Vaccine 19 (2001) 3865– 3869 www.elsevier.com/locate/vaccine
Present anti-measles immunity in Jordan Salwa Bdour *, Naji Batayneh Department of Biological Sciences, Faculty of Science, Uni6ersity of Jordan, Amman, Jordan Received 10 October 2000; received in revised form 13 March 2001; accepted 26 March 2001
Abstract The immunity of adults and the prevalence of measles was determined in order to evaluate the adequacy of current measles vaccination policy in Jordan. A total of 307 sera, collected from adults aged 18 – 40 years, were tested for anti-measles antibodies by ELISA technique. The overall prevalence of anti-measles antibodies was 94.8% and there was no significant difference in the seropositivity rate between males (95.7%) and females (94%). Of the tested adults, 71% were vaccinated and 29% escaped vaccination. In Jordan, measles outbreaks occur periodically and predominantly attack children aged 5 – 14 years. Our data support introducing the compulsory MMR vaccine in the year 2000 to improve the vaccination coverage of measles; since the optional single dose vaccination has not interrupted the circulation of the measles virus. A second dose of MMR vaccine could be offered to Jordanians either at school entry or at the age of 11 – 12 years, based on the outcome of the compulsory single dose of MMR vaccine. © 2001 Elsevier Science Ltd. All rights reserved. Keywords: Measles; Vaccination; Immunity
1. Introduction Acute measles is normally a mild disease in children and young adults resulting from infection with the highly contagious measles virus. Marked reduction in measles incidence has been reported in many countries where measles vaccine has been widely used for many years [1–4]. Since the vaccination era began, the trend of measles infections has been shifted to sporadic outbreaks among children and young adults of high school age [5 – 7]. These outbreaks were believed to occur in individuals who escaped or failed to respond to primary immunization as infants. Therefore, a two-dose vaccination schedule has been introduced in many countries [8 – 10], to improve vaccine coverage and to prevent accumulation of susceptible persons and periodic outbreaks. In Jordan, a single dose of combined measles, mumps and rubella (MMR) vaccine was introduced to the private sectors in 1979 and given optionally to children at the age of 9 months. This dose may not be * Corresponding author. Tel.: + 962-6-5355000; fax: +962-65348939. E-mail address:
[email protected] (S. Bdour).
adequate for the control and elimination of measles unless vaccination coverage is compulsory. Therefore, the program of national compulsory single dose of MMR vaccine was adopted in May 2000 for children aged 18–24 months. The prevalence of the measles infection has never been examined in Jordan. Therefore, in the present work we investigate the prevalence of measles in different age groups and the prevalence of anti-measles antibodies in young adults. The chief objective was to make an empirical evaluation of the need for mass immunization, including a second compulsory dose of measles vaccine in order to control and eliminate the measles infection in Jordan.
2. Methods
2.1. The immunity of adults The study was carried out at the University of Jordan during the academic year 1999 –2000. Blood samples were obtained by venous puncture from 307 students, aged 17–40 years, who agreed to take part in this study and signed the consent form. The samples were cen-
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trifuged and sera were frozen at − 20°C until the serological analysis was performed. The enzyme linked immunosorbent assay (ELISA) (DiaSorin, Italy) was used to determine the level of specific IgG antibodies to measles. The positive and negative controls included in the kit were used as calibrators to create a standard curve. The actual absorbance of each sample was located on the standard curve and the arbitrary unit (AU) was calculated using the appropriate computer program of ELISA reader (DIGISCAN SA 1000, ASYS HITECH, Austria). When the value of the sample was \ 40 AU, the result was regarded as positive (immune). When the value of the sample was B27 AU, the result was regarded as negative (susceptible). Values between 27 and 40 AU could not be clearly defined and were regarded as equivocal. The 2-test was used to evaluate differences in prevalence between sexes. P B 0.05 was considered statistically significant. A questionnaire, which was used to collect some demographic information about the students, included: age, sex, measles history and previous measles vaccination status.
shows the prevalence and the seropositivity rate in males and females at different age groups. The overall prevalence was 94.8%. The overall seropositivity rate in males (95.7%) was not significantly different from that of females (94%). Similarly, there were no statistical differences among the studied age groups. In the 17–20 year age group, the prevalence of anti-measles antibodies was 93% in both males and females, while in the 21–24 age group, it was 96.8% in males and 94.3% in females. From 25 years upward, the prevalence was 100% in both sexes. On the other hand, there was no significant difference in the seronegativity rate between males (2.9%) and females (4.8%). Of the students, B 2% had equivocal titers.
