- Open Access
Review of the temporal and geographical distribution of measles virus genotypes in the prevaccine and postvaccine eras
© Riddell et al; licensee BioMed Central Ltd. 2005
- Received: 03 June 2005
- Accepted: 22 November 2005
- Published: 22 November 2005
Molecular epidemiological investigation of measles outbreaks can document the interruption of endemic measles transmission and is useful for establishing and clarifying epidemiological links between cases in geographically distinct clusters. To determine the distribution of measles virus genotypes in the prevaccine and postvaccine eras, a literature search of biomedical databases, measles surveillance websites and other electronic sources was conducted for English language reports of measles outbreaks or genetic characterization of measles virus isolates. Genotype assignments based on classification systems other than the currently accepted WHO nomenclature were reassigned using the current criteria. This review gives a comprehensive overview of the distribution of MV genotypes in the prevaccine and postvaccine eras and describes the geographically diverse distribution of some measles virus genotypes and the localized distributions of other genotypes.
- Measle Virus
- Measle Vaccine
- Subacute Sclerosing Panencephalitis
- Measle Case
Although measles virus (MV) is serologically monotypic, the genetic characterization of wild-type viruses has identified eight clades (A – H), which have been divided into 22 genotypes and one proposed genotype. Clades B, C, D, G and H each contain multiple genotypes (B1 – 3, C1 – 2, D1 – 10, G1 – 3, H1 – 2) while clades A, E and F each contain a single genotype (A, E, F) [1, 2]. The sequences of the vaccine strains indicate that the wild type viruses from which they were derived were all members of genotype A. All measles genotypes can be neutralized by serum from vaccinated persons in vitro, although with varying efficiency [3, 4]. There are no known biological differences between viruses of different genotypes. Specific measles genotypes are not associated with differences in severity of disease, likelihood of developing severe sequela such as subacute sclerosing panencephalitis or inclusion body encephalitis, or variability in sensitivity of laboratory diagnosis.
Analysis of the variability in the nucleotide sequences of wild-type MVs has enabled the use of molecular epidemiologic techniques for measles surveillance. The molecular data, when used in conjunction with standard case reporting and investigation, can help to identify epidemiological links between geographically distinct cases and outbreaks as well as track importations of MV. [5–7]. Also, approximately 5% of vaccine recipients experience mild symptoms (rash and fever) after vaccination and these cases could be misclassified as wild-type measles . Genetic characterization of viral isolates or RT-PCR products is the only laboratory test that can differentiate between vaccine-associated cases and wild-type infection [6, 9, 10].
In 1998, the World Health Organization (WHO) recommended a standard protocol for the designation of measles genotypes. These recommendations, updated in 2001 and 2003, also included a standard analysis protocol and designation of standard reference strains (see Additional file 2) against which all newly characterized isolates should be compared [2, 11, 12]. The minimum amount of sequence data required to assign a virus to a genotype are the 450 nucleotides encoding the carboxy terminus of the N protein. The entire sequence of the coding region of the H gene should be obtained from representative isolates . New genotypes are designated if the nucleotide sequence differs from the closest reference sequence by more than 2.5% in N and 2.0% in H . Additionally, phylogenetic analysis should produce similar tree topographies using at least two different analysis methods. Several isolates or clinical specimens should be sequenced and at least one viral isolate should be available as the reference strain. Finally, new genotype classifications should be useful for epidemiological studies, by providing a means to identify the source or transmission pathway of infection and by contributing to our understanding of the global distribution of MV genotypes .
The purpose of this summary is to collate all available reports of MV genotypes and to standardize the published genotype nomenclature, according to the current WHO criteria, with the aim of giving a comprehensive overview of the distribution of MV genotypes in the prevaccine and postvaccine eras.
An examination of the National Library of Medicine "PubMed"  search engine using the keyword "measles" combined with "genotypes" and "sequence" was performed to identify English language publications or abstracts describing measles genotyping.
Additional sources included the reference lists of articles identified by "PubMed" and electronic sources such as the CDC and PAHO measles network Internet pages and the NCBI Genbank website [14–16]. Measles outbreak alerts were received through the WHO network, which distributes outbreak notifications. In addition, subscription based electronic newsletters such as ProMED mail  and Immunization newsbrief  were scrutinized for information relating to measles outbreaks. Direct contact was made with the notifying laboratory or health unit requesting genotype information if available.
A table produced by participants at the 1998 WHO meeting listed older classification systems and the comparable genotype classifications under the universally accepted system. This table was used to reclassify genotypes cited in publications prior to 1998 . In some cases, later publications from the same or other groups were used to assign current genotypes to viruses classified before 1998.
