LETTERS

4°75′Ε) during May–June 2010. All 2. Fijan N, Matasin Z, Petrinec Z, Val- Rift Valley and larvae were euthanized as part of an potiç I, Zwillenberg LO. Isolation of an iridovirus-like agent from the green frog West Nile Virus invasive species eradication project (Rana esculenta L.). Vet Arch Zagreb. and stored at –20°C until further 1991;3:151–8. Antibodies use. At necropsy, liver tissues were 3. Cunningham AA, Langton TES, Bennet in Camels, collected, and DNA was extracted PM, Lewin JF, Drury SEN, Gough RE, et al. Pathological and microbiological North Africa by using the Genomic DNA Mini fi ndings from incidents of unusual mor- Kit (BIOLINE, London, UK). PCR tality of the common frog (Rana tempo- To the Editor: Different to detect ranavirus was performed as raria). Philos Trans R Soc Lond B Biol arboviral diseases have expanded described by Mao et al. (10). Sci. 1996;351:1539–57. doi:10.1098/ rstb.1996.0140 their geographic range in recent times. Three samples showed positive 4. Hyatt AD, Gould AR, Zupanovic Z, Of them, Rift Valley fever, West Nile results with this PCR. These samples Cunningham AA, Hengstberger S, Whit- fever, and African horse sickness were sequenced by using primers tington RJ, et al. Comparative studies of are of particular concern. They are M4 and M5 described by Mao et al. piscine and amphibian iridoviruses. Arch Virol. 2000;145:301–31. doi:10.1007/ endemic to sub-Saharan Africa but (10) and blasted in GenBank. A 100% s007050050025 occasionally spread beyond this area. homology with the common midwife 5. Balseiro A, Dalton KP, Del Cerro A, Mar- Trade and transport of animals and toad (A. obstetricans) ranavirus partial quez I, Cunningham AA, Parra F, et al. animal products, along with wildlife major capsid protein gene (GenBank Pathology, isolation and molecular char- acterisation of a ranavirus from the com- movements, are considered the accession no. FM213466.1) was mon midwife toad Alytes obstetricans on driving factors in the spread of these found (5). Despite the low prevalence the Iberian Peninsula. Dis Aquat Organ. pathogens. of Ranavirus infection (0.75%) in 2009;84:95–104. doi:10.3354/dao02032 In wide regions of Africa, the bullfrog tadpoles examined, this 6. Ficetola GF, Coic C, Detaint M, Berro- neau M, Lorvelec O, Miaud C. Pattern 1-humped camels (Camelus study shows that invasive bullfrogs, a of distribution of the American bullfrog dromedarius) are valuable livestock known reservoir of chytridiomycosis, Rana catesbeiana in Europe. Biol In- appreciated as a meat source and as are also a likely carrier of ranaviral vasions. 2007;9:767–72. doi:10.1007/ a means for transportation of goods. disease in Europe. s10530-006-9080-y 7. Schloegel LM, Ferreira CM, James TY, Camels are susceptible to infection by Hipolito M, Longcore JE, Hyatt AD, et al. Rift Valley fever virus (RVFV), West This study was partly performed The North American bullfrog as a reser- Nile virus (WNV), and African horse in the framework of European Union voir for the spread of Batrachochytrium sickness virus (AHSV), although their Interreg IVA project IVA-VLANED-2.31 dendrobatidis in Brazil. Anim Conserv. epidemiologic role in these diseases is “Invasieve exoten in Vlaanderen en Zuid- 2010;13(S1):53–61. doi:10.1111/j.1469- 1795.2009.00307.x uncertain (1–3). Movements of camels Nederland–INVEXO.” 8. Daszak P, Strieby A, Cunningham AA, across the Sahara Desert could carry Longcore JE, Brown CC, Porter D. Ex- these pathogens to northern Africa. To Mojdeh Sharifi an-Fard, perimental evidence that the bullfrog (Rana catesbeiana) is a potential carrier test this hypothesis, we conducted a Frank Pasmans, of chytridiomycosis, an emerging fungal serologic survey in 1-humped camels Connie Adriaensen, disease of amphibians. Herpetolog J. intercepted at different points by the Sander Devisscher, 2004;14:201–7. Moroccan Veterinary Services in Tim Adriaens, Gerald Louette, 9. Miller DL, Gray MJ, Rajeev S, Schmutzer AC, Burton EC, Merril A, et al. Pathologi- 2009. The camels were coming from and An Martel cal fi ndings in larval and juvenile anurans the southeastern part of the Sahara Author affi liations: Ghent University, inhabiting farm ponds in Tennessee, USA. Desert going to the northwest. Merelbeke, Belgium (M. Sharifi an-Fard, F. J Wildl Dis. 2009;45:314–24. 