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LETTERS
References Imported Mollusks Meretrix lyrata, n = 3; and Donax sp.,
n = 5), oysters (Crassostrea angulata,
1. Charrel RN, Gallian P, Navarro-Mari JM, and Dissemination n = 1), cockles (Cerastoderma edule,
Nicoletti L, Papa A, Sánchez-Seco MP, et
al. Emergence of Toscana virus in Europe. of Human Enteric n = 1), and razor clams (Solen mar-
Emerg Infect Dis. 2005;11:1657–63.
2. Dionisio D, Esperti F, Vivarelli A, Valas-
Viruses ginatus, n = 1 and Ensis sp., n = 8).
Digestive tissue was dissected from
sina M. Epidemiological, clinical and
laboratory aspects of sandfly fever. Curr
To the Editor: The globaliza- duplicated samples (10–20 individual
Opin Infect Dis. 2003;16:383–8. DOI: tion of food production and trade has mollusks) and homogenized with 0.1%
10.1097/00001432-200310000-00003 increased the potential risk for infec- peptone water (pH 7.4), centrifuged at
3. Weidmann M, Sanchez-Seco MP, Sall AA, tious foodborne diseases. Hepatitis 1,000 × g for 5 min, and supernatant
Ly PO, Thiongane Y, Lô MM, et al. Rapid
detection of important human pathogenic
A virus (HAV) and norovirus (NoV) recovered. RNA was extracted by us-
Phleboviruses. J Clin Virol. 2008;41:138– constitute the most important food- ing both Total Quick RNA extraction
42. borne pathogens of humans in terms Cells and Tissue kit (Talent, Trieste,
4. Ronquist F, Huelsenbeck JP. Mrbayes 3: of numbers of outbreaks and persons Italy) and Nucleospin RNA Virus Kit
Bayesian phylogenetic inference under
mixed models. Bioinformatics. 2003;
affected in industrialized countries (Macherey-Nagel, Düren, Germany).
19:1572–4. DOI: 10.1093/bioinformatics/ (1,2). In these countries, improvement NoV and HAV were detected by
btg180 of health conditions and development real-time reverse transcription–PCR
5. Dobler G, Treib J, Haass A, Frösner G, of specific vaccines are changing the (RT-PCR) by using the Platinum
Woesner R, Schimrigk K. Toscana virus
infection in German travellers return-
epidemiologic pattern of diseases such Quantitative RT-PCR Thermoscript
ing from the Mediterranean. Infection. as hepatitis A, decreasing their preva- 1-step system (Invitrogen, Carlsbad,
1997;25:325. DOI: 10.1007/BF01720413 lence and increasing the susceptibility CA, USA) (25 μL final volume) with
6. Sonderegger B, Hachler H, Dobler G, of the unvaccinated adult population 5 μL of template RNA, and primers,
Frei M. Imported aseptic meningitis due
to Toscana virus acquired on the island of
(1). In recent years, numerous cases probes, and conditions as described
Elba, Italy, August 2008. Euro Surveill. of gastroenteritis caused by NoV and (7). A sample that displayed a cycle
2009;14:pii=19079. hepatitis A linked to imported shellfish threshold value <41 was considered
7. Charrel RN, Moureau G, Temmam S, Izri have been reported (2–5). In Spain, 2 positive. AsV was detected by stan-
A, Marty P, Parola P, et al. Massilia virus, a
novel Phlebovirus (Bunyaviridae) isolated
notable hepatitis A outbreaks associ- dard RT-PCR (7), coupled with hy-
from sandflies in the Mediterranean. Vec- ated with clams (Donax sp.) imported bridization by using specific biotin-
tor Borne Zoonotic Dis. 2009;9:519–30. from Peru occurred in 1999 and 2008. labeled probes with the commercial
DOI: 10.1089/vbz.2008.0131 In both situations, the Spanish Min- Kit Hybridowell universal (Argene,
8. Collao X, Palacios G, Sanbonmatsu-
Gámez S, Pérez-Ruiz M, Negredo AI,
istry of Health activated the National Varilhes, France).
