Eradication of gastric Helicobacter spp by triple therapy in dogs

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(1)Original Paper. Veterinarni Medicina, 58, 2013: (11): 582–586. Eradication of gastric Helicobacter spp. by triple therapy in dogs S. Mirzaeian1, A.A. Sarchahi2, A. Shojaee Tabrizi1, A. Derakhshandeh1 1 2. Faculty of Veterinary Medicine, Shiraz University, Shiraz, Iran Faculty of Veterinary Medicine, Ferdowsi University of Mashhad, Mashhad, Iran. ABSTRACT: The aim of this study was to determine the efficacy of a triple anti-Helicobacter therapy using omeprazole, amoxicillin and clarithromycin (OAC) in dogs. A total of 15 healthy adult stray dogs with naturally acquired Helicobacter infection were evaluated using polymerase chain reaction and rapid urease test. Subsequently, they received a 21-day triple regimen. One day after the discontinuation of treatment, a second molecular analysis of gastric biopsies revealed complete eradication of Helicobacter DNA with negative quantitative urease testing in all 15 dogs. Our results confirmed the high prevalence of gastric Helicobacter-like organisms (GHLOs) in the stray dog population of Shiraz, Iran, and the effectiveness of our therapeutic regimen for the complete eradication of these microorganisms in stray dogs. In conclusion, for the complete elimination of non-pylori Helicobacter spp. from the gastric mucosa of dogs, a 21-day three-drug regimen with omeprazole, amoxicillin and clarithromycin is suggested. Keywords: Helicobacter spp.; dog; amoxicillin; clarithromycin; omeprazole. Many humans have close interactions with companion animals which leads to the sharing of many diseases. Gastric Helicobacter spp. is one of the common infections in dogs, which may occur without clinical signs of gastritis (Simpson 2010). However, some human patients suffer from gastric disorders due to Non-pylori Helicobacter spp. (Heilmann and Borchard 1991; Andersen 2001; De Groote et al. 2005; Van den Bulck et al. 2005a; Duquenoy and Luyer 2009). Unlike H. pylori, gastric Helicobacter-like organisms (GHLOs) induce milder degrees of gastritis in humans, but more severe disorders such as gastric erosion/ulcers and cancer are also reported (Morgner et al. 2000; Yoshimura et al. 2002; Alon et al. 2010). It is almost certain that such infections in humans originate from animals, including dogs, through direct contact (Meining et al. 1998; Haesebrouck et al. 2009). Therefore, eradication of Helicobacter infections in dogs that have close contact with humans should be considered as one of the methods to control this zoonotic infection. The efficacy of different therapeutic regimens has been evaluated in dogs, cats 582. and humans. However, an optimal method has yet to be established (DeNovo and Magne 1995; Neiger and Simpson 2000; Graham et al. 2003; Fischbach et al. 2004; Gatta et al. 2005; Gisbert et al. 2005; Qasim et al. 2005; Khoshnegah et al. 2011; Georgopoulos et al. 2012). In fact, previous studies have shown that triple or quadruple therapies are not 100% effective and, thus, further studies are needed in this regard. The aim of this study was to evaluate a 21-day triple Helicobacter species therapy in dogs with naturally acquired infection.. MATERIAL AND METHODS Animals. Gastric biopsies of 15 asymptomatic, adult (mean age = 1.5 years), stray dogs were used in this study. All dogs were isolated from different locations of Shiraz, Iran. The animals were kept under supervision for seven days for observation and to ensure their health status using clinical and laboratory examinations. The dogs then underwent a 12 h fast and were subsequently tranquillized.

