Along with the implementation of measles case-based surveillance, measles vaccine-associated rash illness (VARI) cases were detected in China. To better understand the characteristics of VARI, 101 VARI cases confirmed by measles virus genotyping in 2011 to 2018 were analyzed in this study. With the decrease in measles incidence, the detection rate of VARI cases increased among the cases confirmed by genotyping. Compared with genotype H1 wild-type measles, VARI occurred throughout the year, without obvious seasonal distribution.
KEYWORDS: measles, vaccine-associated rash illness, epidemiological characteristics, clinical symptoms, genetic variation
ABSTRACT
Along with the implementation of measles case-based surveillance, measles vaccine-associated rash illness (VARI) cases were detected in China. To better understand the characteristics of VARI, 101 VARI cases confirmed by measles virus genotyping in 2011 to 2018 were analyzed in this study. With the decrease in measles incidence, the detection rate of VARI cases increased among the cases confirmed by genotyping. Compared with genotype H1 wild-type measles, VARI occurred throughout the year, without obvious seasonal distribution. Infants and children of ages 8 to 23 months were the main population of VARI. VARI mainly occurred within 14 days after measles vaccination. The number of VARI cases peaked on the 8th day after measles vaccination, which was later than that of genotype H1 wild-type measles cases with a measles vaccination history. VARI presents clinical symptoms similar to those of measles. The frequencies of the “3Cs” (cough, coryza, and conjunctivitis), Koplik spots, and complications in VARI cases were significantly lower than those in wild-type measles cases. In total, 94.06% of sequences from VARI cases were identical to measles vaccine strain S191 in the C-terminal 450-nucleotide sequence of the nucleoprotein (N-450) gene. A few substitutions were found in N-450 sequences of the VARI cases. The confirmation of VARI has become an emerging issue in the process of measles elimination. Rapid confirmation of VARI is critical for measles surveillance and will help to determine the response measures for measles, especially in measles preelimination and elimination settings. The suspected measles cases with measles-containing vaccine (MCV) vaccination were recommended to be tested by the laboratory to identify wild-type measles or VARI.
INTRODUCTION
Measles is a highly contagious vaccine-preventable disease caused by the measles virus (MeV) and is characterized by fever, maculopapular rash, and at least one of the “3Cs,” including cough, coryza, and conjunctivitis, as clinical symptoms. Before the introduction of the measles vaccine, measles was widespread worldwide, with high morbidity and mortality, especially in children. To date, a total of 24 MeV genotypes of eight clades (A to H) have been recognized by the World Health Organization (WHO) based on the C-terminal 450-nucleotide sequence of the nucleoprotein (N-450) gene and the entire coding region of the hemagglutinin (H) gene (1–4).
Live attenuated measles vaccines were developed in the 1960s, and a two-dose measles-containing vaccine (MCV) is recommended by the WHO to prevent infection by wild-type MeV. All measles vaccine strains were derived from genotype A, which has been extinct and is not associated with documented transmission in any part of the world (5, 6). Because MeV is a single serotype, the measles vaccine could protect susceptible populations from infection from all genotypes of wild-type MeV. In China, the measles vaccine S191 was developed using a locally isolated strain and has been used for measles immunization throughout China (7). With the wide implementation of the two-dose MCV strategy, the global incidence of measles has decreased significantly (8).
However, measles vaccine-associated rash illness (VARI) was detected during the measles case-based surveillance (9–12). VARI is a reaction that occurs after measles vaccination in 5 to 15% of recipients (13). VARI does not pose any health risk because there is no evidence for transmission of vaccine viruses (14). However, VARI might be severe in a vaccinated individual who is immunocompromised. Due to the similar clinical symptoms, VARI may be misdiagnosed as measles and lead to unnecessary initiation of control measures and a substantial waste of public health resources (15). To better understand the characteristics of VARI, in this study, a total of 101 VARI cases reported in China in 2011 to 2018 were analyzed based on epidemiological, clinical, and laboratory data.
MATERIALS AND METHODS
Source of VARI cases and wild-type genotype H1 measles cases.
