Japanese Encephalitis Outbreak, Yuncheng, China, 2006

LETTERS

Yohei Doi,* Jennifer Adams,* Japanese WNV-specifi c or dengue vi- Alexandra O’Keefe,* Zubair rus–specifi c IgM was not detected in Quereshi,* Lindsay Ewan,* and Encephalitis any samples. JEV-specifi c IgM was David L. Paterson*1 Outbreak, detected in 27 (80%) patients, which *University of Pittsburgh School of Medi- Yuncheng, China, indicated recent JEV infections. The cine, Pittsburgh, Pennsylvania, USA other 7 patients were negative for JEV 2006 by ELISA and reverse transcription– References To the Editor: Japanese encepha- PCR (RT-PCR). Increases >4-fold in litis (JE) epidemics have occurred only neutralizing antibodies were detected 1. Paterson DL, Bonomo RA. Extended- in acute- and convalescent-phase se- spectrum beta-lactamases: a clinical in Asia. More than 50,000 cases of JE update. Clin Microbiol Rev. 2005;18: with ≈10,000 deaths have been report- rum samples from 9 patients (10 se- 657–86. ed since 1998 (1,2). The People’s Re- rum pairs were collected during the 2. Livermore DM, Canton R, Gniadkowski public of China reported 5,104 cases outbreak). M, Nordmann P, Rossolini GM, Arlet G, Attempts were made to detect et al. CTX-M: changing the face of ESBLs and 214 deaths in 2005. Most of these in Europe. J Antimicrob Chemother. 2007; deaths occurred in infants (3,4). virus in CSF of patients and in 2,400 [Epub 2006 Dec 6]. During July and August 2006, mosquitoes. Mosquitoes (mainly Cu- 3. Pitout JD, Gregson DB, Church DL, El- an outbreak of viral encephalitis oc- lex spp.) were collected in cow sheds sayed S, Laupland KB. Community-wide and hog pens around houses and pro- outbreaks of clonally related CTX-M-14 curred in Yuncheng, Shanxi Province, beta-lactamase–producing Escherichia People’s Republic of China. A total of cessed into pools of 100. Total RNA coli strains in the Calgary health region. J 66 cases (1.32/100,000 population) was extracted from CSF or mosquito Clin Microbiol. 2005;43:2844–9. were reported, including 19 deaths homogenate by using the QIAamp 4. Moland ES, Black JA, Hossain A, Han- viral RNA extraction kit (QIAGEN, son ND, Thomson KS, Pottumarthy S. (case-fatality rate 28.8%). The cases Discovery of CTX-M-like extended-spec- had a widespread distribution over 9 Valencia, CA, USA) according to the trum beta-lactamases in Escherichia coli counties and involved 37 towns and manufacturer’s specifi cations. RT was isolates from fi ve U.S. states. Antimicrob 61 administrative villages. The ratio performed by using Ready-To-Go-You Agents Chemother. 2003;47:2382–3. Prime First Strand Beads (Amersham 5. Livermore DM, Hawkey PM. CTX-M: of male-to-female patients was 1:0.89. changing the face of ESBLs in the UK. J A distinct clinical feature of this out- Pharmacia Biotech, Piscatawy, NJ, Antimicrob Chemother. 2005;56:451–4. break was the age distribution. More USA) and a seminested PCR to ampli- 6. Rodriguez-Bano J, Navarro MD, Romero than 86% of the patients were >30 fy 492-bp gene fragments of the pre- L, Martinez-Martinez L, Muniain MA, membrane (PrM) sequence of JEV by Perea EJ, et al. Epidemiology and clinical years of age, with only 10% of pa- features of infections caused by extended- tients <7 years of age; ≈95% of the using the Takara LA Taq PCR kit (Ta- spectrum beta-lactamase-producing Esch- deaths occurred in patients >50 years kara Bio Inc., Shiga, Japan). The prim- erichia coli in nonhospitalized patients. J of age (5). ers were derived from Ishikawa strain Clin Microbiol. 2004;42:1089–94. genome sequences (GenBank acces- 7. Fridkin SK, Hageman JC, Morrison M, We report serologic and virologic Sanza LT, Como-Sabetti K, Jernigan JA, fi ndings for the 2006 outbreak of viral sion no. AB051292). Primers PrMF: et al. Methicillin-resistant Staphylococcus encephalitis. Forty-six clinical speci- 5′-CGT TCT TCA AGT TTA CAG aureus disease in three communities. N mens collected from 34 patients who CAT TAG C-3′ (251–275), PrMR1: Engl J Med. 2005;352:1436–44. 