Epidemiological Distribution of Rodents As Potent Reservoirs For

Infectious Disease Reports 2017; volume 9:6900

Epidemiological distribution of rodents in the three provinces were identi- of rodents as potent reservoirs fied as Rattus (R.) norvegicus (67.3%), R. rat- Correspondence: Hossein Nahrevanian, tus (13.6%), Apodemus sylvaticus (13.9%), Department of Parasitology, Pasteur Institute for infectious diseases in the Arvicola (1%), Mus musculus (0.3%), of Iran, Tehran, Iran. provinces of Mazandaran, Gilan Nesokia indica (2.5%), Cricetulus migrates Tel./Fax: +98.21.66968855. and Golestan, northern Iran (0.7%) and Rhombomys opimus (0.7%). The E-mail: [email protected] results of this study determined the geographic distribution of the rodents in the three Key words: Rodents; Iran; Infectious Disease; 1 Reservoir; Mazandaran; Gilan; Golestan. Behzad Esfandiari, northern provinces of Iran. It is indicated the 2 Hossein Nahrevanian, association of various distribution and diver- 3 Acknowledgments: this study was supported Mohammad Reza Pourshafie, sity of rodents with provincial location. The 4 by Pasteur Institute of Iran, in collaboration Mohammad Mehdi Gouya, overall distribution frequency of eight genera with the Microbiology Department, Razi 5 1 Pejvak Khaki, Ehsan Mostafavi, of rodents was recognized in the above three Vaccine and Serum Research Institute, Karaj, Jamshid Darvish,6 Hamed Hanifi1 provinces geographical locations. This study Iran and the Centre for Diseases Control and 1Department of Epidemiology and confirms epidemiological distribution of var- Prevention, Ministry of Health, Tehran, Iran. ious rodents as potent reservoirs for infec- Results presented in this article are part of a Biostatistics, 2Department of tious diseases, such as leptospirosis, salmo- PhD thesis (Behzad Esfandiari) from the Parasitology, 3Department of nellosis, tularemia, leishmaniasis, etc. in the Pasteur Institute of Iran, Tehran, Iran under Bacteriology, Pasteur Institute of Iran, three provinces. the second and third authors’ supervision. Tehran; 4Centre for Diseases Control and Prevention, Ministry of Health, Contributions: HN, MRP, study concept and Tehran; 5Department of Microbiology, design; BE, HH, field sampling; EM, analysis and interpretation of data; MMG, field man- Razi Vaccine and Serum Research Introduction agement; PK, laboratory diagnosis; JD, roden- Institute, Agricultural Research, Rodents are mammals of the order tology. All authors read and approved the final Education and Extension Organization manuscript. 6 Rodentia. Order of rodents comprises more only (AREEO), Karaj; Department of than 2000 species and approximately 30 Conflict of interest: the authors declare no Biology, Ferdowsi University families.1 There are many biological and eco- potential conflict of interest. of Mashhad, Iran logical differences among rodents. Many variations are observed in shape, sizeuse and Funding: this work was entirely supported by weight of them; whereas the smallest rodents the Pasteur Institute of Iran, (Project No. 739). (mice), weighing 5 grams and the largest 1 Abstract rodent, weighing more than 70 kg. Some Received for publication: 22 September 2016. species live above the trees while others live Revision received: 10 November 2016. underground and are rarely out of the Accepted for publication: 30 January 2017. Rodents are mammals that comprise ground. Some of the rodents are dependent more than 2000 species and approximately 30 on the water and they live behind the water, This work is licensed under a Creative families. There are many morphological and while others are accustomed to living in dry Commons Attribution-NonCommercial 4.0 International License (CC BY-NC 4.0). ecological differences among them as varia- and desert areas. The different behaviors tions in their shape, size, weight and habitat. observed among various rodents, particularly ©Copyright B. Esfandiari et al., 2017 In addition to significant economic losses, various and different motor behaviors and Licensee PAGEPress, Italy rodents have a major role in the dissemination characteristicscommercial such as jumping, climbing, Infectious Disease Reports 2017; 9:6900 of infectious diseases caused by viruses, bac- swimming, running, fast movements, dig- doi:10.4081/idr.2017.6900 teria, parasites or other micro-organisms. ging and moving underground. Also, there Rodents are important reservoirs of diseases are different systems in rodents in terms of which have been observed in many cities of social life. Rodents are able to eat a variety of Iran provinces especially along CaspianNon Sea foods, including animal and plants such as estimated that each year, approximately 20 border to Alborz Mountain. The aim of this roots, stems, bark, leaves, fruits and seeds of percent of the world’s food supply is con- study is to assess the geographical distribu- plants, insects and small creatures, and even sumed or damaged by rodents.5,6 According tion of rodents in three provinces of northern rodent droppings and other animals. They to the World Health Organization (WHO) part of Iran as reservoir of potential endemic play a special role in the chain in natural report, about 3 million tons of food (5% of infectious diseases. Rodents in 10 major parts communities; they are considered as food for the total global food production) annually of each of the three provinces of Mazandaran, many species of predators and on the other destroyed by mice that will be adequate to Gilan and Golestan, northern Iran were col- hand, by feeding on small creatures such as feed 130 million hungry people.7 lected and a total of 404 rodents were trapped insects and arthropods, they control their Diseases carried by rodents include viral, alive. They were determined by the key char- populations.1,2 Rats by feeding on crops, live- bacterial, parasitic infections.5,8 The disease acteristics such as gender, genus, species, dif- stock, stored grains and foods can cause loss can be transmitted to humans in a number of ferent locations and topological situation. of economic resources and also by chewing ways including animal bite, contact with ani- Statistical analysis was performed to charac- wires and telephone and damaging to electri- mal waste, eating food or water contaminat- terize the study sample and to correlate all cal appliances, they expose installations and ed by rodent waste or through parasites that variables and parameters. The distribution houses to great risks.3,4 Rodents can do dam- use rodents and humans as hosts e.g. fleas frequencies of three, five and six genera of age to products in a wide range, before and and ticks.9,10 rodents were identified in Mazandaran, Gilan after harvest. In addition to significant eco- Rats are potential important reservoirs and Golestan provinces respectively. The nomic losses, rodents have a major role in of infectious disease from human in Iran.3 overall distribution frequency of eight genera the dissemination of infectious diseases. It is Due to the spread of these diseases there is