10. Mao J, Hedrick RP, Chichar VB. Molecu- Serum samples were obtained Pasmans, C. Adriaensen, A. Martel); and lar characterization, sequence analysis, in Smara-Laayoune, Dakhla, and Research Institute for Nature and Forest, and taxonomic position of newly isolated Tata (Table). Most samples (71 of Brussels, Belgium (S. Devisscher, T. fi sh iridoviruses. Virology. 1997;229:212– 100 total samples) were from male Adriaens, G. Louette) 20. doi:10.1006/viro.1996.8435 camels. Samples were also grouped by age of the camels (Table). RVFV DOI: http://dx.doi.org/10.3201/eid1712.110236 Address for correspondence: An Martel, antibodies were detected by using a Department of Pathology, Bacteriology and competitive ELISA (4), and samples References Avian Diseases, Faculty of Veterinary Medicine, yielding positive ELISA results were Ghent University, Salisburylaan 133, B-9820 1. Ariel E, Kielgast J, Svart HE, Larsen K, confi rmed by virus-neutralization Tapiovaara H, Jensen BB, et al. Ranavi- Belgium; email: [email protected] rus in wild edible frogs Pelophylax kl. test. WNV-specifi c antibodies were esculentus in Denmark. Dis Aquat Organ. detected by ELISA (5), and positive 2009;85:7–14. doi:10.3354/dao02060 results were confi rmed by virus-

2372 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 17, No. 12, December 2011 LETTERS neutralization test. AHSV-specifi c 15 RVFV-positive samples, 12 were these are known to reemerge under antibodies were detected by using also positive for WNV antibodies, and certain circumstances in locations the ELISA prescribed by the World 12 of 29 WNV-positive samples were where they have occurred in the past. Organisation for Animal Health. also positive for RVFV (χ2 = 8.37, The results of this study support Fifteen of 100 samples were df = 1, p < 0.05). that camels moving across the Sahara positive for RVFV-specifi c antibodies Antibodies to 2 zoonotic have contact with RVFV and WNV, by competitive ELISA, all of which arboviruses, i.e., RVFV and WNV, and frequently the same animals have were confi rmed by virus-neutralization were present in camels moving to been infected by both agents. In a test, with neutralization titers ranging the northwestern part of the Sahara particularly dry environment such as from 40 to 1,280 (geometric mean Desert, and antibodies to AHSV were the desert, particular attention should titer = 229). With regard to WNV absent in the populations examined. be paid to singular wet areas such antibodies, the ELISA detected 44 Despite the higher percentage of as oases. The presence of water in positive samples and 1 doubtful seropositivity for WNV than for these areas results in an abundance sample, of which 29 were confi rmed RVFV, the epidemiologic consequence of competent mosquitoes and hosts, as positive by virus-neutralization test of RVFV-specifi c antibodies in this which in turn makes these viruses (virus-neutralization test titers ranging population could be higher than that likely to cycle and infect domestic from 10 to 640; geometric mean for WNV antibodies. Camels can act animals such as camels coming to titer = 20). As for AHSV antibodies, as reservoir hosts for RVFV (6) but drink and rest. none of the samples was positive by are unlikely to do so for WNV, which ELISA. Prevalence data were analyzed cycles between mosquitoes and wild Acknowledgments by generalized linear model with birds with mammals usually being We thank the Ministry of Agriculture locality (Dakhla or Smara), sex, and dead-end hosts. High prevalence of of Morocco for technical assistance on age as fi xed factors. No differences by antibodies to RVFV in camels has been sample collection. origin or sex were found in prevalence described in different sub-Saharan and for WNV (p>0.14) but antibodies Sahelian countries (7–9). Camels have This research was supported by were more prevalent in camels >3 been involved in the spread of disease Biopharma and INIA-MARM agreement years of age (χ2 = 14.04, 3 df, p = in some instances (10). Immunity to no. CC08-020. 