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Characterization of oral double balloon endoscopy in the dog
The Veterinary Journal 195 (2013) 331–336
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The Veterinary Journal journal homepage: www.elsevier.com/locate/tvjl
Characterization of oral double balloon endoscopy in the dog R. Sarria a, O. López Albors a, F. Soria b, I. Ayala c, E. Pérez Cuadrado d, P. Esteban d, R. Latorre a,⇑ a
Department of Anatomy and Comparative Pathology, Veterinary Faculty, University of Murcia, Spain Minimally Invasive Surgery Centre Jesús Usón, Campus Universitario, Cáceres, Spain c Department of Veterinary Surgery and Medicine, Veterinary School, University of Murcia, Spain d Digestive Service, Hospital Morales Meseguer, Murcia, Spain b
a r t i c l e
i n f o
Article history: Accepted 18 June 2012
Keywords: Double balloon endoscopy Dog Intestine Pancreatitis Gastrointestinal diseases
a b s t r a c t Exploration of the canine small intestine using conventional endoscopy is restricted to the duodenum and/or the ileum. Double balloon endoscopy (DBE) is a ‘push and pull’ technique that has been described in humans and permits a complete exploration of the small intestine. In this study, oral DBE was performed on 12 healthy dogs (10–34 kg) to characterize for the first time the efficiency, exploration dynamics and safety of the technique. DBE was successful in 83% of dogs; the average estimated insertion depth of the endoscope was 287 ± 36 cm, and the average duration of the exploration was 84 ± 8 min. No complications or relevant adverse clinical effects were observed, and there was no indication of post-procedure pancreatitis based on serology of two specific markers of pancreatitis (amylase and lipase) and the immediate nonspecific inflammatory mediator C-reactive protein. The study showed that oral DBE is viable and safe in the dog, allowing for the diagnosis and treatment of gastrointestinal diseases deep in the small intestine to an extent that has not previously been possible using conventional endoscopy. Ó 2012 Elsevier Ltd. All rights reserved.
Introduction Most diseases of the gastrointestinal tract in the dog and cat are diffuse and extend along the length of the small intestine (Tams, 2003). However, the severity of the inflammation may vary depending on the anatomical location (Moore, 2003) and since deep areas of the bowel cannot be explored by routine endoscopy, some pathologies, such as lymphomas located in the jejunum or ileum, might not be diagnosed (Tams, 2003). Recently, CasamianSorrosal et al. (2010) demonstrated that definitive histopathological diagnosis of some bowel diseases varied depending on the sampling site and would have been different in most cases if duodenal biopsies only had been obtained. With traditional endoscopy it is not possible to progress further than a few centimetres into the jejunum using the oral approach, or a similar distance into the ileum via the anal approach (Tams, 2003). Thus, the use of current endoscopic techniques to explore, biopsy and treat digestive disorders warrants further investigation. The technique of double balloon endoscopy (DBE) was first reported in 2001 (Yamamoto et al., 2001). Based on ‘push endoscopy’, DBE is a form of deep endoscopy which not only allows exploration, but also treatment of the most common digestive disorders of the small intestine in humans, such as obscure gastroin-
⇑ Corresponding author. Tel.: +34 868 884697. E-mail address: [email protected] (R. Latorre). 1090-0233/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tvjl.2012.06.023
testinal bleeding (Pérez-Cuadrado et al., 2006; Penazzio, 2008), tumours (Mitsui et al., 2009), Crohn’s disease (Decker et al., 2008) and polyps (Ohmiya et al., 2010; Sakamoto et al., 2011). The equipment consists of a 200 cm endoscope (external diameter 9.4 mm) and a 145 cm overtube (diameter 13.2 mm), both of which have a latex balloon attached to the tip (Fig. 1A). The two balloons are inflated and deflated in an alternating sequence to allow the endoscope to progress (pushing phase) or fold the explored intestine behind the balloons (pulling phase). DBE is a non-invasive, safe technique with a similar complication rate in humans to conventional endoscopy. Perforation (0.3%), post-procedure pancreatitis (0.5%) and bleeding (0.8%) are the most common complications (Mensink, 2008; Gerson et al., 2009; Xin et al., 2011). Since pancreatitis is one of the most serious complications, it should be considered as a potential risk in any experimental or elective procedure. The first attempt at DBE in veterinary medicine was successfully performed by Latorre et al. (2007) in two dogs. However, in order to improve the reliability of this technique in veterinary practice, further information concerning insertion depth, duration and safety is needed. According to a recent anatomical study, DBE is feasible in medium to large size dogs using the same type of endoscope used in humans (López Albors et al., 2011). The diameter of the intestinal lumen is closely correlated with body parameters such as antebrachial length, and a minimum diameter of 2 cm is required to allow the passage of the overtube and the associated balloon, making dogs with antebrachii of >18 cm probably suitable for DBE.
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R. Sarria et al. / The Veterinary Journal 195 (2013) 331–336
Fig. 1. (A) Double balloon endoscope (EN-450T5, Fujinon). (B and C) Fluoroscopic examination during oral DBE in dog 12. (B) Intestine-endoscope loop in the jejunum. (C) Position of the endoscope after the loop has been resolved.
