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    Relationships among pol (A) and capsid (B) nucleotide sequences of 8 norovirus strains isolated in Djibouti from 2002 to 2003 and prototype viruses using a neighbor-joining tree (Phylip version 3.6). The input alignment file was generated using Clustal W version 1.8. The Genbank accession numbers are as follows: Norwalk: M87661; Southampton: L07418; Desert Shield: U04469; Chiba: AB022679; Musgrove: AJ277614; Hesse: AF093797; Winchester: AJ277609; Boxer: AF538679; SaitamaKU8GI/99/JP: AB058547; Hawaii: U07611; Melksham: X81879; Toronto: U2030; Bristol: X76716; Hillingdon: AJ277607; Seacroft: AJ277620; Leeds: AJ277608; Amsterdam: AF195848; Idaho-Falls: AY054299: Erfurt-546: AF427118; Limburg: AY077644; SW918: AB074893; Wortley: AJ277618; Fayetteville: AY113106; M7: AY130761; J23: AY130762; Tiffin: AY502010; CS-E1: AY502009; SaitamaT29: AB112221; Alphatron: AF195847.

  • 1

    Bon F, Fascia P, Dauvergne M, Tenenbaum D, Planson H, Petion AM, Pothier P, Kohli E, 1999. Prevalence of group A rotavirus, human calicivirus, astrovirus, and adenovirus type 40 and 41 infections among children with acute gastroenteritis in Dijon, France. J Clin Microbiol 37 :3055–3058.

    • Search Google Scholar
    • Export Citation
  • 2

    Chikhi-Brachet R, Bon F, Toubiana L, Pothier P, Nicolas JC, Flahault A, Kohli E, 2002. Virus diversity in a winter epidemic of acute diarrhea in France. J Clin Microbiol 40 :4266–4272.

    • Search Google Scholar
    • Export Citation
  • 3

    De Wit MA, Koopmans MP, Kortbeek LM, van Leeuwen NJ, Bartelds AI, van Duynhoven YT, 2001. Gastroenteritis in sentinel general practices, The Netherlands. Emerg Infect Dis 7 :82–91.

    • Search Google Scholar
    • Export Citation
  • 4

    Fankhauser RL, Monroe SS, Noel JS, Humphrey CD, Bresee JS, Parashar UD, Ando T, Glass RI, 2002. Epidemiological and molecular trends of “Norwalk-like viruses” associated with outbreaks of gastroenteritis in the United States. J Infect Dis 186 :1–7.

    • Search Google Scholar
    • Export Citation
  • 5

    Green KY, 2001. Human caliciviruses. Green KY, Kapikian RC, eds. Lippincott Williams and Wilkins Fields Virology. Fourth Edition. New York: Lippincott Williams and Wilkins, 841–873.

  • 6

    Kageyama T, Shinohara M, Uchida K, Fukushi S, Hoshino FB, Kojima S, Takeda N, Katayama K, 2004. Coexistence of multiple genotypes, including newly identified genotypes, in outbreaks of gastroenteritis due to Norovirus in Japan. J Clin Microbiol 42 :2988–2995.

    • Search Google Scholar
    • Export Citation
  • 7

    Vinje J, Hamidjaja RA, Sobsey MD, 2004. Developmental and application of a capsid VP1 (region D) based reverse transcription PCR assay for genotyping of genogroup I and II noroviruses. J Virol Methods 116 :109–117.

    • Search Google Scholar
    • Export Citation
  • 8

    Zheng DP, Ando T, Fankhauser RL, Beard RS, Glass RL, Monroe SS, 2006. Norovirus classification and proposed strain nomenclature. Virology 15 :312–323.

    • Search Google Scholar
    • Export Citation
  • 9

    Ouattara FS, Ekaza E, Kacou-n’douba A, Acoua-Koffi GC, Dosso C, 2004. Screening for Calicivirus in children under five years of age, in an Abidjan low-income district. Med Mal Infect 34 :566–567.

    • Search Google Scholar
    • Export Citation
  • 10

    Armah GE, Gallimore CI, Binka FN, Asmah RH, Green J, Ugoji U, Anto F, Brown DWG, Gray J, 2006. Characterization of norovirus strains in rural Ghanaian children with acute diarrhea. J Med Virol 78 :1480–1485.