One hundred and twenty eight studies were identified through the PubMed search, 67 of which described the genotype of MV isolates. Four internet websites were identified (including Genbank) and a further 27 articles were identified from the reference lists of cited publications or from outbreak notification lists such as ProMED  and Immunization Newsbrief .
Distribution of MV genotypes by WHO geographical region 1950s – 2004. Countries in which MV virus has been detected. No distinction has been made between endemic transmission or instances of MV importation. (data reflects publications available as of August 2005). Refer to Additional file 1 for details of endemic transmission and imported measles cases and for complete referencing of data.
Romania, UK Finland, Russia, Czech Republic, Slovakia
Brazil, USA, Argentina,
Gabon South Africa, Angola
Gambia, Nigeria, Kenya, Ghana, Algeria, Cameroon, Rep. of Congo, Dem. Rep. of Congo Burkina Faso, Equatorial Guinea
Sudan, Tunisia, Libya
France, Spain Germany, UK,
Nth Ireland, Spain, Germany
USA, Canada, Argentina
Austria, France, Belgium, Netherlands, Czech Republic, Slovakia, Spain, Italy, Germany, UK, Luxembourg, Denmark,
USA, Brazil, Canada,
UK, Nth Ireland
South Africa, Zambia
Ireland, UK, Spain
Micronesia, Philippines, PNG, Japan, Australia, Taiwan
South Africa, Namibia, Kenya, Ethiopia
Pakistan, Lebanon, Afghanistan, Syria, Iran
UK, Denmark, Netherlands, Germany, Spain, Croatia, Russia,
Japan, Malaysia, Micronesia, Australia, New Zealand, Cambodia, Guam, Rep. of Korea
South America, USA, Canada, Brazil
UK, Ireland, Spain, Germany, Austria, Italy, Greece, Croatia, Turkey, Ukraine, Poland, Russia, Luxembourg, Bosnia, Israel, Norway, Denmark, Netherlands
USA, Canada, Brazil, Bolivia, Argentina, Uruguay, Dominican Republic \Haiti
Sri Lanka, Myanmar (Burma), India
UK, Germany, Sweden, Europe, France, Spain, Italy
El Salvador, USA, Canada, Mexico
India, Bangladesh, Nepal
UK, Spain, Yugoslavia, Albania, Italy, Lithuania
Netherlands, UK, Germany
E. Timor, Indonesia
Australia, China, New Zealand, Mongolia, Singapore, Japan, Rep. of Korea, Rep. of Marshall Islands
UK, Spain, Netherlands, Denmark, Germany
USA, Canada, Chile, Mexico
China, Vietnam, Australia
Routine molecular characterization of wild-type measles viruses was initiated in response to a global resurgence of measles disease in the late 1980s and the concurrent availability of sensitive techniques (e.g. RT-PCR and automated sequencing) for the investigation of viral genomes. Prior to that date, only a few isolates of measles were available for molecular characterization and reliable epidemiologic information was not available for many of these isolates. In the era before the widespread use of measles vaccine, genotypes A, C1, and D1 were detected. Genotype A virus includes the prototype Edmonston strain, the progenitor for most of the current measles vaccines. Analysis of MV sequences obtained from SSPE cases, resulting from initial infections that occurred during the 1950s and 1960s, detected genotypes C1, D1, E and F, providing further evidence that genotype A was not the only genotype detected during the prevaccine era [19–24]. However, data from these earlier studies must be interpreted cautiously due to the large number of mutations in SSPE sequences and the lack of standardization. Of course, detection of various genotypes in SSPE cases reflects efforts to study this devastating illness and should not be taken as an indication that one genotype is more likely to cause SSPE than another . Retrospective sequence analysis of viral isolates collected during the 1970s showed continued detection of genotypes C1 and D1 and the first detections of genotypes C2, D2, D4, E and F.
As virologic surveillance expanded in the late 1980s and 1990s, the number of genotypes detected in cases and outbreaks increased substantially to include the 23 genotypes now recognized by the WHO. However, some genotypes (B1, D1, E, F, G1) have not been detected in the last 15 years and are considered inactive.
Genotype A has been detected in acute cases of measles in South and North America, China, Japan, Eastern Europe, Finland and the UK over the last 40 years. Since, it is difficult to distinguish wild-type viruses in genotype A from vaccine strains, these reports must be interpreted with caution since some of the sequences may have been derived from vaccine associated cases or been the result of laboratory contamination [22, 26, 27]. In the future, detection of genotype A viruses in association with acute cases of measles will need to be thoroughly scrutinized and additional sequence data will need to be obtained from both clinical samples and corresponding viral isolates.
Genotype B2, previously considered inactive , has recently been detected in South Africa and Angola . Genotype B3 was first detected in 1993 in Gambia but has subsequently been detected in cases from Cameroon, Nigeria, Ghana, Burkina Faso, DR Congo and the Sudan. This genotype is the endemic genotype of West and Central Africa and has been imported into numerous countries including France, Germany and the USA.