Navarro-Marí JM, et al. Genetic di- System of Epidemiologic Surveil- Negative and specific positive
versity of Toscana virus. Emerg Infect lance and the European Community controls for HAV, NoV, and AsV were
Dis. 2009;15:574–7. DOI: 10.3201/ Rapid Alert System for Foodstuffs. introduced in each run. Real-time RT-
eid1504.081111
9. Towards regional economic development
The implicated shellfish batches were PCR included appropriate external
2006/2010. Tourism and innovations ob- immobilized or removed, and all the controls in each analysis to avoid un-
jectives and instruments [in Italian]. 2006 shellfish from Peru were banned from derestimation of viral load. A mutant,
[cited 2010 Apr 1]. http://www.provincia. the European Union (6). We present nonvirulent, infective strain of men-
livorno.it/economia/turismo/forumtur-
ismo2006/FormatLivorno4aprile2006.pdf
further evidence that imported shell- govirus (vMC0) (103 PFU) was used
fish from developing countries, where as control for extraction. To calculate
Address for correspondence: Jonas Schmidt- these pathogens are endemic, can be the real-time RT-PCR efficiencies, ex-
Chanasit, Department of Virology, Clinical a vehicle for viral gastroenteritis and ternal viral RNA (HAV, 103 copies)
Virology LaboratoryBernhard Nocht Institute HAV infections in areas where they or synthetic DNA (NoV, 105 copies)
for Tropical Medicine, Bernhard Nocht Strasse are not endemic. controls for the respective virus were
74, D-20359 Hamburg, Germany; email: Fifty mollusk samples imported co-amplified with each template viral
jonassi@gmx.de into Spain during September 2006– RNA as described (8). The number of
March 2009 were analyzed for NoV RNA viral genome copies per gram of
genotype I (GI) and GII, HAV and digestive tissue (RNA copies/g diges-
astrovirus (AsV). Countries of ori- tive tissue) was estimated by using
Use of trade names is for identification only gin were Morocco, Peru, Vietnam, standard curves generated from RNA
and does not imply endorsement by the Pub- and South Korea (Table). The species transcripts and synthetic DNA (8) and
lic Health Service or by the U.S.
Department of Health and Human Services.
studied were clams (Callista chione, corrected with the extraction and real-
n = 25; Transanella pannosa, n = 6; time RT-PCR efficiencies.
1036 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 16, No. 6, June 2010
LETTERS
Table. Viral detection and quantification in imported mollusk samples*
Norovirus positive
Country of origin HAV positive† GI‡ GII§ Astrovirus
(no. samples) No. (%) QR No. (%) QR No. (%) QR positive, no. (%)¶
4 7 5 5
Morocco (34) 5 (15) 3.5 x 10 –1.1 x 10 2 (6) 1.4 x 10 –8.9 x 10 7 (21)
3 5 7 5 6
Peru (13) 1 (8) 4.7 x 10 4 (31) 2 x 10 –1.8 x 10 2 (15) 1 x 10 –1.4 × 10 1 (8)
7 6 7
Vietnam (2) 1 (50) 4.4 x 10 2 (100) 3.3 x 10 –7.7 x 10 1 (50)
6
South Korea (1) 1 (100) 1.2 × 10 –
3 7 4 7 5 6
Total (50) 2 (4) 10 –10 12 (24) 10 –10 4 (8) 10 –10 9 (18)
*HAV, hepatitis A virus; GI, genotype I; QR, quantification range (RNA copies/g digestive tissue).
†Obtained from Donax sp. and Meretrix lyrata.
‡Obtained from Donax sp., Callista chione, Transanella pannosa, M. lyrata, and Ensis sp.
§Obtained from Donax sp., T. pannosa, and Ensis sp.
¶Obtained from C. chione, T. pannosa, M. lyrata, and Ensis sp.
Twenty (40%) of 50 samples were is noteworthy because the attack rate References
contaminated by >1 virus (Table), al- for different batches of shellfish is
1. Koopmans M, Duizer E. Foodborne vi-
though all the mollusk imports com- dose dependent (6). ruses: an emerging problem. Int J Food
plied with the current sanitary stan- Determining the association of a Microbiol. 2004;90:23–41. DOI: 10.1016/
dards. NoV GI was most prevalent, viral infection with a particular con- S0168-1605(03)00169-7
detected in 24% of samples, followed taminated product is often compli- 2. Webby RJ, Carville KS, Kirk MD, Green-
ing G, Ratcliff RM, Crerar SK, et al. Inter-
by AsV (18%), NoV GII (8%), and cated, and the epidemiologic inves- nationally distributed frozen oyster meat
HAV (4%). One sample showed a low tigations necessary for finding this causing multiple outbreaks of norovirus
extraction efficiency (<1%), yielding association are time consuming and infection in Australia. Clin Infect Dis.