    • Search Google Scholar
    • Export Citation
  • 11

    Dove W, Cunliffe NA, Gondwe JS, Broadhead RL, Molyneux ME, Nakagomi O, Hart CA, 2005. Detection and characterization of human caliciviruses in hospitalized children with acute gastroenteritis in Blantyre, Malawi. J Med Virol 77 :522–527.

    • Search Google Scholar
    • Export Citation
  • 12

    Smit TK, Steele AD, Peenze I, Jiang X, Estes MK, 1997. Study of Norwalk virus and Mexico virus infections at Ga-Rakuwa Hospital, Ga-Rankuwa, South Africa. J Clin Microbiol 35 :2381–2385.

    • Search Google Scholar
    • Export Citation
  • 13

    Bon F, Giraudon H, Sancey C, Barranger C, Joannes M, Pothier P, Kohli E, 2004. Development and evaluation of a new commercial test allowing the simultaneous detection of noroviruses. J Clin Microbiol 42 :2218–2220.

    • Search Google Scholar
    • Export Citation
  • 14

    Vinje J, Koopmans MP, 1996. Molecular detection and epidemiology of small round-structured viruses in outbreaks of gastroenteritis in the Netherlands. J Infect Dis 174 :610–615.

    • Search Google Scholar
    • Export Citation
  • 15

    Le Guyader F, Estes MK, Hardy ME, Neill FH, Green J, Brown DW, Atmar RL, 1996. Evaluation of a degenerate primer for the PCR detection of human caliciviruses. Arch Virol 141 :2225–2235.

    • Search Google Scholar
    • Export Citation
  • 16

    Noel JS, Liu BL, Humphrey CD, Rodriguez EM, Lambden PR, Clarke IN, Dwyer DM, Ando T, Glass RI, Monroe SS, 1997. Parkville virus: a novel genetic variant of human calicivirus in the Sapporo virus clade, associated with an outbreak of gastroenteritis in adults. J Med Virol 52 :173–178.

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    Kojima S, Kageyama T, Fukushi S, Hoshino F, Shinohara M, Uchida K, Natori K, Takeda N, Katayama K, 2002. Geno-group-specific PCR primers for detection of Norwalk-like viruses. J Virol Methods 100 :107–114.

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  • 18

    Ambert-Balay K, Bon F, Le Guyader F, Pothier P, Kohli E, 2005. Characterization of new recombinant noroviruses. J Clin Microbiol 43 :5179–5186.

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  • 19

    Green J, Gallimore CI, Norcott JP, Lewis D, Brown DW, 1995. Broadly reactive reverse transcriptase polymerase chain reaction for the diagnosis of SRSV-associated gastroenteritis. J Med Virol 47 :392–398.

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    Noel JS, Ando T, Leite JP, Green KY, Dingle KE, Estes MK, Seto Y, Monroe SS, Glass RI, 1997. Correlation of patient immune responses with genetically characterized small round-structured viruses involved in outbreaks of nonbacterial acute gastroenteritis in the United States, 1990 to 1995. J Med Virol 53 :372–383.

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  • 21

    Koopmans M, Vennema H, Heersma H, van Strien E, van Duynhoven Y, Brown D, Reacher M, Lopman B, 2003. Early identification of common-source foodborne virus outbreaks in Europe. Emerg Infect Dis 9 :1136–1142.

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    Farkas T, Zhong WM, Jing Y, Huang PW, Espinosa S, Martinez M, Morrow N, Ruiz-Palacios AL, Pickering GM, Jiang X, 2004. Genetic diversity among sapoviruses. Arch Virol 149 :1309–1323.

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  • 23

    Bon F, Ambert-Balay K, Giraudon H, Kaplon J, Le Guyader S, Pommepuy M, Gallay A, Vaillant V, de Valk H, Chikhi-Brachet R, Flahaut A, Kohli E, 2005. Molecular epidemiology of caliciviruses detected in sporadic and outbreak cases of gastroenteritis in France from December 1998 to February 2004. J Clin Microbiol 43 :4659–4664.

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  • 24

    Cheng AC, McDonald JR, Thielman NM, 2005. Infectious diarrhea in developed and developing countries. J Clin Gastroenterol 39 :757–773.