The aim of this study was to characterize the exploration dynamics of DBE in the dog in terms of maximum insertion depth, number of push and pull cycles and procedure duration. A secondary goal was to evaluate the safety of the technique by monitoring animal health during and after the procedure. Serological values for the immediate nonspecific inflammatory mediator C-reactive protein (CRP) and two specific markers of pancreatitis (amylase and lipase) were studied in five dogs. Materials and methods Twelve dogs (six Beagles, four American Foxhounds and two English Setters) underwent oral enteroscopy. The dogs came from the animal facility of Murcia University, where Animal Care and Use Guidelines according to the European Convention for the Protection of Vertebrate Animals are followed for Experimental and other Scientific Purposes (Council Directive 86/609/EEC). The dogs’ weight range was 10–34 kg and the proportion of males to females was 10:2. None of the dogs had a history of digestive disease. In eight animals, the forelimb length, an estimator of the small intestine diameter (López Albors et al., 2011), was measured. Dogs were fasted for 36 h before the enteroscopy and premedicated with a combination of 0.05 mg/kg acepromazine and 0.3 mg/kg butorphanol, administered IM. Anaesthesia was induced with a dose of 5 mg/kg propofol, administered IV to effect, and after orotracheal intubation the animals were maintained with isofluorane (1–1.2 minimum alveolar concentration) and 100% oxygen, using an anaesthetic breathing system adapted to their size. During the enteroscopy, blood pressure, heart rate, respiratory rate and oxygen saturation were monitored. Enteroscopies were carried out by two of the authors (EP-C, FS) who have routinely performed DBE for more than 5 years, using an EN-450T5 (Fujinon) enteroscope (Fig. 1A). During enteroscopy exploration, the distance advanced for each
cycle and the time taken for the procedure were recorded in a worksheet (May et al., 2005). To reduce subjectivity, the distance advanced was decided by consensus between the endoscopist and a second author. The exploration depth was measured from just after the pylorus and the end of exploration was established after the repetition of 5–6 unsuccessful push and pull manoeuvres (no advance of the endoscope). In some animals (n = 3), the progress of the endoscope was surveyed by fluoroscopy (PHILIPS BV-300). This allowed us to visualize the position of the tip of the endoscope and overtube within the abdominal cavity. In five dogs, blood samples were obtained at the beginning and end of DBE, and at 24 h and 7 days after the procedure. Serum concentrations of CRP, amylase and lipase were used as indicators of potential inflammation and/or pancreatic damage. After recovery from anaesthesia, the dogs were examined twice a day for 7 days to rule out possible complications, such as an altered behaviour or activity, vomiting, diarrhoea, decreased food ingestion or abdominal discomfort. All data were included in a worksheet and statistical analysis was performed using SPSS 17.0. Descriptive statistics including the Shapiro–Wilks W test for normality and Levene’s test for homogeneity of variance were initially obtained for all experimental variables. Enzyme values were evaluated by analysis of variance (ANOVA, linear model with repeated measures), considering the timing of blood sampling as a within-subject factor. CRP values were subjected to a logarithmic transformation to comply with the assumptions of the analysis. Data for the number of cycles and time were plotted against the explored distance using regression analysis. All statistics were performed using a significance level of P < 0.05.
Results Insertion depth and exploration dynamics Bodyweight, forelimb length, explored distance, time and the number of cycles are shown in Table 1. Dogs 3 and 12 were not
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R. Sarria et al. / The Veterinary Journal 195 (2013) 331–336 Table 1 Summary of data for oral double balloon endoscopy in dogs. Dog 1 2 3 4 5 6 7 8 9 10 11 12 a b
Bodyweight (kg)
Forelimb lengtha (cm)
Estimated insertion depth (cm)
Time (min)
Number of cycles
16 18.5 21.5 19 18 19.5 19.5 13
495 270 90 220 320 232 210 415 385 185 144 120
102 109 37 98 125 70 55 96 77 55 54 19
25 20 3 16 25 19 10 32 32 20 16 6
b
23 17.5 13 13 10 13 18 32 26 33 34 16.9
b
b
From the lateral epicondyle of the humerus to the accessory carpal bone (palpable landmarks). Indicates that fluoroscopy was also used.
included in the statistical analysis, because soon after beginning exploration there was no progress of the endoscope and the procedure was terminated. In the remaining 10 dogs, the average insertion depth was 287 ± 36 cm (range 144–495 cm) and the average duration of the procedure was 84 ± 8 min (range 54–125 min). Exploration efficiency expressed as advanced distance per push and pull cycle was represented by a negative logarithm regression model (Fig. 2). After a phase of maximum efficiency at the beginning of the exploration, a progressive decrease in efficiency was observed. The first push manoeuvre was the most effective cycle with an average value of 35 cm. Thereafter, the efficiency decreased progressively to >10 cm at the end of procedure. By plotting the numbers of cycles (push and pull manoeuvres) against the accumulated explored distance (Fig. 3), it was demonstrated that five complete cycles were necessary to cover the first metre of small intestine. The second metre was explored after eight additional cycles (13 cycles in total) and the third metre after nine more cycles (22 cycles in total). The average number of cycles per procedure was 21.5 ± 2.2 (10–32), but 25 or more cycles were performed in four dogs. The exploration dynamics expressed vs. time are shown in Fig. 4. The explored distance was highest at the beginning of the procedure and decreased progressively according to a potential regression model. Approximately 20 min were necessary to reach 1 m of insertion; 30 additional min to reach 2 m (50 min in total); and 50 additional min to reach 3 m (100 min in total). All dogs underwent enteroscopic exploration for >50 min and half of the dogs underwent the procedure for >90 min. Impediments to the smooth progress of the endoscope after the second or third cycles were common and in those cases, several push and pull manoeuvres were necessary to advance the endoscope as little as 5 cm. The experience level of the endoscospist and fluoroscopic guidance were crucial in solving this problem and in order to continue the exploration. Fluoroscopy not only helped to locate the position of the endoscope within the abdominal cavity, but often revealed the formation of loops, which were usually the cause of reduced endoscopic progress (Fig. 1B and C). Intestinal loops could also be located by abdominal palpation and sometimes changes were required to the position of the dog to solve the problem. Safety of the technique In all dogs, none of the parameters monitored during the procedure (blood pressure, heart rate, respiratory rate and oxygen saturation) showed any significant alteration. Food intake was normal by the day after procedure, and no clinical signs of abdominal pain, vomiting, diarrhoea or altered sensory behaviour were observed.