3.2. The 6accination status of adults As shown in Table 2, 218 (71%) of the tested university students were vaccinated by the single dose of MMR vaccine. Seventy-nine (36.2%) of the vaccinees were born and vaccinated abroad. Ninety of the vaccinees had measles and 82 (91.1%) were seropositive for measles. Measles history was not reported for 128 of the vaccinees and 124 (96.9%) were seropositive. With measles history, the seropositivity rate was 94.7% in males and 88.5% in females. While without measles history, the seropositivity was 95.7% in males and 97.5% in females. Table 3 shows that 89 of the students escaped measles vaccination. Thirty-nine had measles and 36 (92.3%) were seropositive. Fifty of the students who escaped vaccination had no measles and 49 (98%) were seropositive for measles. The overall seropositivity with measles history was 100% in males and 82.4% in females and without measles history was 97% in males and 100% in females. There was no significant difference in the overall seropositivity among students, regardless of measles history, age, vaccination and sex (Tables 2 and 3).
2.2. Pre6alence of measles and 6accination co6erage Data of measles vaccination coverage and reported measles cases in Jordan were obtained from the Department of Notifiable Communicable Diseases, Health Ministry, Jordan.
3. Results
3.1. The immunity of adults A total of 307 Jordan University students (140 males and 167 females) were tested for the prevalence of anti-measles antibodies in their blood samples. Table 1
Table 1 Prevalence of antibodies against measles in Jordan University students grouped by age and sexa Sex
Age (year)
No. tested
Negative
Equivocal
Positive
95% CI for % positive
No.
(%)
No.
(%)
No.
(%)
Males
17–20 21–24 \24 Total
61 62 17 140
3 1 0 4
4.9 1.6 0 2.9
1 1 0 2
1.6 1.6 0 1.4
57 60 17 134
93.4 96.8 100 95.7
93 9 0.064 97 9 0.042 100 90.00 96 90.032
Females
17–20 21–24 \24 Total
93 70 4 167
5 3 0 8
5.4 4.3 0 4.8
1 1 0 2
1.1 1.5 0 1.2
87 66 4 157
93.6 94.3 100 94
94 90.048 94 90.056 100 90.00 94 9 0.036
307
12
3.9
4
1.3
291
94.8
95 9 0.024
Total a
2 for sex difference = 0.7829 (P= 0.90).
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Table 2 The measles history of the vaccinated Jordan University students Sex
Age (year)
Vaccinated
Total No. of students
Measles history
No measles history
No.
Seropositivity No. (%)
No.
Seropositivity No. (%)
Males
17–20 21–24 \24 Total
14 20 4 38
13 19 4 36
(92.9) (95.0) (100.0) (94.7)
26 16 5 47
24 16 5 45
(92.3) (100.0) (100.0) (95.7)
40 36 9 85
Females
17–20 21–24 \24 Total
24 27 1 52
21 24 1 46
(87.5) (88.9) (100.0) (88.5)
49 30 2 81
47 30 2 79
(95.9) (100.0) (100.0) (97.5)
73 57 3 133
90
82 (91.1)
Total
128
124 (96.9)
218
3.3. The pre6alence of measles in Jordan
4. Discussion
The total natural measles cases recorded in Jordan from 1988 to 1999 are shown in (Table 4). Despite the vaccination coverage of 56– 98% in Jordan [11], measles outbreaks occur approximately every 4– 5 years (Table 4). The highest measles incidence (7026 cases) was in 1997, followed by 1988 (4810 cases) and 1993 (2985 cases). The lowest incidence was observed in 1999 (115 cases). The total number of infected males (9636 cases) during the period 1988– 1999 was approximately similar to that of females (9885 cases). The peak age of incidence is 5– 14 years in both males and females. The incidence in this group represents 65.5% of the total cases in both sexes (Table 4). The number of measles cases below the age of 5 years represent 24.4% of the total cases in both sexes. However, 5.9% of the total cases occur in children below the age of 1 year. The number of cases decreases with age. Adults of both sexes, 15– 24 and 25– 54 years contribute to 9.2 and 0.9%, respectively of the total cases.
This is the first survey of the prevalence of antimeasles antibodies in young adults and the incidence of measles in Jordan. Measles outbreaks occur periodically and attack predominantly the elementary school age children (5 to 14-year-old) (Table 4), indicating that measles spread very quickly among kindergarten children and elementary school students. The crowded conditions in Jordanian schools play a role in the spreading of the virus among students. The susceptibility of this target group to measles could be explained by (a) failure to respond to the single dose of MMR vaccine; (b) the vaccine given to some subjects of this group was effective for : 12 years [12]; or (c) some subjects of this group escaped immunization, which was not compulsory. This resulted in accumulation of susceptible individuals and periodic measles outbreaks. It is expected that the introduction of a compulsory single dose MMR vaccine in the year 2000 will improve
Table 3 The measles history of the unvaccinated Jordan University students Sex
Age (year)
Escaped vaccination
Total No. of students
Measles history
No measles history
No.
Seropositivity No. (%)
No.