 

 

 

 

Detection and Characterization of Human Caliciviruses Associated with Sporadic Acute Diarrhea in Adults in Djibouti (Horn of Africa)

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  • 1 Laboratoire de Biologie Clinique, Groupement Médico Chirurgical Bouffard, République de Djibouti; Laboratoire de Biologie Clinique, Hôpital d’Instruction des Armées du Val de Grâce, Paris, France; Laboratoire de Virologie, Reference Laboratory for Enteric Viruses, Hopital du Bocage, Dijon, France; Département Epidémiologie et Santé Publique Nord, Ecole d’Application du Service de Santé des Armées, St Mandé, France

Recent advances in molecular diagnostics have allowed us to recognize Human caliciviruses (HuCVs) as important agents of acute diarrhea in industrialized countries. Their prevalence and genetic diversity in developing countries remains unknown. We report on the characterization of HuCVs among adults presenting acute diarrheas in Djibouti; 108 stool samples collected were screened by EIA, RTPCR, or cell cultures for the group A Rotaviruses, Adenoviruses, Astroviruses, and HuCVs, which were further characterized by genotyping. Among stool samples screened for HuCVs, 25.3% were positive. The other enteric viruses were less prevalent. The 11 HuCV strains sequenced revealed a large diversity (3 sapoviruses and 8 noroviruses). GII strains noroviruses were predominant, five were newly described genotypes, and two were recombinant with a pol gene related to GGIIb strains with the particularity to associate a unique pol gene to different capsid genes. These results could help to the knowledge of HuCV infections in Tropical Africa.

INTRODUCTION

Acute infectious diarrhea represents a public health concern throughout the world. In industrialized countries, the role and the diversity of the 4 main viruses causing gastroenteritis, group A rotaviruses (RV), human caliciviruses (HuCVs), astroviruses (AsV), and enteric adenoviruses (AdV) have now been well documented. HuCVs have notably been identified as the second leading cause of acute gastroenteritis in young children1 and as a major cause of non-bacterial gastroenteritis in sporadic and outbreak cases in all age groups.24 HuCVs are a very diverse group of single-stranded RNA viruses of the Caliciviridae family. They are divided into 2 genera, Norovirus and Sapovirus5; human noroviruses are divided into 3 distinct genogroups, GI, GII, and GIV, each including genotypes. The classification is constantly evolving with the discovery of new strains. Recently Kageyama and others6 proposed a classification with 31 genotypes (14 for GI and 17 for GII). At the same time, Vinje and others7 identified 15 genotypes in the GII. Also, Zheng and others8 defined 8 and 17 genotypes in the GI and II, respectively.

In Africa where acute diarrhea causes high morbidity and mortality in children under 5 years of age,9 the role and diversity of viruses other than RV has been sparsely documented, particularly among adults. Studies in Ghana, Malawi, and South Africa1012 have reported a frequency of 8.5–15.3% for HuCVs in hospitalized children with acute diarrhea. A rather large diversity with a predominance of GII strains and new described genotypes was reported in Ghana and Malawi.10,11

We report here a study that we conducted in Djibouti (Horn of Africa) in patients over 15 years old, most of them were European soldiers, during an 18-month period (2002–2004) with the aim to investigate the prevalence of enteric viruses among adults presenting with sporadic acute diarrhea and to determine the role and diversity of HuCVs in this African tropical area. Compared with pediatric data, data concerning sporadic acute diarrhea in adults are relatively rare. Hence the data we present in this study of sporadic diarrhea in adults are of particular interest, especially where military forces deployed overseas are concerned.

MATERIALS AND METHODS

Patients and samples.

Djibouti, situated in the Horn of Africa, is surrounded by Eritrea, Ethiopia, and Somalia; it is an important regional crossroads for trade and exchange. The total population of Djibouti is estimated about 600,000, two-thirds of which live in the city of Djibouti. The French Military Hospital Bouffard (Djibouti city) is open to expatriates (French, American, and other European soldiers are the majority), Djiboutians (especially soldiers and their families), and more rarely patients from other countries of the Horn of Africa living in Djibouti.

Patients were enrolled in the study from September 2002 to February 2004. They were all over 15 years old, largely urban, seen for acute diarrhea (more than 3 stools per day for a duration of less than 7 days) at Bouffard Hospital. For each patient, the physician filled out an epidemiologic and clinical questionnaire, and a stool sample was immediately sent to the laboratory for bacteriological and parasitological analysis. Only negative samples were further tested for viruses.

Virus detection.