(2) Veterinarni Medicina, 58, 2013 (11): 582–586 with an intramuscular injection of xylazine hydrochloride (Alfasan, Woerden, Holland) (0.5 mg/kg) and acepromazine maleate (Castran, Interchemie, Holland) (0.05 mg/kg), and anaesthetised with a combination of diazepam (Phoenix Pharma Ltd, Gloucester, England) (0.25–0.5 mg/kg), and ketamine hydrochloride (Alfasan, Woerden, Holland) (5–10 mg/kg). Gastroscopy was performed with a 7.9 mm diameter gastroduodenoscope (MEDIT, Canada) to obtain three pairs of biopsies from the cardia, fundic and antral regions of the stomach. Quantitative urease test. One of the gastric biopsy specimens from each of the mentioned regions was placed into urea broth media (DIFCO, USA) and incubated at 37 °C for 24 h. Colour transformation from yellow to pink/red within 24 h was considered as a positive result with the following degrees: colour change within the first 2 h (+3), between 2 and 6 h (+2) and between 6 and 24 h (+1). No colour transformation within 24 h was considered negative (0) (Ricci et al. 2007). DNA extraction and PCR assays. DNA was extracted from the gastric biopsy specimens using a DNeasy tissue kit (Qiagen, Germany) according to the manufacturer’s instructions. Polymerase chain reaction (PCR) amplifications were performed in a final volume of 25 µl containing 100 ng of extracted DNA, 2.5 µl of 10× PCR buffer (Fermentas, Lithuania), 0.2mM of dNTP, 1.5mM MgCl2, 25 pmol/ µl of each primer and 0.2 IU of Taq DNA polymerase (Fermentas, Lithuania). The PCR was carried out using a MJ-Mini BioRad thermal cycler (BioRad, USA) with an initial denaturing cycle at 94 °C for 4 min, followed by 33 cycles of 94 °C for 1 min, 62 °C for 1 min, and 72 °C for 1 min. A final extension step. Original Paper was performed at 72 °C for 7 min. The resulting PCR products underwent gel electrophoresis (1.0% agarose gel with ethidium bromide (0.5 mg/l) and were visualised under a UV transilluminator. The primer sequences used in this study for the detection of Helicobacter spp. were (F): 5'-AAG GAT GAA GCT TCT AGC TTG CTA-3’, (R): 5'-GTG CTT ATT CGT GAG ATA CCG TCA T-3’. The size of the expected fragment (398 bp) was compared to a 100 bp reference marker (Fermentas). Therapeutic protocol. All Helicobacter spp.positive dogs in this study received omeprazole 0.5–1 mg/kg, SID (one capsule per day for animals less than 15 kg body weight [BW], and two capsules for those with more than 15 kg BW), amoxicillin 20 mg/kg, BID, and clarithromycin 7.5 mg/kg, BID, for 21 days. All dogs were kept in isolation during this study. The second molecular analysis and rapid urease testing (RUT) were performed on the day after the end of the treatment.. RESULTS According to RUT, 15/15 (100%) of the gastric specimens were mild to moderately positive for Helicobacter spp. and no severe degrees were detected. Genus-specific PCR also identified 15/15 (100%) of the subjects as Helicobacter spp.-positive (Figure 1). After three weeks, the successful eradication rate was 100%, and the second analysis revealed no signs of gastric Helicobacter infection neither by PCR nor RUT in any of the 15 dogs (Figure 2).. Figure 1. PCR amplification of DNA extracted from biopsy samples before treatment with species-specific Helicobacter primers. Lane M = 100 bp molecular ladder; lanes 1–16 = biopsy samples; lane C+ = positive control; lane C– = negative control. 583.

(3) Original Paper. Veterinarni Medicina, 58, 2013: (11): 582–586 Figure 2. PCR amplification of DNA extracted from biopsy samples after treatment with speciesspecific Helicobacter primers. (Up) lane M = 100 bp molecular ladder; lanes 1–14  = biopsy samples. (Down) lane M = 100 bp molecular ladder; lanes 1–3 = biopsy samples; lane C+  = positive control; lane C– = negative control. DISCUSSION Gastric infection with non-pylori Helicobacter spp. is rare, but is known to be associated with chronic active gastritis, peptic ulcers, and lowgrade mucosa-associated lymphoid tissue lymphoma in humans (Morgner et al. 2000; Yoshimura et al. 2002; Van den Bulck et al. 2005; Alon et al. 2010). In contrast to H. pylori, various Helicobacter species colonise the stomachs of domestic animals, which might be a reservoir for transmission to humans. Although the exact route of this zoonotic transmission is not clearly understood, maintaining close contact with dogs and cats may put people, especially immunocompromised persons, at high risk for this infection (Alon et al. 2010). Therefore, to prevent this zoonotic infection, an efficient therapeutic protocol for dogs and cats is required. In the current study, a high prevalence of GHLO infection (100%) was detected, which is in agreement with another study conducted in our area by (Shabestari et al. 2008) (93%). The susceptibilities of Helicobacter spp. isolated from the stomach of cats and dogs to 10 antimicrobial agents were estimated by Van den Bulck et al. (2005b) via determination of the minimal inhibitory concentration (MIC) using the agar dilution method (Van den Bulck et al. 2005b). Helicobacter species were all highly susceptible to ampicillin, clarithromycin, tetracycline, tylosin, enrofloxacin, gentamicin, and neomycin, as demonstrated 584. by low MICs. In a veterinary study, clinical signs in 90% of 63 dogs and cats were resolved by using a combination of metronidazole, amoxicillin and famotidine, and 74% of 19 animals had no evidence of Helicobacter species in gastric biopsies (DeNovo and Magne 1995). The outcome is obviously better if agents to which the organism is susceptible are used for treatment. Therefore, in the current study we used omeprazole (as a proton pump inhibitor), clarithromycin and amoxicillin. The variability of treatment success with an individual regimen has been related to the occurence of antimicrobial resistance, compliance with the drug regimen, and duration of therapy (Vakil et al. 2004). Recent studies suggest that the success rate of triple regimens can be improved if the duration is extended to 14 days or if an additional antibiotic is given (Nakayama and Graham 2004; Vilaichone et al. 2006). Khoshnegah et al. (2011) assessed a quadruple therapy (omeprazole, amoxicillin, metronidazole and clarithromycin for 14 days) in 13 asymptomatic, naturally infected cats, but they suggested that antibiotic regimens that are effective against Helicobacter pylori in people cannot eliminate Helicobacter species in cats with naturally acquired infections (Khoshnegah et al. 2011). However, our results showed the effectiveness of a 21-day threedrug regimen in dogs using omeprazole, amoxicillin and clarithromycin. Our results show that extending the duration of therapy can be more effective than using additional.