all samples high real-time RT-PCR ef- allow the virus to spread before the 2007;44:1026–31. DOI: 10.1086/512807
3. Romalde JL, Torrado I, Ribao C, Barja
ficiencies (>10%) (9). problem is recognized. Furthermore, JL. Global market: shellfish imports as a
Six samples (30% of positive there are analytical difficulties in de- source of reemerging food-borne hepatitis
samples) were positive for >1 vi- tecting and quantifying virus in shell- A virus infections in Spain. Int Microbiol.
rus. Thus, 2 samples from Morocco fish samples and in monitoring them; 2001;4:223–6. DOI: 10.1007/s10123-001-
0041-0
showed contamination with NoV GI other problems include ascertaining 4. Liko J, Keene WE. Use of templates to
and AsV. From Peru, 1 sample was the representativeness of the sample identify source of norovirus outbreak.
contaminated with both genogroups (2,6) and the high cost of applying the Emerg Infect Dis. 2009;15:839–40. DOI:
of NoV and another with NoV GI, technique in areas with extensive mol- 10.3201/eid1505.081625
5. Simmons G, Garbutt C, Hewitt J, Green-
NoV GII, and AsV. Samples from lusk production. ing G. A New Zealand outbreak of norovi-
Vietnam (n = 2) were contaminated The inadequacy of the bacte- rus gastroenteritis linked to the consump-
with HAV–NoV GI and NoV GI– rial indicators makes it necessary to tion of imported raw Korean oysters. N Z
AsV. Co-infection with different vi- develop new prevention strategies, Med J. 2007;120:U2773.
6. Pintó RM, Costafreda MI, Bosch A.
ruses or multiple virus strains could based on microbial risk assessment, Risk assessment in shellfish-borne out-
lead to more severe symptoms and to ensure the sanitary quality of shell- breaks of hepatitis A. Appl Environ Mi-
the occurence of 2 episodes of the fish, both in production areas and in crobiol. 2009;75:7350–5. DOI: 10.1128/
same or different diseases and also be international trade operations. Imple- AEM.01177-09
7. Vilariño ML, Le Guyader FS, Polo D,
a way to facilitate emergence of new menting these methods and providing Schaeffer J, Kröl J, Romalde JL. Asses-
recombinant strains (10). training to laboratories in developing ment of human enteric viruses in cultured
Contamination levels for NoV countries are essential to achieving and wild bivalve molluscs. Int Microbiol.
GI ranged from 3.5 × 104 to 7.7 × 107 these objectives. 2009;12:145–51.
8. Costafreda MI, Bosch A, Pintó RM. De-
RNA copies/g digestive tissue; for velopment, evaluation and standarization
NoV GII, from 1.03 × 105 to 8.9 ×105 David Polo, M. Luz Vilariño, of a real time TaqMan RT-PCR assay
RNA copies/g digestive tissue; and Carmen F. Manso, for quantification of hepatitis A virus in
for HAV, from 4.7 × 103 to 4.4 × 107 and Jesús L. Romalde clinical and shellfish samples. Appl En-
viron Microbiol. 2006;72:3846–55. DOI:
RNA copies/g digestive tissue (Table). Authors affiliations: Universidad de Santia-
10.1128/AEM.02660-05
For HAV, these values are in the same go de Compostela. Santiago de Compos-
range or even higher than in the co- tela, Spain
quina clams from Peru implicated in DOI: 10.3201/eid1606.091748
the outbreak in Spain in 2008, which
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 16, No. 6, June 2010 1037
LETTERS
9. da Silva AK, Le Saux JC, Parnaudeau S, to obstructive uropathy. His baseline Patient B, a 45-year-old Ma-
Pommepuy M, Elimelech M, Le Guyader creatinine level was 300–400 μmol/L. laysian–Chinese man with diabetes
FS. Evaluation of removal of noroviruses
during wastewater treatament, using real For 3 years, he had ingested tradi- mellitus, had undergone a cadaveric
time RT-PCR: different behaviors of tional Chinese medicine, which we liver transplant in 2001 for hepatitis
genogroups I and II. Appl Environ Mi- suspect was contaminated by steroids B liver cirrhosis. He was receiving
crobiol. 2007;73:7891–7. DOI: 10.1128/ because he appeared cushingoid. An immunosuppressants (azathioprine
AEM.01428-07
10. Lees D. Virus and bivalve shellfish. Int J outbreak of CHIKV infection was and prednisolone). He was admitted
Food Microbiol. 2000;59:81–116. DOI: reported at his workplace. He was in August 2008 after experiencing fe-
10.1016/S0168-1605(00)00248-8 admitted to National University Hos- ver, headache, and abdominal bloat-
pital, Singapore, in July 2008 with ing for 3 days. He had no neurologic
Address for correspondence: Jesús L. Romalde, abdominal pain, vomiting, and fever symptoms. Acute self-limiting febrile
Departamento de Microbiología y Parasitología, of 1 day. He had no joint symptoms. illnesses with arthritis had occurred
Centro de Investigaciones Biológicas (CIBUS)– Clinically, he had systemic inflamma- in his hometown; CHIKV infections
Facultad de Biología, Universidad Santiago de tory response syndrome complicated were suspected.