After shipment of frozen samples (stored at −80°C in dry ice) to the Teaching Military Hospital Val de Grâce in Paris, France, specimens were screened by enzyme immunoassay (EIA) for the presence of group A RV (IDEIA™ Rotavirus, Dako Ltd.), AdV (IDEIA™ Adenovirus, Dako Ltd.), and AstV (Amplified IDEIA™ Astrovirus, Dako Ltd). Cell cultures (Vero, MRC-5) were inoculated for AdV detection by immunofluorescence with monoclonal antibodies (11-020, Argene, France). HuCVs and also AsV were detected by a commercial reverse transcription polymerase chain reaction test (RT-PCR) (Calici/Astrovirus Consensus™, Argene, France).13

HuCVs characterization.

HuCVs were further characterized by genotyping by the National Reference Center for enteric viruses in Dijon, France. Strains were sequenced in the polymerase gene using the following primers: JV12-JV1314 for noroviruses and SR80/p11015,16 for sapoviruses. Some strains were sequenced in the capsid gene using primers G1SKF/G1SKR for genogroup I and G2SKF/G2SKR17 for genogroup II noroviruses, respectively, and 3 of them were also sequenced in the region spanning ORF1/2 junction as previously reported.18 Briefly, a RT-PCR was performed with primers JV12 and G1SKR or NI19 and Mon38320 depending on genogroup I or II, and the PCR products were cloned into the pGEM-T Easy Vector System (Promega Corporation, Madison, WI). The cycling conditions were as follows: one cycle of reverse transcription at 42°C for 15 min; PCR: denaturation for 2 min at 94°C; 40 amplification cycles with denaturation for 30 sec at 94°C, annealing for 1 min at 50°C, and extension for 1 min at 72°C; and a final cycle of incubation at 72°C for 15 min. Genotyping was realized by direct sequencing of the PCR products or plasmids using the ABI Prism Big Dye Terminator Cycle Sequencing Ready Reaction Kit on an automated sequencer (model 3100 DNA Sequencing System), both from Applera Corporation, Foster City, California, United States. Sequence alignments with the GenBank library were carried out by using Fasta Version 3.3t06. For the RNA polymerase, alignments were also performed with reference strains available in the database of the European Foodborne Viruses network.21

For the phylogenetic analyses, sequences were first aligned using CLUSTAL-W program in the PHYLIP format. Replicate data sets (N = 100) were generated by bootstrap re-sampling and were analyzed by the neighbor-joining method.

Nucleotide sequence accession numbers.

The nucleotide sequences determined in this study have been deposited in Genbank under accession numbers EF190918, EF190919, and EF190920 for samples VDG5, VDG50, and VDG66, respectively.

RESULTS

Virological testing.

A total of 108 fecal samples were collected; 103–105 samples were first analyzed with an immunologic test, and 75 were analyzed by RT-PCR (the difference between the total fecal samples collected and the samples analyzed was due to the amount of stool collected). Ninety-five questionnaires were usable. The characteristics of the population are presented in Table 1. In expatriates, the majority of diarrheas occurred during the first 2 months after arriving in Djibouti (Table 2). The average number of stools was 8 per day (predominately watery), and 33 cases needed treatment (30.5%) with anti-secretory agents (19/33) and intestinal coating agents (15/33). Only 6 patients (all with fever) received antibiotics.

Patients presenting nausea were the most often treated (19/44, 43%) in comparison with those without nausea (12/51, 23.5%), P = 0.03.

The results of virological testing are presented in Table 3. Nineteen samples (25.3%) were positive for HuCVs. The other enteric viruses were less prevalent: AstV: 4.8% and 4% by EIA and RT-PCR, respectively (the AstV were not phylogenetically investigated); AdV: 3.8% and 4.8% by EIA and IFI respectively; RV: 1.9%. No co-infection was detected. The ELISA technique allowed us to identify 5 AstV strains; the PCR only 3. However, the numbers analyzed were different for the 2 techniques (105 and 75 stool samples, respectively). For the AdVs, the difference can be explained by the higher expected sensitivity of the IFI. There was no significant difference (P > 0.05) between the patients with HuCV infection and patients with infection caused by another virus with regards to sex, origin, age, status, and number of stools per day (mean = 8/day). The frequency of asthenia was higher among patients infected by HuCVs (P = 0.03). There was no significant difference regarding the other symptoms (abdominal pain, vomiting, nausea, fever, myalgia), but this may arise from the low number of comparable cases of each virus in each age group.

HuCV characterization.