(4) Veterinarni Medicina, 58, 2013 (11): 582–586 antibiotics in the therapeutic protocol such as was carried out in the study of Khoshnegah et al. (2011). Although, a previous study has shown that triple therapy for seven days using clarithromycin, amoxicillin and lansoprazole was effective in 100% of dogs (Anacleto et al. 2011), in human medicine, therapies of shorter duration are no longer recommended since it has been demonstrated that a 14-day triple therapy has an approximately 12% better cure rate than a 7-day therapy (Vilaichone et al. 2006). Our study confirms this finding in dogs. Consequently, a 21-day triple or quadruple therapy can be considered a reasonable therapeutic period for the eradication of Helicobacter spp. from gastric mucosa of dogs. The results of PCR and RUT were not positive in any of the dogs in the second evaluation suggesting that recrudescence is unlikely. However, to more definitively determine this, recrudescence and/or reinfection should be assessed for longer periods of time after drug therapy. In conclusion, for complete elimination of nonpylori Helicobacter spp. from the gastric mucosa of dogs, a 21-day three-drug regimen with omeprazole, amoxicillin and clarithromycin is suggested. However, further controlled trials of antibiotic therapy with different durations of treatment in infected dogs and evaluation of re-infection are obviously required before guidelines regarding the treatment of gastric Helicobacter species in dogs can be made.. Acknowledgement Funding was provided by research grant from the Research Council of Shiraz University¸ Shiraz, Iran.. REFERENCES Alon D, Paitan Y, Ben-Nissan Y, Chowers M (2010): Persistent Helicobacter canis bacteremia in a patient with gastric lymphoma. Infection 38, 62–64. Anacleto TP, Lopes LR, Andreollo NA, Bernis Filho WO, Resck MCC, Macedo A (2011): Studies of distribution and recurrence of Helicobacter spp. gastric mucosa of dogs after triple therapy. Acta Cirurgica Brasileira 26, 82–87. Andersen LP (2001): New Helicobacter species in humans. Digestive Diseases 19, 112–115. De Groote D, Van Doorn LJ, Van den Bulck K, Vandamme P, Vieth M, Stolte M, Debongnie JC, Burette A, Haesebrouck F, Ducatelle R (2005): Detection of. Original Paper non-pylori Helicobacter species in “Helicobacter heilmannii” – infected humans. Helicobacter 10, 398–406. DeNovo RC, Magne ML (1995): Current concepts in the management of Helicobacter – associated gastritis. In: Proceedings 13 th Annual ACVIM Veterinary Forum, Lake Buena Vista, FL, American College of Veterinary Internal Medicine. Duquenoy A, Luyer B (2009): Gastritis caused by Helicobacter heilmannii probably transmitted from dog to child. Archives de Pediatrie 16, 426–429. Fischbach LA, Zanten SV, Dickason J (2004): Metaanalysis: the efficacy, adverse events, and adherence related to first-line anti-Helicobacter pylori quadruple therapies. Alimentary Pharmacology and Therapeutics 20, 1071–1082. Gatta L, Zullo A, Perna F, Ricci C, De Francesco V, Tampieri A, Bernabucci V, Cavina M, Hassan C, Ierardi E (2005): A 10-day levofloxacin-based triple therapy in patients who have failed two eradication courses. Alimentary Pharmacology and Therapeutics 22, 45–49. Georgopoulos SD, Papastergiou V, Karatapanis S (2012): Helicobacter pylori eradication therapies in the era of increasing antibiotic resistance: A paradigm shift to improved efficacy. Gastroenterology Research and Practice 2012, 9 pp. Gisbert JP, Gonzalez L, Calvet X (2005): Systematic review and meta-analysis: proton pump inhibitor vs. ranitidine bismuth citrate plus two antibiotics in Helicobacter pylori eradication. Helicobacter 10, 157–171. Graham DY, Hammoud F, El-Zimaity HMT, Kim JG, Osato MS, El-Serag HB (2003): Meta-analysis: proton pump inhibitor or H2-receptor antagonist for Helicobacter pylori eradication. Alimentary Pharmacology and Therapeutics 17, 1229–1236. Haesebrouck F, Pasmans F, Flahou B, Chiers K, Baele M, Meyns T, Decostere A, Ducatelle R (2009): Gastric helicobacters in domestic animals and nonhuman primates and their significance for human health. Clinical Microbiology Reviews 22, 202–223. Heilmann KL, Borchard F (1991): Gastritis due to spiral shaped bacteria other than Helicobacter pylori: clinical, histological, and ultrastructural findings. Gut 32, 137–140. Khoshnegah J, Jamshidi S, Mohammadi M, Sasani F (2011): The efficacy and safety of long-term Helicobacter species quadruple therapy in asymptomatic cats with naturally acquired infection. Journal of Feline Medicine and Surgery 13, 88–93. Meining A, Kroher G, Stolte M (1998): Animal reservoirs in the transmission of Helicobacter heilmannii: results of a questionnaire-based study. Scandinavian Journal of Gastroenterology 33, 795–798.. 585.