There were no significant changes to the serum amylase and lipase levels from the commencement of DBE to 7 days after procedure (Table 2). Serum CRP values increased at 24 h and 7 days after exploration, although these changes did not achieve statistical significance (P > 0.05). Discussion This is the first prospective study to characterize the potential use of DBE in dogs, a new endoscopic technique that could be useful in veterinary medicine for the diagnosis and therapeutic intervention of small intestine disorders (Latorre et al., 2007). As oral DBE was successfully performed in 10/12 dogs (83%), it can be considered a viable technique for canine practice, using the same equipment as is used in human medicine (EN-450T5, Fujinon). However, some veterinary limitations must be considered and the size of the dog is the most important of these. Since a minimum intestinal diameter of 2 cm was required for the smooth passage of both endoscope and overtube in a series of 55 dog cadavers of various sizes and breeds, it was recently established that a minimum forelimb length of 18 cm is recommended (López Albors et al., 2011). In practice, this estimate has proven accurate, but it is not definitive. In the present study, one of the two dogs which were unsuccessfully explored (case 12) had a forelimb length below this value, but another dog (case 5) with a shorter antebrachium than the reference value was successfully explored (Table 1). Moreover, no correlation between the total explored distance and several body parameters including bodyweight and antebrachium length was observed. It is possible that factors unrelated to dog size but related to the endoscopic technique could explain these findings. The literature for DBE in humans refers to the formation of loops, the excessive accumulation of air bubbles behind the overtube’s balloon, inexperience by the endoscopist and possible individual anatomical restrictions such as adhesions or congenital small bowel malrotation as important factors that could limit the use of the technique (Mehdizadeh et al., 2006; Pérez-Cuadrado et al., 2007; Sunada and Yamamoto, 2008). In our study, a persistent loop in the trajectory of the endoscope impeded exploration progress in dogs 3 and 12. In those cases, the loop was verified by fluoroscopy or abdominal palpation, but despite repeating the push and pull manoeuvres and changing the dog positioning, the final result was unsatisfactory. Loops also appeared in most of the other dogs, but in those cases they were overcome and the exploration continued at a normal pace. In the opinion of the endoscopists involved in our study, loops were more frequent in dogs than in humans and this was perhaps related to the anatomy of the dog’s duodenum. In humans, most of the duodenum is retroperitoneal and remains firmly attached
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Fig. 2. Exploration efficiency expressed as advanced distances per push and pull cycle. The plot is fitted to the logarithm regression model E = 4.7155 ln C + 24.402 (r2 = 0.612) where C is the number of cycles from the beginning of the procedure and E is cm advanced per push and pull cycle. Numbers above the dots represent the remaining dogs.
Fig. 3. Exploration dynamics representing the accumulated explored distance related to the cycles. The plot is fitted to the potential regression model D = 32.644C0.7122 (r2 = 0.99) where D is the explored distance and C is the number of cycles from the beginning of procedure.
Fig. 4. Exploration dynamics representing the accumulated explored distance related to the duration of the exploration. The plot is fitted to potential regression model D = 16.715T0.626 (r2 = 0.97) where D is the explored distance and T is the time since the beginning of procedure.
Table 2 Average serum level and SEM of total amylase, lipase and C-reactive protein (CRP) before exploration (basal), end exploration (end), 24 h and 7 days after DBE. Different superscripts in the values of the same row indicate significant differences (P < 0.05).
Amylase (UI/L) Lipase (UI/L) CRP (mg/L)
Basal
End
24 h
7 days
704 ± 108 a 225 ± 30 a 8.94 ± 3.44 a
623 ± 80 a 209 ± 30 b 9.48 ± 3.03
791 ± 147 a 257 ± 35 a 23.48 ± 4.92 a
802 ± 91 a 268 ± 49 a,b 26.08 ± 9.81 ª
a
through the ligament of Treitz (Stranding and Gray, 2008) so movement is minimal during the passage of the endoscope. These anatomical features facilitate firm anchoring of the overtube’s
balloon, which helps to push the endoscope forward. In the dog, however, the large, flexible mesoduodenum facilitates duodenal movement and probably results in looser anchoring of the overtube’s balloon, thereby predisposing to the formation of loops. No clinical signs associated with DBE were observed after the procedure. All of the dogs followed the conventional post-endoscopy protocol of food ingestion without any particular alteration. Similarly, regarding the potential risk of post-procedure pancreatitis, there was no clinical suspicion or any adverse serological evidence. In the five dogs evaluated for possible pancreatitis using serum amylase and lipase measurements, no significant changes were found during or after the procedure. CRP is not specifically an indicator of pancreatitis, but rather a non-specific marker of
R. Sarria et al. / The Veterinary Journal 195 (2013) 331–336
acute inflammation, and a recent study suggested that CRP is a useful indicator of gastrointestinal mucosal injury in dogs (Bayramli and Ulutas, 2008). The CRP increase on days 1 and 7 after DBE was most probably caused by iatrogenic effects of the technique, as it involves some compression of the mucosa, folding the intestine behind the balloons and strengthening the mesentery. In humans, the diagnosis of pancreatitis requires the fulfilment of two of three conditions, namely (1) upper abdominal pain; (2) amylase and/or lipase levels P3 times the upper limit of normal, and (3) compatible radiological findings on CT or MRI (Bollen et al., 2008). The absence of increased serum amylase and lipase in the dogs reported here, together with the lack of any clinical suspicion of pancreatitis, indicate that this complication in dogs is improbable. In addition, the anatomy of the canine pancreas (which is intraperitoneal and movable, in contrast with the human pancreas, which is retroperitoneal and almost immovable) could perhaps protect the dog from post-DBE pancreatitis. Nevertheless, considering the number of cases in this study (n = 12) and the low incidence of post-DBE pancreatitis in humans, a larger sample size is required to evaluate potential post-DBE pancreatitis in the dog. The insertion depth of the endoscope was estimated according to the methodology of May et al. (2005). Although other estimation methods exist, this is the only method that was accepted by 50% of the endoscopists at the First International Congress of Double Balloon Endoscopy (Sugano and Marcon, 2007). The use of this method allowed us to obtain accurate experimental plots representing the efficiency and dynamics of oral DBE in the dog that could be used for reference in the future. Knowledge of the insertion depth (either in terms of the number of cycles or duration of the procedure) is useful in estimating the approximate location of the tip of the endoscope in relation to the location of a focal lesion or the site where biopsies are taken. On average, in our study, the total insertion depth was nearly 3 m, which was approximately 60% of the total small intestinal length of 1.8–4.8 m (Nickel et al., 1979). The average time taken to cover that distance was 84 min. Thus, it can be concluded that a typical oral DBE in the dog takes approximately 1.5 h to explore the duodenum and almost half of the jejunum. These figures are quite similar to those published in humans for oral DBE (Araki et al., 2006; Pérez-Cuadrado et al., 2006; Lin et al., 2008; Hegde et al., 2010). DBE could be helpful in diagnosing localized lesions in the jejunum, and bowel pathologies that are diffuse or that change depending on the affected section of the small intestine, such as irritable bowel disease (Tams, 2003; Casamian-Sorrosal et al., 2010; Ayala et al., 2011) or lymphangiectasia (Tams, 2003). The first case of lymphocytic–plasmacytic jejunitis diagnosed by DBE in a dog was recently reported (Ayala et al., 2011). Sampling biopsies in several segments of the jejunum reduces the likelihood of an inaccurate diagnosis due to insufficient sampling (by traditional endoscopy duodenum or ileum only) and has the advantage of being less invasive and producing less scarring compared to laparotomy-assisted biopsies of the intestinal wall. Also, the working channel of the Fujinon EN-450T5 endoscope (2.8 mm) is wider than the channel of most conventional gastroduodenoscopes (2.2–2.4 mm) and this facilitates the collection of biopsies of higher quality. Further benefits are expected as both the oral and anal approaches can be combined to totally explore the small intestine, which has proved very useful in human medicine (Kita et al., 2005; Mönkemüller et al., 2008; Xin et al., 2011). In the dog, histological abnormalities are sometimes more readily detected in the ileal mucosa than in the duodenal mucosa (Casamian-Sorrosal et al., 2010), so anal DBE could be used to evaluate pathologies which are suspected to affect the colon, ileum and distal jejunum in the same procedure. However, there has only been one report of canine DBE in the veterinary literature (Latorre et al., 2007). The retrograde approach to canine DBE is an interesting direction for further investigation.