Eleven strains of HuCVs could be genotyped in the pol and/or the capsid region. A diversity of strains was observed; among them, 8 (73%) were noroviruses and 3 (27%) were sapoviruses. Two of the sapoviruses were related to Parkville virus (Accession number: U73124, 90.8% and 92% nucleotide identity in a 285 bp region of the pol gene, respectively) and one showed 85.8% nucleotide identity with Mexico/339/1991 virus (Accession number: AY157865).22 Among the noroviruses (Figure 1), 1 belonged to genogroup I (VDG50) and was close to Saitama-KU8G1/99/JP virus, which has been proposed recently as a new GI genotype (GI-11),6 6 belonged to genogroup II and 1, VDG63, to genogroup IV (Alphatron). The 6 GII strains were the following: 2 M7/99/US-like strains, VDG68 and VDG82 (new proposed genotype, GII-14),8 1 Idaho Falls, VDG66 (new proposed genotype GII-9),8 and 1 CS-E1-like strain, VDG39 (new proposed genotype GII-17)8 and 2 putative recombinants showing a pol gene that could not be assigned to any known genotype but was close to GGIIb recombinant strains.23 For one of them, a capsid gene belonging to GII-2 (Melksham genotype), the second capsid gene could not be sequenced.

DISCUSSION

Viral gastroenteritis is now well documented in industrialized countries, in contrast to Africa where epidemiologic data concerning viruses other than RV are still lacking. This may be attributed to the fact that methods for the detection of these viruses, especially HuCVs, are costly and require specialized laboratories. Moreover, local adaptation of surveys remains difficult because of preservation and shipment of samples.

In this survey, which was focused on the detection and characterization of Human Caliciviruses associated to acute diarrhea among adults (outside of the context of an outbreak) the results of virological testing confirm the relative frequencies generally observed in industrialized countries for HuCVs (and also RV, AstV, AdV) in this age group.24 RV, which remains the main agents of gastroenteritis among children is more rare in adults, HuCVs being the most prevalent in this age group. It is important to recognize the diversity of HuCVs strains that were probably contracted in Djibouti. We sequenced 11 of the HuCV detected and observed a large diversity of strains with 3 sapoviruses and 8 noroviruses in this area. Among noroviruses, GII strains were predominant as previously shown in industrialized countries but also more recently in African countries.1012 Five of the 8 noroviruses were newly described genotypes, GI-11,6 GII-9, GII-14, and GII-178 and 2 of them were recombinant strains showing a pol gene related to GGIIb strains. These strains, which were detected first in 2000 in France23 have been predominant in Europe since 2004; they have the particularity to associate a unique pol gene with different capsid genes, here belonging to GII-2 genotype. Of note, a strain (E673) showing a great similarity with strain Djibouti VDG5 (97.7% identity in the region spanning ORF1/2, Acc. N° AY682549) has been previously reported in France in 2004.18 Such a diversity with new described genotypes and recombinant strains has also been reported in Ghana (rGII-8/GII14)10 and in Malawi (GII/11, GII/13, GII/16, GII/20).11

In conclusion, this study shows the occurrence and diversity of HuCVs among adults presenting acute diarrheas in a tropical area (Djibouti, Horn of Africa). Considering a virus as readily transmissible as norovirus, we cannot judge if the strains are really endemic and if the traffic in and out of Djibouti has played a role in the introduction of new strains from elsewhere. The majority of our patients were European soldiers at the beginning of their deployment in Djibouti. Because their deployment in other countries before coming to Djibouti were for months at a time, it is likely that they contracted the diarrhea in Djibouti. Moreover they did not present any gastroenteritis before their arrival. Still, it is difficult to extrapolate our findings to the Djiboutian population in general. Surely, the development of RT-PCR assays among some references laboratories in tropical Africa should be considered to survey those viruses.

Table 1

Characteristics of the population

* French soldiers posted in Djibouti (2–3 years).
Sex (N = 108)Male 86 (80%)Female 22 (20%)Ratio (M/F) 3.9
Origin (N = 108)European 82 (76%)Djiboutian 17 (16%)Others 9 (8%)
Age (y)Mean 29.5Median 29Range [15–49]
Status (N = 108)Military* 77 (71%)Civilian 31 (29%)
Table 2

Time after arrival in Djibouti and characteristics of the diarrhea

Delay arrival date/First clinical signs
    Mean 1 monthMedian 2 monthsRange [1 day–2 years]
Number of stools/day
    Mean 8Median 8Range [1–24]
Stool aspect (N = 65)
    Watery 48 (74%)Mucous 4(6%)Bloody 2 (3%)Other 11 (17%)
Table 3

Results of the Virological testing

Stool samples (N)VirusMethodPositive samples (N)%
105AdenovirusEIA43.8
105AstrovirusEIA54.8
103RotavirusEIA21.9
105AdenovirusIFI54.8
75CalicivirusRT-PCR1925.3
75AstrovirusRT-PCR34
Figure 1.
Figure 1.