(5) Original Paper Morgner A, Lehn N, Andersen LP, Thiede C, Bennedsen M, Trebesius K, Neubauer B, Neubauer A, Stolte M, Bayerrffer E (2000): “Helicobacter heilmannii” – associated primary gastric low-grade MALT lymphoma: complete remission after curing the infection. Gastroenterology 118, 821–828. Nakayama Y, Graham DY (2004): Helicobacter pylori infection: diagnosis and treatment. Expert Review of Ati-infective Therapy 2, 599–610. Neiger R, Simpson KW (2000): Helicobacter infection in dogs and cats: facts and fiction. Journal of Veterinary Internal Medicine 14, 125–133. Qasim A, Sebastian S, Thornton O, Dobson M, McLoughlin R, Buckley M, O’Connor H, O’Morain C (2005): Rifabutin- and furazolidone-based Helicobacter pylori eradication therapies after failure of standard first- and second-line eradication attempts in dyspepsia patients. Alimentary Pharmacology and Therapeutics 21, 91–96. Ricci C, Holton J, Vaira D (2007): Diagnosis of Helicobacter pylori: invasive and non-invasive tests. Best Practice and Research Clinical Gastroenterology 21, 299–313. Shabestari AS, Mohammadi M, Jamshidi S, Sasani F, Bahadori A, Oghalaie A (2008): Assessment of chronic gastritis in pet dogs and its relation with helicobacterlike organisms. Pakistan Journal of Biological Sciences 11, 1443–1448.. Veterinarni Medicina, 58, 2013: (11): 582–586 Simpson KW (2010): Diseases of the Stomach. In: Ettinger SJ, Feldman EC (eds.): Textbook of Veterinary Internal Medicine: Diseases of the Dog and Cat. 7th ed. Saunders Elsevier Inc., St. Louis. 1504–1526. Vakil N, Lanza F, Schwartz H, Barth J (2004): Seven-day therapy for Helicobacter pylori in the United States. Alimentary Pharmacology and Therapeutics 20, 99–107. Van den Bulck K, Decostere A, Baele M, Driessen A, Debongnie JC, Burette A, Stolte M, Ducatelle R, Haesebrouck F (2005a): Identification of non-Helicobacter pylori spiral organisms in gastric samples from humans, dogs, and cats. Journal of Clinical Microbiology 43, 2256–2260. Van den Bulck K, Decostere A, Gruntar I, Baele M, Krt B, Ducatelle R, Haesebrouck F (2005b): In vitro antimicrobial susceptibility testing of Helicobacter felis, H. bizzozeronii, and H. salomonis. Antimicrobial Agents and Chemotherapy 49, 2997–3000. Vilaichone RK, Mahachai V, Graham DY (2006): Helicobacter pylori diagnosis and management. Gastroenterology Clinics of North America 35, 229–247. Yoshimura M, Isomoto H, Shikuwa S, Osabe M, Matsunaga K, Omagari K, Mizuta Y, Murase K, Murata I, Kohno S (2002): A case of acute gastric mucosal lesions associated with Helicobacter heilmannii infection. Helicobacter 7, 322–326. Received: 2013–03–12 Accepted after revision: 2013–11–20. Corresponding Author: Ali Asghar Sarchahi, Department of Clinical Sciences, Faculty of Veterinary Medicine, Ferdowsi University of Mashhad, PO Box: 9177948974-173, Mashhad, Iran Tel. +98 511 8805596, Fax +98 511 8763852, E-mail: sarchahi@um.ac.ir, aliasgharsarchahi@yahoo.com. 586.

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