Equine Gastric Ulcer Syndrome in adult donkeys: Investigation on prevalence, anatomical distribution, and severity.
Sgorbini M1, Bonelli F1, Papini R3, Busechian S2, Briganti A1, Laus F4, Faillace V4, Zappulla F2,
Rizk A5, Rueca F2
1Veterinary Teaching Hospital “Mario Modenato”, Department of Veterinary Sciences, via
Livornese snc, 56122 San Piero a Grado (PI), Italy
2Department of Clinical Sciences, University of Perugia, Perugia, Italy. 3 Department of Veterinary Sciences, viale delle Piagge 2, 56124 Pisa, Italy
4School of Biosciences and Veterinary Medicine, University of Camerino, Via Circonvallazione
93/95, 62024, Matelica (MC).
5Department of Surgery, Anesthesiology and Radiology, Faculty of Veterinary Medicine, Mansoura
University, 35516 Mansoura, Egypt.
Corresponding author Dr Micaela Sgorbini
Veterinary Teaching Hospital “Mario Modenato” Via Livornese snc, 56122 San Piero a Grado (PI), Italy 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20
Abstract
The study was performed on 39 live donkeys that underwent gastroscopic examination. The lesions were recorded in accordance with the ECEIM Consensus Statement guidelines. The presence of Gasterophilus sp. larvae was also recorded. Larvae were collected and identified to species level. Fisher’s exact test was used to compare different prevalence values for sex, age, and anatomical distribution of lesions.
Gastric lesions were present in 20/39 (51.3% 35.6-67%) donkeys; 19/39 (48.7% 95% CI=33-64.4%) were affected only by ESGD, while 1/39 (2.6% 0-7.5%) showed both ESGD and EGGD, thus 95% of positive donkeys showed lesions located in the non-glandular mucosa. The ESGD grade was 0/4 (48.7% 33-64.4%) in 19/39, 1/4 (12.8% 2.3-23.3%) in 5/39, 2/4 (25.6% 11.9-39.5%) in 10/39, 3/4 in 4/39 (10.3% 0.7-19.8%) and 4/4 in 1/39 (2.6% 0-7.5%) donkeys, respectively. The EGGD lesion was a mild depression in the ventral glandular fundus. ESGD was primary in all the donkeys included and lesions were located around the cardia and along the lesser curvature. Gasterophilus sp larvae were present in all animals and were identified as third-stage larvae of Gasterophilus intestinalis. No animals showed clinical signs of EGUS. No significant differences relating to sex, age, or breed were found in the prevalence of EGUS in this study, while the proportion of donkeys affected by ESGD was statistically higher than those affected by EGGD. To the best of our knowledge, this is the first report on the gastroscopic evaluation of EGUS in live donkeys. Our results show a higher prevalence of EGUS in live donkeys than values previously reported by other authors in dead/euthanized donkeys. The detection of third-stage G. intestinalis larvae was not unexpected since L3 can be retrieved throughout the year, and G. instestinalis has been reported as the most common Gasterophilus species in Italy.
Key words:
Donkey, EGUS, ESGD, EGGD, gastroscopic evaluation. 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 66 67 68 69 70 71 72
Introduction
Worldwide interest in the welfare of donkeys (Equus asinus) has been increasing mostly because of the recent new use of these animals for milk production for use in children with intolerance to cow’s milk (Carroccio et al. 2000; Muraro et al. 2002; Monti et al. 2012) or in animal-assisted ther-apy and activities (Borioni et al. 2012). The renewed interest in these animals is demonstrated by the number of different types of studies carried out in various countries including Italy over the last 10 years (Nardoni et al. 2007; Laus et al. 2010; Sgorbini et al. 2013; Veronesi et al. 2014; Crisci et al. 2014; Kim et al. 2014; Piantedosi et al. 2014; Laus et al. 2015a; Laus et al. 2015b; Carluccio et al. 2015; Bonelli et al. 2016).
