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Transabdominal ultrasonographic appearance of the gastrointestinal viscera of healthy camels (Camelus dromedaries)
Research in Veterinary Science 93 (2012) 1015–1020
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Research in Veterinary Science journal homepage: www.elsevier.com/locate/rvsc
Transabdominal ultrasonographic appearance of the gastrointestinal viscera of healthy camels (Camelus dromedaries) Mohamed Tharwat a,1, Fahd Al-Sobayil a, Ahmed Ali a, Sébastien Buczinski b,⇑ a b
Department of Veterinary Medicine, College of Agriculture and Veterinary Medicine, Qassim University, Saudi Arabia Clinique Ambulatoire Bovine, Departement des Sciences Cliniques, Faculté de Médecine Vétérinaire, Université de Montréal, Saint-Hyacinthe, Canada
a r t i c l e
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Article history: Received 6 July 2011 Accepted 11 December 2011
Keywords: Camel Dromedary Gastrointestinal Normal Ultrasonography
a b s t r a c t The purpose of this study was to describe the ultrasonographic picture of the gastrointestinal tract in healthy camels (Camelus dromedarius). For this purpose, 22 camels were examined. The rumen and its glandular sacs were filling most of the left side of the abdomen. The rumen wall was smooth and echogenic. The ventral part of the reticulum could be best imaged in 17 (77%) camels from the left and right paramedian region just behind to the sternal pad. The reticulum in these animals had a thick wall (1.17 ± 0.27 cm) that appeared as a half-moon-shaped structure with a biphasic contraction. The omasum was best viewed through the right 8th to 6th intercostal spaces in 18 (82%) camels. In the remaining 4 (18%), it was visualized through four consecutive intercostal spaces (right 9th to 6th). It had a wall thickness of 1.1 ± 0.7 cm and a transverse diameter of 8.74 ± 3.4 cm. The abomasum could be best visualized from the right 9th and 8th intercostal spaces in 14 (64%) camels, while it was observed in the 9th intercostal space in 3 (14%) animals and in the 8th and 7th intercostal space in 5 (22%) camels. Small intestinal structures were best seen low in the right paralumbar fossa. It was thin-walled (0.43 ± 0.14 cm) and had a diameter of 2.62 ± 0.47 cm. The cecum was imaged chiefly in the caudal right flank. It was thin-walled (0.37 ± 0.05 cm), had a diameter of 13.8 ± 1.6 cm. The proximal loop of the large colon appeared as thick, echogenic, continuous and slightly curved lines. It was thin-walled (0.51 ± 0.08 cm) and had a diameter of 3.5 ± 0.8 cm. The spiral colon was confined in all camels to the caudal ventral half of the abdomen. It appeared as structures with thick echoic lateral walls with a number of echogenic arched lines next to each other. Free peritoneal fluid pockets were imaged in two locations in 19 (86%) camels. Ultrasoundguided abdominocentesis was successful in 15 (68%) of the examined camels. This study provides the ultrasonographic appearance of the normal gastrointestinal tract in healthy camels that could be used as a reference for the interpretation of suspected digestive abnormalities. Ó 2012 Published by Elsevier Ltd.
1. Introduction The dromedary camel is important specie in Africa, Middle-East and Australia. Despite its valuable use as draft animals, it is also used for milk and meat production. In the northern hemisphere, it is mainly used as a companion animal or in circus and can therefore have a worldwide veterinary importance. Diseases of the gastrointestinal tract of the camel are of great importance including impaction, bloat, ulceration and swallowed foreign bodies, enteritis, constipation, abomasal and intestinal obstruction, peritonitis, as well as abdominal hemorrhage, ascites and neoplasia (Al-Ani and Qureshi, 2004; Ramadan et al., 2008; Fowler, 2010). Many of these diseases can be effectively treated in their early stages, but ⇑ Corresponding author. Tel.: +1 450 778 8123; fax: +1 450 778 8120. E-mail address: [email protected] (S. Buczinski). Permanent address: Department of Animal Medicine, Faculty of Veterinary Medicine, Zagazig University, Egypt. 1
0034-5288/$ - see front matter Ó 2012 Published by Elsevier Ltd. doi:10.1016/j.rvsc.2011.12.003
efforts to recognize them or their severity are hampered by camel stoic nature and vague clinical signs (Fowler, 2010). Due to largesized abdomen of camels, even experienced clinicians may not be able to pinpoint the organ affected and diagnose the gastrointestinal disease. In addition, transrectal palpation in camels gives access only to the caudal viscera (Al-Ani and Qureshi, 2004; Ramadan et al., 2008). Exploratory laparotomy is usually performed in cases of camels with unexplained gastrointestinal illness (Ramadan et al., 2008). Most owners consent to this invasive procedure only when the prognosis is good, and when there is a reasonable chance that the animal can be cured. Exploratory laparotomy should be avoided in camels with a poor prognosis because it may inflict additional pain, it can be considered as an expansive diagnostic test and the animal cannot be slaughtered for human consumption waiting for withdrawal times (Fowler, 2010). In cattle, abdominal ultrasonography is an interesting diagnostic tool that can also be used as a prognostic tool in some diseases
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since the extension and importance of the disease are better assessed. The procedure is an ideal diagnostic tool for the investigation of gastrointestinal disorders that can also be used directly on the farm. It helps in deciding whether the animal should undergo surgical or medical treatment or be slaughtered (Braun, 2003, 2005, 2009). Ultrasonography has been described in examination of the reticulum (Braun and Gotz, 1994), omasum (Braun and Blessing, 2006), abomasum (Braun et al., 1997), small and large intestines (Braun and Marmier, 1995; Braun and Amrein, 2001). In llamas and alpacas, specific transabdominal ultrasonographic appearance of the gastrointestinal viscera has been described in order to help in the management of New World camelids’ gastrointestinal diseases (Cebra et al., 2002). In camel practice, ultrasonography has been used mainly for examination of the reproductive tract (Skidmore et al., 2009; Wani and Skidmore, 2010; Skidmore and Billah, 2011). The data on the use of ultrasound in medical and surgical diseases of camel are rare. Recently, we reported the use of transcutaneous ultrasound to determine intestinal wall thickness in camels with paratuberculosis and detecting enlarged mesenteric lymph nodes, image peritoneal fluid in cases with chronic trypanosomiasis, detect distended intestines in camels with intestinal obstruction (Mohamed et al., 2011a,b). However, despite success with this imaging technique, experiences are anecdotal. Data are still lacking concerning the normal appearance of gastrointestinal viscera in camels. The present study was therefore designed for establishing normal appearance, size, shape, and position of various gastrointestinal organs in dromedary camels. 2. Materials and methods 2.1. Stomach compartment subdivisions There are many reports on the subdivisions of the stomach of the camel. From the 19th century, descriptions of the stomach in camel have reflected those of ox and sheep. Some investigations regard the camel as a monogastric animal or divide the stomach of the camel into two, three, and four stomachs (Boas, 1890; Hegazi, 1950; Hansen and Schmidt-Nielsen, 1957; Purohit and Rathor, 1962; Smuts and Bezuidenhout, 1987; Wang et al., 2000). The camel stomach has additional glandular sacs that may have special digestive functions (Wang et al., 2000). In this report, we used the same nomenclature as in cattle as every part of the stomach appeared different by ultrasound examination so was not possible to merge stomach compartments into two or three parts.
