on line editionAcute gastroenterocolitis caused by Salmonella Chester Short SCientifiC ArtiCle id 1 Department of internal medicine, Slovenj Gradec General Hospital, Slovenj Gradec 2 Department of paediatrics, Slovenj Gradec General Hospital, Slovenj Gradec 3 Regional Unit Ravne na Koroškem, National Institute of Public Health, Ravne na Koroškem Correspondence: tajda Keber, e: tajda.keber@gmail. com Key words: Salmonella Chester; turtles; gastroenterocolitis; gastroenteritis Cite as: Zdrav Vestn. 2017; 86:207–11. received: 23. 10. 2016 Accepted: 9. 2. 2017 Zdrav Vestn | Maj – June 2017 | Volume 86 Metabolic and hormonal disordersShort scientific article Acute gastroenterocolitis caused by Salmonella Chester tajda Keber,1 eta Mijoč,2 neda hudopisk,3 Marjana Simetinger,3 Klemen Mojškerc1 Abstract Turtles are common pets and represent a known reservoir for salmonellosis. There are few epidemic outbreaks of salmonellosis linked to ingestion of undercooked turtle meat described in the literature. A few cases of pet turtle borne infection and infection due to aquarium water contamination have been described. We present two female patients hospitalized d with acute gastroenterocolitis caused by Salmonella Chester, and give an epidemiological report of the events related to the infection out- break. The infection was transmitted from the water of a private aquarium housing two pet turtles. Cite as: Zdrav Vestn. 2017; 86:207–11. 1. Introduction Turtles are popular pets, widely acces- sible in pet stores. Reptiles are common salmonellosis reservoir, because they carry Salmonella spp. as part of com- mensal flora in their intestines. Salmo- nella spp. were found in 50–90 % of their faeces samples  (1,2).Children are often infected because they spend a lot of time in close contact with their pets (3). The paper describes two patients (Pa- tients 1 and 2) who were hospitalized with acute gastroenterocolitis caused by Salmonella Chester transferred from the water contaminated by yellow-necked turtles. An epidemiological report on the events associated with the infection is given. 2. Case reports 2.1. Group 1 A 55-yearold female with the diag- nosis of Raynaud’s phenomenon, hiatal hernia, reflux oesophagitis type A, and mixed connective tissue disease treated with methylprednisolone, (Patient 1) was hospitalized with a 5-day history of vomiting and diarrhoea. She passed at least ten green watery stools a day. She had diffuse abdominal pain relieved by defecation. She had a headache and a temperature of up to do 38 °C. Three to four days before the outbreak of her symptoms her granddaughter fell ill with vomiting and diarrhoea. The pa- tient was febrile (37,9 °C) and tachy- on line edition Zdrav Vestn | Maj – June 2017 | Volume 86 MetAboliC And horMonAl diSorderS cardic; on palpation her abdomen was painful in the lower quadrants. Labora- tory measurements showed high levels of C-reactive protein and procalcitonin without leucocytosis or lactate elevation. Laboratory criteria for dehydration with impaired renal function were present. Abdominal ultrasound showed signs of gastroenterocolitis with a thickened hy- poechoic colonic wall, especially in the right hemicolon. During the first days of hospital stay she was febrile (tem- perature of up to 39,6 °C) and had low blood pressure (around 90/60 mmHg). Low blood pressure returned to nor- mal after parenteral hydration. The pa- tient complained of moderate headache. After four days of antibiotic treatment with ciprofloxacin and azithromycin her inflammatory markers levels were normalized. She received antibiotics for ten days. After parenteral hydration her renal function returned to normal. Hae- mocultures remained sterile. Salmonella Chester, sensitive to all the tested anti- biotics (ampicillin, cefotaxime, ceftriax- one, ciprofloxacin, trimethoprim with sulfamethoxazole) was isolated from stool samples. Before bacteria isolation, there was suspicion of an infectious dis- ease outbreak because several family members experienced the same symp- toms. On reviewing the patient’s history we connected the outbreak of symptoms with exposure to new family pets- two yellow-necked turtles. The Regional Unit of the National Institute of Public Health was notified about the outbreak, and epidemiological monitoring was performed. 