Relationships among pol (A) and capsid (B) nucleotide sequences of 8 norovirus strains isolated in Djibouti from 2002 to 2003 and prototype viruses using a neighbor-joining tree (Phylip version 3.6). The input alignment file was generated using Clustal W version 1.8. The Genbank accession numbers are as follows: Norwalk: M87661; Southampton: L07418; Desert Shield: U04469; Chiba: AB022679; Musgrove: AJ277614; Hesse: AF093797; Winchester: AJ277609; Boxer: AF538679; SaitamaKU8GI/99/JP: AB058547; Hawaii: U07611; Melksham: X81879; Toronto: U2030; Bristol: X76716; Hillingdon: AJ277607; Seacroft: AJ277620; Leeds: AJ277608; Amsterdam: AF195848; Idaho-Falls: AY054299: Erfurt-546: AF427118; Limburg: AY077644; SW918: AB074893; Wortley: AJ277618; Fayetteville: AY113106; M7: AY130761; J23: AY130762; Tiffin: AY502010; CS-E1: AY502009; SaitamaT29: AB112221; Alphatron: AF195847.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 78, 3; 10.4269/ajtmh.2008.78.522

*

Address correspondence to Jérôme Maslin, Laboratoire de Biologie Clinique, Groupement Médico Chirurgical Bouffard, SP 85024–00812 Armées-Djibouti. E-mail: maslin_j@yahoo.com

Authors’ addresses: Jérôme Maslin, Laboratoire de Biologie Clinique, Groupement Médico Chirurgical Bouffard, SP 85024–00812 Armées – Djibouti, E-mail: maslin_j@yahoo.com. Elisabeth Nicand, Laboratoire de Biologie Clinique, Hôpital d’Instruction des Armées du Val de Grâce, 74 Bd de Port Royal, 75230 Paris cedex 05, France. Katia Ambert-Balay, Laboratoire de Virologie-Reference Laboratory for Enteric Viruses-Hôpital du Bocage, Service de Microbiologie Medicale, 21079 Dijon cedex, France. Christine Fouet, Laboratoire de Biologie Clinique, Hôpital d’Instruction des Armées du Val de Grâce, 74 Bd de Port Royal, 75230 Paris cedex 05, France. Jérôme Kaplon, Laboratoire de Virologie-Reference Laboratory for Enteric Viruses-Hôpital du Bocage, Service de Microbiologie Medicale, 21079 Dijon cedex, France. Rachel Haus, Département Epidémiologie et Santé Publique Nord-Ecole d’Application du Service de Santé des Armées–Hôpital d’Instruction des Armées Bégin, 69 Av de Paris, 00498 Armées, St. Mandé, France. Pierre Pothier, Laboratoire de Virologie-Reference Laboratory for Enteric Viruses-Hôpital du Bocage, Service de Microbiologie Medicale, 21079 Dijon cedex, France. Evelyne Kohli, Laboratoire de Virologie-Reference Laboratory for Enteric Viruses-Hôpital du Bocage, Service de Microbiologie Medicale, 21079 Dijon cedex, France.

Acknowledgments: The authors thank Dr. R. Thiel for the proofreading of this article. We also gratefully acknowledge the contributions by Drs. J. J. Depina, P. Mathecowitsch, and H. Dampierre.

REFERENCES

  • 1

    Bon F, Fascia P, Dauvergne M, Tenenbaum D, Planson H, Petion AM, Pothier P, Kohli E, 1999. Prevalence of group A rotavirus, human calicivirus, astrovirus, and adenovirus type 40 and 41 infections among children with acute gastroenteritis in Dijon, France. J Clin Microbiol 37 :3055–3058.

    • Search Google Scholar
    • Export Citation
  • 2

    Chikhi-Brachet R, Bon F, Toubiana L, Pothier P, Nicolas JC, Flahault A, Kohli E, 2002. Virus diversity in a winter epidemic of acute diarrhea in France. J Clin Microbiol 40 :4266–4272.

