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There are few studies about the presence of murine typhus in Greece. Our objective was to conduct a large scale retrospective investigation to determine the clinical and epidemiological features of patients diagnosed with murine typhus in Greece. From to serum samples from hospitalized patients and outpatients throughout Greece suspected for murine typhus infection were tested by immunofluorescence assay for Rickettsia typhi. Immunofluorescence positive samples obtained since were also tested by qPCR targeting R. Clinical and epidemiological data were retrospectively collected for the patients with confirmed murine typhus. Overall, we tested 5, different patients and, in total, patients from all geographic regions of Greece were diagnosed with murine typhus. Severe infections with complications including acute renal failure or septic shock were not recorded. Our results may reflect the reemergence of murine typhus in Greece and we highlight the importance of awareness of this difficult-to-recognize undifferentiated febrile illness. Murine typhus, a febrile disease caused by Rickettsia typhi , is often misdiagnosed due to its non-specific presentation. Evidence suggests that murine typhus is more prevalent in Greece than originally believed. We retrospectively collected clinical and epidemiological data for all the patients with confirm and probable murine typhus diagnosed in our laboratory the last eight years and we found evidence of murine typhus throughout Greece. Comparing this evidence to other studies, we found that most of Greek patients presented rash and the typical triad probably due to the awareness of physicians, as during our interrogation, most of physicians mentioned that they considered murine typhus based on rash appearance. Finally, we found that most murine typhus cases in the city of Athens were associated with sunbathing on the beach and we raise the question of beach littering in murine typhus endemic areas. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Competing interests: The authors have declared that no competing interests exist. Murine typhus, an acute zoonotic infection caused by Rickettsia typhi , is transmitted to humans by Xenopsylla cheopis , a flea that infests rats \\\\\\\\\\\\\[ 1 \\\\\\\\\\\\\]. The emergence of murine typhus has become apparent mostly in the field of travel medicine, as increasing numbers of individuals are being exposed \\\\\\\\\\\\\[ 2 , 3 \\\\\\\\\\\\\]. Indeed, the 2. The clinical features of murine typhus are non-specific and include fever, rash, headache, myalgia and gastrointestinal symptoms \\\\\\\\\\\\\[ 5 , 6 \\\\\\\\\\\\\]. While the clinical course of murine typhus is typically uncomplicated, serious complications have been associated with acute infections, such as central nervous system abnormalities. Murine typhus was first described in Greece in and, in , 1, cases of murine typhus and 17 deaths were reported \\\\\\\\\\\\\[ 8 \\\\\\\\\\\\\]. Since then, the disease is considered endemic on the Greek islands of Crete \\\\\\\\\\\\\[ 9 \\\\\\\\\\\\\] and Euboea \\\\\\\\\\\\\[ 10 \\\\\\\\\\\\\] whereas sporadic cases have been reported in northern Greece \\\\\\\\\\\\\[ 11 \\\\\\\\\\\\\] and in the island of Kasos \\\\\\\\\\\\\[ 12 \\\\\\\\\\\\\]. Because of murine typhus nonspecific clinical presentation and the lack of awareness by physicians we raised the question of the under-diagnosis of R. As a reference laboratory for the diagnosis of rickettsial infections in Greece, we routinely receive serum samples from patients suspected of having murine typhus. To gain a better understanding of murine typhus in Greece, we retrospectively collected clinical and epidemiological data for all the patients diagnosed with R. This study is based on routine diagnosis samples. We studied serum samples from patients with suspected murine typhus that were sent to our laboratory from January to December We received sera from hospitalized patients and outpatients with suspected rickettsioses throughout Greece. For each patient, an acute-phase serum sample was obtained within three weeks after the onset of symptoms and, when possible, a convalescent-phase serum sample i. Clinical data, medical history and complications during illness, habitat and environmental characteristics, presence of pets, livestock, or rodents, daily activities in the 30 days before symptom onset and travel during the previous one month were documented with structured conversations for R. The density of R. The supernatants of 15 flasks were pelleted by centrifugation at g for 15 min and resuspended in 1 mL of phosphate-buffered saline PBS at pH 7. Cells were fragmented by sonication, and cellular debris was removed by two successive centrifugations g, 10 min each. Positive and negative controls were diluted at and Sera found positive against R. Finally, to exclude false-positive results due to cross-reactivity between R. When cross-reactions were observed, a rickettsial antigen was considered to represent the infectious agent if cumulated titres of IgG and IgM antibodies against this antigen were at least twice as high as those of the others. All reactions were