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Conclusions This study shows that oral DBE in the dog is viable and safe. Plots reported in this manuscript which illustrate the exploration dynamics and efficiency of the procedure could be useful reference values for future diagnosis and treatment of diseases in deep portions of the canine small intestine. Future studies which describe DBE by the anal route in the dog would allow portions of the distal jejunum to be explored, enabling a complete exploration of the small intestine by combining both oral and anal routes, as is practiced in human medicine.
Conflict of interest statement None of the authors have any financial or personal relationships that could inappropriately influence or bias the content of the paper. Acknowledgements This work was supported by the following Projects PI070712 (Instituto de Salud Carlos III, Ministerio de Sanidad y Consumo, Spain) and 12024/PI/09 (Fundación Séneca, Comunidad Autónoma de la Región de Murcia, Spain). The authors are grateful to J. Ceron and F. Tecles for their assistance in the biochemical analysis and to J.L. Calvo, C. Lagares and N. García for technical support during the experimental work. References Araki, A., Tsuchiya, K., Oshima, S., Okada, E., Kanai, T., Watanabe, M., 2006. Doubleballoon enteroscopy: First one year experience and modified technique (double-over tube method). Gastrointestinal Endoscopy 63, AB186. Ayala, I., Latorre, R., Soria, F., Carballo, F., Lopez-Albors, O., Buendia, A.J., PerezCuadrado, E., 2011. A case of lymphocytic–plasmacytic jejunitis diagnosed by double-balloon enteroscopy in a dog. Journal of the American Animal Hospital Association 47, 262–267. Bayramli, G., Ulutas, B., 2008. Acute phase protein response in dogs with experimentally induced gastric mucosal injury. Veterinary Clinical Pathology 37, 312–316. Bollen, T.L., Van Santvoort, H.C., Besselink, M.G., Van Leeuwen, M.S., Horvath, K.D., Freeny, P.C., Gooszen, H.G., 2008. The Atlanta classification of acute pancreatitis revisited. British Journal of Surgery 95, 6–21. Casamian-Sorrosal, D., Willard, M.D., Murray, J.K., Hall, E.J., Taylor, S.S., Day, M.J., 2010. Comparison of histopathologic findings in biopsies from the duodenum and ileum of dogs with enteropathy. Journal of Veterinary Internal Medicine 24, 80–83. Decker, G.A., Pasha, S.F., Leighton, J.A., 2008. Utility of double balloon enteroscopy for the diagnosis and management of Crohn’s disease. Techniques in Gastrointestinal Endoscopy 10, 83–86. Gerson, L.B., Tokar, J., Chiorean, M., Lo, S., Decker, G.A., Cave, D., BouHaidar, D., Mishkin, D., Dye, C., Haluszka, O., Leighton, J.A., Zfass, A., Semrad, C., 2009. Complications associated with double balloon enteroscopy at nine US centers. Clinical Gastroenterology and Hepatology 7, e1173. Hegde, S.R., Iffrig, K., Li, T., Downey, S., Heller, S.J., Tokar, J.L., Haluszka, O., 2010. Double-balloon enteroscopy in the elderly: Safety, findings, and diagnostic and therapeutic success. Gastrointestinal Endoscopy 71, 983–989. Kita, H., Yamamoto, H., Nakamura, T., Shirakawa, K., Terano, A., Sugano, K., 2005. Bleeding polyp in the mid small intestine identified by capsule endoscopy and treated by double-balloon endoscopy. Gastrointestinal Endoscopy 61, 628–629. Latorre, R., Ayala, I., Soria, F., Carballo, F., Ayala, M.D., Perez-Cuadrado, E., 2007. Double-balloon enteroscopy in two dogs. Veterinary Record 161, 587–590. Lin, T.K., Balint, J.P., Erdman, S.H., 2008. Double-balloon enteroscopy: A pediatric experience. DDW Abstract Issue 2008, Digestive Disease Week 2008, vol. 67, pp. AB252–AB252. López Albors, O., Rojo, D., Sarriá, R., Soria, F., Pérez Cuadrado, E., Latorre, R., 2011. Morphometry of the canine intestine with reference to the use of double balloon endoscopy. The Veterinary Journal 190, 113–118. May, A., Nachbar, L., Schneider, M., Neumann, M., Ell, C., 2005. Push-and-pull enteroscopy using the double-balloon technique: Method of assessing depth of insertion and training of the enteroscopy technique using the Erlange endotrainer. Endoscopy 37, 66–70. Mehdizadeh, S., Ross, A., Gerson, L., Leighton, J., Chen, A., Schembre, D., Chen, G., Semrad, C., Kamal, A., Harrison, E.M., Binmoeller, K., Waxman, I., Kozarek, R., Lo, S.K., 2006. What is the learning curve associated with double-balloon
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Characterization of oral double balloon endoscopy in the dog R. Sarria a, O. López Albors a, F. Soria b, I. Ayala c, E. Pérez Cuadrado d, P. Esteban d, R. Latorre a,⇑ a
Department of Anatomy and Comparative Pathology, Veterinary Faculty, University of Murcia, Spain Minimally Invasive Surgery Centre Jesús Usón, Campus Universitario, Cáceres, Spain c Department of Veterinary Surgery and Medicine, Veterinary School, University of Murcia, Spain d Digestive Service, Hospital Morales Meseguer, Murcia, Spain b