Outbreaks involving genotype C1 have occurred in Canada, Japan, Germany and most recently in the early 1990s in Argentina, which was the last reported outbreak involving genotype C1 circulation. Genotype C2 has circulated widely throughout the European continent and has been exported to the USA and Canada from France, Italy and Germany, where it was known to be an endemic genotype until 2001. This genotype was also identified in Australia from 1990 to 1991 and Morocco in 1998 & 1999. An importation of genotype C2 to the USA was linked with travel from Zimbabwe in 1998 although there are no reports to indicate that this strain was circulating in Southern Africa during this time .
Characterization of archived MV isolates in Australia from 1971, suggest that genotype D1 may have been the endemic strain in Australia during the pre-vaccine era. Sequences from SSPE cases in Northern Ireland and the UK indicate that genotype D1 was also detected in Britain before the widespread use of vaccine. Genotype D1 has not been detected since 1986 and is considered inactive. Genotype D2 appears to have been the endemic strain of Southern Africa from the late 1970s to 2000. This genotype was also responsible for the large outbreak in Ireland in 1999 – 2000, which resulted in importations to both the UK and USA. Genotype D3 is currently endemic in Papua New Guinea and possibly the Philippines, given that several measles cases in the USA have been linked with travel from the Philippines. Additionally this genotype has been associated with a case of SSPE in South Africa, and has been detected in Australia, USA and Canada, the UK and Denmark, in most cases with epidemiological links of importation from Japan or the Philippines. Genotype D4 is widely distributed and has been associated with multiple outbreaks on the Indian sub-continent, East and South Africa and a large outbreak in Quebec Province, Canada in 1989. Recently genotype D4 viruses, imported from the Indian sub-continent and East and South Africa, have been epidemiologically linked with cases in Canada, the USA, the UK, other European countries and Australia. Genotypes D4 and D2 appear to have been co-circulating in Southern Africa from the late 1970s to the late 1990s. Genotype D5 is endemic in Cambodia and has been associated with measles cases detected in the Americas, the UK, Germany and Australia. Epidemiological investigations have identified Japan and Thailand as the main sources for these importations. Until recently both genotype D3, and genotype D5 were endemic in Japan [26, 29–31]. However, recent evidence suggests that these genotypes may no longer be predominant in Japan . Genotype D6 has circulated widely throughout the European continent and may have been the endemic genotype of Europe, in conjunction with genotype C2, since the 1990s. This genotype is endemic in Turkey  and the Russian Federation . Genotype D7 circulated in the UK and Australia during the 1980s. Chains of transmission of this genotype have been associated, through epidemiological investigations, with Sweden and other European countries, including Italy where it was identified in the large measles outbreak in 2002. Genotype D7 has been imported into the US from multiple European sources from 2001 to 2003. Recently this genotype replaced genotypes C2 and D6 as the most commonly isolated genotype in Germany . Genotype D8 appears to be co-circulating with genotype D4 on the Indian sub-continent and Ethiopia, although the first known description of this genotype was in the UK, from where it has been regularly detected. However, investigations have linked UK cases with importations of virus not only from the Indian sub-continent but also from the Balkans and Oman . Genotype D8 has been imported into Australia and the USA from India and Bangladesh. Genotype D9, first described after importation to Australia from Indonesia (Bali) in 1999, was isolated during the large outbreak in 2000 – 2001 in Colombia and Venezuela. D9 was associated with an outbreak in Japan in 2004. Analysis of wild-type viruses isolated in Uganda in 2000–2002 indicated the presence of a new genotype, which has been proposed as genotype d10 [Genbank accession numbers AY923185 through AY923212] .
A few genotype E viruses and related SSPE cases were reported in the early 1970s. Genotype F sequences have been identified on two occasions, both were SSPE cases wherein acute measles infection was documented in 1967 and 1968. Thus both genotypes E and F probably circulated in the pre-vaccine era [19, 22].
Clade G, previously consisting of one genotype (G), has recently been expanded to contain three genotypes. The original genotype G (now G1) had not been detected since 1983 and was thought to have been extinct. However, recent investigations have identified two new genotypes (G2 & G3), both of which have been predominantly associated with chains of transmission within and importation from Indonesia and Malaysia [38–40].
Clade H viruses originally consisted of a single genotype but recently this clade has been expanded to contain two genotypes (H1 & H2). Both genotypes are predominant in the Asian and South East Asian regions. Genotype H1 has mainly been associated with transmission within or importations from China and was detected during the large measles epidemic in Korea in 2000 – 2001 . Genotype H1 may now be dominant in Japan [32, 42]. The WHO Western Pacific Regional Reference Laboratory for measles recently confirmed circulation of this genotype in Mongolia. Genotype H2, first described from samples recovered from China, has been more recently associated with importations from Vietnam .