    • Search Google Scholar
    • Export Citation
  • 3

    De Wit MA, Koopmans MP, Kortbeek LM, van Leeuwen NJ, Bartelds AI, van Duynhoven YT, 2001. Gastroenteritis in sentinel general practices, The Netherlands. Emerg Infect Dis 7 :82–91.

    • Search Google Scholar
    • Export Citation
  • 4

    Fankhauser RL, Monroe SS, Noel JS, Humphrey CD, Bresee JS, Parashar UD, Ando T, Glass RI, 2002. Epidemiological and molecular trends of “Norwalk-like viruses” associated with outbreaks of gastroenteritis in the United States. J Infect Dis 186 :1–7.

    • Search Google Scholar
    • Export Citation
  • 5

    Green KY, 2001. Human caliciviruses. Green KY, Kapikian RC, eds. Lippincott Williams and Wilkins Fields Virology. Fourth Edition. New York: Lippincott Williams and Wilkins, 841–873.

  • 6

    Kageyama T, Shinohara M, Uchida K, Fukushi S, Hoshino FB, Kojima S, Takeda N, Katayama K, 2004. Coexistence of multiple genotypes, including newly identified genotypes, in outbreaks of gastroenteritis due to Norovirus in Japan. J Clin Microbiol 42 :2988–2995.

    • Search Google Scholar
    • Export Citation
  • 7

    Vinje J, Hamidjaja RA, Sobsey MD, 2004. Developmental and application of a capsid VP1 (region D) based reverse transcription PCR assay for genotyping of genogroup I and II noroviruses. J Virol Methods 116 :109–117.

    • Search Google Scholar
    • Export Citation
  • 8

    Zheng DP, Ando T, Fankhauser RL, Beard RS, Glass RL, Monroe SS, 2006. Norovirus classification and proposed strain nomenclature. Virology 15 :312–323.

    • Search Google Scholar
    • Export Citation
  • 9

    Ouattara FS, Ekaza E, Kacou-n’douba A, Acoua-Koffi GC, Dosso C, 2004. Screening for Calicivirus in children under five years of age, in an Abidjan low-income district. Med Mal Infect 34 :566–567.

    • Search Google Scholar
    • Export Citation
  • 10

    Armah GE, Gallimore CI, Binka FN, Asmah RH, Green J, Ugoji U, Anto F, Brown DWG, Gray J, 2006. Characterization of norovirus strains in rural Ghanaian children with acute diarrhea. J Med Virol 78 :1480–1485.

    • Search Google Scholar
    • Export Citation
  • 11

    Dove W, Cunliffe NA, Gondwe JS, Broadhead RL, Molyneux ME, Nakagomi O, Hart CA, 2005. Detection and characterization of human caliciviruses in hospitalized children with acute gastroenteritis in Blantyre, Malawi. J Med Virol 77 :522–527.

    • Search Google Scholar
    • Export Citation
  • 12

    Smit TK, Steele AD, Peenze I, Jiang X, Estes MK, 1997. Study of Norwalk virus and Mexico virus infections at Ga-Rakuwa Hospital, Ga-Rankuwa, South Africa. J Clin Microbiol 35 :2381–2385.

    • Search Google Scholar
    • Export Citation
  • 13

    Bon F, Giraudon H, Sancey C, Barranger C, Joannes M, Pothier P, Kohli E, 2004. Development and evaluation of a new commercial test allowing the simultaneous detection of noroviruses. J Clin Microbiol 42 :2218–2220.

    • Search Google Scholar
    • Export Citation
  • 14

    Vinje J, Koopmans MP, 1996. Molecular detection and epidemiology of small round-structured viruses in outbreaks of gastroenteritis in the Netherlands. J Infect Dis 174 :610–615.

    • Search Google Scholar
    • Export Citation
  • 15

    Le Guyader F, Estes MK, Hardy ME, Neill FH, Green J, Brown DW, Atmar RL, 1996. Evaluation of a degenerate primer for the PCR detection of human caliciviruses. Arch Virol 141 :2225–2235.

    • Search Google Scholar
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Author Notes

Reprint requests: Jérôme Maslin, HIA Ste Anne, Bd ste Anne-BP 600, 83800 Toulon Armées, France, E-mail: maslin_j@yahoo.com.
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