a r t i c l e
i n f o
Article history: Accepted 18 June 2012
Keywords: Double balloon endoscopy Dog Intestine Pancreatitis Gastrointestinal diseases
a b s t r a c t Exploration of the canine small intestine using conventional endoscopy is restricted to the duodenum and/or the ileum. Double balloon endoscopy (DBE) is a ‘push and pull’ technique that has been described in humans and permits a complete exploration of the small intestine. In this study, oral DBE was performed on 12 healthy dogs (10–34 kg) to characterize for the first time the efficiency, exploration dynamics and safety of the technique. DBE was successful in 83% of dogs; the average estimated insertion depth of the endoscope was 287 ± 36 cm, and the average duration of the exploration was 84 ± 8 min. No complications or relevant adverse clinical effects were observed, and there was no indication of post-procedure pancreatitis based on serology of two specific markers of pancreatitis (amylase and lipase) and the immediate nonspecific inflammatory mediator C-reactive protein. The study showed that oral DBE is viable and safe in the dog, allowing for the diagnosis and treatment of gastrointestinal diseases deep in the small intestine to an extent that has not previously been possible using conventional endoscopy. Ó 2012 Elsevier Ltd. All rights reserved.
Introduction Most diseases of the gastrointestinal tract in the dog and cat are diffuse and extend along the length of the small intestine (Tams, 2003). However, the severity of the inflammation may vary depending on the anatomical location (Moore, 2003) and since deep areas of the bowel cannot be explored by routine endoscopy, some pathologies, such as lymphomas located in the jejunum or ileum, might not be diagnosed (Tams, 2003). Recently, CasamianSorrosal et al. (2010) demonstrated that definitive histopathological diagnosis of some bowel diseases varied depending on the sampling site and would have been different in most cases if duodenal biopsies only had been obtained. With traditional endoscopy it is not possible to progress further than a few centimetres into the jejunum using the oral approach, or a similar distance into the ileum via the anal approach (Tams, 2003). Thus, the use of current endoscopic techniques to explore, biopsy and treat digestive disorders warrants further investigation. The technique of double balloon endoscopy (DBE) was first reported in 2001 (Yamamoto et al., 2001). Based on ‘push endoscopy’, DBE is a form of deep endoscopy which not only allows exploration, but also treatment of the most common digestive disorders of the small intestine in humans, such as obscure gastroin-
⇑ Corresponding author. Tel.: +34 868 884697. E-mail address: [email protected] (R. Latorre). 1090-0233/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tvjl.2012.06.023
testinal bleeding (Pérez-Cuadrado et al., 2006; Penazzio, 2008), tumours (Mitsui et al., 2009), Crohn’s disease (Decker et al., 2008) and polyps (Ohmiya et al., 2010; Sakamoto et al., 2011). The equipment consists of a 200 cm endoscope (external diameter 9.4 mm) and a 145 cm overtube (diameter 13.2 mm), both of which have a latex balloon attached to the tip (Fig. 1A). The two balloons are inflated and deflated in an alternating sequence to allow the endoscope to progress (pushing phase) or fold the explored intestine behind the balloons (pulling phase). DBE is a non-invasive, safe technique with a similar complication rate in humans to conventional endoscopy. Perforation (0.3%), post-procedure pancreatitis (0.5%) and bleeding (0.8%) are the most common complications (Mensink, 2008; Gerson et al., 2009; Xin et al., 2011). Since pancreatitis is one of the most serious complications, it should be considered as a potential risk in any experimental or elective procedure. The first attempt at DBE in veterinary medicine was successfully performed by Latorre et al. (2007) in two dogs. However, in order to improve the reliability of this technique in veterinary practice, further information concerning insertion depth, duration and safety is needed. According to a recent anatomical study, DBE is feasible in medium to large size dogs using the same type of endoscope used in humans (López Albors et al., 2011). The diameter of the intestinal lumen is closely correlated with body parameters such as antebrachial length, and a minimum diameter of 2 cm is required to allow the passage of the overtube and the associated balloon, making dogs with antebrachii of >18 cm probably suitable for DBE.
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Fig. 1. (A) Double balloon endoscope (EN-450T5, Fujinon). (B and C) Fluoroscopic examination during oral DBE in dog 12. (B) Intestine-endoscope loop in the jejunum. (C) Position of the endoscope after the loop has been resolved.