performed in dark room and at least two people performed each microscopical examination. Total genomic DNA was retrospectively extracted from samples obtained from to with a positive R. Samples were handled under sterile conditions to avoid cross-contamination. Samples were screened by qPCR targeting a fragment of the Rpr P gene coding for a hypothetical protein, as described previously \\\\\\\\\\\\\[ 15 \\\\\\\\\\\\\]. Positive results were confirmed by qPCR targeting the glycosyltransferase gene using a previously described Rpr system \\\\\\\\\\\\\[ 15 \\\\\\\\\\\\\]. The quality of DNA handling and extraction of human samples was verified by qPCR for a housekeeping gene encoding beta-actin \\\\\\\\\\\\\[ 10 \\\\\\\\\\\\\]. EpiInfo version 6. The Mantel-Haenszel test or the Fisher exact test was used to test for significance. We tested 5, different sera obtained from 5, patients and we identified patients positive by IFA Table 1. Indeed, 11 acute and 1 convalescent-phase sera were positive by qPCR. For two patients qPCR was positive although serology was negative Table 2. As a result, in total we diagnosed 98 confirmed and 76 probable patients with murine typhus. Overall, we found autochthonous murine typhus patients whereas two patients reported a recent travel to Cyprus and one had recently returned from Uruguay. Finally, two patients reported a recent travel to Cyprus and one had recently returned from Uruguay. A, Murine typhus patients throughout Greece; B, Seasonal distribution of patients diagnosed for murine typhus, in Greece and in Athens, — Red stars: present murine typhus cases. Blue stars: previous murine typhus reported cases based on the researched of PubMed for peer-reviewed, articles published in English up to June Positive murine typhus cases were plotted for each month to identify seasonal distributions from through Fig 1B. The seasonality of murine typhus cases slightly differed for Athens than for other regions, as all cases were observed from April through October Fig 1B. Epidemiological information was obtained for 43 patients and eight reported a recent travel in Greece outside Athens whereas three reported a travel abroad. None of these patients mentioned a direct contact with rodents. This high percentage of hospitalization is probably because we obtained clinical data mostly from patients who had previously presented to hospitals. All hospitalized patients presented pulmonary manifestations including pneumonia or pulmonary infiltrates. Finally, severe infections with complications including acute renal failure or septic shock were not recorded. We report a large series of R. Our immunofluorescence and molecular assays were sensitive and versatile and have been routinely used for the detection and diagnosis of murine typhus \\\\\\\\\\\\\[ 13 — 15 \\\\\\\\\\\\\]. Furthermore, we routinely included large numbers of negative controls in our assays that were processed identically to the test samples. Serological tests are the easiest methods for the diagnosis of R. We detected two samples positive by qPCR but negative by IFA and a limitation of our study was that samples were retrospectively tested using molecular assays as we have managed to test only immunofluorescence positive samples since Indeed, it is very possible that this number could be higher if sera were routinely tested by qPCR on the basis of both clinical and epidemiology data also. Finally, we cannot exclude that some patients were false-positive diagnosed with murine typhus before as only samples after were also tested for SFG rickettsioses. Previously in Greece, R. Although autochthonous cases of murine typhus have not been described in the countries of North Europe, sporadic cases are commonly identified in travelers who visited endemic areas \\\\\\\\\\\\\[ 7 , 15 , 20 \\\\\\\\\\\\\]. In Cyprus although to date many cases of murine typhus have been described, the first confirmed case was reported in a Swedish woman who developed fever, severe headache, myalgia and rash, three weeks after a visit to Cyprus \\\\\\\\\\\\\[ 21 \\\\\\\\\\\\\]. The diagnosis of murine typhus has been characterized as a challenge because many physicians are unfamiliar with the nonspecific symptoms during the early stages of illness. Similarly, in previous studies the typical triad for murine typhus occurred in less than half of the patients \\\\\\\\\\\\\[ 6 , 7 , 22 \\\\\\\\\\\\\]. In our study, most of patients presented rash and the typical triad. We believe that this higher rate of rash as a symptom is due to the awareness of physicians, as during our interrogation, most of physicians mentioned that they considered murine typhus based on rash appearance. Our findings show that the number of murine cases in Greece varies by season. In studies where seasonal variation was recorded, at least half of cases were diagnosed during summer and early autumn \\\\\\\\\\\\\[ 6 , 15 \\\\\\\\\\\\\]. A similar seasonality was also previously described in Greece where most cases occurred during summer with a peak on the late summer \\\\\\\\\\\\\[ 10 \\\\\\\\\\\\\]. In other studies, the highest incidence was observed in May and June \\\\\\\\\\\\\[ 23 , 24 \\\\\\\\\\\\\] suggesting that