2.2. Group 2 A 4.5-year-old female (Patient 2) was admitted to hospital with a 4-day his- tory of abdominal pain, diarrhoea and high temperature. One day before the onset of diarrhoea she vomited 10 to 15 times, and then the vomiting stopped. She had up to 20 watery stools without traces of blood a day. Her body weight decreased by 0.5 kg per day. She had a temperature of up to 39.5 °C. The day before hospitalization she refused food and water intake. Her younger sister had similar symptoms, which lasted for two days; her grandmother was hospi- talized for the same symptoms (Patient 1). Her mother presented with vomiting for two days; her father was nauseous but had no other symptoms. On exami- nation the girl showed no clinical signs of dehydration; she had fever of 38.8 °C, tachycardia, and diffuse abdominal pain on palpation Laboratory tests showed el- evated C-reactive protein, hypokalaemia and dehydration. She received parenteral hydration with potassium supplements; since day two of hospitali stay her oral water intake has been sufficient. During her stay in the hospitali we once noticed a small amount of blood in her stool. Her haemocultures remained sterile. Salmo- nella Chester, sensitive to all the tested antibiotics (ampicillin, cefotaxime, cef- triaxone, ciprofloxacin, trimethoprim with sulfamethoxazole) was isolated from stool samples. The patientwas dis- charged after eight days of hospitaliza- tion. She had fever for 15 days and di- arrhoea for 16 days. Salmonella Chester persisted in stool samples of our patient and her younger sister after three and six weeks, respectively.Other family mem- bers had negative stool samples at that time. Stool samples of the affected girls were negative after nine weeks. 3. Epdemiological report After the notification of the suspect- ed infectious disease outbreak in a fam- ily, we performed an epidemiological survey following the infectious bowel on line editionAcute gastroenterocolitis caused by Salmonella Chester Short SCientifiC ArtiCle diseases protocol. Six family members, five females and one male,, aged two to 56 years were admitted to hospital. Five presented with the signs of gastroen- terocolitis (two sisters, the mother and the grandmother). Two of them, i.e. the grandmother and the granddaughter- were hospitalized. The survey showed that the affected persons lived in the same house with separate and occasionally common household. None of them worked in food industry, health, school or kinder- garten services. A few days before the onset of symp- toms they had bought two yellow- necked turtles in a pet store. They had no direct contact with turtles except when cleaning the aquarium. In view of the time course and connection between symptoms and new pets there was a high suspicion of animal-human disease transmission. We consulted the Admin- istration of the Republic of Slovenia for Food Safety, Veterinary Sector and Plant Protection (UVHVVR) and a local vet- erinary station. The local veterinarian checked the health status of turtles and sent the turtle cloaca for further testing to the Leipzig IDEXX laboratory. After receiving nega- tive cloaca results, samples of aquarium water were sent for analysis. Water sam- ples were positive for Salmonella Ches- ter. UVHVVR contacted the turtle dis- tributor and warned them about possi- ble animal-human disease transmission. Data from pet shop showed that four yellow-necked turtles of the Testudo species had been delivered to the shop in one shipment. Two buyers bought two turtles each. One buyer was the member of the diseased family. Another buyer was contacted and alerted, but never re- sponded. Cleaning and disinfection of the pet shop was performed; none of the employees fell ill. Three of the persons with symptoms (Patients 1 and 2 and the younger sister of Patient 2) had confirmed Salmonella Chester infection. 4. Discussion The literature mentions turtle meat as a reservoir for Salmonella infections. During reptile breeding their meat be- comes contaminated. It depends on the accommodation and feeding hygiene conditions. The quality of water in con- tact with the aquatic animal is also im- portant  (2). In the 1970s precautions were taken in several countries around the world to reduce the transmission of turtle-borne infections; from banning the sale of turtles as pets to testing tur- tles for the presence of bacterial coloni- sation (4). Several examples of minor epidemic outbreaks have been described in con- nection to consuming raw or poorly heat-treated meat and offal of turtles (2). An example of the transmission of Sal- monella infection from the turtle aquar- ium water was described, but the type of Salmonella was different than that in our case (1). Salmonella Chester was isolated from sea turtle meat and water in a restaurant in Australia, with 36 people infected, but the investigators were unable to connect the infections with the ingestion of turtle as the diseased had several common risk factors for the disease (2,5). In the past, Salmonella infections transmitted from pets were common, but there is no evidence in the literature