[page 62] [Infectious Disease Reports 2017; 9:6900] Article a strengthen fight against rats.11 Iran, lying tail, claw, fur, nose, vibrissa, digit and aimed to correlate all statistical variables on the crossroad of several biogeographic pinna. and parameters. regions, supports a diverse mammal fauna. More than 79 rodent species have been 12 Data analysis recorded from Iran (38.2% of species). Statistical analysis was performed in Three species of the genus Rattus Fisher, two stages using SPSS version 17. The first Results 1803 have been reported from Iran: R. was a descriptive which aimed to character- The distribution frequency of three gen- norvegicus (brown rat, Berkenhout, 1769) , R. rattus (black rat, Linnaeus, 1758) and R. ize the study sample. The second stage was era of rodents identified in Mazandaran pyctoris (Himalayan rat, Hodgson, 1845) The first two species of Rattus genre have a worldwide distribution. The brown rat has also moved from central Asia to the border of the Caspian Sea and to Gorgan and Rasht cities in the north.13 There are numerous cytogenetic studies about Black rats. These studies indicate the value of diversity chro- mosomes within this genus.14 Rodents are reported to be almost one third of the species of mammals in Iran.1,2 The temper- ate and humid climate ranges from the plains along Caspian Sea border to northern foothills of Alborz Mountainin Iran. In this region, rice planting is the predominant occupation and the most peasants are farm- only ers and keep one or more livestock in their houses. In mentioned region, surface waters or rivers are mainly used for agriculture.3 The aim of this paper is to assess the geo- use graphical and epidemiological distribution of various rodents as potential reservoirs and vector for human infectious diseases in the three provinces of Mazandaran, Gilan and Golestan, northern Iran (Middle East – Asian region).

Materials and Methods

Study area and sample collection commercial This study was performed during the summer of 2013 close to Caspian sea (Latitude 41°N and Longitude 50°E; the average altitude above sea levelNon is 1305 m/4281 ft) in three northern provinces of Iran, Mazandaran Province (Sari, Nour and Figure 1. Map of study area in the three provinces of Mazandaran, Gilan and Golestan, Noshahr districts), Gilan Province northern Iran. (Roodsar, Langerood, Lahijan, Rasht, Fooman, Some’esara, Masouleh, Bandar Table 1. The genus and number of the rodents in three northern provinces of Iran. Anzali, Talysh and Astara) and Golestan Rodent species Mazandaran Gilan Golestan Total Province (Gorgan, Kordkuy, Kohneh, Azadshahr, MinooDasht, Kalaleh, Rattus norvegicus 116 102 54 272 GonbadKavoos, Maraveh Tappeh, Incheh Rattus rattus 9 32 14 55 Boroun and Bandar Torkaman). In this Apodemus sylvaticus 26 12 18 56 study, active colonies of rodents in 10 major Arvicola spp. 0 4 0 4 parts of each of the three provinces and a total of 404 rodents were trapped alive Mus musculus 0 1 0 1 (Figure 1). They were determined and cate- Nesokia indica 0 0 10 10 gorized by the key characteristics such as Cricetulus migratus 0 0 3 3 gender, genus, species, different locations, Rhombomys opimus 0 0 3 3 topological situation and morphological Total 151 151 102 404 characters including the shape and size of