climatic conditions are the main factors contributing to different seasonal distributions of human cases in different geographical areas. Human infection with murine typhus has been associated with the presence of rats and their fleas. This probably explains the two seasonal peaks during June and September that we observed due to the higher abundance of X. Surprisingly we observed that most cases of murine typhus in Athens were associated with sunbathing on the beach. As the most of the reported human cases of murine typhus have been associated in sites with large rat populations we believe that during summer rats infest beach environments probably because of littering and humans are infected by the rat fleas while sunbathing Fig 2. Although adult X. Indeed unfed adult X. Survival of X. In conclusion, we provide evidence that R. Our data affect local practice as we found that physicians consider murine typhus mostly when rash is presented. Murine typhus cases are frequently described to travelers visiting Greece \\\\\\\\\\\\\[ 4 , 7 \\\\\\\\\\\\\] and although further work needs to be done to confirm our hypothesis, we believe that some of the travelers are possibly infected on the beach environments considering that tourists spend most of their time on the beach side. Finally, we raise the question of beach littering in murine typhus endemic areas as it is associated with increased rodent populations and as a consequence increased risk of infection by R. Abstract Background There are few studies about the presence of murine typhus in Greece. Author summary Murine typhus, a febrile disease caused by Rickettsia typhi , is often misdiagnosed due to its non-specific presentation. Data Availability: All relevant data are within the manuscript. Funding: The author s received no specific funding for this work. Introduction Murine typhus, an acute zoonotic infection caused by Rickettsia typhi , is transmitted to humans by Xenopsylla cheopis , a flea that infests rats \\\\\\\\\\\\\[ 1 \\\\\\\\\\\\\]. Materials Ethics statement This study is based on routine diagnosis samples. Patients We studied serum samples from patients with suspected murine typhus that were sent to our laboratory from January to December Molecular assays Total genomic DNA was retrospectively extracted from samples obtained from to with a positive R. Statistical analysis EpiInfo version 6. Results We tested 5, different sera obtained from 5, patients and we identified patients positive by IFA Table 1. Download: PPT. Table 1. Rickettsia typhi results of serology and PCR assays. Table 2. IF assay antibody titers for the confirmed murine typhus patients. Geographical distribution of cases and epidemiological data Overall, we found autochthonous murine typhus patients whereas two patients reported a recent travel to Cyprus and one had recently returned from Uruguay. Seasonality Positive murine typhus cases were plotted for each month to identify seasonal distributions from through Fig 1B. Discussion We report a large series of R. References 1. Murine typhus, Reunion, France, — Emerg Infect Dis ;— Murine typhus as a cause of Fever in travelers from Tunisia and mediterranean areas. J Travel Med ;— Rickettsioses and Q fever in travelers — Travel Med Infect Dis ;— Multicenter GeoSentinel analysis of rickettsial diseases in international travelers, — Flea-Borne Rickettsioses and Rickettsiae. Am J Trop Med Hyg ;— Clinical and laboratory characteristics, epidemiology, and outcomes of murine typhus: A systematic review. Acta Trop ;— Typhus Group Rickettsiosis, Germany, 1. Dimissas KA. Epidemic diseases trasmitted by instects; , pp — View Article Google Scholar 9. Murine typhus in elderly patients: a prospective study of 49 patients. Scand J Infect Dis ;— Murine typhus in central Greece: epidemiological, clinical, laboratory, and therapeutic-response features of 90 cases. Int J Infect Dis ;e—e Jpn J Infect Dis ;— Case Rep Med ; Comparison of real-time quantitative PCR and culture for the diagnosis of emerging Rickettsioses. Detection of rickettsioses and Q fever in Sri Lanka. Murine typhus in returned travelers: a report of thirty-two cases. Murine typhus as a common cause of fever of intermediate duration: a year study in the south of Spain. Arch Intern Med ;— Murine typhus in Cyprus: a 9-year survey. Current knowledge of rickettsial diseass in Italy. Ann N Y Acad Sci ;— Epidemiological features of Mediterranean spotted fever, murine typhus, and Q fever in Split-Dalmatia County Croatia , — Epidemiol Infect ;— Seek and Find! PCR analyses of skin infections in West-European travelers returning from abroad with an eschar. Strand O, Stromberg A. Ciprofloxacin treatment of murine Typhus. Emergence of murine typhus in La Reunion, France, — Med Mal Infect ;— Trends in clinical diagnoses of typhus group rickettsioses among a large U. Zoonoses Public Health Effect of temperature and relative humidity on the development times and survival of Synopsyllus fonquerniei and Xenopsylla cheopis , the flea vectors of plague in Madagascar. Parasit Vectors ; Burroughs AL. Sylvatic plague studies. Survival of rodent fleas in the laboratory. Parasitology ;—

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