2.3. Ultrasonographic examination First, the foreleg of each camel was bent and tied with a rope on the carpal joint. The head was then held and the animal was pushed till lay in a position of sternal recumbency. The fore-andhind legs were then tied by a rope near the carpal and hock joints, respectively. On both sides of thorax and abdomen, the fleece was clipped and the skin was shaved. If necessary, animals were slightly sedated using xylazine (0.02 mg/kg IV, Bomazine 10%, Bomac Laboratories Ltd., New Zealand). Ultrasonographic examination was carried out using a 3.5 MHz sector transducer with a maximal depth of 22 cm (SSD-500, Aloka, Tokyo, Japan). After the application of transmission gel to the transducer, the animals were examined beginning at the caudal abdomen and extending forward to the level of the sternal pad. The rumen, reticulum omasum, abomasum, small and large intestines as well as peritoneal fluid were imaged. Each flank was examined through the paralumbar fossa. To best imaging the reticulum, the camel was placed in a lateral recumbency and where the transducer was directed forward in a 30° angle perpendicular to the animal ventrum. Measurements of wall thickness and lumen diameter, whenever possible, were made by ultrasound cursors; their motility was also assessed. In addition, two sites (10 cm cranial to the umbilicus and just behind the sternal pad) were evaluated as suitable locations for ultrasound-guided abdominocentesis. Gastrointestinal structures were identified by their ultrasonographic similarity to their known physical appearance and location. For determination of the topographical anatomy of gastrointestinal viscera, two camels were euthanized and preserved with 10% formalin solution as per Grossman’s technique (1959). In addition, in eight of the camels ultrasonography of each stomach compartment and intestines was carried out, and then this part was injected transcutaneously with a colored dye. The animals were then immediately euthanized and examined postmortem for confirmation of sonography results. Data are expressed as means ± SD. 3. Results 3.1. Ultrasonography of the rumen and glandular sacs The rumen and its glandular sacs were visualized occupying the major portion of the abdominal cavity, filling most of the left side of the abdomen. It was best seen in the left paralumbar fossa. In the later region, the large caudodorsal ruminal sac was visualized close
2.2. Animals, history and physical examination Twenty-two adult camels (Camelus dromedarius) (age: 8.8 ± 3.8 years) were examined at the Veterinary Teaching Hospital, Qassim University, Saudi Arabia. Of the camels, 2 (9%) were males and 5 (25%) were 2–3 month pregnant, while the others were non-pregnant and non-lactating females. Camels underwent a thorough physical examination including general behavior and condition, auscultation of the heart, lungs, rumen and intestine, detection of heart and respiratory rates and rectal temperature (Köhler-Rollefson et al., 2001). All camels were clinically healthy based on physical and laboratory evaluation (complete cell blood count and chemistry panel), and they had full access to feed and water before and after examination. Based on a 1 (very thin) to 5 (fat) scale, the body condition score (BCS) of camels was determined as previously reported (Sghiri and Driancourt, 1999); it was 3.4 ± 0.3. The experimental protocol has been accepted by the Animal Ethical Committee, Deanship for Scientific Research, Qassim University, Saudi Arabia.
Fig. 1. Ultrasonogram of the caudodorsal ruminal sac in a camel. Image was taken in the caudal left paralumbar fossa. The sac is visualized close to the spleen and left kidney. The rumen wall is smooth and echogenic. The contents of the rumen could not be seen because of reflection of the ultrasound waves by gas contents. DS = dorsal; VT = ventral.
M. Tharwat et al. / Research in Veterinary Science 93 (2012) 1015–1020
to the spleen and left kidney (Fig. 1). The rumen wall was smooth and echogenic with an average wall thickness of 0.3 ± 0.11 cm. Reverberation artifacts running parallel to the ruminal wall were seen in the region of the dorsal gas cap. In all examined camels, the contents of the rumen could not be seen. Motility of the rumen was seen as shifting, retreating, and eventual replacement of portions of the wall during gastric contraction cycles. Because of the lack of penetration and large volume of the rumen, it was not possible to measure the size of the rumen. The cranial glandular sacs were seen deep in the right and left 5th intercostal spaces in 20 (91%) camels. In the other 2 (9%) cases, these glandular sacs were visualized deep in the 6th intercostal spaces to the right and left of the thorax. The caudal glandular sacs were imaged in the 9th intercostal space just ventral to the abomasum and liver in 18 (82%) animals. The ventral parts of the caudal glandular sacs in these 18 camels could be imaged lying against the paramedian region 10 cm to the right of the umbilicus. In the other 4 (18%) cases, these glandular sacs could not be imaged at all. The contents of glandular sacs appeared echogenic with gaseous inclusions, and hypoechogenic fluid. The cranial and caudal glandular sacs had a wall thickness of 0.64 ± 0.22 cm. Both of them could be seen as series of hyperechoic, semicircular protrusions, curving away from the ventral body wall (Fig. 2). 3.2. Ultrasonography of the reticulum The ventral part of the reticulum was best imaged in 17 (77%) camels from the left and right paramedian region just behind the sternal pad, about 33 ± 9 cm cranial to the umbilicus. In the other 5 (23%) camels, the reticulum could not be imaged from this position. In these animals the reticulum could not be imaged as it is not possible to perform ultrasonography in the standing animal. The reticulum had a thick wall (1.17 ± 0.3 cm) that appeared as a half-moon-shaped structure with an even contour (Fig. 3). The reticulum had a biphasic contraction, and the period between 2 successive biphasic contractions was 50 ± 13 s in camels in which reticulum could be imaged. The first contraction was incomplete and was followed by an interval of incomplete relaxation; this was followed immediately by a second complete contraction where the reticulum could not be seen on the monitor. An interval of complete relaxation follows, in which the reticulum returned to its initial position. 3.3. Ultrasonography of the omasum The omasum was best imaged through the right 6th to 8th intercostal spaces in 18 (82%) camels. In the remaining 4 (18%)
Fig. 2. Ultrasonogram of the caudal glandular sacs in a camel. Image was taken in the right ventral abdomen 10 cm to the right of the umbilicus. 1 = liver; 2 = caudal glandular sacs; DS = dorsal; VT = ventral.