The aim of this study was to characterize the exploration dynamics of DBE in the dog in terms of maximum insertion depth, number of push and pull cycles and procedure duration. A secondary goal was to evaluate the safety of the technique by monitoring animal health during and after the procedure. Serological values for the immediate nonspecific inflammatory mediator C-reactive protein (CRP) and two specific markers of pancreatitis (amylase and lipase) were studied in five dogs. Materials and methods Twelve dogs (six Beagles, four American Foxhounds and two English Setters) underwent oral enteroscopy. The dogs came from the animal facility of Murcia University, where Animal Care and Use Guidelines according to the European Convention for the Protection of Vertebrate Animals are followed for Experimental and other Scientific Purposes (Council Directive 86/609/EEC). The dogs’ weight range was 10–34 kg and the proportion of males to females was 10:2. None of the dogs had a history of digestive disease. In eight animals, the forelimb length, an estimator of the small intestine diameter (López Albors et al., 2011), was measured. Dogs were fasted for 36 h before the enteroscopy and premedicated with a combination of 0.05 mg/kg acepromazine and 0.3 mg/kg butorphanol, administered IM. Anaesthesia was induced with a dose of 5 mg/kg propofol, administered IV to effect, and after orotracheal intubation the animals were maintained with isofluorane (1–1.2 minimum alveolar concentration) and 100% oxygen, using an anaesthetic breathing system adapted to their size. During the enteroscopy, blood pressure, heart rate, respiratory rate and oxygen saturation were monitored. Enteroscopies were carried out by two of the authors (EP-C, FS) who have routinely performed DBE for more than 5 years, using an EN-450T5 (Fujinon) enteroscope (Fig. 1A). During enteroscopy exploration, the distance advanced for each
cycle and the time taken for the procedure were recorded in a worksheet (May et al., 2005). To reduce subjectivity, the distance advanced was decided by consensus between the endoscopist and a second author. The exploration depth was measured from just after the pylorus and the end of exploration was established after the repetition of 5–6 unsuccessful push and pull manoeuvres (no advance of the endoscope). In some animals (n = 3), the progress of the endoscope was surveyed by fluoroscopy (PHILIPS BV-300). This allowed us to visualize the position of the tip of the endoscope and overtube within the abdominal cavity. In five dogs, blood samples were obtained at the beginning and end of DBE, and at 24 h and 7 days after the procedure. Serum concentrations of CRP, amylase and lipase were used as indicators of potential inflammation and/or pancreatic damage. After recovery from anaesthesia, the dogs were examined twice a day for 7 days to rule out possible complications, such as an altered behaviour or activity, vomiting, diarrhoea, decreased food ingestion or abdominal discomfort. All data were included in a worksheet and statistical analysis was performed using SPSS 17.0. Descriptive statistics including the Shapiro–Wilks W test for normality and Levene’s test for homogeneity of variance were initially obtained for all experimental variables. Enzyme values were evaluated by analysis of variance (ANOVA, linear model with repeated measures), considering the timing of blood sampling as a within-subject factor. CRP values were subjected to a logarithmic transformation to comply with the assumptions of the analysis. Data for the number of cycles and time were plotted against the explored distance using regression analysis. All statistics were performed using a significance level of P < 0.05.
Results Insertion depth and exploration dynamics Bodyweight, forelimb length, explored distance, time and the number of cycles are shown in Table 1. Dogs 3 and 12 were not
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R. Sarria et al. / The Veterinary Journal 195 (2013) 331–336 Table 1 Summary of data for oral double balloon endoscopy in dogs. Dog 1 2 3 4 5 6 7 8 9 10 11 12 a b
Bodyweight (kg)
Forelimb lengtha (cm)
Estimated insertion depth (cm)
Time (min)
Number of cycles
16 18.5 21.5 19 18 19.5 19.5 13
495 270 90 220 320 232 210 415 385 185 144 120
102 109 37 98 125 70 55 96 77 55 54 19
25 20 3 16 25 19 10 32 32 20 16 6
b
23 17.5 13 13 10 13 18 32 26 33 34 16.9
b
b
From the lateral epicondyle of the humerus to the accessory carpal bone (palpable landmarks). Indicates that fluoroscopy was also used.
included in the statistical analysis, because soon after beginning exploration there was no progress of the endoscope and the procedure was terminated. In the remaining 10 dogs, the average insertion depth was 287 ± 36 cm (range 144–495 cm) and the average duration of the procedure was 84 ± 8 min (range 54–125 min). Exploration efficiency expressed as advanced distance per push and pull cycle was represented by a negative logarithm regression model (Fig. 2). After a phase of maximum efficiency at the beginning of the exploration, a progressive decrease in efficiency was observed. The first push manoeuvre was the most effective cycle with an average value of 35 cm. Thereafter, the efficiency decreased progressively to >10 cm at the end of procedure. By plotting the numbers of cycles (push and pull manoeuvres) against the accumulated explored distance (Fig. 3), it was demonstrated that five complete cycles were necessary to cover the first metre of small intestine. The second metre was explored after eight additional cycles (13 cycles in total) and the third metre after nine more cycles (22 cycles in total). The average number of cycles per procedure was 21.5 ± 2.2 (10–32), but 25 or more cycles were performed in four dogs. The exploration dynamics expressed vs. time are shown in Fig. 4. The explored distance was highest at the beginning of the procedure and decreased progressively according to a potential regression model. Approximately 20 min were necessary to reach 1 m of insertion; 30 additional min to reach 2 m (50 min in total); and 50 additional min to reach 3 m (100 min in total). All dogs underwent enteroscopic exploration for >50 min and half of the dogs underwent the procedure for >90 min. Impediments to the smooth progress of the endoscope after the second or third cycles were common and in those cases, several push and pull manoeuvres were necessary to advance the endoscope as little as 5 cm. The experience level of the endoscospist and fluoroscopic guidance were crucial in solving this problem and in order to continue the exploration. Fluoroscopy not only helped to locate the position of the endoscope within the abdominal cavity, but often revealed the formation of loops, which were usually the cause of reduced endoscopic progress (Fig. 1B and C). Intestinal loops could also be located by abdominal palpation and sometimes changes were required to the position of the dog to solve the problem. Safety of the technique In all dogs, none of the parameters monitored during the procedure (blood pressure, heart rate, respiratory rate and oxygen saturation) showed any significant alteration. Food intake was normal by the day after procedure, and no clinical signs of abdominal pain, vomiting, diarrhoea or altered sensory behaviour were observed.