Equine Gastric Ulcer Syndrome (EGUS) is the most common disease of the equine stomach with a high prevalence reported in sport horses (Bell et al. 2007; Bezdekova et al. 2005; Tamzali et al. 2011; Cate et al. 2012; Sykes et al. 2015) as well as in leisure horses, breeding mares and young horses (Le Jeune et al. 2009; Luthersson et al. 2009; Niedźwiedź et al. 2013). The term Equine Gas-tric Ulcer Syndrome was first adopted by the EGUS Council in 1999 (Andrews et al. 1999). It in-cludes a set of pathological conditions characterized by ulcers in the terminal portion of the oesoph-agus, in the proximal (squamous) and distal (glandular) parts of the stomach, and in the proximal part of the duodenum of equids (Andrews et al. 1999). Various authors (Sykes and Jokisalo, 2014; Sykes and Jokisalo, 2015 a,b) and the European College of Equine Internal Medicine (ECEIM) Consensus Statement (Sykes et al. 2015) have provided a new nomenclature of EGUS, and have proposed updated guidelines regarding pathophysiology, diagnosis, and treatment.
EGUS appears to have been rarely described in donkeys, and findings are limited to animals sub-mitted for necropsy (Burden et al. 2009; Morrow et al. 2011; Al-Mokaddem et al. 2014; Morales Briceño et al. 2015). Thus, in order to provide further insight, we investigated the prevalence and anatomical distribution of EGUS in a cohort of 39 live adult donkeys. The effect of age and sex was also investigated.
Materials and methods
The study was performed between April 2014 and March 2016 and was approved by the Ethics Committee of the University of Pisa (n. 9069/2014). Owner’s written consent was also obtained for performing a gastroscopy on the donkeys included.
A total of 39 donkeys (Amiata donkeys n=33, and cross-bred donkeys n=6) with no clinical signs of EGUS, underwent gastroscopic examination to evaluate the presence of gastric lesions. The animals were not selected randomly, and an opportunistic sampling strategy was adopted. Seventeen out of 39 donkeys were owned by the regional authority and administrative body of Tuscany (Italy). They donkeys were permanently housed at the Department of Veterinary Sciences’ (13/39) or regional authority’s stud farm’ facilities in Pisa (4/39) for reproduction activities. The remaining donkeys (22/39) were owned by two private stud farms located in Camerino and Perugia, also used for reproduction activities.
All the donkeys were eligible to participate in the study (see study inclusion criteria below), and were thus recruited. All the animals were kept in sand paddocks for at least 1 year before the gastroscopy. Jennies were grouped (5-6 animals/paddock), while jacks were housed in single small paddocks maintaining eye contact with the other animals. All the donkeys were fed meadow hay ad libitum and commercial feed for horses (humidity 12%, protein 15-16.5%, oils and lipids 1.5-2%; cellulose 6.8%; ashes 2.6%; sodium 75 mg/kg) (Equifioc®, Molitoria Val di Serchio, Lucca, Italy),
in accordance with the NRC recommendations for energy. All the donkeys included in this study had never been vaccinated and had not received anti-parasitic drug treatments for at least one year. The inclusion criteria were: 1) non athletes and non-working donkeys, 2) breeding animals, 3) no administration of NSAIDs or corticosteroids for at least 20 days immediately prior to gastroscopy. The day before gastroscopy a clinical examination and routine blood work was performed on all the donkeys enrolled. The animals were then housed in 4X4 m boxes 15 h before gastroscopy. The examination was performed under sedation after 15 h of fasting with detomidine 60 µg kg-1
(Detogesic)1 and butorphanol 50 µg kg-1 (Nargesic)2 intramuscularly injected before entering the
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examination room. Gastroscopy was performed as described by Bain et al. (2004), using a portable processor Gastropack3 and a 300 cm long scope (60130PKS)3. The long gastroscope was passed
into the stomach, which was insufflated with air through an air-flow system attached to the biopsy channel of the endoscope until the internal stomach folds appeared flattened. Feed material adherent to the non-glandular mucosa was flushed away with sterile water in order to visualize the entire non-glandular portion of the stomach, including the greater curvature, the lesser curvature, and the dorsal fundus.
The images were recorded on a digital media for subsequent revaluation and storage. The lesions were graded and described in accordance with the ECEIM Consensus Statement guidelines (Sykes et al. 2015). Equine Squamous Gastric Disease (ESGD) lesions were scored using the scale proposed by the EGUS Council (1999), while Equine Glandular Gastric Disease (EGGD) was not scored, but described as the presence or absence, anatomical location, distribution, and appearance of lesions. The occurrence of Gasterophilus larvae in the stomach and proximal duodenum was also determined during the gastroscopic examination. A few (3-5) larvae were collected via the biopsy channel of the endoscope using a biopsy pincer from each infested animal, placed in plastic vials containing saline solution (NaCl 0.9%), examined under a stereomicroscope, and identified by their morphological features to species level according to Zumpt (1965).