Some genotypes of MV are associated with a particular geographical region, while other genotypes are more widely distributed. In particular, clade B is predominant in measles transmission in Sub Saharan and Central Africa, clade G in South East Asia and clade H in South East Asia and China. Clade D viruses, on the other hand, appear to be more widely distributed and are endemic in Eastern Africa, parts of Europe and the Indian sub-continent.
Determination of measles genotypes in countries that have not yet conducted molecular surveillance can be investigated, by proxy, from cases epidemiologically linked to imported cases. For example, the Philippines have not reported an endemic MV genotype but multiple importations to the USA associated with travel to, or contact with, the Philippines have resulted in the supposition that genotype D3 is the predominant circulating genotype in the Philippines [6, 44]. However, caution must be taken when identifying genotypes by proxy as the genotype detected may not be the type that is endemic in the region. In some cases, genotypes have been epidemiologically linked to countries with no history of circulation of that genotype. For example, genotype G2 has been reportedly associated with importations to the UK from Mexico, South Africa and Australia, none of which have reported endemic circulation of genotype G2 . In these cases infection may have occurred while the patient was in transit or at venues frequented by other travellers and might not reflect the circulating genotype.
Simultaneous circulation of multiple genotypes has been reported in several regions. Genotypes D3 and D5 co-circulated in Japan since the mid 1980s and the relative number of isolations changed over time. During the late 1980s genotype D3 was detected more frequently, but by 1990 D5 was more common [42, 45]. Genotypes D2 and D4 appear to be co-circulating throughout Eastern and Southern Africa. Genotypes C2 and D6 continue to be detected in some parts of Europe and North Africa .
Rima et al described a shift from genotype C2 to genotype D6 in Spain in the early 1990s . Santibanez et al recently demonstrated the shift from detection of mostly genotypes C2 and D6 in Germany to detection of mostly genotype D7 . The shift of genotypes occurs in countries that have sub-optimal measles control programs, resulting in interruption of endemic transmission for short periods. However, failure to maintain high levels of population immunity results in the accumulation of susceptible individuals and creates conditions that favour the rapid transmission of a newly introduced genotype. Therefore, the apparent genotype switching is most likely due to changes in the distribution of susceptible individuals in the region.
Nine new MV genotypes have been identified since 1990 reflecting increased surveillance of measles cases and technological advances, rather than recent evolution. The designation of new genotypes, such as the newly proposed genotype d10, is likely to continue as the molecular analysis of viral isolates becomes routinely integrated into more countries within the global WHO measles laboratory network and more sequence data are added to the database. For example, genotype B3 may eventually be reclassified as two separate genotypes since this genotype contains viruses in two distinct clusters [47–49]. Characterization of viruses imported into Australia has detected three previously unrecognised genotypes (D7, D9 & G3) due partly to the frequency of travel between South East Asia and Australia and also to the comprehensive measles surveillance conducted by Australian laboratories [7, 38, 50].
The mutation rate amongst field isolates of MV is low and appears to be random rather than driven by vaccine pressure or immune responses [3, 24, 26]. Within a genotype, nucleotide differences (virus lineage) can assist in distinguishing separate episodes of transmission [24, 51, 52]. In countries or regions with endemic (ongoing and constant MV transmission) measles, many lineages of a single genotype may co-exist; however as countries begin to move from endemic to epidemic measles (MV transmission resulting in a higher number of cases than normally expected, typically against a background of little or no MV transmission), the diversity of sequences within the circulating genotypes decreases [43, 54–57]. In fact, the genotype D6 virus associated with a large measles outbreak that occurred in several South American countries between 1996 and 1997 had identical N gene sequences suggesting rapid spread of a single lineage . Analysis of measles viruses circulating in Burkina Faso, before and after a mass vaccination campaign, showed that the number of circulating lineages was greatly reduced following the campaign. Sequence analysis of viruses isolated from outbreaks that occurred after the vaccination campaign suggested that virus was introduced from a single source .
Many recent measles outbreaks have been reported with no accompanying molecular genotyping investigations, for instance in Afghanistan , Niger  and the Philippines . These outbreaks highlight the need to extend molecular surveillance capabilities to regions where measles remains endemic. Recent studies have described the recovery of MV RNA by RT-PCR from oral fluid, dried blood and dried oral fluid [61–63]. These samples, which are easy to collect, prepare and transport by post to laboratories capable of MV genotyping, have the potential to extend molecular surveillance for measles virus to remote settings and countries with limited infrastructure. However conventional samples such as nasopharyngeal swabs, urine and peripheral blood lymphocytes should continue to be collected, if logistically possible, because of the higher sensitivity of these sample types for detecting MV RNA.