There were no significant changes to the serum amylase and lipase levels from the commencement of DBE to 7 days after procedure (Table 2). Serum CRP values increased at 24 h and 7 days after exploration, although these changes did not achieve statistical significance (P > 0.05). Discussion This is the first prospective study to characterize the potential use of DBE in dogs, a new endoscopic technique that could be useful in veterinary medicine for the diagnosis and therapeutic intervention of small intestine disorders (Latorre et al., 2007). As oral DBE was successfully performed in 10/12 dogs (83%), it can be considered a viable technique for canine practice, using the same equipment as is used in human medicine (EN-450T5, Fujinon). However, some veterinary limitations must be considered and the size of the dog is the most important of these. Since a minimum intestinal diameter of 2 cm was required for the smooth passage of both endoscope and overtube in a series of 55 dog cadavers of various sizes and breeds, it was recently established that a minimum forelimb length of 18 cm is recommended (López Albors et al., 2011). In practice, this estimate has proven accurate, but it is not definitive. In the present study, one of the two dogs which were unsuccessfully explored (case 12) had a forelimb length below this value, but another dog (case 5) with a shorter antebrachium than the reference value was successfully explored (Table 1). Moreover, no correlation between the total explored distance and several body parameters including bodyweight and antebrachium length was observed. It is possible that factors unrelated to dog size but related to the endoscopic technique could explain these findings. The literature for DBE in humans refers to the formation of loops, the excessive accumulation of air bubbles behind the overtube’s balloon, inexperience by the endoscopist and possible individual anatomical restrictions such as adhesions or congenital small bowel malrotation as important factors that could limit the use of the technique (Mehdizadeh et al., 2006; Pérez-Cuadrado et al., 2007; Sunada and Yamamoto, 2008). In our study, a persistent loop in the trajectory of the endoscope impeded exploration progress in dogs 3 and 12. In those cases, the loop was verified by fluoroscopy or abdominal palpation, but despite repeating the push and pull manoeuvres and changing the dog positioning, the final result was unsatisfactory. Loops also appeared in most of the other dogs, but in those cases they were overcome and the exploration continued at a normal pace. In the opinion of the endoscopists involved in our study, loops were more frequent in dogs than in humans and this was perhaps related to the anatomy of the dog’s duodenum. In humans, most of the duodenum is retroperitoneal and remains firmly attached
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Fig. 2. Exploration efficiency expressed as advanced distances per push and pull cycle. The plot is fitted to the logarithm regression model E = 4.7155 ln C + 24.402 (r2 = 0.612) where C is the number of cycles from the beginning of the procedure and E is cm advanced per push and pull cycle. Numbers above the dots represent the remaining dogs.
Fig. 3. Exploration dynamics representing the accumulated explored distance related to the cycles. The plot is fitted to the potential regression model D = 32.644C0.7122 (r2 = 0.99) where D is the explored distance and C is the number of cycles from the beginning of procedure.
Fig. 4. Exploration dynamics representing the accumulated explored distance related to the duration of the exploration. The plot is fitted to potential regression model D = 16.715T0.626 (r2 = 0.97) where D is the explored distance and T is the time since the beginning of procedure.
Table 2 Average serum level and SEM of total amylase, lipase and C-reactive protein (CRP) before exploration (basal), end exploration (end), 24 h and 7 days after DBE. Different superscripts in the values of the same row indicate significant differences (P < 0.05).
Amylase (UI/L) Lipase (UI/L) CRP (mg/L)
Basal
End
24 h
7 days
704 ± 108 a 225 ± 30 a 8.94 ± 3.44 a
623 ± 80 a 209 ± 30 b 9.48 ± 3.03
791 ± 147 a 257 ± 35 a 23.48 ± 4.92 a
802 ± 91 a 268 ± 49 a,b 26.08 ± 9.81 ª
a
through the ligament of Treitz (Stranding and Gray, 2008) so movement is minimal during the passage of the endoscope. These anatomical features facilitate firm anchoring of the overtube’s
balloon, which helps to push the endoscope forward. In the dog, however, the large, flexible mesoduodenum facilitates duodenal movement and probably results in looser anchoring of the overtube’s balloon, thereby predisposing to the formation of loops. No clinical signs associated with DBE were observed after the procedure. All of the dogs followed the conventional post-endoscopy protocol of food ingestion without any particular alteration. Similarly, regarding the potential risk of post-procedure pancreatitis, there was no clinical suspicion or any adverse serological evidence. In the five dogs evaluated for possible pancreatitis using serum amylase and lipase measurements, no significant changes were found during or after the procedure. CRP is not specifically an indicator of pancreatitis, but rather a non-specific marker of
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acute inflammation, and a recent study suggested that CRP is a useful indicator of gastrointestinal mucosal injury in dogs (Bayramli and Ulutas, 2008). The CRP increase on days 1 and 7 after DBE was most probably caused by iatrogenic effects of the technique, as it involves some compression of the mucosa, folding the intestine behind the balloons and strengthening the mesentery. In humans, the diagnosis of pancreatitis requires the fulfilment of two of three conditions, namely (1) upper abdominal pain; (2) amylase and/or lipase levels P3 times the upper limit of normal, and (3) compatible radiological findings on CT or MRI (Bollen et al., 2008). The absence of increased serum amylase and lipase in the dogs reported here, together with the lack of any clinical suspicion of pancreatitis, indicate that this complication in dogs is improbable. In addition, the anatomy of the canine pancreas (which is intraperitoneal and movable, in contrast with the human pancreas, which is retroperitoneal and almost immovable) could perhaps protect the dog from post-DBE pancreatitis. Nevertheless, considering the number of cases in this study (n = 12) and the low incidence of post-DBE pancreatitis in humans, a larger sample size is required to evaluate potential post-DBE pancreatitis in the dog. The insertion depth of the endoscope was estimated according to the methodology of May et al. (2005). Although other estimation methods exist, this is the only method that was accepted by 50% of the endoscopists at the First International Congress of Double Balloon Endoscopy (Sugano and Marcon, 2007). The use of this method allowed us to obtain accurate experimental plots representing the efficiency and dynamics of oral DBE in the dog that could be used for reference in the future. Knowledge of the insertion depth (either in terms of the number of cycles or duration of the procedure) is useful in estimating the approximate location of the tip of the endoscope in relation to the location of a focal lesion or the site where biopsies are taken. On average, in our study, the total insertion depth was nearly 3 m, which was approximately 60% of the total small intestinal length of 1.8–4.8 m (Nickel et al., 1979). The average time taken to cover that distance was 84 min. Thus, it can be concluded that a typical oral DBE in the dog takes approximately 1.5 h to explore the duodenum and almost half of the jejunum. These figures are quite similar to those published in humans for oral DBE (Araki et al., 2006; Pérez-Cuadrado et al., 2006; Lin et al., 2008; Hegde et al., 2010). DBE could be helpful in diagnosing localized lesions in the jejunum, and bowel pathologies that are diffuse or that change depending on the affected section of the small intestine, such as irritable bowel disease (Tams, 2003; Casamian-Sorrosal et al., 2010; Ayala et al., 2011) or lymphangiectasia (Tams, 2003). The first case of lymphocytic–plasmacytic jejunitis diagnosed by DBE in a dog was recently reported (Ayala et al., 2011). Sampling biopsies in several segments of the jejunum reduces the likelihood of an inaccurate diagnosis due to insufficient sampling (by traditional endoscopy duodenum or ileum only) and has the advantage of being less invasive and producing less scarring compared to laparotomy-assisted biopsies of the intestinal wall. Also, the working channel of the Fujinon EN-450T5 endoscope (2.8 mm) is wider than the channel of most conventional gastroduodenoscopes (2.2–2.4 mm) and this facilitates the collection of biopsies of higher quality. Further benefits are expected as both the oral and anal approaches can be combined to totally explore the small intestine, which has proved very useful in human medicine (Kita et al., 2005; Mönkemüller et al., 2008; Xin et al., 2011). In the dog, histological abnormalities are sometimes more readily detected in the ileal mucosa than in the duodenal mucosa (Casamian-Sorrosal et al., 2010), so anal DBE could be used to evaluate pathologies which are suspected to affect the colon, ileum and distal jejunum in the same procedure. However, there has only been one report of canine DBE in the veterinary literature (Latorre et al., 2007). The retrograde approach to canine DBE is an interesting direction for further investigation.