Compostela, 15782, Santiago de Compostela, by acute-on-chronic renal failure. His Results of his examination on
Spain; email: jesus.romalde@usc.es creatinine level was elevated at 921 admission were normal, except for bi-
μmol/L on admission. A complete lateral enlarged cervical lymph nodes.
blood count showed leukocytosis Chest radiograph results were unre-
(19.24 × 109 cells/L) with neutro- markable. He had mild transaminitis
philia and thrombocytopenia (62 × (alanine aminotransferase 173 U/L,
109 cells/L). Initial blood and urine aspartate aminotransferase 170 U/L),
cultures and serologic results were elevated C-reactive protein (107
Atypical negative for dengue virus, but serum mg/L), and thrombocytopenia (120
reverse transcription–PCR (RT-PCR) × 109 cells/L) without leukocytosis.
Chikungunya Virus and indirect immunofluorescent as- Results of comprehensive serum and
Infections in say for immunoglobulin G (IgG) urine microbial studies were negative
Immuno- (Euroimmun Medizinische Labor- for posttransplant infections. Results
diagnostika, Lubeck, Germany) and of serum RT-PCR were negative for
compromised IgM (CTK Biotech, Inc, San Diego, CHIKV, but IgG and IgM tests were
Patients CA, USA) were positive for CHIKV positive for CHIKV.
(3,4). Computed tomographic scans Brain magnetic resonance im-
To the Editor: Chikungunya fe- of the abdomen showed dilated small aging was performed because of the
ver was first described in Tanganyika bowel loops. patient’s persistent severe headache
(now Tanzania) in 1952 and is now An urgent laparotomy did not and transient drowsiness. It showed
emerging in Southeast Asia. Chi- show bowel perforation, but peritone- several nonspecific areas of enhance-
kungunya virus (CHIKV) infection, al cultures yielded Klebsiella pneumo- ment, which suggested encephalitis,
a self-limiting febrile illness, shares niae, Escherichia coli, and Candida given the clinical scenario (Figure).
similarities with dengue fever such glabrata, and RT-PCR from the con- However, a lumbar puncture was not
as headache and myalgia. Addition- centrated peritoneal fluid was positive performed, and hence, whether the
ally, patients with CHIKV infection for CHIKV (3). He was administered patient’s cerebrospinal fluid contained
typically have arthralgia, arthritis, appropriate antimicrobial drugs. He CHIKV could not be determined.
and tenosynovitis (1). Although usu- required repeat laparotomies because Bilateral frontoparietal white mat-
ally benign, CHIKV infection may of elevated intraabdominal pres- ter lesions with restricted diffusion
on rare occasions lead to neurologic sure. He subsequently received broad has been suggested as an early sign
and hepatic manifestations with high spectrum antimicrobial drugs to treat of viral encephalitis (5). However, a
illness and mortality rates (2). We re- secondary intraabdominal infections retrospective series demonstrated that,
port 2 immunocompromised patients caused by P. aeruginosa and Entero- in CHIKV encephalitis, abnormalities
with CHIKV infection associated with coccus faecalis. on magnetic resonance imaging were
peritonitis, encephalitis, and second- Ventilator-associated pneumonia uncommon, and no pathognomonic
ary bacterial infections. also developed. Despite maximal sup- features were found (6).
Patient A, a 66-year-old Singa- port and prolonged antimicrobial ther- Hospital-acquired pneumonia also
porean-Chinese man, had a history apy, this patient died after 5 months of developed and was treated with broad-
of chronic renal disease secondary hospitalization. spectrum antimicrobial drugs. Bron-
1038 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 16, No. 6, June 2010
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