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Fig. 3. Ultrasonogram of the reticulum in a camel. Image was taken in the right paramedian region just behind to the sternal pad. 1 = liver; 2 = caudal glandular sacs. D = diaphragm; F = free peritoneal fluid; DS = dorsal; VT = ventral.
camels, it was visualized through four consecutive intercostal spaces (right 6th to 9th). The omasum was visible as a tubular structure extending between these intercostal spaces and coursing along the body wall approximately parallel to the long axis of the camel. Only the wall of the organ closest to the transducer was visible; its wall appeared as a thick echogenic line. It had a wall thickness of 1.1 ± 0.7 cm and a transverse diameter of 8.74 ± 3.4 cm. The content of the omasum could not be seen probably because of its content. The organ appeared largest in the 7th intercostal space and decreased in size cranially and caudally from this point (Fig. 4). The distance between the dorsal limit of the omasum and the midline of the back was 66 ± 14, 76 ± 16 and 84 ± 15 cm at the right 8th, 7th and 6th intercostal spaces, respectively. In the 6th intercostal space, the cranioventral ruminal sac was visible ventral to the omasum. Similar to the reticulum, an active motility was visualized in the omasum, but in a shorter duration (23 ± 14 s). 3.4. Ultrasonography of the abomasum The abomasum could be best visualized from the right 9th and 8th intercostal spaces in 14 (64%) camels, while in 3 (14%) animals it could be observed in the 9th intercostal space and in 5 (22%) camels in the 8th and 7th intercostal space. Its diameter was largest in the 8th intercostal space (9.1 ± 1.1 cm), followed by the 9th (7 ± 1.6 cm) and the 7th (5.4 ± 0.45 cm) intercostal spaces (Fig. 5).
Fig. 4. Ultrasonogram of the omasum in a camel. Image was taken in the right 6th intercostal space. PV = portal vein; HV = hepatic vein; DS = dorsal; VT = ventral.
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At postmortem examination, the abomasum was differentiated from the duodenum by its large diameter. Duodenum at necropsy had a diameter of 3.8 ± 0.32 cm. The abomasum had a wall thickness of 0.76 ± 0.46 cm. In the 9th intercostal space, the abomasum lies between the glandular sacs of the caudodorsal ruminal sac and the hepatic parenchyma. The abomasal wall appeared as a narrow echogenic line and the contents appeared as a haeterogeneous, moderately echogenic structure with echogenic stippling. Abomasal contractions were not observed in any of the examined camels, but movement of the abomasum contents was seen. In none of the 22 examined animals the pylorus was identified and imaged. 3.5. Ultrasonography of the small intestine Small intestinal structures were best seen low in the right paralumbar fossa. It had had a wall thickness of 0.43 ± 0.14 cm and a mean diameter of 2.62 ± 0.47 cm. Its contents were almost very hypoechoic, haeterogeneous and it contracted every few seconds. Boluses of hypoechoic fluid ingesta could be seen, but were rarely present more than those few seconds before the intestine contracted. Individual segments of intestine were difficult to discern in areas of collapsed intestine because of the lack of contrast between wall and lumen; gas shadowing was not seen. Because of the absence of the gallbladder in camels, it was very difficult to identify and image the duodenum in any of the examined cases. Therefore, the duodenum, jejunum and ileum could not be differentiated from one another ultrasonographically. More than 10 loops of small intestine were imaged adjacent to one another from the lower right flank and lateral abdominal wall and from the 9th to 11th intercostal spaces (Fig. 6). 3.6. Ultrasonography of the large intestine The large intestine was usually easy to differentiate from the small intestine based on its marked gas content and relatively large diameter. Because of the gas, only the wall of the large intestine close to the transducer was imaged where it appeared as a thick echogenic line. The wall of the large intestine furthest from the transducer could not be imaged. The cecum was imaged chiefly in the caudal right flank. It was thin-walled (0.37 ± 0.05 cm), had a diameter of 13.8 ± 1.6 cm. Its lateral wall appeared as a thick echoic, crescent-shaped line. Owing to the presence of gas, the content of the cecum could not be imaged in any of the camels (Fig. 7). The tip of the cecum could also not be imaged because of its caudal position. Segments of ascending colon could be seen in the right paralumbar fossa. The proximal loop of the large colon appeared as thick, echogenic, continuous and slightly curved lines.
Fig. 5. Ultrasonogram of the abomasum in a camel. Image was taken in the right 8th intercostal space. DS = dorsal; VT = ventral.
Fig. 6. Ultrasonogram of the jejunum in a camel. Image was taken low in the right paralumbar fossa. J = jejunum; DS = dorsal; VT = ventral.
It was thin-walled (0.51 ± 0.08 cm) and had a diameter of 3.5 ± 0.8 cm. The spiral colon was confined in all camels to the caudal ventral half of the abdomen. It appeared as structures with thick echoic lateral walls with a number of echogenic arched lines next to each other (Fig. 8). 3.7. Abdominocentesis Free peritoneal fluid was imaged in two locations in 19 (86%) of the 22 examined camels. Despite the absence of visualization of free fluid, we tried to tap the 3 remaining camels, however no fluid was collected. Fluid could be seen first in the triangular space between the dorsal ruminal sac and reticulum. It was therefore best visualized during reticular contraction. The transducer was located at the ventral midline just behind the sternal pad and directed cranially. Free fluid could be seen also around the umbilicus between the ventral to the spiral colon. Ultrasound-guided abdominocentesis was successful in 15 (68%) of the examined camels. The volume of collected peritoneal fluid from the camels ranged from 7 to 25 (13 ± 6) ml. 4. Discussion Transabdominal ultrasonography is a non-invasive diagnostic tool that is more and more used in ruminant medicine and surgery.