A measles surveillance system (MSS) has been implemented in China since 2009 as a national case-based system of measles surveillance with laboratory support (16). The Chinese Measles Laboratory Network (CMLN) was established in 2001 and is composed of 1 national, 32 provincial, and 339 prefectural laboratories, which perform measles-specific IgM enzyme-linked immunosorbent assay (ELISA), real-time reverse transcription-PCR (RT-PCR), virus isolation, and genotype identification for the clinical specimens obtained from suspected measles cases (17). The high-quality surveillance of the MSS and CMLN provided strong support for measles elimination programs by providing both epidemiological and laboratory data in China.
According to the national measles surveillance program in China, the clinical samples of about 10% of measles surveillance cases are collected for MeV genotyping identification every year based on the principle of continuity and representativeness of measles surveillance in each province (18). Cases of VARI and wild-type measles were confirmed by MeV genotyping based on the N-450 nucleotide sequence in the laboratories of the CMLN (11, 19). In this study, VARI and genotype H1 wild-type measles cases with complete epidemiological, clinical, and genotyping information in 2011 to 2018 were collected to analyze the characteristics of VARI.
The annual measles incidence and the number of reported measles cases from 2011 to 2018 were obtained from the National Notifiable Disease Reporting System (NNDRS) of the Chinese Center for Disease Control and Prevention (China CDC). The epidemiological information from VARI and genotype H1 wild-type measles cases was collected from the MSS.
Epidemiological and statistical analyses.
The cases were stratified into seven groups based on age: <8 months, 8 to 23 months, 2 to 6 years, 7 to 19 years, 20 to 29 years, 30 to 39 years, and ≥40 years. The vaccination status of cases was collected by documentation of doses received or as recalled by the patient or patient's family. Comparisons of clinical symptoms and complications were conducted between VARI and genotype H1 wild-type measles cases. The number and rate of VARI and wild-type measles cases were calculated using Microsoft Excel. P values were computed using chi-square tests with R statistical software (R Project for Statistical Computing, R version 3.5.1). P values of <0.05 were considered statistically significant.
Identification and sequence analysis of MCV strains obtained from VARI cases.
Clinical samples, including throat swabs and/or urine samples, were collected from suspected measles cases in 2011 to 2018 in China. Virus isolation was conducted in the provincial laboratory. RT-PCR with primers MeV216/MeV214 and genotype identification were performed by the national laboratory as previously described (11, 20). If virus isolates were not available, the MeV genotype was confirmed by N-450 sequences directly obtained from clinical specimens. The alignment and genetic analyses of the N-450 sequence were performed with Molecular Evolutionary Genetics Analyses (MEGA) software (version 5.05). In this study, nucleotide positions are reported in reference to the genomic sequence of the Edmonston strain (MeV prototype strain, GenBank accession no. AF266288).
Ethics statement.
This study was approved by the second session of the Ethics Review Committee of the National Institute for Viral Disease Control and Prevention of the China CDC under ethics approval no. IVDC2018 no. 012, and the methods were performed in accordance with the approved guidelines.
RESULTS
Epidemiological characteristics of VARI.
In 2011 to 2018, a total of 173,462 measles cases were reported to the NNDRS in China. Of these cases, 15,169 cases were confirmed by genotyping based on the N-450 nucleotide sequence of MeV in the CMLN. A total of 101 VARI cases and 14,902 genotype H1 wild-type measles cases were confirmed (Table 1). The number of VARI cases each year was relatively stable, whereas measles cases associated with wild-type MeV exhibited a resurgence in 2013 to 2016 and then decreased substantially in 2017 to 2018. With the decrease in measles incidence, the detection rate of VARI cases gradually increased among the cases confirmed by genotyping during the measles case-based surveillance in China.
TABLE 1.
Number of measles cases and measles incidence from 2011 to 2018
| Yr | Measles incidence per milliona | No. of measles casesa | No. (%) of cases confirmed by genotypingb
|
||
|---|---|---|---|---|---|
| Total | Genotype H1 wild-type measles | VARI | |||
| 2011 | 7.4 | 9,943 | 294 | 288 (97.96) | 3 (1.02) |
| 2012 | 4.6 | 6,183 | 474 | 454 (95.78) | 6 (1.27) |
| 2013 | 20.4 | 27,646 | 2,327 | 2,217 (95.27) | 15 (0.64) |
| 2014 | 38.8 | 52,628 | 4,915 | 4,868 (99.04) | 24 (0.49) |
| 2015 | 31.1 | 42,361 | 3,969 | 3,952 (99.57) | 16 (0.40) |
| 2016 | 18.1 | 24,820 | 2,468 | 2,455 (99.47) | 10 (0.41) |
| 2017 | 4.3 | 5,941 | 421 | 397 (94.30) | 13 (3.09) |
| 2018 | 2.8 | 3,940 | 301 | 271 (90.03) | 14 (4.65) |
| Total | NAc | 173,462 | 15,169 | 14,902 (98.24) | 101 (0.67) |
Source: National Notifiable Disease Reporting System (NNDRS).