Molecular surveillance undertaken in the early stages of measles control can facilitate identification of endemic genotypes. Over time or after intervention programs continued molecular surveillance, in conjunction with case based epidemiological investigations, can detect the interruption of endemic transmission . Additionally, molecular analysis of specimens from cases facilitates both linkage to, and separation from, contemporaneous cases and clusters, assisting classical epidemiological investigations and the tracking of chains of transmission [7, 64].
Thanks to Doris Chibo, Graham Tipples, David Brown, Li Jin for helpful suggestions and clarification of genotypes included in the table. Thanks to Doris Chibo and Heath Kelly for critical review of the earlier drafts of the manuscript. MAR received funding through a National Health and Medical Research Council Public Health PhD Research Scholarship. The authors welcome amendments, additions and updates to the comprehensive table submitted as Additional file 1. Regularly updated versions of the additional file will be available from the measles Global Specialized Laboratory at the Centers for Disease Control and Prevention, Atlanta Georgia, USA http://www.cdc.gov/ncidod/dvrd/revb/measles/index.htm
- Rota PA, Bellini WJ: Update on the global distribution of genotypes of wild type measles viruses. J Infect Dis 2003, 187 (Suppl 1): S270-276. 10.1086/368042View ArticleGoogle Scholar
- World Health Organization: Nomenclature for describing the genetic characteristics of wild-type measles viruses (update). Part I. Wkly Epidemiol Rec 2001, 76: 242-247.Google Scholar
- Tamin A, Rota PA, Wang ZD, Heath JL, Anderson LJ, Bellini WJ: Antigenic analysis of current wild type and vaccine strains of measles virus. J Infect Dis 1994, 170: 795-801.View ArticlePubMedGoogle Scholar
- Klingele M, Hartter HK, Adu F, Ammerlaan W, Ikusika W, Muller CP: Resistance of recent measles virus wild-type isolates to antibody-mediated neutralization by vaccinees with antibody. J Med Virol 2000, 62: 91-98. 10.1002/1096-9071(200009)62:1<91::AID-JMV14>3.0.CO;2-BView ArticlePubMedGoogle Scholar
- Mulders MN, Truong AT, Muller CP: Monitoring of measles elimination using molecular epidemiology. Vaccine 2001, 19: 2245-2249. 10.1016/S0264-410X(00)00453-9View ArticlePubMedGoogle Scholar
- Rota PA, Liffick SL, Rota JS, Katz RS, Redd S, Papania M, Bellini WJ: Molecular epidemiology of measles viruses in the United States, 1997-2001. Emerg Infect Dis 2002, 8: 902-908.PubMed CentralView ArticlePubMedGoogle Scholar
- Chibo D, Riddell MA, Catton MG, Lyon M, Lum G, Birch CJ: Studies of measles viruses circulating in Australia between 1999 and 2001 reveals a new genotype. Virus Res 2003, 91: 213-221. 10.1016/S0168-1702(02)00273-3View ArticlePubMedGoogle Scholar
- Redd SC, Markowitz LE, Katz SL: Measles Vaccine. In Vaccines. 3rd edition. Edited by: Plotkin SA and Orenstein WA. Philadelphia, Saunders, W. B.; 1999:222 -2266.Google Scholar
- Jenkin GA, Chibo D, Kelly HA, Lynch PA, Catton MG: What is the cause of a rash after measles-mumps-rubella vaccination? Med J Aust 1999, 171: 194-195.PubMedGoogle Scholar
- Rota PA, Khan AS, Durigon E, Yuran T, Villamarzo YS, Bellini WJ: Detection of measles virus RNA in urine specimens from vaccine recipients. J Clin Microbiol 1995, 33: 2485-2488.PubMed CentralPubMedGoogle Scholar
- World Health Organization: Expanded Programme on Immunization (EPI). Standardization of the nomenclature for describing the genetic characteristics of wild-type measles viruses. Wkly Epidemiol Rec 1998, 73: 265-269.Google Scholar
- World Health Organization: Update of the nomenclature for describing the genetic characteristics of wild- type measles viruses: new genotypes and reference strains. Wkly Epidemiol Rec 2003, 78: 229-232.Google Scholar