Statistical analysis
Total prevalence values of EGUS, ESGD, EGGD, single scores (0 to 4), groups of scores ranging from 1 to 2-4, and Gasterophilus infestations were determined. In addition, the corresponding 95% confidence intervals (CIs) were calculated with Jeffrey’s method
(http://epitools.ausvet.com.au/content.php?page=CIProportion). Prevalence values and 95% CIs of EGUS according to anatomical location (ESGD and EGGD), sex, age (≤3 years and >3 years), and breed (Amiata and crossbreed) as well as distribution of scores of ESGD according to sex, age, and breed were also calculated. Fisher’s exact test was used to compare differences between groups. Statistical analysis was performed with commercial software4. Differences were considered
significant and highly significant when P values were <0.05 and <0.01, respectively.
Results
The donkeys enrolled in this study consisted of 16 female donkeys (jennies) and 23 male donkeys (jackasses), aged 1-18 years (median age = 3 years). A 15-hour feed withdrawal time was adequate in order to visualize of the 95% of the stomach (Fors et al. 2001). The gastroscopy was performed in all the donkeys enrolled (39/39, 100%). The anatomy was similar to observations described by others (Fors et al. 2001; Jerbi et al. 2014).
Lesions attributable to EGUS were not present in 19/39 (48.7% 95% CI=33-64.4%) donkeys, while 20/39 (51.3% 35.6-67%) donkeys had lesions consistent with EGUS. Of the 20 donkeys with lesions consistent with EGUS, 19/39 (48.7% 33-64.4%) animals had ESGD, while a 1-year-old crossbreed jack out of 39 (2.6% 0-7.5%) showed ESGD concurrent with EGGD. Scores for ESGD were 0/4 in 19/39 (48.7% 33-64.4%), 1/4 in 5/39 (12.8% 2.3-23.3%), 2/4 in 10/39 (25.6% 11.9-39.5%), 3/4 in 4/39 (10.3% 0.7-19.8%) and 4/4 in 1/39 (2.6% 0-7.5%) donkeys, respectively.
On the basis of the scores proposed by Andrews and colleagues (1999) and Sykes et al. (2015), grade 1 is characterized by an intact squamous gastric mucosa with the presence of hyperemia and/or hyperparakeratosis, while grades 2-4 are characterized by the presence of squamous gastric ulcers. Thus, the total prevalence of donkeys with gastric lesions obtained in this study (51.3% [35.6-67%) included 12.8% (5.1-25.8%) of donkeys showing hyperkeratosis and/or hyperemia (score 1) and 38.4% (24.5-54.1%) showing ulcers in the non-glandular mucosa (scores 2-4).
The EGGD lesion consisted of a mild depression in the ventral glandular fundus and was associated with ESGD lesions scoring 2. ESGD was considered primary in all the positive (19/19, 100%) donkeys enrolled with alterations located around the cardia and along the lesser curvature. Tables 1 and 2 summarize the results for the prevalence of EGUS according to anatomical location of lesions (ESGD or ESGD/EGGD), sex, age (≤3 years or >3 years), and breed (Amiata or crossbreed), as 125 126 127 128 129 130 131 132 133 134 135 136 137 138 139 140 141 142 143 144 145 146 147 148 149 150 151 152 153 154 155 156 157 158 159 160 161 162 163 164 165 166 167 168 169 170 171 172 173 174 175 176
well as distribution of scores for ESGD according to sex, age, and breed, respectively. All the animals (39/39, 100%) showed the occurrence of Gasterophilus larvae attached in groups near the margo plicatus curvature, irrespective of the presence or absence of EGUS. No Gasterophilus larvae were found in the proximal duodenum. In agreement with Al-Mokaddem et al. (2014), after removal, Gasterophilus larvae left small shallow erosions at their attachment sites. All larvae collected during the study period were identified as third-stage larvae of Gasterophilus intestinalis. Statistical analysis showed no significant differences in the prevalence of EGUS with respect to sex (p=0.75) age (p=1), and breed (p=0.37), while the difference between the number of donkeys affected by ESGD and those affected by ESGD/EGGD was highly significant (P<0.0001). Similarly, the difference between the prevalence of donkeys affected by grade 1 lesions (hyperemia and/or hyperparakeratosis) and the prevalence of donkeys affected by grade 2-4 lesions (ulcers) was statistically significant (12.8% [2.3-23.3%] vs. 38.5% [23.2-53.7%], P=0.0183).