Fig. 7. Ultrasonogram of the cecum in a camel. Image was taken in the caudal right paralumbar fossa. DS = dorsal; VT = ventral.
M. Tharwat et al. / Research in Veterinary Science 93 (2012) 1015–1020
Fig. 8. Ultrasonogram of the spiral colon in a camel. Image was taken in caudal ventral half of the abdomen caudal to the umbilicus. S = spiral colon; DS = dorsal; VT = ventral.
In dromedary camels, there are no published data concerning ultrasonographic diagnosis for medical and surgical diagnosis. However, ultrasound can be used to assess abdominal organs without inflicting pain avoiding more invasive ancillary tests such as explorative laparotomy. The camel practitioners should be familiar with the ultrasonographic anatomy of healthy animals so as to be able to interpret abnormal findings. The stomach of the camel is divided into compartments, as in all ruminants, namely a rumen, reticulum, omasum, and abomasum (Smuts and Bezuidenhout, 1987). In this study, the same names will be used for these compartments although they differ greatly in shape and structure from typical design encountered in cattle. The caudodorsal ruminal sac was imaged in the left paralumbar fossa and in the entire half of the left abdomen. Its wall was smooth and echogenic and, because of reflection of the ultrasound waves by gas, the contents of the rumen could not be seen in all examined camels. The wall of the ruminal glandular sacs was thicker than the rest of the ruminal wall and this made it easy for differentiation. The cranial and caudal glandular sacs could be imaged as series of hyperechoic, semicircular protrusions. They could be visualized from four positions. The cranial glandular sacs were seen deep in the right and left 5th intercostal spaces just caudal to the sternal pad. The caudal glandular sacs were visualized in the 9th intercostal space just ventral to the abomasum and liver. Their ventral parts could be imaged lying against the paramedian region 10 cm to the right of the umbilicus. On the contrary to ruminal contents, the contents of glandular sacs appeared echogenic with gaseous inclusions, and the fluid is hypoechogenic. Like in cattle, the reticulum in the camels appeared as a halfmoon-shaped structure with an even contour (Braun and Gotz, 1994). The advantage of ultrasonography of the reticulum is that the contour and motility of the organ can be reliably assessed, contents of the reticulum, however, can be rarely assessed because of their partial gaseous composition. Disadvantage of reticulum examination is that the animal should be placed in a lateral recumbency because doing it in standing position is not possible. During examination of the reticulum, biphasic reticular contractions were seen that was similar to other ruminants (Braun and Gotz, 1994; Braun and Jacquat, 2011). The ultrasonographic examination of the omasum was straightforward in all 22 camels. Because of its position immediately adjacent to the costal part of the right abdominal wall, the omasum was clearly visible and easily identified on the ultrasonograms. The contents of the omasum could not be visualized because of their gaseous nature, similar to that of
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the cattle (Braun and Blessing, 2006). In contrast with the reticulum in cattle (Braun and Gotz, 1994), the omasum in this study had an active motility and this may be due to the tube-structure of the organ. In all examined camels; the abomasum was easily accessible to ultrasonography, because it is situated immediately adjacent to the right abdominal wall. The abomasum could be imaged from the 9th to 7th intercostal spaces. The abomasal folds could be poorly imaged ultrasonographically. This may be due to the abomasal folds are undulating and thus not always visible on a two dimensional image. In this study, the pylorus was not imaged in any of the examined camels. A possible explanation may be that the pylorus can be imaged only when it is situated immediately adjacent to the abdominal wall and runs longitudinally. In a study of 47 cows, only in 1 cow the pylorus had been imaged (Braun et al., 1997). In contrast with the reticulum, in which biphasic contractions was visualized ultrasonographically, no abomasal motility was observed in this study. In the present study, transabdominal ultrasonography was an useful technique to differentiate between the small and large intestine. Generally, our findings were similar to descriptions of the small (Braun and Marmier, 1995) and large (Braun and Amrein, 2001) intestine in cattle. The duodenum could not be imaged in any of the examined camels. In cattle, presence of the gallbladder facilitates the identification of the duodenum; however because of the absence of the gallbladder in camels, it was difficult to differentiate the duodenum from the jejunum and ileum. The jejunum and ileum were most often seen in the ventral region of the right flank. This is in contrast to cattle in which they were always seen in the 11th and 12th intercostal spaces (Braun and Marmier, 1995). The intestinal diameter of the small intestine was in most of time less than 3 cm. This can be of particular importance for the diagnosis of paralytic or obstructive ileus in camels. Because of intraluminal gas, only the wall of the large intestine closest to the transducer could be imaged as a thick echoic line. The success rate of the abdominocentesis procedure was 86%, almost similar to the 91.6% in a recently reported study in cattle (Wittek et al., 2010). Similar success rates have been reported by Anderson et al. (1994) who obtained peritoneal fluid from 20 of 22 cows, and by Wilson et al. (1985) who were successful in 19 of 21 cows. The volumes of peritoneal fluid obtained here were larger to those (0–5 ml) obtained by Oehme (1969) and Wilson et al. (1985). Ultrasonography allowed particularly good evaluation of free peritoneal fluid. This is likely to be of practical value, because the most common surgical and many severe medical lesions of the camel gastrointestinal tract lead to abnormalities in these regions: excess accumulation of peritoneal fluid with peritonitis or strangulating obstructions and fluid-distended, atonic bowel with intraluminal or enteritis. This study also confirmed the relative usefulness of two sites for abdominocentesis, just cranial to the umbilicus and behind caudal to the sternal pad.
5. Conclusions This study indicates that the gastrointestinal tract in dromedary camels is easily accessible to ultrasonography, because it is situated immediately adjacent to the ventrolateral right and left abdominal wall. The procedure is a valuable supplementary technique for the assessment of the camel’s gastrointestinal tract. Knowledge of the ultrasonographic appearance of the normal gastrointestinal tract in the camel provides a reference for the interpretation of the gastrointestinal tract in camels with suspected digestive abnormalities. Ultrasonography could be used as a noninvasive diagnostic tool in order to detect gastrointestinal diseases in the dromedary camel.