- Centers for Disease Control and Prevention: Global Laboratory Network for Measles Surveillance : USA Genotyping Results 2000 - 2004.[http://www.cdc.gov/ncidod/dvrd/revb/measles/us_geno_rslt.htm]
- Pan American Health Organization: Measles main page.[http://www.paho.org/english/AD/FCH/IM/Measles.htm]
- Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Wheeler DL: GenBank: update. Nucleic Acids Res 2004, 32: D23-6. 10.1093/nar/gkh045PubMed CentralView ArticlePubMedGoogle Scholar
- International Society for Infectious Diseases: ProMED mail.[http://www.promedmail.org]
- Infectious Diseases Society of America: Immunization Newsbrief.[http://www.infoinc.com/imnews2/imnews.html]
- Rima BK, Earle JA, Yeo RP, Herlihy L, Baczko K, ter Meulen V, Carabana J, Caballero M, Celma ML, Fernandez-Munoz R: Temporal and geographical distribution of measles virus genotypes. J Gen Virol 1995, 76: 1173-1180.View ArticlePubMedGoogle Scholar
- Rota JS, Bellini WJ, Rota PA: Measles. In Molecular Epidemiology of Infectious Diseases. Edited by: Thompson RCA. London, Arnold; 2000:168-180.Google Scholar
- Rota PA, Bloom AE, Vanchiere JA, Bellini WJ: Evolution of the nucleoprotein and matrix genes of wild-type strains of measles virus isolated from recent epidemics. Virology 1994, 198: 724-730. 10.1006/viro.1994.1086View ArticlePubMedGoogle Scholar
- Christensen LS, Scholler S, Schierup MH, Vestergaard BF, Mordhorst CH: Sequence analysis of measles virus strains collected during the pre- and early-vaccination era in Denmark reveals a considerable diversity of ancient strains. APMIS 2002, 110: 113-122. 10.1034/j.1600-0463.2002.100201.xView ArticlePubMedGoogle Scholar
- Jin L, Beard S, Hunjan R, Brown DW, Miller E: Characterization of measles virus strains causing SSPE: a study of 11 cases. J Neurovirol 2002, 8: 335-344. 10.1080/13550280290100752View ArticlePubMedGoogle Scholar
- Rima BK, Earle JA, Baczko K, ter Meulen V, Liebert UG, Carstens C, Carabana J, Caballero M, Celma ML, Fernandez-Munoz R: Sequence divergence of measles virus haemagglutinin during natural evolution and adaptation to cell culture. J Gen Virol 1997, 78: 97-106.View ArticlePubMedGoogle Scholar
- Rima BK: Molecular biological basis of measles virus strain differences. In Measles and Poliomyelitis Vaccines, Immunization and Control. Edited by: Kurstak E. Vienna, Springer-Verlag; 1993:149-160.View ArticleGoogle Scholar
- Rota PA, Rota JS, Bellini WJ: Molecular epidemiology of measles virus. Semin Virol 1995, 6: 379-386. 10.1016/S1044-5773(05)80015-0View ArticleGoogle Scholar
- Bellini WJ, Rota PA: Genetic diversity of wild-type measles viruses: implications for global measles elimination programs. Emerg Infect Dis 1998, 4: 29-35.PubMed CentralView ArticlePubMedGoogle Scholar
- Smit SB, Hardie D, Tiemessen CT: Measles virus genotype B2 is not inactive: evidence of continued circulation in Africa. J Med Virol 2005,77(4):550-557. 10.1002/jmv.20491View ArticlePubMedGoogle Scholar
- Takahashi M, Nakayama T, Kashiwagi Y, Takami T, Sonoda S, Yamanaka T, Ochiai H, Ihara T, Tajima T: Single genotype of measles virus is dominant whereas several genotypes of mumps virus are co-circulating. J Med Virol 2000, 62: 278-285. 10.1002/1096-9071(200010)62:2<278::AID-JMV21>3.0.CO;2-1View ArticlePubMedGoogle Scholar
- Nakayama T, Mori T, Yamaguchi S, Sonoda S, Asamura S, Yamashita R, Takeuchi Y, Urano T: Detection of measles virus genome directly from clinical samples by reverse transcriptase-polymerase chain reaction and genetic variability. Virus Res 1995, 35: 1-16. 10.1016/0168-1702(94)00074-MView ArticlePubMedGoogle Scholar
- Katayama Y, Shibahara K, Kohama T, Homma M, Hotta H: Molecular epidemiology and changing distribution of genotypes of measles virus field strains in Japan. J Clin Microbiol 1997, 35: 2651-2653.PubMed CentralPubMedGoogle Scholar