Discussion
The aim of the present study was to present the prevalence, and anatomical distribution of EGUS in a cohort of live adult donkeys. To the best of the authors’ knowledge, this is the first report that considers the gastroscopic evaluation of EGUS in live donkeys.
The gastroscopic examination was performed in all the donkeys enrolled in the present study, no damage to the oesophageal or gastric mucosa due to the passage of the endoscope was detected and the stomach was reached easily.
The prevalence of gastric lesions consistent with EGUS obtained in this study was 51.3% (35.6-67%) and 38.5% (23.2-53.7%) of the animals had ulcers (grade 2/4-4/4). In addition, the squamous portion of the stomach was predominantly affected. Morrow and colleagues (2011) reported a prevalence of 42.1% (39.6-44.7%) of gastric ulcers, alone or in combination with other disorders, in a retrospective post-mortem study; they did not describe the localisation of the lesions (ESGD or EGGD) or the lesions’ score. Burden and colleagues (2009) found a prevalence of 41% in eutha-nized/dead donkeys and did not describe the localisation of the lesions or the scoring. Al-Mokad-dem and colleagues (2014) found a lower prevalence (20%) of gastric lesions (erosions/ulcerations) in 35 euthanized mature draught donkeys. In a study conducted in Spain on 10 dead donkeys, Morales Briceño et al. (2015) reported a 90% prevalence of gastric ulcers, and performed a lesion scoring (0/4-4/4) similar to ours, as proposed by others (Andrews et al. 1999). Our results, obtained in apparently healthy donkeys examined alive, showed a similar prevalence of EGUS to the value reported by Morrow et al. (2011), considering the 95% CIs, higher than values reported by other au-thors (Burden et al. 2009; Al-Mokadden et al. 2014), and lower than the findings of Morales Briceño and colleagues (2015) obtained in dead/euthanized donkeys.
None of the donkeys enrolled in above mentioned studies were working animals, instead they had a sedentary life style, like the donkeys included in this survey. However, the donkeys enrolled in pre-vious studies (Burden et al. 2009; Morrow et al. 2011) were elderly (mean age: 30.5 and 30.6 years, respectively), while in the present study we enrolled younger animals (mean age: 5 years). In the survey carried out by Morrow and colleagues, 92.6% of the donkeys were humanely destroyed, 4.8% were found dead and 2.6% died under treatment for different diseases. Burden and colleagues (2009) enrolled donkeys affected by different pathologies, which were dead or were euthanized be-cause of problems in one of the main body systems.
In the present paper, 48.7% (33-64.4%) of the animals showed ESGD of grade 0/4, while 48.7% (33-64.4%) had lesions graded 1/4-3/4, with a very low prevalence (2.6%, 0.0-7.5%) of grade 4/4. In the report by Morales Briceño and colleagues (2015), the evaluation of gastric lesions in dead donkeys revealed an ESGD with the highest prevalence of grade 2/4. These differences could be re-lated to the inclusion of alive vs. dead donkeys and to the higher number of animals evaluated in the present study compared to the previous one (39 vs. 10).
No differences related to sex, age or breed were found in this study. This is in line with reports performed both in donkeys (Burden et al. 2009) and horses (Vatistas et al. 1999; Rabuffo et al. 2002; Bezdekova et al. 2005; Bell et al. 2007; Lester et al. 2008; Hepburn 2014), but in contrast 177 178 179 180 181 182 183 184 185 186 187 188 189 190 191 192 193 194 195 196 197 198 199 200 201 202 203 204 205 206 207 208 209 210 211 212 213 214 215 216 217 218 219 220 221 222 223 224 225 226 227 228
with other authors (Sandin et al. 2000).
All our donkeys did not have clinical signs attributable to EGUS or other diseases, in accordance with Morales Briceño and colleagues (2014), who enrolled asymptomatic donkeys that died due to non-digestive causes. The majority of donkeys enrolled by Burden et al (2009) were euthanized or died due to a problem in one of the main body organ systems. On the other hand, Morrow et al. (2011) reported that only 2.6% of the donkeys enrolled were euthanized under treatment of a non-specified disease. Finally, Al-Mokadden and colleagues (2014) included donkeys euthanized for diseases not related to EGUS, which were predominantly long bone fractures.