Seropositivity No. (%)
Males
17–20 21–24 \24 Total
8 13 1 22
8 13 1 22
(100.0) (100.0) (100.0) (100.0)
13 13 7 33
12 13 7 32
(92.3) (100.0) (100.0) (97.0)
21 26 8 55
Females
17–20 21–24 \24 Total
10 6 1 17
9 5 0 14
(90.0) (83.3) (0.00) (82.4)
10 7 0 17
10 7 0 17
(100.0) (100.0) (0.00) (100.0)
20 13 1 34
39
36 (92.3)
50
49 (98.0)
Total
89
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the immunization coverage of measles and reduces the incidence rate among school children. This dose would not confer life-long immunity and would not be adequate to limit circulation of measles unless a second dose is considered. A two-dose vaccination program against measles was adopted by different countries and the twice-vaccinated recipients were better protected against epidemic measles [4,13– 15]. Our results demonstrated that the overall prevalence of anti-measles antibodies in Jordan University students was 94.8% (Table 1). Only 71% of the students were vaccinated at 9 months of age. However, they have probably been exposed to the wild virus that resulted in reinfection, especially that the measles vaccine has been found to be effective for at least 12 years [12]. A History of measles was reported in 90 (41.3%) of vaccinated students who received one-dose of MMR vaccine and were not given a booster dose at primary or secondary school. The booster dose was not included in the Jordanian vaccination policy. However, a history of measles was not reported in 128 (58.7%) of vaccinated students, indicating asymptomatic reinfection. Asymptomatic reinfection was reported and the measles virus was isolated from previously, naturally-immune individuals asymptomatically infected with measles while in close contact with actually infected family members [16]. Lack of vaccination was reported for 29% of the students. They could have acquired their immunity from natural infection by wild type measles virus or asymptomatic reinfection. Similar results were reported
for the health care students at the University of Barcelona, Spain [17]. Approximately 4% of the students of both sexes are seronegative for measles (Table 1). This number of susceptible subjects could explain the reported measles cases in Jordan for the age groups 15–24 and 25–35 years (Table 4) and it is sufficient to produce outbreaks. Outbreaks have been reported even when the immunity due to vaccination coverage is 98% [18,19]. In the UK, cases of measles in four universities or colleges have been reported since the beginning of 1996 [20]. Of the childbearing females in the present study (Table 1), :5% were seronegative for measles. Under these conditions, they will not be able to transmit protective immunity to their infants. Normally, the immunity is transferred passively from mothers to infants protecting them from natural measles until they are : 12 months old [21]. The lack of immunity in some Jordanian females could be correlated with susceptibility and infection of children below the age of 1 year with measles (Table 4). Our data support the idea of introducing the compulsory measles vaccine incorporated with the MMR vaccine. A second dose of MMR vaccine could be given to school age children either at school entry or at the age of 11–12 years, based on the outcome of the compulsory single dose of MMR vaccine. However, the Advisory Committee on Immunization Practice (ACIP) has recommended a second dose of MMR vaccine at the age of 4–6 years [13]. The twice-vaccinated recipients in various countries [4,14,15] were better protected against epidemic measles than the single dose recipients.
Table 4 Number of measles cases as diagnosed in Jordan during the period 1988–1999, stratified by age and sex Sex
Age
Number of cases
Total
1988
1989
1990
1991
1992
1993
1994
1995
1996
1997
1998
1999
No.
%
Males
B1 1–4 5–14 15–24 25–34 35–44 45–54 \55 Total
195 500 1721 43 9 2 0 0 2470
47 153 450 16 0 0 0 0 666
15 41 64 15 0 0 0 0 135
8 16 28 0 0 0 0 0 52
39 87 346 7 0 0 0 0 479
70 255 1020 93 2 0 1 1 1442
27 64 134 20 0 0 0 0 245
14 51 93 11 0 0 0 0 169
26 46 117 30 1 0 0 0 220
146 558 2105 619 48 7 2 1 3486
7 50 146 11 2 0 0 0 216
6 13 35 2 0 0 0 0 56
600 1834 6259 867 62 9 3 2 9636
3.1 9.4 32.1 4.4 0.3 0.05 0.02 0.01 49.4
Females
B1 1–4 5–14 15–24 25–34 35–44 45–54 \55 Total
152 492 1644 43 6 3 0 0 2340
30 161 519 15 6 0 0 0 731
12 36 71 33 1 1 1 0 155
17 22 51 1 0 0 0 0 91
37 105 436 14 0 0 0 0 592
70 236 1126 101 8 0 1 1 1543
47 60 120 16 1 1 0 0 245
23 34 79 11 2 0 0 0 149
16 58 133 17 4 0 0 0 228
130 532 2158 653 50 11 5 1 3540
8 41 147 16 0 0 0 0 212
2 16 38 2 0 1 0 0 59
544 1793 6522 922 78 17 7 2 9885
2.8 9.2 33.4 4.7 0.4 0.09 0.04 0.01 50.6
4810
1397
290
143
1071
2985
490
318
448
7026
428
115
19521
Total
100
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Acknowledgements We gratefully thank Dua’ Salah Nazzal for her assistance and typing of the manuscript.
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