- Zhou J, Fujino M, Inou Y, Kumada A, Aoki Y, Iwata S, Nakayama T: H1 genotype of measles virus was detected in outbreaks in Japan after 2000. J Med Virol 2003, 70: 642-648. 10.1002/jmv.10443View ArticlePubMedGoogle Scholar
- Guris D, Bayazit Y, Ozdemirer U, Buyurgan V, Yalniz C, Toprak I, Aycan S: Measles epidemiology and elimination strategies in Turkey. J Infect Dis 2003, 187 Suppl 1: S230-4.View ArticlePubMedGoogle Scholar
- Ignatyev G, Agafonov AP, Kameneva S, Atrasheuskaya A: Molecular epidemiological study of measles in Western Siberia (Russia) during 1995 - 2001: in XIIth International Congress of Virology. Volume Poster Abstract 143V- #V1302. IUMS Paris, France; 2002.Google Scholar
- Tischer A, Santibanez S, Siedler A, Heider A, Hengel H: Laboratory investigations are indispensable to monitor the progress of measles elimination--results of the German Measles Sentinel 1999-2003. J Clin Virol 2004, 31: 165-178. 10.1016/j.jcv.2004.05.007View ArticlePubMedGoogle Scholar
- Ramsay ME, Jin L, White J, Litton P, Cohen B, Brown D: The elimination of indigenous measles transmission in England and Wales. J Infect Dis 2003, 187 (Suppl 1): S198-207. 10.1086/368024View ArticleGoogle Scholar
- Muwonge A, Nanyunja M, Rota PA, Bwogi J, Lowe L, Liffick S, Bellini WJ, Sylvester S: New genotype of measles virus detected in Uganda. Emerg Infect Dis 2005,11(10):1522-1526.PubMed CentralView ArticlePubMedGoogle Scholar
- Chibo D, Riddell M, Catton M, Birch C: Novel measles virus genotype, East Timor and Australia. Emerg Infect Dis 2002, 8: 735-737.PubMed CentralView ArticlePubMedGoogle Scholar
- de Swart RL, Wertheim-van Dillen PM, van Binnendijk RS, Muller CP, Frenkel J, Osterhaus AD: Measles in a Dutch hospital introduced by an immuno-compromised infant from Indonesia infected with a new virus genotype. Lancet 2000, 355: 201-202. 10.1016/S0140-6736(99)04652-8View ArticlePubMedGoogle Scholar
- Rota PA, Liffick S, Rosenthal S, Heriyanto B, Chua KB: Measles genotype G2 in Indonesia and Malaysia. Lancet 2000, 355: 1557-1558. 10.1016/S0140-6736(05)74612-2View ArticlePubMedGoogle Scholar
- Na BK, Lee JS, Shin GC, Mi Shin J, Lee JY, Chung JK, Ha DR, Lee JK, Ma SH, Cho HW, Kang C, Kim WJ: Sequence analysis of hemagglutinin and nucleoprotein genes of measles viruses isolated in Korea during the 2000 epidemic. Virus Res 2001, 81: 143-149. 10.1016/S0168-1702(01)00346-XView ArticlePubMedGoogle Scholar
- Nakayama T, Zhou J, Fujino M: Current status of measles in Japan. J Infect Chemother 2003, 9: 1-7. 10.1007/s10156-002-0206-6View ArticlePubMedGoogle Scholar
- Xu W, Tamin A, Rota JS, Zhang L, Bellini WJ, Rota PA: New genetic group of measles virus isolated in the People's Republic of China. Virus Res 1998, 54: 147-156. 10.1016/S0168-1702(98)00020-3View ArticlePubMedGoogle Scholar
- Rota JS, Rota PA, Redd SB, Redd SC, Pattamadilok S, Bellini WJ: Genetic analysis of measles viruses isolated in the United States, 1995-1996. J Infect Dis 1998, 177: 204-208.View ArticlePubMedGoogle Scholar
- Kubo H, Iritani N, Seto Y: Co-circulation of two genotypes of measles virus and mutual change of the prevailing genotypes every few years in Osaka, Japan. J Med Virol 2003, 69: 273-278. 10.1002/jmv.10278View ArticlePubMedGoogle Scholar
- Santibanez S, Tischer A, Heider A, Siedler A, Hengel H: Rapid replacement of endemic measles virus genotypes. J Gen Virol 2002, 83: 2699-2708.View ArticlePubMedGoogle Scholar
- Truong AT, Kreis S, Ammerlaan W, Hartter HK, Adu F, Omilabu SA, Oyefolu AO, Berbers GA, Muller CP: Genotypic and antigenic characterization of hemagglutinin proteins of African measles virus isolates. Virus Res 1999, 62: 89-95. 10.1016/S0168-1702(99)00072-6View ArticlePubMedGoogle Scholar
- El Mubarak HS, van de Bildt MW, Mustafa OA, Vos HW, Mukhtar MM, Ibrahim SA, Andeweg AC, El Hassan AM, Osterhaus AD, de Swart RL: Genetic characterization of wild-type measles viruses circulating in suburban Khartoum, 1997-2000. J Gen Virol 2002, 83: 1437-1443.View ArticlePubMedGoogle Scholar