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Acknowledgment This study was supported by the Deanship for Scientific Research (SR-D-010-078), Qassim University, Saudi Arabia.
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Contents lists available at SciVerse ScienceDirect
Research in Veterinary Science journal homepage: www.elsevier.com/locate/rvsc
Transabdominal ultrasonographic appearance of the gastrointestinal viscera of healthy camels (Camelus dromedaries) Mohamed Tharwat a,1, Fahd Al-Sobayil a, Ahmed Ali a, Sébastien Buczinski b,⇑ a b
Department of Veterinary Medicine, College of Agriculture and Veterinary Medicine, Qassim University, Saudi Arabia Clinique Ambulatoire Bovine, Departement des Sciences Cliniques, Faculté de Médecine Vétérinaire, Université de Montréal, Saint-Hyacinthe, Canada
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Article history: Received 6 July 2011 Accepted 11 December 2011
Keywords: Camel Dromedary Gastrointestinal Normal Ultrasonography
a b s t r a c t The purpose of this study was to describe the ultrasonographic picture of the gastrointestinal tract in healthy camels (Camelus dromedarius). For this purpose, 22 camels were examined. The rumen and its glandular sacs were filling most of the left side of the abdomen. The rumen wall was smooth and echogenic. The ventral part of the reticulum could be best imaged in 17 (77%) camels from the left and right paramedian region just behind to the sternal pad. The reticulum in these animals had a thick wall (1.17 ± 0.27 cm) that appeared as a half-moon-shaped structure with a biphasic contraction. The omasum was best viewed through the right 8th to 6th intercostal spaces in 18 (82%) camels. In the remaining 4 (18%), it was visualized through four consecutive intercostal spaces (right 9th to 6th). It had a wall thickness of 1.1 ± 0.7 cm and a transverse diameter of 8.74 ± 3.4 cm. The abomasum could be best visualized from the right 9th and 8th intercostal spaces in 14 (64%) camels, while it was observed in the 9th intercostal space in 3 (14%) animals and in the 8th and 7th intercostal space in 5 (22%) camels. Small intestinal structures were best seen low in the right paralumbar fossa. It was thin-walled (0.43 ± 0.14 cm) and had a diameter of 2.62 ± 0.47 cm. The cecum was imaged chiefly in the caudal right flank. It was thin-walled (0.37 ± 0.05 cm), had a diameter of 13.8 ± 1.6 cm. The proximal loop of the large colon appeared as thick, echogenic, continuous and slightly curved lines. It was thin-walled (0.51 ± 0.08 cm) and had a diameter of 3.5 ± 0.8 cm. The spiral colon was confined in all camels to the caudal ventral half of the abdomen. It appeared as structures with thick echoic lateral walls with a number of echogenic arched lines next to each other. Free peritoneal fluid pockets were imaged in two locations in 19 (86%) camels. Ultrasoundguided abdominocentesis was successful in 15 (68%) of the examined camels. This study provides the ultrasonographic appearance of the normal gastrointestinal tract in healthy camels that could be used as a reference for the interpretation of suspected digestive abnormalities. Ó 2012 Published by Elsevier Ltd.
1. Introduction The dromedary camel is important specie in Africa, Middle-East and Australia. Despite its valuable use as draft animals, it is also used for milk and meat production. In the northern hemisphere, it is mainly used as a companion animal or in circus and can therefore have a worldwide veterinary importance. Diseases of the gastrointestinal tract of the camel are of great importance including impaction, bloat, ulceration and swallowed foreign bodies, enteritis, constipation, abomasal and intestinal obstruction, peritonitis, as well as abdominal hemorrhage, ascites and neoplasia (Al-Ani and Qureshi, 2004; Ramadan et al., 2008; Fowler, 2010). Many of these diseases can be effectively treated in their early stages, but ⇑ Corresponding author. Tel.: +1 450 778 8123; fax: +1 450 778 8120. E-mail address: [email protected] (S. Buczinski). Permanent address: Department of Animal Medicine, Faculty of Veterinary Medicine, Zagazig University, Egypt. 1
0034-5288/$ - see front matter Ó 2012 Published by Elsevier Ltd. doi:10.1016/j.rvsc.2011.12.003
efforts to recognize them or their severity are hampered by camel stoic nature and vague clinical signs (Fowler, 2010). Due to largesized abdomen of camels, even experienced clinicians may not be able to pinpoint the organ affected and diagnose the gastrointestinal disease. In addition, transrectal palpation in camels gives access only to the caudal viscera (Al-Ani and Qureshi, 2004; Ramadan et al., 2008). Exploratory laparotomy is usually performed in cases of camels with unexplained gastrointestinal illness (Ramadan et al., 2008). Most owners consent to this invasive procedure only when the prognosis is good, and when there is a reasonable chance that the animal can be cured. Exploratory laparotomy should be avoided in camels with a poor prognosis because it may inflict additional pain, it can be considered as an expansive diagnostic test and the animal cannot be slaughtered for human consumption waiting for withdrawal times (Fowler, 2010). In cattle, abdominal ultrasonography is an interesting diagnostic tool that can also be used as a prognostic tool in some diseases
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since the extension and importance of the disease are better assessed. The procedure is an ideal diagnostic tool for the investigation of gastrointestinal disorders that can also be used directly on the farm. It helps in deciding whether the animal should undergo surgical or medical treatment or be slaughtered (Braun, 2003, 2005, 2009). Ultrasonography has been described in examination of the reticulum (Braun and Gotz, 1994), omasum (Braun and Blessing, 2006), abomasum (Braun et al., 1997), small and large intestines (Braun and Marmier, 1995; Braun and Amrein, 2001). In llamas and alpacas, specific transabdominal ultrasonographic appearance of the gastrointestinal viscera has been described in order to help in the management of New World camelids’ gastrointestinal diseases (Cebra et al., 2002). In camel practice, ultrasonography has been used mainly for examination of the reproductive tract (Skidmore et al., 2009; Wani and Skidmore, 2010; Skidmore and Billah, 2011). The data on the use of ultrasound in medical and surgical diseases of camel are rare. Recently, we reported the use of transcutaneous ultrasound to determine intestinal wall thickness in camels with paratuberculosis and detecting enlarged mesenteric lymph nodes, image peritoneal fluid in cases with chronic trypanosomiasis, detect distended intestines in camels with intestinal obstruction (Mohamed et al., 2011a,b). However, despite success with this imaging technique, experiences are anecdotal. Data are still lacking concerning the normal appearance of gastrointestinal viscera in camels. The present study was therefore designed for establishing normal appearance, size, shape, and position of various gastrointestinal organs in dromedary camels. 2. Materials and methods 2.1. Stomach compartment subdivisions There are many reports on the subdivisions of the stomach of the camel. From the 19th century, descriptions of the stomach in camel have reflected those of ox and sheep. Some investigations regard the camel as a monogastric animal or divide the stomach of the camel into two, three, and four stomachs (Boas, 1890; Hegazi, 1950; Hansen and Schmidt-Nielsen, 1957; Purohit and Rathor, 1962; Smuts and Bezuidenhout, 1987; Wang et al., 2000). The camel stomach has additional glandular sacs that may have special digestive functions (Wang et al., 2000). In this report, we used the same nomenclature as in cattle as every part of the stomach appeared different by ultrasound examination so was not possible to merge stomach compartments into two or three parts.