The detection of third-stage G. intestinalis larvae was not unexpected since L3 can be retrieved throughout the year and G. instestinalis has been reported as the most common Gasterophilus species in Italy (Otranto et al., 2005). G. intestinalis larvae were found to be attached along the margo plicatus in all our donkeys. These findings are in agreement with other authors who detected a 100% infestation rate in Egypt (Al-Mokadden et al. 2014). However, lower prevalence values of 30% and 0.4% have also been reported in Spain (Morales Briceño et al. 2015) and in the United Kingdom (Morrow et al. 2011), respectively. Differences in prevalence rates of G. intestinalis may be due to environmental and climatic conditions influencing the spread of parasites. Some geographical areas may therefore be favorable than others for the transmission of equine gastric myasis. It is also possible that lower prevalences were associated with the use of drugs that are effective against gastric stages of G. intestinalis. Unfortunately, other researchers did not provide information in this regard in their studies (Morrow et al. 2011; Morales Briceño et al. 2015). The role of parasites in the pathogenesis of gastric lesions is unclear. Previous reports have suggested that Gasterophilus spp. can cause gastric and intestinal ulceration (Sandin et al., 2000; Sequeira et al. 2001). Since larvae were found both in donkeys with and without EGUS, the authors cannot rule out whether infestation by G. intestinalis could be a risk factor for EGUS in this host species. The starch/grain intake has been associated with a higher risk of EGUS, both in horses (Vatistas et al. 1999; Frank et al. 2005; Luthersson et al. 2009) and donkeys (Burden et al. 2009). All the donkeys included in the present study were fed on carbohydrates in the same manner; therefore this risk factor could not be evaluated.
Conclusions
EGUS has been described in horses and donkeys. In this study, we report EGUS in a population of donkeys in Italy. Our results highlight that EGUS had high prevalence in the examined donkeys' population although there were no clinical signs and that the squamous portion of the stomach was much more frequently affected than the glandular region. This suggests that EGUS may be more common in donkeys than it was previously thought, but it is routinely overlooked. Further studies are needed to investigate the aetiology, pathogenesis, clinical significance and risk factors for this condition in donkeys.
Manufacturers’ addresses’
1 Zoetis Italia srl, Roma, Italy; 2 ACME s.r.l., Cavriago, Italy; 3 Karl Storz, Germany;
4 GraphPad Prism 7, USA.
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References
1. Al-Mokaddem, A.K., Ahmed K.A., and Doghaim R.E. (2014) Pathology of gastric lesions in donkeys: A preliminary study. Equine Vet. J. 47(6), 684-688.
2. Andrews, F., Bernard, W., Byars, D., Cohen, N., Divers, T., MacAllister, C., McGladdery, A., Merritt, A., Murray, M., Orsini, J., Snyder, J., Vatistas, N. (1999) Recommendations for the diagnosis and treatment of equine gastric ulcer syndrome (EGUS). Equine vet. Educ.
11(5): 262-272.
3. Bain, F.T., Petrizzi, L., Valbonetti, L., Muttini, A. (2004) Gastroscopy and duodenoscopy. In Atlas of equine endoscopy, Ed: Slovis, N.M., Mosby-Elsevier, St. Lois, Missouri, USA, pp. 147-168.
4. Bell, R.J.W., Kingston, J.K., Mogg, T.D., and Perkins N.R. (2007) The prevalence of gastric ulceration in racehorses in New Zealand. New Zealand Vet. J. 55(1), 13-18.
5. Bezdukova, B., Jahn, P., Vyskocil, M., and Plach, J. (2005) Prevalence of Equine Gastric Ulceration in Standardbred Racehorses in Czech Republic. Acta Vet. Brno, 74, 59-65. 6. Bonelli, F., Rota, A., Corazza, M., Serio, D., and Sgorbini, M. (2016) Hematological and
biochemical findings in pregnant, postfoaling, and lactating jennies Theriogenol. 85, 1233– 1238.
7. Borioni, M., Marinaro, P., Celestini, S., Del Sole, F., Magro, R., Zoppi, D., Mattei, F., Dall’Ami, V., Mazzarella, F., Cesario, A., and Bonassi, S. (2012) Effect of equestrian ther-apy and onotherther-apy in physical and psycho-social performances of adults with intellectual disability: a preliminary study of evaluation tools based on the ICF classification. Disabil. Rehabil. 34(4): 279-97.