that such infections were caused by Sal- monella Chester (4). Salmonellosis usually presents with gastroenterocolitis, the illness lasts three on line edition Zdrav Vestn | Maj – June 2017 | Volume 86 MetAboliC And horMonAl diSorderS to seven days, most people recover with- out specific treatment. Infection can lead to septicaemia or complications outside of the intestines. Complications are more common in people over the age of 50 years, in chil- dren under three months of age, in pa- tients with associated chronic illnesses, diabetes, artificial heart valves, artificial joints, vascular implants, in cancer pa- tients and in immunocompromised pa- tients (1,3,6). Patient 1 belonged to a group of elder- ly patients with immunodeficiency and was treated with methylprednisolone. Etiological diagnosis is based on stool sampling and cultivation, which is posi- tive in approximately 6 % of patients with acute disease (3). In our study, the diagnosis was etio- logically confirmed in three of five pa- tients. In highrisk groups of patients and/ or in patients with a severe course of the disease the treatment of infectious diar- rhoea empirically begins with one of the quinolones  (3). Patient 1 received anti- biotics because of immunodeficiency, whereas the rest of the patients had no antibiotic therapy. Because of initially etiologically unexplained diarrhoea, she was put on combination therapy with ciprofloxacin and azithromycin, as cam- pylobacters as a possible cause of gastro- enterocolitis can be resistant to cipro- floxacin (7). Empirical antibiotic therapy is con- traindicated in immunocompetent chil- dren without known pathogen isolated from stool samples because of the pos- sibility of haemolytic-uremic syndrome development  (8). Retrospective studies in children show that short-term anti- biotic therapy prolonged carrying the pathogens in stool, and is indicated only in a group of children at risk of compli- cations (6,9). In Salmonella-induced diarrhoea these pathogens can occur in stools for several weeks (in adults on average for four to five weeks and in children for up to seven weeks), which can be danger- ous when the diseased are involved in the preparation and distribution of food. The carriage lasts longer in patientstreat- ed with antibiotics. Up to 4 % of patients remain permanent carriers (3,9). Contrary to the literature data, the antibiotic-treated Patient 1 no longer excreted Salmonellas in the stool after a month. Patient 2 and her sister remained carriers after three and six weeks, respec- tively. Their stool cultures were negative for the pathogen as late as after nine weeks. In micro-epidemic outbreaks of acute gastroenterocolitis the source of infec- tion is not always obvious. Our paper demonstrates that pets can be disease carriers. The paucity of literature data strongly suggests that these diseases are commonly overlooked. References 1. Nagano N, Oana S, Nagano Y, Arakawa Y. A severe Salmonella enterica serotype Paratyphi B infection in a child related to a pet turtle, Trachemys scripta elegans. Japanese journal of infectious diseases. 2006;59(2):132–4. 2. Magnino S, Colin P, Dei-Cas E, Madsen M, McLauchlin J, Nöckler K, et al. Biological risks associated with consumption of reptile prod- ucts. International Journal of Food Microbiology. 2009;134(3):163–75. 3. Logar M, Zakotnik B. Infekcijska driska. In: Tomažič J, Strle F, ur. Infekcijske bolezni, 1.ponatis. Ljubljana: Združenje za Infektologijo, Slovensko zdravniško društvo; 2014/2015. p.335–43. 4. Bowering DJ, Jessop J, Black W. Human salmonel- losis and pet turtles. Canadian family physician Medecin de famille canadien. 1987;33:1265–8. 5. O’Grady KA, Krause V. An outbreak of salmonel- losis linked to a marine turtle. The Southeast Asian journal of tropical medicine and public health. 1999;30(2):324–7. on line editionAcute gastroenterocolitis caused by Salmonella Chester Short SCientifiC ArtiCle 6. Guarino A, Ashkenazi S, Gendrel D, Lo Vecchio A, Shamir R, Szajewska H. European Society for Pediatric Gastroenterology, Hepatology, and Nu- trition/European Society for Pediatric Infectious Diseases Evidence-Based Guidelines for the Man- agement of Acute Gastroenteritis in Children in Europe. Journal of Pediatric Gastroenterology and Nutrition. 2014;59(1):132–52. 7. Adedayo O, Kirkpatrick BD. Campylobacter jejuni infections: Update on presentation, diagnosis and management. Hospital Physician. 2008;44:9–15. 8. Fleisher G. Evaluation of diarrhea in children. In: Uptodate 2015, Teach SJ, Duryea TK (Ed), Upto- date, Waltham, MA, 2015. 9. Hohmann EL. Approach to the patient with nonty- phoidal Salmonella in a stool culture. 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