2.3. Ultrasonographic examination First, the foreleg of each camel was bent and tied with a rope on the carpal joint. The head was then held and the animal was pushed till lay in a position of sternal recumbency. The fore-andhind legs were then tied by a rope near the carpal and hock joints, respectively. On both sides of thorax and abdomen, the fleece was clipped and the skin was shaved. If necessary, animals were slightly sedated using xylazine (0.02 mg/kg IV, Bomazine 10%, Bomac Laboratories Ltd., New Zealand). Ultrasonographic examination was carried out using a 3.5 MHz sector transducer with a maximal depth of 22 cm (SSD-500, Aloka, Tokyo, Japan). After the application of transmission gel to the transducer, the animals were examined beginning at the caudal abdomen and extending forward to the level of the sternal pad. The rumen, reticulum omasum, abomasum, small and large intestines as well as peritoneal fluid were imaged. Each flank was examined through the paralumbar fossa. To best imaging the reticulum, the camel was placed in a lateral recumbency and where the transducer was directed forward in a 30° angle perpendicular to the animal ventrum. Measurements of wall thickness and lumen diameter, whenever possible, were made by ultrasound cursors; their motility was also assessed. In addition, two sites (10 cm cranial to the umbilicus and just behind the sternal pad) were evaluated as suitable locations for ultrasound-guided abdominocentesis. Gastrointestinal structures were identified by their ultrasonographic similarity to their known physical appearance and location. For determination of the topographical anatomy of gastrointestinal viscera, two camels were euthanized and preserved with 10% formalin solution as per Grossman’s technique (1959). In addition, in eight of the camels ultrasonography of each stomach compartment and intestines was carried out, and then this part was injected transcutaneously with a colored dye. The animals were then immediately euthanized and examined postmortem for confirmation of sonography results. Data are expressed as means ± SD. 3. Results 3.1. Ultrasonography of the rumen and glandular sacs The rumen and its glandular sacs were visualized occupying the major portion of the abdominal cavity, filling most of the left side of the abdomen. It was best seen in the left paralumbar fossa. In the later region, the large caudodorsal ruminal sac was visualized close
2.2. Animals, history and physical examination Twenty-two adult camels (Camelus dromedarius) (age: 8.8 ± 3.8 years) were examined at the Veterinary Teaching Hospital, Qassim University, Saudi Arabia. Of the camels, 2 (9%) were males and 5 (25%) were 2–3 month pregnant, while the others were non-pregnant and non-lactating females. Camels underwent a thorough physical examination including general behavior and condition, auscultation of the heart, lungs, rumen and intestine, detection of heart and respiratory rates and rectal temperature (Köhler-Rollefson et al., 2001). All camels were clinically healthy based on physical and laboratory evaluation (complete cell blood count and chemistry panel), and they had full access to feed and water before and after examination. Based on a 1 (very thin) to 5 (fat) scale, the body condition score (BCS) of camels was determined as previously reported (Sghiri and Driancourt, 1999); it was 3.4 ± 0.3. The experimental protocol has been accepted by the Animal Ethical Committee, Deanship for Scientific Research, Qassim University, Saudi Arabia.
Fig. 1. Ultrasonogram of the caudodorsal ruminal sac in a camel. Image was taken in the caudal left paralumbar fossa. The sac is visualized close to the spleen and left kidney. The rumen wall is smooth and echogenic. The contents of the rumen could not be seen because of reflection of the ultrasound waves by gas contents. DS = dorsal; VT = ventral.
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to the spleen and left kidney (Fig. 1). The rumen wall was smooth and echogenic with an average wall thickness of 0.3 ± 0.11 cm. Reverberation artifacts running parallel to the ruminal wall were seen in the region of the dorsal gas cap. In all examined camels, the contents of the rumen could not be seen. Motility of the rumen was seen as shifting, retreating, and eventual replacement of portions of the wall during gastric contraction cycles. Because of the lack of penetration and large volume of the rumen, it was not possible to measure the size of the rumen. The cranial glandular sacs were seen deep in the right and left 5th intercostal spaces in 20 (91%) camels. In the other 2 (9%) cases, these glandular sacs were visualized deep in the 6th intercostal spaces to the right and left of the thorax. The caudal glandular sacs were imaged in the 9th intercostal space just ventral to the abomasum and liver in 18 (82%) animals. The ventral parts of the caudal glandular sacs in these 18 camels could be imaged lying against the paramedian region 10 cm to the right of the umbilicus. In the other 4 (18%) cases, these glandular sacs could not be imaged at all. The contents of glandular sacs appeared echogenic with gaseous inclusions, and hypoechogenic fluid. The cranial and caudal glandular sacs had a wall thickness of 0.64 ± 0.22 cm. Both of them could be seen as series of hyperechoic, semicircular protrusions, curving away from the ventral body wall (Fig. 2). 3.2. Ultrasonography of the reticulum The ventral part of the reticulum was best imaged in 17 (77%) camels from the left and right paramedian region just behind the sternal pad, about 33 ± 9 cm cranial to the umbilicus. In the other 5 (23%) camels, the reticulum could not be imaged from this position. In these animals the reticulum could not be imaged as it is not possible to perform ultrasonography in the standing animal. The reticulum had a thick wall (1.17 ± 0.3 cm) that appeared as a half-moon-shaped structure with an even contour (Fig. 3). The reticulum had a biphasic contraction, and the period between 2 successive biphasic contractions was 50 ± 13 s in camels in which reticulum could be imaged. The first contraction was incomplete and was followed by an interval of incomplete relaxation; this was followed immediately by a second complete contraction where the reticulum could not be seen on the monitor. An interval of complete relaxation follows, in which the reticulum returned to its initial position. 3.3. Ultrasonography of the omasum The omasum was best imaged through the right 6th to 8th intercostal spaces in 18 (82%) camels. In the remaining 4 (18%)
Fig. 2. Ultrasonogram of the caudal glandular sacs in a camel. Image was taken in the right ventral abdomen 10 cm to the right of the umbilicus. 1 = liver; 2 = caudal glandular sacs; DS = dorsal; VT = ventral.