- Kouomou DW, Nerrienet E, Mfoupouendoun J, Tene G, Whittle H, Wild TF: Measles virus strains circulating in Central and West Africa: Geographical distribution of two B3 genotypes. J Med Virol 2002, 68: 433-440. 10.1002/jmv.10222View ArticlePubMedGoogle Scholar
- Chibo D, Birch CJ, Rota PA, Catton MG: Molecular characterization of measles viruses isolated in Victoria, Australia, between 1973 and 1998. J Gen Virol 2000, 81: 2511-2518.View ArticlePubMedGoogle Scholar
- Oliveira MI, Rota PA, Curti SP, Figueiredo CA, Afonso AM, Theobaldo M, Souza LT, Liffick SL, Bellini WJ, Moraes JC, Stevien KE, Durigon EL: Genetic homogeneity of measles viruses associated with a measles outbreak, Sao Paulo, Brazil, 1997. Emerg Infect Dis 2002, 8: 808-813.PubMed CentralView ArticlePubMedGoogle Scholar
- Taylor MJ, Godfrey E, Baczko K, ter Meulen V, Wild TF, Rima BK: Identification of several different lineages of measles virus. J Gen Virol 1991, 72: 83-88.View ArticlePubMedGoogle Scholar
- Last JM: A Dictionary of Epidemiology. 4th edition. New York, Oxford University Press; 2001.Google Scholar
- Mbugua FM, Okoth FA, Gray M, Kamau T, Kalu A, Eggers R, Borus P, Kombich J, Langat A, Maritim P, Lesiamon J, Tipples GA: Molecular epidemiology of measles virus in Kenya. J Med Virol 2003, 71: 599-604. 10.1002/jmv.10515View ArticlePubMedGoogle Scholar
- Horm SV, Dumas C, Svay S, Feldon K, Reynes JM: Genetic characterization of wild-type measles viruses in Cambodia. Virus Res 2003, 97: 31-37. 10.1016/S0168-1702(03)00219-3View ArticlePubMedGoogle Scholar
- Hanses F, Truong AT, Ammerlaan W, Ikusika O, Adu F, Oyefolu AO, Omilabu SA, Muller CP: Molecular epidemiology of Nigerian and Ghanaian measles virus isolates reveals a genotype circulating widely in western and central Africa. J Gen Virol 1999, 80: 871-877.View ArticlePubMedGoogle Scholar
- Mulders MN, Nebie YK, Fack F, Kapitanyuk T, Sanou O, Valea DC, Muyembe-Tamfum JJ, Ammerlaan W, Muller CP: Limited diversity of measles field isolates after a national immunization day in Burkina Faso: progress from endemic to epidemic transmission? J Infect Dis 2003, 187: S277-82. 10.1086/368036View ArticlePubMedGoogle Scholar
- Ahmad K: Measles epidemic sweeps through Afghanistan. Lancet 2000, 355: 1439. 10.1016/S0140-6736(05)74645-6View ArticlePubMedGoogle Scholar
- BBC News online: Niger: About 700 measles cases reported in capital Niamey.[http://news.bbc.co.uk]
- Deutsche Presse Agentur: Seven Children Die from Measles In Southern Philippine Village.[http://www.dpa.de]
- Nigatu W, Jin L, Cohen BJ, Nokes DJ, Etana M, Cutts FT, Brown DW: Measles virus strains circulating in Ethiopia in 1998-1999: Molecular characterisation using oral fluid samples and identification of a new genotype. J Med Virol 2001, 65: 373-380. 10.1002/jmv.2044View ArticlePubMedGoogle Scholar
- De Swart RL, Nur Y, Abdallah A, Kruining H, El Mubarak HS, Ibrahim SA, Van Den Hoogen B, Groen J, Osterhaus AD: Combination of Reverse Transcriptase PCR Analysis and Immunoglobulin M Detection on Filter Paper Blood Samples Allows Diagnostic and Epidemiological Studies of Measles. J Clin Microbiol 2001, 39: 270-273. 10.1128/JCM.39.1.270-273.2001PubMed CentralView ArticlePubMedGoogle Scholar
- Chibo D, Riddell MA, Catton MG, Birch CJ: Applicability of Oral Fluid Collected onto Filter Paper for Detection and Genetic Characterization of Measles Virus Strains. J Clin Microbiol 2005, 43: 3145-3149. 10.1128/JCM.43.7.3145-3149.2005PubMed CentralView ArticlePubMedGoogle Scholar
- Rota JS, Heath JL, Rota PA, King GE, Celma ML, Carabana J, Fernandez-Munoz R, Brown D, Jin L, Bellini WJ: Molecular epidemiology of measles virus: identification of pathways of transmission and implications for measles elimination. J Infect Dis 1996, 173: 32-37.View ArticlePubMedGoogle Scholar
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