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Province were Rattus (R.) norvegicus biological vectors including Colorado Tick rative study on diagnosis of rodent lep- (76.8%), R. rattus (6.0%) and Apodemus Fever, Leishmaniasis, Anaplasmosis, La tospirosis in Mazandaran Province, (A.) sylvaticus (17.2%). Moreover, five gen- Crosse Encephalitis, Lyme Disease, Murine northern Iran. Epidemiol Health era of rodents were recognized in Gilan Typhus, Omsk Hemorrhagic Fever, 2015;37:e2015012. Province as R. norvegicus (67.5%), R. rat- Powassan Virus, Scrub Typhus, Rickettsial 4. Tobin ME, Fall MW. Pest control: tus (21.2%), A. sylvaticus (7.9%), Arvicola pox, Relapsing Fever, Rocky Mountain rodents. USDA National Wildlife spp. (2.6%) and Mus musculus (0.7%) and Spotted Fever, Sylvatic Typhus, Tularemia, Research Center-Staff Publications. finally six genera of rodents were reported Plague and West Nile Encephalitis (see 2004:67. in Golestan Province as R. norvegicus Appendix).9,15-17 5. Meerburg BG, Singleton GR, Kijlstra (54%), R. rattus (13.7%), A. sylvaticus There are several reports indicating the A. Rodent-borne diseases and their (17.6%), Nesokia indica (9.8%), Cricetulus potential important role of synanthropic risks for public health. Critic Rev migrates (2.9%) and Rhombomys opiimus rodents as key reservoirs of several infec- Microbiol 2009;35:221-70. (2.9%) (Table 1). tious diseases in Iran. According to 6. Ehrlich PR, Ehrlich AH, Daily GC. The overall distribution frequency of Wikipedia, 2017 the major rodents Genera Food security, population and environ- eight genera of rodents in the three reported in Iran are Hystrix, Sciurus, ment. Pop Develop Rev 1993:1-32. provinces of Mazandaran, Gilan and Spermophilopsis, Spermophilus, Castor, 7. Von der Weid D, Dillon J, Falquet J. Golestan were identified as R. norvegicus Dryomys, Myomimus, Glis, Allactaga, Malnutrition: a silent massacre. (67.3%), R. rattus (13.6%), Apodemus syl- Pygeretmus, Dipus, Jaculus, Spalax, Geneva: Antenna Technologies; 2000. vaticus (13.9%), Arvicola (1%), Mus mus- Calomyscus, Cricetulus, Mesocricetus, 8. Waugh CA, Lindo JF, Foronda P, et al. culus (0.3%), Nesokia indica (2.5%), Arvicola, Blanfordimys, Ellobius, Microtus, Population distribution and zoonotic Cricetulus migrates (0.7%) and Acomys, Gerbillus, Meriones, Rhombomys, potential of gastrointestinal helminths Rhombomys opimus (0.7%) (Table 1). Apodemus, Golunda, Mus, Nesokia and of wild rats Rattus rattus and R. Rattus. The main infectious diseases were norvegicus from Jamaica. J Parasitol transmitted by rodents reported to be 2006;92:1014-8. Leptospirosis, Tularemia, Plague, 9. Bitamonly I, Dittmar K, Parola P, et al. Fleas Discussion and Conclusions Leishmaniasis, leprosy, Tuberculosis, Rat- and flea-borne diseases. J Infect Dis bite fever, Cryptosporidiosis, 2010;14:e667-76. Echinococcosis and several Ectoparasites, The results of this study determined the 10. Han BA, Schmidt JP, Bowden SE, et al. Endoparasitic protozoa and helminthes. geographic distribution of the rodents in the Rodent reservoirs of future zoonotic Major infectious diseases which are trans-use three Northern provinces of Iran. It is indi- diseases. Proc Natl Acad Sci USA mitted by rodents have been almost cated the association of various distribution 2015;112:7039-44. observed in almost entire provinces of and diversity of rodents with provincial 11. Pourmohammadi B, Motazedian M, Iran.18-21 Therefore, the issue in the fight location. The distribution frequencies of Kalantari M. Rodent infection with against rodents has become more important three, five and six genera of rodents were Leishmania in a new focus of human than past. Iran, lying on the crossroad of identified in Mazandaran, Gilan and cutaneous leishmaniasis, in northern several bio-geographic regions, supports a Golestan provinces respectively. The over- Iran. Ann Trop Med Parasitol diverse mammal