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Conclusions This study shows that oral DBE in the dog is viable and safe. Plots reported in this manuscript which illustrate the exploration dynamics and efficiency of the procedure could be useful reference values for future diagnosis and treatment of diseases in deep portions of the canine small intestine. Future studies which describe DBE by the anal route in the dog would allow portions of the distal jejunum to be explored, enabling a complete exploration of the small intestine by combining both oral and anal routes, as is practiced in human medicine.
Conflict of interest statement None of the authors have any financial or personal relationships that could inappropriately influence or bias the content of the paper. Acknowledgements This work was supported by the following Projects PI070712 (Instituto de Salud Carlos III, Ministerio de Sanidad y Consumo, Spain) and 12024/PI/09 (Fundación Séneca, Comunidad Autónoma de la Región de Murcia, Spain). The authors are grateful to J. Ceron and F. Tecles for their assistance in the biochemical analysis and to J.L. Calvo, C. Lagares and N. García for technical support during the experimental work. References Araki, A., Tsuchiya, K., Oshima, S., Okada, E., Kanai, T., Watanabe, M., 2006. Doubleballoon enteroscopy: First one year experience and modified technique (double-over tube method). Gastrointestinal Endoscopy 63, AB186. Ayala, I., Latorre, R., Soria, F., Carballo, F., Lopez-Albors, O., Buendia, A.J., PerezCuadrado, E., 2011. A case of lymphocytic–plasmacytic jejunitis diagnosed by double-balloon enteroscopy in a dog. Journal of the American Animal Hospital Association 47, 262–267. Bayramli, G., Ulutas, B., 2008. Acute phase protein response in dogs with experimentally induced gastric mucosal injury. Veterinary Clinical Pathology 37, 312–316. Bollen, T.L., Van Santvoort, H.C., Besselink, M.G., Van Leeuwen, M.S., Horvath, K.D., Freeny, P.C., Gooszen, H.G., 2008. The Atlanta classification of acute pancreatitis revisited. British Journal of Surgery 95, 6–21. Casamian-Sorrosal, D., Willard, M.D., Murray, J.K., Hall, E.J., Taylor, S.S., Day, M.J., 2010. Comparison of histopathologic findings in biopsies from the duodenum and ileum of dogs with enteropathy. Journal of Veterinary Internal Medicine 24, 80–83. Decker, G.A., Pasha, S.F., Leighton, J.A., 2008. Utility of double balloon enteroscopy for the diagnosis and management of Crohn’s disease. Techniques in Gastrointestinal Endoscopy 10, 83–86. Gerson, L.B., Tokar, J., Chiorean, M., Lo, S., Decker, G.A., Cave, D., BouHaidar, D., Mishkin, D., Dye, C., Haluszka, O., Leighton, J.A., Zfass, A., Semrad, C., 2009. Complications associated with double balloon enteroscopy at nine US centers. Clinical Gastroenterology and Hepatology 7, e1173. Hegde, S.R., Iffrig, K., Li, T., Downey, S., Heller, S.J., Tokar, J.L., Haluszka, O., 2010. Double-balloon enteroscopy in the elderly: Safety, findings, and diagnostic and therapeutic success. Gastrointestinal Endoscopy 71, 983–989. Kita, H., Yamamoto, H., Nakamura, T., Shirakawa, K., Terano, A., Sugano, K., 2005. Bleeding polyp in the mid small intestine identified by capsule endoscopy and treated by double-balloon endoscopy. Gastrointestinal Endoscopy 61, 628–629. Latorre, R., Ayala, I., Soria, F., Carballo, F., Ayala, M.D., Perez-Cuadrado, E., 2007. Double-balloon enteroscopy in two dogs. Veterinary Record 161, 587–590. Lin, T.K., Balint, J.P., Erdman, S.H., 2008. Double-balloon enteroscopy: A pediatric experience. DDW Abstract Issue 2008, Digestive Disease Week 2008, vol. 67, pp. AB252–AB252. López Albors, O., Rojo, D., Sarriá, R., Soria, F., Pérez Cuadrado, E., Latorre, R., 2011. Morphometry of the canine intestine with reference to the use of double balloon endoscopy. The Veterinary Journal 190, 113–118. May, A., Nachbar, L., Schneider, M., Neumann, M., Ell, C., 2005. Push-and-pull enteroscopy using the double-balloon technique: Method of assessing depth of insertion and training of the enteroscopy technique using the Erlange endotrainer. Endoscopy 37, 66–70. Mehdizadeh, S., Ross, A., Gerson, L., Leighton, J., Chen, A., Schembre, D., Chen, G., Semrad, C., Kamal, A., Harrison, E.M., Binmoeller, K., Waxman, I., Kozarek, R., Lo, S.K., 2006. What is the learning curve associated with double-balloon
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