0.003). No differences in prevalence RVFV indicates previous infection. of RVFV antibodies were found by Our results showed that seroprevalence Mehdi El-Harrak, sex (p = 0.29), but prevalence was of RVFV was higher among older Raquel Martín-Folgar, higher in Smara (χ2 = 3.74, p = 0.05) than younger camels, indicating Francisco Llorente, and among camels >6 years of age that contact could have occurred Paloma Fernández-Pacheco, (χ2 = 8.37, df = 3, p = 0.04) (Table). some years ago. Nevertheless, these Alejandro Brun, Jordi Figuerola, We also examined the co-occurrence populations should be monitored for and Miguel Ángel Jiménez- of antibodies to RVFV and WNV. Of RVFV and other arboviroses because Clavero Author affi liations: Biopharma, Rabat, Table. Results of testing of camels for virus antibodies, by location, age group, and sex Morocco (M. El-Harrak); Centro de of camels examined, North Africa, 2009* Investigación en Sanidad Animal, No. No. positive for antibody Valdeolmos, Spain (R. Martín-Folgar, F. Camel characteristic samples RVFV WNV AHSV RVFV and WNV Llorente, P. Fernández-Pacheco, A. Brun, Origin M.Á. Jiménez-Clavero); and Estación Tata 2 0 0 0 0 Biológica de Doñana, Seville, Spain (J. Smara-Laayoune 58 13 20 0 11 Figuerola). Dakhla 40 2 9 0 1 Age group, y DOI: http://dx.doi.org/10.3201/eid1712.110587 <1 18 1 1 0 1 1–2 25 0 1 0 0 3–5 7 1 3 0 1 6–10 27 6 12 0 10 References >10 23 7 12 0 0 1. Dauphin G, Zientara S, Zeller H, Murgue Sex B. West Nile: worldwide current situation M 71 10 15 0 7 in animals and humans. Comp Immunol F 29 5 14 0 5 Microbiol Infect Dis. 2004;27:343–55. Total 100 15 29 0 12 doi:10.1016/j.cimid.2004.03.009 *RVFV, Rift Valley fever virus; WNV, West Nile virus; AHSV, African horse sickness virus.

Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 17, No. 12, December 2011 2373 LETTERS

2. Elfadil AA, Hasab-Allah KA, Dafa-Allah Brucellosis, were negative for hepatitis B virus, OM. Factors associated with Rift Valley hepatitis A virus, cytomegalovirus, fever in south-west Saudi Arabia. Rev Sci Taiwan, 2011 Tech. 2006;25:1137–45. and Epstein-Barr virus infections. 3. Mellor PS, Hamblin C. African horse To the Editor: Human brucellosis Abdominal ultrasound indicated sickness. Vet Res. 2004;35:445–66. is the most common zoonosis mild splenomegaly and no evidence doi:10.1051/vetres:2004021 of vegetation. Abdominal and pelvic 4. Martín-Folgar R, Lorenzo G, Boshra H, worldwide (1–4). The disease is Iglesias J, Mateos F, Borrego B, et al. De- transmitted to humans through the computed tomography showed focal velopment and characterization of mono- consumption of infected meat and raw splenic infarction with splenomegaly. clonal antibodies against Rift Valley fever dairy products from domestic livestock Empirical ceftriaxone (1 g every virus nucleocapsid protein generated by 12 h) and doxycycline (100 mg every DNA immunization. MAbs. 2010;2:275– or by direct or indirect contact with 84. doi:10.4161/mabs.2.3.11676 infected animals (1–3). The disease is 12 h) were administered, and fever 5. Sotelo E, Llorente F, Rebollo B, Camuñas multisystemic and shows wide clinical subsided 5 days later. Two aerobic A, Venteo A, Gallardo C, et al. Develop- polymorphism (2–4). culture bottles (BacT/ALERT, ment and evaluation of a new epitope- bioMérieux Inc., La Balme les blocking ELISA for universal detection A 54-year-old woman reported of antibodies to West Nile virus. J Virol high fever, poor appetite, epigastralgia, Grottes, France) from different sets Methods. 