated them Proximal Compartment (PC), Intermediate Compartment (IC) and Distal Compartment (DC).

The major omentum in the camelids is a simple thin blade. In the true ruminants, it is composed by a superficial anda deep sheets (Galotta and Galotta, 1987). The gastric furrow is composed for a single lip. The process of regurgitation is associated with the cranial sack of the PC, instead of being related to a net or reticulum, as in cattle (Vallenas, 1970b). The torus piloricus, located in the DC, is similar to the one present in cattle, sheep and pigs (Barone, 1996).

The PC and the IC present two areas very different in their histological structure. The nonglandular region has a stratified plane epithelium, different to that of the bovines (Amasaki et al. 1988), ovines (Weyrauch & Schmorr, 1979) and of other ruminants (Hoffmann, 1973). It doesn't present crests and for that reason it is difficult to draw homologies between camelids and other ruminants. The glandular region, absent in the bovine and ovine compartments (Barone, 1996), is formed by tubular glands arranged in glandular bags. They contribute to increase the surface of the glandular epithelium (Rubsamen and von Engelhardt, 1979; Luciano et al., 1979).

The mucosa of the glandular region of the DC is similar in their structure to the fundic portion of the monogastric mammals (Alzola et al., 2000) and to that of the guanacos (Luciano et al., 1980). These glands are of the quite rectilinear, of ramified simple tubular type and they are observed occupying all the thickness of the lamina propria (Alzola et al., 1997).

Lymphoid tissue is abundant in the glandular portion of the IC, in the region of the isthmus at the IC and DC, and in the first portion of the DC (Alzola et al., 1997). This elements are absent in the stomach of the true ruminants. Lymphoid tissue is present in the caudal and pyloric stomach of the pig (Trautmann & Fiebiger, 1950).

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Direccion para correspondencia:

M. V. Msc. Ricardo Horacio Alzola

Facultad de Ciencias Veterinarias

Universidad Nacional del Centro de la Provincia de Buenos Aires

Campus Universitario 7000

Tandil

ARGENTINA

Fone- Fax (02293) 422357 / 426667

e-mail ralzola@vet.unicen.edu.ar

Received: 27-04-2003

Accepted: 22-04-2004

* Ricardo Horacio Alzola; * Marcelo Daniel Ghezzi; ** Eduardo Juan Gimeno; * Maria Cristina Lupidio; * Alejandra Nelly Castro; *** Julio Armando Rodriguez

* Lab. Cs. Morfologicas, Depto. Cs. Biologicas, Fac. Cs. Veterinarias, Universidad Nacional del Centro, Buenos Aires, Tandil, Argentina.

** Departmento de Patologia, Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata, (1900) La Plata, Argentina.

*** Lab. de Biologia Celular, Depto. de Cs. Biologicas, Fac. de Cs. Veterinarias, Universidad Nacional del Centro, Buenos Aires, Tandil, Argentina. SECyT-UNICEN proyecto No.03/H 126 GIB (Grupo pequeno de Investigaciones Biologicas).
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Author:Horacio Alzola, Ricardo; Ghezzi, Marcelo Daniel; Gimeno, Eduardo Juan; Lupidio, Maria Cristina; Cast
Publication:International Journal of Morphology
Date:Jun 1, 2004
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