Source: the Chinese Measles Laboratory Network (CMLN).
NA, not applicable.
In this study, 76 of 101 VARI cases and 9,533 of 14,902 genotype H1 measles cases with complete epidemiological, clinical, and genotyping information were selected for further analysis. All 76 VARI cases were suspected sporadic cases. The genotype H1 wild-type measles cases were mainly concentrated during March and May, presenting an obvious seasonal distribution. Contrary to genotype H1 wild-type measles, VARI cases were distributed throughout the year, without obvious seasonal distribution, but more cases were detected in March and May.
Excluding the unknown gender data of cases, the male/female ratios of VARI and wild-type measles were 0.95:1 (37/39) and 1.37:1 (5,511/4,022), respectively. Seventy-two (94.74%) of 76 VARI cases were infants/children of ages 8 to 23 months. Only 2 cases were children of ages 7 to 19 years, and 2 cases were adults of age >30 years. Infants/children (41.16% [3,924/9,533]) under 2 years of age and adults 45.71% [4,358/9,533] > 20 years of age comprised the majority of genotype H1 wild-type measles cases. Seventy-five of 76 VARI cases received one-dose MCV vaccination, and only one case received two-dose MCV vaccination. Among 9,533 cases of genotype H1 wild-type measles, 737 (7.73%) cases had an MCV vaccination history, including 485 cases with one-dose MCV vaccination and 252 cases with at least two-dose MCV vaccination.
Time distribution since last measles vaccination to rash onset among cases of VARI and genotype H1 wild-type measles having the MCV vaccination history.
The time since the last measles vaccination to rash onset differed between VARI and genotype H1 wild-type measles cases (Fig. 1). All 76 VARI cases occurred within 31 days after MCV vaccination. Among them, 74 (97.37%) cases occurred within 14 days after MCV vaccination. The other two VARI cases occurred on the 16th and 31st days after MCV vaccination, separately. Two VARI cases occurred within 4 days after MCV vaccination. Then the number of cases increased gradually, peaked on the 8th day, and decreased thereafter.
FIG 1.
Time from MCV vaccination to rash onset among VARI and genotype H1 wild-type measles cases. Panels A, B, and C indicate the time interval in years, months, and days, respectively. The black columns indicate the number of VARI cases, whereas gray columns indicate the number of genotype H1 wild-type measles cases.
For genotype H1 wild-type measles, 413 (56.04%) of 737 cases occurred within 1 year of the last MCV vaccination. In addition, 239 (32.43%) cases occurred within 31 days after MCV vaccination. A total of 222 (30.12%) cases occurred within 14 days, and the proportion was less than that of VARI cases. In total, 515 (69.88%) measles cases occurred 14 days after MCV vaccination, which might be associated with vaccine failure. Four measles cases occurred on the day of MCV vaccination. The number of measles cases rapidly increased and peaked on the 4th to ∼6th days, which was earlier than that of VARI cases. Then the number of measles cases decreased.
Clinical symptoms of VARI cases.
VARI presents clinical symptoms similar to measles, such as moderate fever, rash, and one of the “3Cs,” making it difficult to distinguish VARI from wild-type MeV infection. Fever and rash were the main clinical symptoms of VARI and genotype H1wild-type measles cases (Table 2). However, the frequencies of the “3Cs,” Koplik spots, and complications in VARI cases were reduced compared with wild-type measles cases, demonstrating significant differences between these conditions (P < 0.05). In addition, 1,230 (12.90%) of 9,533 of genotype H1 wild-type measles patients exhibit complications, including pneumonia, diarrhea, enteritis, otitis, encephalitis, and meningitis. Pneumonia and diarrhea were the main complications of genotype H1 wild-type measles. However, the complications of VARI were very few, and only diarrhea was found as a complication among 3 (3.95%) of 73 VARI cases.
TABLE 2.
