Historically, clade H of MeV was associated with Asian countries, with genotype H1 being prevalent in China [27
], and genotype H2 linked to Vietnam [26
]. Baseline virological surveillance was not conducted in many Asian countries so the exact distribution of the clade H viruses in the pre-vaccine era is unknown.
This report contains the first analysis of the genetic characteristics of MeVs circulating in Taiwan over the seventeen year period from 1992 to 2008. In Taiwan, measles vaccination started in 1978, but epidemiologic information was not available until 1991. Laboratory-based surveillance was initiated in 1991, but routine virological sampling did not occur until 2002. Before 2000, only serum samples were collected and the percentage of sampling from all reported cases was variable (range: 52% to 85%). The low sampling rate from 1995, 1996, and 1999, of 59.5%, 59.6%, and 52.2% respectively, could have contributed to the absence of confirmed measles cases for those years.
Even though virological surveillance was not conducted in Taiwan before 1992, the data presented here suggest that MeV genotype H1, the most frequently detected genotype in the study, represented the indigenous genotype in Taiwan. Genotype H1 viruses were detected almost every year beginning in 1992 with the exception of 1995, 1996, 1998, 1999, and 2004 (Table ). Importation of measles from China was evident beginning in 2001 and accounted for 10 of 14 detections of genotype H1 after 2006. It is interesting to note that genotype H1 viruses were detected in Taiwan before they were documented in China. It is also possible that genotype D3, which was an indigenous genotype in Asian countries including the Philippines, could have been an endemic genotype in Taiwan at one time [17
] although D3 was only detected twice in 1992 and 2000.
Recent virological surveillance has documented the spread of MeV in the Western Pacific Region. A large measles outbreak that occurred in Korea in 2000 was caused by genotype H1 viruses [28
] and genotypes H1 and D9 were imported into Japan [22
]. The most recent outbreaks in Japan were due to importation of genotype D5 [33
]. This report documents the importation of MeV into Taiwan which began to introduce the foreign laborers from countries of Indonesia, Malaysia, Philippines, Thailand, and Vietnam in the beginning of 1989. The number of foreign workers reached 330,000 by end of 2006, accounting for 1.4% of the total population. The multiple genotypes and sporadic cases detected after 2003, except for two cases in 2005, and one in 2008, were all documented to be the result of importation and the genotypes detected, D3, D5, D9, G2, H1 and H2, are or were circulating in nearby Asian countries. The observation that two genotypes, H1 (4 cases) and H2 (1 case), were detected in the 1994 outbreak implied that there were at least two different chains of transmission associated with the outbreak.
In the dendrogram derived from the N gene sequences (Figure ), two clusters of sequences within genotype H1 were observed. The majority of the sequences were more closely related to the H1 reference strain and related viruses have been detected on an ongoing basis in China where this group of viruses is referred to as cluster 1 [25
]. Five of the sequences from Taiwan, including MVs/Taipei.TWN/36.97, MVs/Taoyuan.TWN/45.01, MVs/Taipei.TWN/26.02, MVs/Taichung.TWN/36.02/1, and MVs/Taipei.TWN/36.02/2, were clustered together and were more distinct from H1 reference strain. This group of viruses has also been detected in China and is referred to as cluster 2 [25
The diversity of genotypes and the low number of cases in Taiwan is similar to what has been described in other countries that are in elimination phases of measles control [9
]. The situation in Taiwan is different from some other countries in the elimination phase because the genotype H1 is continually being reintroduced by importation from neighboring Asian countries, so it is difficult to document interruption of transmission of the suspected indigenous genotype. However, both molecular and epidemiologic data were used to link the more recently detected genotype H1 viruses to international importation. While virological surveillance will help to document the sources of measles cases, formal documentation of elimination will depend on meeting a number of criteria, from both laboratory-based and epidemiologic studies. Of course, the nosocomial measles outbreak that occurred in 2008 highlighted the vulnerability of infants younger than 12 months of age, unimmunized adults, and the high risk of importation associated with international travel. These events underscored the importance of strengthening immunization programs, disease surveillance, and laboratory confirmation.