8. Burden, F.A., Gallagher, J., Thiemann, A.K., and Trawford, A.F. (2009) Necropsy survey of gastric ulcers in a population of aged donkeys: prevalence, lesion description and risk fac-tors. Animal, 3, 287-293.
9. Carluccio, A., Gloria, A., Veronesi, M.C., De Amicis, I., Noto, F., and Contri, A. (2015) Factors affecting pregnancy length and phases of parturition in Martina Franca jennies. Theriogenol. 84(4), 650-655.
10. Carroccio, A., Cavataio, F., and Montalto, G. (2000) Intolerance to hydrolysed cow’s milk proteins in infants: clinical characteristic and dietary treatment. Clin. Exp. Allergy 30, 1597-1603.
11. Cate, R.E., Nielsen, B.D., Spooner, H.S., O’Connor-Robison, C.I., and Schott II H.C. (2012) Prevalence of gastric ulcers and relationship to other parameters in Standardbred racehorses. Comp. Exercise Physiol. 8(1), 47-52.
12. Crisci, A., Rota, A., Panzani, D., Sgorbini, M., Ousey, J.C., and Camillo, F. (2014) Clinical, ultrasonographic, and endocrinological studies on donkey pregnancy. Theriogenol. 81, 275-283.
13. Frank, N., Andrews, F.M., Elliott, S.B., Lew, J. (2005) Effects of dietary oils on the devel-opment of gastric ulcers in mares. Am. J. Vet. Res. 66(11), 2006-2011.
14. Fors, P., Lopez, J., Rodriguez, A., Harran, R. (2001) Endoscopy of the upper airways and the proximal digestive tract in the donkey (Equus asinus). J. Equine Vet. Sci. 21, 17-20. 15. Hepburn, R.J. (2014) Endoscopic examination of the squamous and glandular gastric
mucosa in sport and 562 leisure horses: 684 horses (2005-2011). BMC Vet. Res. 10(S1);11. 16. Jerbi, H., Rejeb, A., Erdoğan, S. and Pérez, W. (2014). Anatomical and morphometric study
of gastrointestinal tract of donkey (Equus africanus asinus). J. Morphol. Sci. 31(1), 18-22. 17. Kim, T.W., Della Rocca, G., Di Salvo, A., Owen, H., Sgorbini, M., and Giorgi, M. (2014)
Pharmacokinetics of the Novel Cyclooxygenase 2 Inhibitor Cimicoxib in Donkeys. J. Equine Vet. Sci. 34, 923–925.
18. Laus, F., Spaterna, A., Faillace, V., Paggi, E., Serri, E., Vullo, C., Cerquetella, M., and Te-sei, B. (2015a) Reference values for hematological and biochemical parameters of mixed breed donkeys (Equus asinus). Wulfenia 22(1), 294-304.
272 273 274 275 276 277 278 279 280 281 282 283 284 285 286 287 288 289 290 291 292 293 294 295 296 297 298 299 300 301 302 303 304 305 306 307 308 309 310 311 312 313 314 315 316 317 318 319 320 321 322
19. Laus, F., Spaterna, A., Faillace, V., Veronesi, F., Ravagnan, S., Beribé, F., Cerquetella, M., Meligrana, M., and Tesei. B (2015b) Clinical investigation on Theileria equi and Babesia caballi infections in donkeys from central Italy. BMC Vet. Res. 11, 100, Doi: 10.1186/s12917-015-0411-z.
20. Le Jeune, S.S., Nieto, J.E., Dechant, J.E., and Snyder, J.R. (2009) Prevalence of gastric ul-cers in Thoroughbred broodmares in pasture: a preliminary report. Vet. J. 181, 251-255. 21. Lester, G.D., Robinson, I., Secombe, C. (2008) Risk Factors for Gastric Ulceration in
Thor-oughbred 567 Racehorses. Canberra: Australian Government: Rural Industries Research and Development Corporation, p. 1-42.
22. Luthersson, N., Nielsen, K.H., Harris, P., and Parkin, T.D. (2009) The prevalence and anatomical distribution of equine gastric ulceration syndrome (EGUS) in 201 horses in Den-mark. Equine Vet. J. 41(7), 619-624.