Frequencies of clinical symptoms in VARI and genotype H1 wild-type measles cases
| Clinical symptom(s) | No. (%) of cases by: |
P value | |
|---|---|---|---|
| VARI (n = 76) | Genotype H1 of wild-type measles (n = 9,533) | ||
| Fever | 75 (98.68) | 9,443 (99.06) | 0.516 |
| Rash | 76 (100.00) | 9,476 (99.40) | 1.000 |
| 3Csa | 37 (48.68) | 8,955 (93.93) | <0.001 |
| Cough | 30 (39.47) | 8,664 (90.88) | <0.001 |
| Coryza | 20 (26.32) | 6,385 (66.98) | <0.001 |
| Conjunctivitis | 14 (18.42) | 6,098 (63.97) | <0.001 |
| Koplik spots | 19 (25.00) | 4,524 (47.46) | <0.001 |
| Complicationb | 3 (3.95) | 1,230 (12.90) | 0.020 |
| Pneumonia | 0 (0.00) | 529 (5.55) | NAc |
| Diarrhea | 3 (3.95) | 730 (7.66) | NA |
| Others | 0 (0.00) | 55 (0.58) | NA |
“3Cs” indicates at least one of the following: cough, coryza, or conjunctivitis.
Complications include pneumonia, diarrhea, enteritis, otitis, encephalitis, and meningitis.
NA, not applicable.
Laboratory identification of MCV strains obtained from VARI cases.
All 101 N-450 sequences obtained from VARI cases exhibit high homology with that of the S191 strain. Among them, 95 sequences were identical to those of the S191 strain. Compared with the S191 strain, a few substitutions occurred in 4 nucleotide sites of N-450 sequences obtained from the six VARI cases (Table 3). Nucleotide substitutions of A/G simultaneously occurred at position 1321 (genomic numbering) from the four VARI cases, which caused amino acid substitutions of lysine/arginine. Among the four VARI cases, two cases occurred in Beijing in 2014, one was from Guizhou Province in 2013, and one was from Yunnan Province in 2017. Of note, arginine occurred at position 1321 of all WHO reference strains of the wild-type MeV genotypes, except genotype A. In addition, one G/T nucleotide substitution occurred at position 1480 in VARI cases, causing amino acid substitutions of arginine/isoleucine. Two nucleotide substitutions of T/C at positions 1487 and 1538 occurred in one VARI case: these did not cause amino acid substitutions.
TABLE 3.
Substitutions of nucleotides and amino acids between the S191 strain and VARI cases
| Location(s)a | No. of VARI cases | Nucleotide substitution in: |
Amino acid substitution in: |
||
|---|---|---|---|---|---|
| S191 | VARI case | S191 | VARI cases | ||
| 1321 | 4 | A | G | Lysine | Arginine |
| 1480 | 1 | G | T | Arginine | Isoleucine |
| 1487, 1538b | 1 | T | C | /c | / |
Nucleotide position in reference to the genomic sequence of Edmonston strain (GenBank accession no. AF266288).
Two substitutions occurred in one VARI case.
“/” indicates no amino acid substitution.
DISCUSSION
A systematic review clarified that no evidence of human-to-human transmission of the measles vaccine virus has been reported (14). Therefore, VARI should not be considered measles. Responses to VARI and wild-type measles differ significantly. For VARI, there is no active response, such as active case identification, contact tracing, and emergency vaccination. Thus, it is very important to identify VARI in a timely manner to determine measles response measures, especially in measles preelimination and elimination settings.
A total of 101 VARI cases were confirmed through the routine measles surveillance in China in 2011 to 2018. The number of VARI cases each year was relatively stable; however, the detection rate of VARI cases gradually increased among the cases confirmed by genotyping with the decrease in measles incidence in China. VARI cases are typically sporadic and occur throughout the year, without obvious seasonal distribution, as described previously (10). However, more cases occurred in March and May, which might be related to an increase in the number of the vaccinated individuals during outbreak responses or supplementary immunization activities (SIAs) at these points. The age distribution of VARI cases differed from that of genotype H1wild-type measles cases. VARI mainly occurred in infants/children of ages 8 to 23 months, most of whom received one-dose MCV vaccination in this study. This finding might be associated with the current measles vaccination strategies in China. The two-dose schedule for routine immunization was used in China. The first dose of MCV was recommended for infants/children at 8 months of age, and the second dose was given at 18 to 24 months of age. Genotype H1wild-type measles cases are mainly concentrated in infants/children less than 2 years old and adults over 20 years old, as described in previous reports (11, 21).