fauna. Due to the wide all distribution frequency of eight genera of 2008;102:127-33. variety of climate and abundance of differ- rodents was recognized in the above three 12. Karami M, Hutterer R, Benda P, et al. ent species of domestic and wild rodents in provinces geographical locations. The Annotated check-list of the mammals of Iran, consistent study is essential to monitor major rodents were reported as R. norvegi- Iran. Lynx (Praha) 2008;39:63-102. the status of density, mobility and variety of cus (67.3%), R. rattus (13.6%) and A. syl- 13. Jalal R, Darvish J, Moghaddam Matin rodentscommercial population. Identification of habi- vaticus (13.9%). These data is supported by M. Identification of three Iranian tats and faunistic composition of these ani- previous report indicated more than 79 species of the genus Rattus (Rodentia, mals should always be considered as a tool rodent species have been recorded from Muridae) using a PCR-RFLP technique to control the rodents. Awareness of local Iran earlier.12 Three species of the genus on mitochondrial DNA. Hystrix-Ita J people about the harmful effects of rodents Rattus have been reported from Iran: R. Mammal 2009;20. Nonis recommended for public health educa- norvegicus, R. rattus and R. pyctoris. The 14. Steen RG, Kwitek-Black AE, Glenn C, tion. Moreover, local health authorities brown rat has also moved from central Asia et al. A high-density integrated genetic should identify the major points of presence to the border of the Caspian Sea and to linkage and radiation hybrid map of the of rodents and activate specific control pro- Gorgan and Rasht cities in the north.13 laboratory rat. Genom Res 1999;9:AP1- grams through the use of anticoagulant According to Centers for Diseases 8. baits. Control and Prevention (CDC), there are 15. Centers for Diseases control and several diseases directly transmitted by Prevention. Diseases from rodents. rodents including Hemorrhagic fever with 2015. Available from: Renal Syndrome, Lassa fever, http://www.cdc.gov/rodents/diseases/in Leptospirosis, Lymphocytic Chorio-menin- References direct.html. gitis (LCM), Omsk Hemorrhagic Fever, 1. Kay EH, Hoekstra HE. Rodents. Curr 16. Helhazar M, Leitão J, Duarte A, et al. Rat-Bite Fever, Salmonellosis, South Biol 2008;18:R406-10. Natural infection of synathropic rodent American Arenaviruses (Argentine hemor- 2. Kumawat M, Singh K, Sen D, et al. species Mus musculus and Rattus rhagic fever, Bolivian hemorrhagic fever, Threatened rodent species of Arunachal norvegicus by Leishmania infantum in Sabiá-associated hemorrhagic fever, Pradesh. Int J Agricult Envir Biotechnol Sesimbra and Sintra-Portugal. Parasit Venezuelan hemorrhagic fever) and 2013;6:657-68. Vector 2013;6:88. Tularemia. In addition, several diseases are 3. Esfandiari B, Pourshafie MR, Gouya 17. Bonnefoy X, Kampen H, Sweeney et al. also indirectly transmitted by rodents with MM, et al. An epidemiological compa- Public health significance of urban

[page 64] [Infectious Disease Reports 2017; 9:6900] Article

pests. Copenhagen: World Health Rodent Coprolites Dated At 500 CE Parasitol 2014;9:548-52. Organization-Regional Office for Sassanid Era in Archeological Site of 21. Yousefi A, Eslami A, Mobedi I, et al. Europe; 2008. 569 pp Chehrabad (Douzlakh), Salt Mine Helminth infections of house mouse 18. Nateghpour M, Motevalli-Haghi A, Northwestern Iran. Iran J Parasitol (Mus musulus) and wood mouse Akbarzadeh K, et al. Endoparasites of 2014;9:188-93. (Apodemus sylvaticus) from the Wild Rodents in Southeastern Iran. J 20. Meshkekar M, Sadraei J, Arthropod Borne Dis 2014;9:1-6. Mahmoodzadeh A, et al. Helminth Suburban Areas of Hamadan City, 19. Mowlavi G, Makki M, Mobedi I, et al. Infections in Rattus ratus and Rattus Western Iran. Iran J Parasitol Paleoparasitological Findings from norvigicus in Tehran, Iran. Iran J 2014;9:511-8.

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