23. Monti, G., Viola, S., Baro, C., and Bertino, E. (2012) Tolerability of donkey's milk in 92 highly-problematic cow's milk allergic children. J. Biol. Regul. Homeost. Agents 26:75-82. 24. Morales Briceño, A., Lamprea Garrido, A., Méndez Sánchez, A. (2015) Gastric ulcers
syn-drome in donkeys. Rev. Med. Vet. 30, 31-35.
25. Morrow, L.D., Smith K.C., Piercy, R.J., du Toit, N., Burden, F.A., Olmos, G., Gregory, N.G. and Verheyen, K.L.P. (2011) Retrospective analysis of post-mortem findings in 1444 aged donkeys. J. Comp. Path. 144, 145-156.
26. Muraro, M.A., Giampietro, P.G. and Galli, E. (2002) Soy formulas and non bovine milk. Ann Allergy Asthma Immunol. 89(S), 97-101.
27. Nardoni, S., Sgorbini, M., Barsotti, G., Corazza, M., and Mancianti, F. (2007) Conjunctival fungal flora in healthy donkeys. Vet. Ophthalmol. 10(4), 207–210.
28. Niedźwiedź, A., Kubiak, K., and Nicpoń. J. (2013) Endoscopic findings of the stomach in pleasure horses in Poland. Acta Vet. Scand. 55, 45-48.
29. Otranto, D., Milillo, P., Capelli, G., Colwell, D.D. (2005) Species composition of Gas-terophilus spp. (Diptera, Oestridae) causing equine gastric myiasis in southern Italy: Parasite biodiversity and risks for extinction. Vet. Parasitol. 133, 111-118.
30. Rabuffo, T.S., Orsini. J.A., Sullivan, E., Engiles, J., Norman, T., and Boston, R. (2002) Associations between age or sex 530 and prevalence of gastric ulceration in Standardbred racehorses in training. J. Am. Vet. Assoc. 221(8), 1156-1159.
31. Sandin, A., Skidde, J., Haggstrom, J. and Nilsson, G. (2000) Post mortem findings of gastric ulcers in Swedish horses older than age one year: a retrospective study of 3715 horses (1924-1996). Equine Vet. J. 32, 36-42.
32. Sequeira, J.L., Tostes, R.A. and Oliveira-Sequeira, T.C. (2001) Prevalence and macro- and microscopic lesions produced by Gasterophilus nasalis (Diptera: Oestridae) in the Botucatu Region, SP, Brazil. Vet. Parasitol. 102, 261-266.
33. Sgorbini, M., Bonelli, F., Rota, A., Baragli, P., Marchetti, V., and Corazza, M. (2013) Hematology and Clinical Chemistry in Amiata Donkey Foals from Birth to 2 Months of Age. J. Equine Vet. Sci. 33(1), 35-39.
34. Sykes, B.W., Jokisalo, J.M. (2014). Rethinking equine gastric ulcer syndrome: Part 1 - Ter-minology, clinical signs and diagnosis. Equine Vet. Educ. 26(10), 543-547.
35. Sykes, B.W., Jokisalo, J.M. (2015a). Rethinking equine gastric ulcer syndrome: Part 2 -Equine squamous gastric ulcer syndrome (ESGUS). -Equine Vet. Educ. 27(5), 264-268. 36. Sykes, B.W., Jokisalo, J.M. (2015b) Rethinking equine gastric ulcer syndrome: Part 3
-Equine glandular gastric ulcer syndrome (EGGUS). -Equine Vet. Educ. 27(7): 372-375. 37. Sykes, B.W., Hewetson, M., Hepburn, R.J., Luthersson, N., and Tamzali, Y. (2015)
Euro-pean College of Equine Internal Medicine Consensus Statement – Equine Gastric Ulcer Syn-drome in Adult Horses, J. Vet. Int. Med. 2015, 29, 1288-1299.
38. Tamzali, Y., Marguet, C., Priymenko, N., and Lyazrhi, F. (2011) Prevalence of gastric ulcer syndrome in high-level endurance horses. Equine Vet. J. 43(2), 141-144.