5′-CGY TTG GAA TGY CTR GTC 8. Meunier D, Jouy E, Lazizzera C, Kobisch had a diagnosis of viral encephalitis, M, Madec JY. CTX-M-1 and CTX-M-15 including 33 serum samples and 13 CG-3′ (724–743), and PrMR2: 5′- type beta-lactamases in clinical Esch- cerebrospinal fl uid (CSF) samples, CCY RTG TTY CTG CCA AGC ATC erichia coli isolates recovered from food- were studied. All serum samples were CAM CC-3′ (901–925) were used. producing animals in France. Int J Antimi- JEV PrM gene was amplifi ed from crob Agents. 2006;28:402–7. screened for immunoglobulin M (IgM) to West Nile virus (WNV) by using the CSF of 6 (46%) of 13 patients and 10 Address for correspondence: David L. WNV IgM-capture ELISA kit (PanBio, of 24 pools of mosquitoes by using the Paterson, Infectious Diseases Unit, University Brisbane, Queensland, Australia) and same seminested RT-PCR. To identify of Queensland, Royal Brisbane and Women’s for IgM to dengue virus or Japanese JEV genotype(s) involved in this out- Hospital, Butterfi eld St, Herston, Queensland, encephalitis virus (JEV) by using the break, PCR products were sequenced. QLD 4029 Australia; email: david.antibiotics@ JE-Dengue IgM Combination ELISA Eleven sequences (GenBank acces- gmail.com kit (PanBio). Results for JEV were con- sion nos. EF434264–EF434274) were fi rmed by using the JE Virus IgM-Cap- obtained from 6 patients and 5 pools 1Current affi liation: University of Queens- ture ELISA kit (Shanghai B & C Enter- of mosquitoes. The 11 sequences were land, Royal Brisbane and Women’s prise Development Co. Ltd, Shanghai, compared phylogenetically with17 Hospital, Herston, Queensland, Australia People’s Republic of China). known JEV strains of the 4 recognized

Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 13, No. 7, July 2007 1123 LETTERS genotypes (classifi ed on the basis of Acknowledgments of China; ‡Shanxi Center for Disease Con- a 240-nt region of the prM gene). As We thank Charles H. Calisher, Zhen trol and Prevention, Taiyuan, People’s Re- shown in the Figure, the 11 sequences F. Fu, and Ichiro Kurane for assistance public of China; §Yuncheng Center for Dis- were those of JEV. with preparation of this article. ease Control and Prevention, Yuncheng, Further analysis showed that these People’s Republic of China; ¶Yuncheng This study was supported by 11 sequences can be grouped into gen- Infectious Diseases Hospital, Yuncheng, grants from the National Science and otypes I and III. Both genotypes were People’s Republic of China. #Beijing Di- Technology Department of China (no. found in patient and mosquito sam- tan Hospital, Beijing, People’s Republic of 2003BA12A08-01) and the Japan Health ples, indicating that these genotypes China; and **Beijing Institute of Biological Science Foundation. co-circulated during this JE outbreak. Products, Beijing, People’s Republic of JE has been endemic in Yuncheng China for many years (6). A vaccine against Li-Hua Wang,* Shi-Hong Fu,* JE (SA14–14–2) has been used in this Huan-Yu Wang,* References area in infants, but not in adults. This Xiao-Feng Liang,† Jing-Xia Cheng,‡ might be 1 reason why a higher adult 1. Parida M, Dash PK, Tripathi NK, Ambuj, incidence was found in this outbreak. Hong-Mei Jing,§ Gen-Lao Cai,¶ Sannarangalah S, Saxena P, et al. Japanese JEV genotype III had been the pre- Xing-Wang Li,# Wen-Yuan Ze,** encephalitis outbreak, India. Emerg Infect dominant genotype in previous years, Xin-Jun Lv,* Hua-Qing Wang,† Dis. 2006;12:1427–30. Ding-Lin Zhang,¶ Yun Feng,* 2. Solomon T, Ni H, Beasley DWC, but genotype I has been recently de- Ekkelenkamp M, Cardosa MJ, Barrett tected at increased frequencies (7–10). Zun-Dong Yin,† AD. Origin and evolution of Japanese en- Detection of 2 JEV genotypes in 1 epi- Xiao-Hong Sun,* Tie-Jun Shui,† cephalitis virus in Southeast Asia. J Virol. demic has not been reported. Whether Ming-Hua Li,* Yi-Xing Li,† 2003;77:3091–8. and Guo-Dong Liang* 3. Liang GD. Arboviruses in China. Chinese simultaneous circulation of >1 geno- Journal of Zoonoses. 