In total, 97.37% of VARI cases occurred within 14 days after MCV vaccination, whereas 30.12% of H1 wild-type measles cases with an MCV vaccination history occurred within 14 days after MCV vaccination. Thus, suspected measles cases occurring within 14 days after MCV vaccination should be the main target population for VARI surveillance. The number of VARI cases peaked on the 8th day after MCV vaccination, which was later than that of genotype H1 wild-type measles cases. The number of genotype H1 wild-type measles cases peaked on the 4th to ∼6th days after the last MCV vaccination. The following two reasons potentially explain why the measles cases occurred after MCV vaccination. First, these cases were potentially infected with wild-type MeV before MCV vaccination or within the early stage after vaccination. Although these cases received the MCV vaccination, they did not produce sufficient antibodies due to the short vaccination time and eventually developed measles. Second, measles cases occurring after MCV vaccination might be also related to vaccine failure.
VARI presents clinical symptoms similar to measles. Fever and rash were the main clinical symptoms in VARI cases in this study. However, the frequencies of the “3Cs,” Koplik spots, and complications in VARI cases were significantly reduced compared with those in genotype H1 wild-type measles cases, which is consistent with another previous report (10). Based on the criteria of VARI recommended by the WHO, VARI cases exhibited a rash illness but did not have cough or other respiratory symptoms related to the rash (https://www.who.int/immunization/monitoring_surveillance/burden/vpd/WHO_SurveillanceVaccinePreventable_11_Measles_R2.pdf?ua=1?). However, cough and coryza were found in a few VARI cases in this study. In addition, approximately one-quarter of VARI cases exhibited Koplik spots, which are typically thought to be pathognomonic for measles. Thus, it is very difficult to clinically distinguish VARI from wild-type measles. The identification of VARI relies on laboratory assays. A standard genotyping method was recommended by the WHO based on the N-450 nucleotide sequence to track the source and transmission pathways of MeV, which could also be used to distinguish VARI from wild-type measles (2, 22). However, this approach is time-consuming and complex, and PCR amplicon contamination is a potential complication. A number of alternative methods were recently developed and used for the identification of VARI, including loop-mediated isothermal amplification, real-time RT-PCR, and RT-PCR–restriction fragment length polymorphism (9, 23–26).
The live-attenuated MCV is considered an effective and safe vaccine (13). Attenuation of measles vaccine is associated with decreased replication in lymphoid tissue, but the molecular basis for this restriction has not been identified (27). Our previous study has also confirmed that the MCV and measles immunization programs currently used in China have effectively reduced the measles incidence in China (21). In this study, a few substitutions were found in the N-450 nucleotide sequences obtained from the VARI cases compared with the S191 strain. The reason for the N-450 nucleotide sequence substitutions might be related to the quasi-species nature of RNA viruses or continuous passages of isolates obtained from clinical samples.
In conclusion, the confirmation of VARI has become an emerging issue in the process of measles elimination. Rapid confirmation of VARI is critical to measles surveillance efforts and will help to determine the response measures for measles, especially in measles preelimination and elimination settings. In this study, the characteristics of VARI cases were clarified based on epidemiological, clinical, and laboratory data, providing a better understanding of VARI. However, of note, some VARI cases might be missed in the current measles surveillance program because clinical samples from only approximately 10% of suspected measles cases were collected for MeV genotyping in China. Therefore, the surveillance of VARI cases should be strengthened. The suspected measles cases with MCV vaccination are recommended to be tested by the laboratory to identify wild-type measles or VARI.
ACKNOWLEDGMENTS
We thank the provincial and prefectural measles and rubella laboratory staff members and the epidemiologists in mainland China.
This work was supported by the Key Technologies R&D Program of the National Ministry of Science (2018ZX10713001-003, 2018ZX10711001, 2018ZX10713002, and 2017ZX10104001-002).
A.C. was responsible for data analysis and manuscript preparation. H.W. was responsible for laboratory testing. A.C., Y.Z., and W.X. designed the study and prepared the manuscript. A.C., H.W., Z.Z., N.M., J.S., and Y.Z. performed the data analysis. All authors equally contributed to data generation and manuscript preparation. All authors read and approved the final manuscript.
The authors have no conflicts of interest.
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