323 324 325 326 327 328 329 330 331 332 333 334 335 336 337 338 339 340 341 342 343 344 345 346 347 348 349 350 351 352 353 354 355 356 357 358 359 360 361 362 363 364 365 366 367 368 369 370 371 372 373
39. Vatistas, N.J., Snyder, J.R., Carlson, G., Johnson, B., Arthu, R.M., Thurmond, M., et al. (1999) Cross-sectional study 527 of gastric ulcers of the squamous mucosa in Thoroughbred racehorses. Equine Vet. J. 31(S29), 34-39.
40. Veronesi, M.C., Gloria, A., Panzani, S., Sfirro, M.P., and Carluccio, A. (2014) Blood analy-sis in newborn donkeys: hematology, biochemistry and blood gases analyanaly-sis. Theriogenol.
82(2), 294-303.
41. Zumpt, F. (1965). Myiasis in Man and Animals in the Old World: a textbook for physicians, veterinarians and zoologists. Butterworths, London, UK.
Table1 – Prevalence values and 95% confidence intervals (95% CI) of Equine Gastric Ulceration Syndrome in donkeys examined alive by gastroscopic examination in Italy, according to anatomical location of the lesions, sex, age, and breed.
Variables No. positive/no. examined Prevalence (95% CI)
Lesion location ESGD* 19/39*^ 48.7% (33-64.4%)
ESGD/EGGD^ 1/39*^ 2.6% (0-7.5%) Sex Females 9/16 56.2% (32.6-77.8%) Males 11/23 47.8% (28.7-67.5%) Age ≤3 years 12/23 52.2% (32.5-71.3% >3 years 8/16 50.0% (27.2-72.8%) Breed Amiata 15/33 45.4% (28.5-62.4%) Crossbreed 5/6 83.3% (53.5-100%) Total 20/39 51.3% (35.6-67%)
*Equine Squamous Gastric Disease (ESGD); ^ESGD in association with Equine Glandular Gastric Disease (EGGD); *^highly significant difference by Fisher’s exact test (P<0.0001).
Table 2 – Distribution of scores of Equine Squamous Gastric Disease according to sex, age, and breed in donkeys examined alive by gastroscopic examination in Italy. Results show the number of positive animals/number of examined animals, prevalence values, and corresponding 95% confidence intervals (in brackets) for each score.
Scores Sex Age Breed Total
Females Males ≤3 years >3 years Amiata Crossbreed
0 7/16 43.7% (19.4-68.1%) 12/23 52.2% (31.8-73.0%) 11/23 47.8% (27.4-68.2%) 8/16 50.0% (25.5-74.5%) 18/33 54.5% (37.8-70.6%) 1/6 16.7% (1.9-55.8%) 19/39 48.7% (33.0-64.4%) 1 5/16 31.2% (8.5-54.0%) 0/23 0.0% (0.0-0.0%) 1/23 4.3% (0.0-12.7%) 4/16 25.0% (3.8-46.2%) 1/33 3.0% (0.33-13.3%) 4/6 66.6% (28.6-92.3%) 5/39 a 12.8% (2.3-23.3%) 2 3/16 18.7% (0.0-37.9%) 7/23 30.4% (11.6-49.2%) 6/23 26.1% (8.1-44.0%) 4/16 25.0% (3.8-46.2%) 9/33 27.3% (14.4-43.9%) 1/6 16.7% (1.9-55.8%) 10/39 b 25.6% (11.9-39.5%) 3 1/16 6.2% (0.0-18.1%) 3/23 13.0% (0.0-26.8%) 4/23 17.4% (1.9-32.8%) 0/16 0.0% (0.0-0.0%) 4/33 12.2% (4.2-26.3%) 0/6 0.0% (0.0-0.0%) 4/39 b 10.3% (0.7-19.8%) 4 0/16 0.0% (0.0-0.0%) 1/23 4.3% (0.0-12.7%) 1/23 4.3% (0.0-12.7%) 0/16 0.0% (0.0-0.0%) 1/33 3.0% (0.33-13.3%) 0/6 0.0% (0.0-0.0%) 1/39 b 2.6% (0.0-7.5%)
a, b Difference between the prevalence of donkeys affected by grade 1 lesions (hyperemia and/or
hyperparakeratosis), and the prevalence of donkeys affected by grade 2-4 lesions (ulcers) was statistically significant (12.8% [2.3-23.3%] vs. 38.5% [23.2-53.7%], P=0.0183). 374 375 376 377 378 379 380 381 382 383 384 385 386 387 388 389 390 391 392 393 394 395 396 397