1997;13:61–4. type during an outbreak indicates a *Institute for Viral Disease Control and Pre- 4. National Data of Class A and B Infectious new type of emergence of JEV or that vention, Beijing, People’s Republic of Chi- Disease in December, 2005. Center for this has occurred and not been detect- na; †Chinese Center for Disease Control Public Health Surveillance and Informa- and Prevention, Beijing, People’s Republic tion Service, Chinese Center for Disease ed is unknown. Control and Prevention. Disease Surveil- lance. 2006;1:4. 5. Nine deaths in outbreak of viral encepha- litis in Yuncheng, Shanxi province, the control and prevention of the outbreak are ongoing. [cited 2007 Apr 12]. Avail- able from http://health.people.com.cn/ GB/26466/69622/4715128.html 6. Ma XF, Li ZM, Xing YH. Epidemic anal- ysis of Japanese encephalitis from 1955 to 1977 in Yuncheng, Shanxi Province, China. Chinese Journal of Epidemiology. 1998;19:3–6. 7. Ali A, Igarashi A. Antigenic and genetic variations among Japanese encephalitis virus strains belonging to genotype I. Mi- crobiol Immunol. 1997;41:241–52. 8. Li XY, Song H, Fu SH, Wang HY, Yu YX, Dong GM, et al. Molecular biology of Japaneses encephalitis viruses isolated in China. Chinese Journal of Virology. 2004;20:200–9. 9. Wang HY, Fu SH, Li XY, Song H, Deng J, Yang YL, et al. Isolation and identifi cation Figure. Phylogenetic analysis of Japanese encephalitis virus strains predicted from of genotype Japanese I encephalitis virus premembrane gene sequences. Neighbor-joining tree was generated by using MEGA in China. Chinese Journal of Microbiol- 3.1 software (www.megasoftware.net) and rooted with Murray Valley encephalitis (MVE) ogy and Immunology. 2004;24:843–9. virus sequence information. Bootstrap confi dence limits for 1,000 replicates are indicated 10. Wang HY, Takasaki T, Fu SH, Sun XH, above each branch. Horizontal branch lengths are proportional to genetic distance; vertical Zhang HL, Wang ZX, et al. Molecular branch lengths have no signifi cance. Scale bar indicates no. nucleotide substitutions epidemiological analysis of Japanese per site. All sequences from this study are in boldface. Genotypes are indicated on the encephalitis virus in China. J Gen Virol. right. Designations are listed fi rst, followed by country, source, and year of isolation. CSF, 2007;88:885–94. cerebrospinal fl uid.

1124 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 13, No. 7, July 2007 LETTERS

Address for correspondence: Guo-Dong Medicine of Amazonas (FMTAM) in vivax malaria outbreaks in malaria- Liang, State Key Laboratory for Infectious Manaus, Brazil, to assess the effi cacy endemic areas within the Amazon. Disease Control and Prevention, Institute for of standard supervised CQ therapy. Viral Disease Control and Prevention, Chinese The test involved 166 volunteers with This study was supported by the Bra- Center for Disease Control and Prevention, 100 uncomplicated vivax malaria. Each zilian Ministry of Health and the US Agen- Yingxin St, Xuanwu District, Beijing 100052, volunteer was administered uncoated, cy for International Development as part People’s Republic of China, email: gdliang@ scored, 150-mg CQ tablets (10 + 7.5 of the scientifi c program of the Amazonian hotmail.com + 7.5 mg/kg at 24-hour intervals) (9). Surveillance Network for Antimalarial Primaquine was withheld until day Drugs Resistance (RAVREDA). 