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Fig. 3. Ultrasonogram of the reticulum in a camel. Image was taken in the right paramedian region just behind to the sternal pad. 1 = liver; 2 = caudal glandular sacs. D = diaphragm; F = free peritoneal fluid; DS = dorsal; VT = ventral.
camels, it was visualized through four consecutive intercostal spaces (right 6th to 9th). The omasum was visible as a tubular structure extending between these intercostal spaces and coursing along the body wall approximately parallel to the long axis of the camel. Only the wall of the organ closest to the transducer was visible; its wall appeared as a thick echogenic line. It had a wall thickness of 1.1 ± 0.7 cm and a transverse diameter of 8.74 ± 3.4 cm. The content of the omasum could not be seen probably because of its content. The organ appeared largest in the 7th intercostal space and decreased in size cranially and caudally from this point (Fig. 4). The distance between the dorsal limit of the omasum and the midline of the back was 66 ± 14, 76 ± 16 and 84 ± 15 cm at the right 8th, 7th and 6th intercostal spaces, respectively. In the 6th intercostal space, the cranioventral ruminal sac was visible ventral to the omasum. Similar to the reticulum, an active motility was visualized in the omasum, but in a shorter duration (23 ± 14 s). 3.4. Ultrasonography of the abomasum The abomasum could be best visualized from the right 9th and 8th intercostal spaces in 14 (64%) camels, while in 3 (14%) animals it could be observed in the 9th intercostal space and in 5 (22%) camels in the 8th and 7th intercostal space. Its diameter was largest in the 8th intercostal space (9.1 ± 1.1 cm), followed by the 9th (7 ± 1.6 cm) and the 7th (5.4 ± 0.45 cm) intercostal spaces (Fig. 5).
Fig. 4. Ultrasonogram of the omasum in a camel. Image was taken in the right 6th intercostal space. PV = portal vein; HV = hepatic vein; DS = dorsal; VT = ventral.
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At postmortem examination, the abomasum was differentiated from the duodenum by its large diameter. Duodenum at necropsy had a diameter of 3.8 ± 0.32 cm. The abomasum had a wall thickness of 0.76 ± 0.46 cm. In the 9th intercostal space, the abomasum lies between the glandular sacs of the caudodorsal ruminal sac and the hepatic parenchyma. The abomasal wall appeared as a narrow echogenic line and the contents appeared as a haeterogeneous, moderately echogenic structure with echogenic stippling. Abomasal contractions were not observed in any of the examined camels, but movement of the abomasum contents was seen. In none of the 22 examined animals the pylorus was identified and imaged. 3.5. Ultrasonography of the small intestine Small intestinal structures were best seen low in the right paralumbar fossa. It had had a wall thickness of 0.43 ± 0.14 cm and a mean diameter of 2.62 ± 0.47 cm. Its contents were almost very hypoechoic, haeterogeneous and it contracted every few seconds. Boluses of hypoechoic fluid ingesta could be seen, but were rarely present more than those few seconds before the intestine contracted. Individual segments of intestine were difficult to discern in areas of collapsed intestine because of the lack of contrast between wall and lumen; gas shadowing was not seen. Because of the absence of the gallbladder in camels, it was very difficult to identify and image the duodenum in any of the examined cases. Therefore, the duodenum, jejunum and ileum could not be differentiated from one another ultrasonographically. More than 10 loops of small intestine were imaged adjacent to one another from the lower right flank and lateral abdominal wall and from the 9th to 11th intercostal spaces (Fig. 6). 3.6. Ultrasonography of the large intestine The large intestine was usually easy to differentiate from the small intestine based on its marked gas content and relatively large diameter. Because of the gas, only the wall of the large intestine close to the transducer was imaged where it appeared as a thick echogenic line. The wall of the large intestine furthest from the transducer could not be imaged. The cecum was imaged chiefly in the caudal right flank. It was thin-walled (0.37 ± 0.05 cm), had a diameter of 13.8 ± 1.6 cm. Its lateral wall appeared as a thick echoic, crescent-shaped line. Owing to the presence of gas, the content of the cecum could not be imaged in any of the camels (Fig. 7). The tip of the cecum could also not be imaged because of its caudal position. Segments of ascending colon could be seen in the right paralumbar fossa. The proximal loop of the large colon appeared as thick, echogenic, continuous and slightly curved lines.
Fig. 5. Ultrasonogram of the abomasum in a camel. Image was taken in the right 8th intercostal space. DS = dorsal; VT = ventral.
Fig. 6. Ultrasonogram of the jejunum in a camel. Image was taken low in the right paralumbar fossa. J = jejunum; DS = dorsal; VT = ventral.
It was thin-walled (0.51 ± 0.08 cm) and had a diameter of 3.5 ± 0.8 cm. The spiral colon was confined in all camels to the caudal ventral half of the abdomen. It appeared as structures with thick echoic lateral walls with a number of echogenic arched lines next to each other (Fig. 8). 3.7. Abdominocentesis Free peritoneal fluid was imaged in two locations in 19 (86%) of the 22 examined camels. Despite the absence of visualization of free fluid, we tried to tap the 3 remaining camels, however no fluid was collected. Fluid could be seen first in the triangular space between the dorsal ruminal sac and reticulum. It was therefore best visualized during reticular contraction. The transducer was located at the ventral midline just behind the sternal pad and directed cranially. Free fluid could be seen also around the umbilicus between the ventral to the spiral colon. Ultrasound-guided abdominocentesis was successful in 15 (68%) of the examined camels. The volume of collected peritoneal fluid from the camels ranged from 7 to 25 (13 ± 6) ml. 4. Discussion Transabdominal ultrasonography is a non-invasive diagnostic tool that is more and more used in ruminant medicine and surgery.