2011;174:35–41. doi:10.1016/j. mild dysuria, generalized myalgia, and of blood cultures on the day before jviromet.2011.03.015 mild left side pain for 6 days before admission yielded unidentifi ed gram- 6. Scott GR, Coackley W, Roach RW, Cowdy negative tiny bacilli after 2 days NR. Rift Valley fever in camels. J Pathol she sought care at and was admitted to Bacteriol. 1963;86:229–31. doi:10.1002/ National Taiwan University Hospital, of incubation. The organism was path.1700860131 Taipei, Taiwan. She had a history of identifi ed as Brucella melitensis by 7. Mariner JC, Morrill J, Ksiazek TG. An- ovarian cancer (clear cell, stage Ic), the Vitek 2 GN identifi cation system tibodies to hemorrhagic fever viruses in (bioMérieux Inc.) (probability of domestic livestock in Niger: Rift Valley which had been treated with surgery fever and Crimean-Congo hemorrhagic and chemotherapy 7 years earlier at identity 99%) and was confi rmed fever. Am J Trop Med Hyg. 1995;53:217– our hospital. She had traveled to many by analysis of partial 16S rRNA 21. countries, most recently to Algeria gene sequencing. Two primers 8. Eisa M. Preliminary survey of domestic were used: 8FPL (5′-AGAGT animals of the Sudan for precipitating an- and Morocco 2 months before this tibodies to Rift Valley fever virus. J Hyg admission. During her stay in North TTGATCCTGGCTCAG-3′) and 1492 (Lond). 1984;93:629–37. doi:10.1017/ Africa, she had close contact with RPL (5′-GGTTACCTTGTTACGAC S0022172400065207 camels, ate cheese and yogurt, and TT-3′). We compared the partial 9. Olaleye OD, Tomori O, Schmitz H. sequences with published sequences Rift Valley fever in Nigeria: infections drank milk, even in the desert. Fever in domestic animals. Rev Sci Tech. occurred 1 month after she returned to in the GenBank database by using the 1996;15:937–46. Taiwan. BLASTN algorithm (www.ncbi.nlm. 10. Abd el-Rahim IH, Abd el-Hakim U, On physical examination, her nih.gov/blast). The closest match was Hussein M. An epizootic of Rift Valley B. melitensis (GenBank accession fever in Egypt in 1997. Rev Sci Tech. body temperature was 39.9°C, blood 1999;18:741–8. pressure was 97/68 mm Hg, and pulse no. CP001852.1; maximal identity rate was 89 beats/min. There was 100%). MICs were determined Address for correspondence: Miguel Ángel mild tenderness on palpation in the by the Etest (AB Biodisk, Solna, Jiménez-Clavero, Centro del Investigación epigastric area. Laboratory analysis Sweden) on Mueller-Hinton agar en Sanidad Animal (INIA), Ctra Algete- El of serum specimens showed elevated (BBL, Becton Dickinson, Sparks, Casar s/n, 28130, Valdeolmos, Spain; email: levels of alanine aminotransferase MD, USA) supplemented with 5% [email protected] (534 U/L), aspartate aminotransferase sheep blood and were interpreted 2 (841 U/L), and alkaline phosphatase days after incubation. The isolate was (337 U/L) but a total bilirubin level susceptible to doxycycline (MIC 0.25 (0.48 mg/dL) within reference limits. μg/mL; susceptible MICs <2 μg/mL) Renal function was within reference but not susceptible to trimethoprim/ ranges (blood urea nitrogen 9.5 mg/ sulfamethoxazole (MIC 1/19 μg/ dL, creatinine 0.6 mg/dL). C-reactive mL; susceptible MICs <0.5 μg/mL) protein was elevated (4.59 mg/dL), (5,6). MIC values of tigecycline and but procalcitonin level was within gentamicin were 0.125 μg/mL and reference range (0.13 ng/mL). The 2.0 μg/mL, respectively. A serum leukocyte count was 4,710 cells/mm3, sample for examination of Brucella and hemoglobin was 11.4 g/dL. antibody by Rose Bengal test using Serologic tests for viral hepatitis B. abortus antigen (VLA Scientifi c,

2374 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 17, No. 12, December 2011