28 (dose regimen of 30 mg/day for 7 days). Among the 109 volunteers who completed the in vivo test, 19 had pos- Franklin Simoes itive blood smears within the 28-day de Santana Filho,* follow-up (1 on day 14, 3 on day 21, Ana Ruth de Lima Arcanjo,* and 15 on day 28). All were required Yonne Melo Chehuan,* Chloroquine- to undergo alternative therapy (mefl o- Monica Regina Costa,* Resistant quine). Adequate CQ absorption was Flor Ernestina Martinez- Plasmodium vivax, confi rmed in these cases on day 2 with Espinosa,*† Jose Luis Vieira,‡ a mean ± SD CQ plasma concentration Maria das Graças Brazilian Amazon of 785.4 ± 800.1 ng/mL) (10) Suspect- Vale Barbosa,*§ To the Editor: Plasmodium vivax ed therapeutic failure (P. vivax CQ re- Wilson Duarte Alecrim,*¶ is the protozoan that causes the second sistance) was confi rmed in 11 (10.1%) and Maria das Graças Costa most common form of malaria. Some of 109 persons with a mean isolated Alecrim*§¶ resistant strains to chloroquine (CQ) choloroquine plasma concentration *Foundation for Tropical Medicine of Ama- occur in a few places in Asia and the >10 ng/mL (356.6 ± 296.1 ng/mL) (9). zonas, Manaus, Amazonas, Brazil; †Foun- Indo-Pacifi c Region (1–4). Although Desethylchloroquine levels in plasma dation for Research Support of Amazonas, resistance of P. vivax to CQ has al- were not measured. Manaus, Amazonas, Brazil; ‡Federal Uni- ready been described in South Ameri- Previously, a CQ effi cacy study versity of Pará, Belém, Pará, Brazil; §Ama- ca (5–7), there are limited data regard- demonstrated that 4.4% of those test- zonas State University, Manaus, Amazonas, ing this issue. ed had CQ-resistant P. vivax (7). In Brazil; and ¶Nilton Lins University, Manaus, CQ plus primaquine is the stan- comparison, the proportion of failures Amazonas, Brazil dard treatment for vivax malaria (10.1%) in the current study seems to worldwide. Presently, this drug regi- be relevant; even though most of the References P. vivax infections (98, 89.9%) were men exhibits satisfactory effi cacy in 1. Marlar-Than, Myat-Phone-Kyaw, Aye- the Brazilian Amazon. However, in successfully evaluated and adequate Yu-Soe, Khaing-Khaing-Gyi, Ma- Sabai, recent years several treatment fail- clinical and parasitologic responses Myint-Oo. Development of resistance ures presumably related to CQ resis- were obtained. Currently, the FMTAM to chloroquine by Plasmodium vivax in Manaus Outpatient Clinic is detecting Myanmar. Trans R Soc Trop Med Hyg. tance, have been reported in the city 1995;89:307–8. of Manaus (Amazonas) where vivax patients from different areas of the city 2. Congpuong K, Na-Bangchang K, Thi- malaria predominates (7). This obser- who show parasitologic recurrences masarn K, Tasanor U, Wernsdorfer WH. vation warrants local attention despite after correct treatment within 28 days Sensitivity of Plasmodium vivax to chlo- of the routine clinical follow-up. This roquine in Sa Kaeo Province, Thailand. these cases having no confi rmation Acta Trop. 2002;83:117–21. of CQ blood levels on the basis of observation is an indirect indicator of 3. Hamedi Y, Nateghpour M, Tan-ariya P, the appearance of asexual parasites the possible regional spread of P. vivax Tiensuwan M, Silachamroon U, Looa- against CQ plus desethylchloroquine CQ-resistant strains (unpub. data). reesuwan S. Plasmodium vivax malaria in We believe our fi ndings are im- southeast Iran in 1999–2001: establishing levels exceeding the minimally effec- the response to chloroquine in vitro and in tive plasma concentration proposed for portant and merit the attention of vivo. Southeast Asian J Trop Med Public sensitive parasite strains (>10 ng/mL) local public health authorities. Con- Health. 2002;33:512–8. (8), according to Pan American Health sidering the possibility of emerging 4. Baird JK, Wiady I, Fryauff DJ, Sutani- underestimated P. vivax CQ resis- hardja MA, Leksana B, Widjaya H, et Organization recommendations (9). al. In vivo resistance to chloroquine by From September 2004 to February tance in Manaus, we feel it is essen- Plasmodium vivax and Plasmodium fal- 2005, a 28-day in vivo test was con- tial to quickly clarify whether such ciparum at Nabire, Irian Jaya, Indonesia. ducted at the Foundation for Tropical documented resistance can copromote Am J Trop Med Hyg. 1997;56:627–31.

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