Fig. 7. Ultrasonogram of the cecum in a camel. Image was taken in the caudal right paralumbar fossa. DS = dorsal; VT = ventral.
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Fig. 8. Ultrasonogram of the spiral colon in a camel. Image was taken in caudal ventral half of the abdomen caudal to the umbilicus. S = spiral colon; DS = dorsal; VT = ventral.
In dromedary camels, there are no published data concerning ultrasonographic diagnosis for medical and surgical diagnosis. However, ultrasound can be used to assess abdominal organs without inflicting pain avoiding more invasive ancillary tests such as explorative laparotomy. The camel practitioners should be familiar with the ultrasonographic anatomy of healthy animals so as to be able to interpret abnormal findings. The stomach of the camel is divided into compartments, as in all ruminants, namely a rumen, reticulum, omasum, and abomasum (Smuts and Bezuidenhout, 1987). In this study, the same names will be used for these compartments although they differ greatly in shape and structure from typical design encountered in cattle. The caudodorsal ruminal sac was imaged in the left paralumbar fossa and in the entire half of the left abdomen. Its wall was smooth and echogenic and, because of reflection of the ultrasound waves by gas, the contents of the rumen could not be seen in all examined camels. The wall of the ruminal glandular sacs was thicker than the rest of the ruminal wall and this made it easy for differentiation. The cranial and caudal glandular sacs could be imaged as series of hyperechoic, semicircular protrusions. They could be visualized from four positions. The cranial glandular sacs were seen deep in the right and left 5th intercostal spaces just caudal to the sternal pad. The caudal glandular sacs were visualized in the 9th intercostal space just ventral to the abomasum and liver. Their ventral parts could be imaged lying against the paramedian region 10 cm to the right of the umbilicus. On the contrary to ruminal contents, the contents of glandular sacs appeared echogenic with gaseous inclusions, and the fluid is hypoechogenic. Like in cattle, the reticulum in the camels appeared as a halfmoon-shaped structure with an even contour (Braun and Gotz, 1994). The advantage of ultrasonography of the reticulum is that the contour and motility of the organ can be reliably assessed, contents of the reticulum, however, can be rarely assessed because of their partial gaseous composition. Disadvantage of reticulum examination is that the animal should be placed in a lateral recumbency because doing it in standing position is not possible. During examination of the reticulum, biphasic reticular contractions were seen that was similar to other ruminants (Braun and Gotz, 1994; Braun and Jacquat, 2011). The ultrasonographic examination of the omasum was straightforward in all 22 camels. Because of its position immediately adjacent to the costal part of the right abdominal wall, the omasum was clearly visible and easily identified on the ultrasonograms. The contents of the omasum could not be visualized because of their gaseous nature, similar to that of
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the cattle (Braun and Blessing, 2006). In contrast with the reticulum in cattle (Braun and Gotz, 1994), the omasum in this study had an active motility and this may be due to the tube-structure of the organ. In all examined camels; the abomasum was easily accessible to ultrasonography, because it is situated immediately adjacent to the right abdominal wall. The abomasum could be imaged from the 9th to 7th intercostal spaces. The abomasal folds could be poorly imaged ultrasonographically. This may be due to the abomasal folds are undulating and thus not always visible on a two dimensional image. In this study, the pylorus was not imaged in any of the examined camels. A possible explanation may be that the pylorus can be imaged only when it is situated immediately adjacent to the abdominal wall and runs longitudinally. In a study of 47 cows, only in 1 cow the pylorus had been imaged (Braun et al., 1997). In contrast with the reticulum, in which biphasic contractions was visualized ultrasonographically, no abomasal motility was observed in this study. In the present study, transabdominal ultrasonography was an useful technique to differentiate between the small and large intestine. Generally, our findings were similar to descriptions of the small (Braun and Marmier, 1995) and large (Braun and Amrein, 2001) intestine in cattle. The duodenum could not be imaged in any of the examined camels. In cattle, presence of the gallbladder facilitates the identification of the duodenum; however because of the absence of the gallbladder in camels, it was difficult to differentiate the duodenum from the jejunum and ileum. The jejunum and ileum were most often seen in the ventral region of the right flank. This is in contrast to cattle in which they were always seen in the 11th and 12th intercostal spaces (Braun and Marmier, 1995). The intestinal diameter of the small intestine was in most of time less than 3 cm. This can be of particular importance for the diagnosis of paralytic or obstructive ileus in camels. Because of intraluminal gas, only the wall of the large intestine closest to the transducer could be imaged as a thick echoic line. The success rate of the abdominocentesis procedure was 86%, almost similar to the 91.6% in a recently reported study in cattle (Wittek et al., 2010). Similar success rates have been reported by Anderson et al. (1994) who obtained peritoneal fluid from 20 of 22 cows, and by Wilson et al. (1985) who were successful in 19 of 21 cows. The volumes of peritoneal fluid obtained here were larger to those (0–5 ml) obtained by Oehme (1969) and Wilson et al. (1985). Ultrasonography allowed particularly good evaluation of free peritoneal fluid. This is likely to be of practical value, because the most common surgical and many severe medical lesions of the camel gastrointestinal tract lead to abnormalities in these regions: excess accumulation of peritoneal fluid with peritonitis or strangulating obstructions and fluid-distended, atonic bowel with intraluminal or enteritis. This study also confirmed the relative usefulness of two sites for abdominocentesis, just cranial to the umbilicus and behind caudal to the sternal pad.
5. Conclusions This study indicates that the gastrointestinal tract in dromedary camels is easily accessible to ultrasonography, because it is situated immediately adjacent to the ventrolateral right and left abdominal wall. The procedure is a valuable supplementary technique for the assessment of the camel’s gastrointestinal tract. Knowledge of the ultrasonographic appearance of the normal gastrointestinal tract in the camel provides a reference for the interpretation of the gastrointestinal tract in camels with suspected digestive abnormalities. Ultrasonography could be used as a noninvasive diagnostic tool in order to detect gastrointestinal diseases in the dromedary camel.
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Acknowledgment This study was supported by the Deanship for Scientific Research (SR-D-010-078), Qassim University, Saudi Arabia.
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