Evaluation of a Single Dose of Diphtheria-Tetanus Toxoids among Adults in Odessa, Ukraine, 1995: Immunogenicity and Adverse Reactions
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1 S203 Evaluation of a Single Dose of Diphtheria-Tetanus Toxoids among Adults in Odessa, Ukraine, 1995: Immunogenicity and Adverse Reactions Anne Golaz, 1 Iain R. Hardy, 1,a Tatiana G. Glushkevich, 2 Evgueni K. Areytchiuk, 3 Adamadia Deforest, 4 Peter Strebel, 1 Melinda Wharton, 1 and Roland W. Sutter 1 1 Child Vaccine Preventable Disease Branch, National Immunization Program, Centers for Disease Control and Prevention, Atlanta, Georgia; 2 Ministry of Health, Kiev, and 3 Polyclinic 29, Odessa, Ukraine; 4 St. Christopher s Hospital for Children, Philadelphia, Pennsylvania Epidemic diphtheria spread to Ukraine in 1991, where it peaked in 1995 with reported cases. To refine epidemic control strategies, immunogenicity of a tetanus-diphtheria toxoids vaccine (Td) containing 2 limits of flocculation (Lf) diphtheria toxoid was evaluated. During a mass vaccination campaign, adults at a clinic in Odessa received one dose of Td. At enrollment, 57.2% of 341 study participants had levels of diphtheria antitoxin (DAT) 0.1 IU/ ml. Thirty and 180 days after receiving one dose of Td, 91.5% and 84.5% of the participants, respectively, had DAT levels 0.1 IU/mL. However, among 40- to 49-year-old participants, only 78.8% and 73.8% had DAT levels 0.1 IU/mL at 30 and 180 days, respectively. This study suggests that one dose of 2 Lf diphtheria toxoid is highly effective in raising DAT to protective levels in most adults; however, the study also shows that certain age groups, particularly persons and, to a lesser degree, years old may require additional doses or a complete three-dose primary vaccination series for optimal protection against diphtheria. In 1990, a large epidemic of diphtheria began in Russia and subsequently spread to Ukraine in 1991 [1, 2]. The epidemic peaked in , with 198,000 cases and 3400 deaths reported from the Newly Independent States (NIS) of the former Soviet Union. In the Russian Federation, Ukraine, and many NIS countries, about two-thirds of the reported diphtheria cases occurred among adults (i.e., persons 15 years of age) [3, 4]. In Ukraine, at the peak of the epidemic in 1995, 5306 cases were reported, of whom 80% were 15 years old [5]. In the mid-1980s, serologic studies from NIS countries suggested that 150% of adults were susceptible to diphtheria [6, 7]; therefore, it was postulated that adults may be an important link in the chain of transmission of Corynebacterium diphtheriae and that successful control of the resurgence of diphtheria would have to address this gap in immunity among adults. In December of 1994 (in Berlin) and February 1995 (in An- The study protocol was reviewed and approved by the Institutional Review Board of the Centers for Disease Control and Prevention (CDC) and by the Ministry of Health, Kiev, Ukraine. Written informed consent was obtained from all study participants. Financial support: United States Agency for International Development, Washington, DC, under a Participating Agency Services Agreement with CDC. a Deceased. Reprints: Information Center, National Immunization Program, Mailstop E-05, Centers for Disease Control and Prevention, 1600 Clifton Road NE, Atlanta, GA Correspondence: Dr. Anne Golaz, Child Vaccine Preventable Disease Branch, National Immunization Program, Mailstop E-61, Centers for Disease Control and Prevention, 1600 Clifton Road NE, Atlanta, GA (acg0@cdc.gov). The Journal of Infectious Diseases 2000;181(Suppl 1):S by the Infectious Diseases Society of America. All rights reserved /2000/18102S-0033$02.00 kara, Turkey), the World Health Organization (WHO), in conjunction with UNICEF and the International Federation of Red Cross and Red Crescent Societies, formulated a strategy to control diphtheria. The strategy relied on (1) high (195%) routine coverage among infants with three doses of diphtheria toxoid containing vaccines in all geopolitical divisions; (2) adult vaccination campaigns, using a single dose of diphtheria toxoid containing vaccine, with the goal of reaching 190% of the target population; and (3) vaccination with three doses of diphtheria toxoid containing vaccine of certain age groups (i.e., those years old) who may have not been primed previously because they escaped natural infection and were not reached by the vaccination program. A study found that 89% of 18- to 67-year-old workers at a Kiev factory had diphtheria antitoxin (DAT) levels of 0.1 IU/ ml, and 73% had levels 1.0 IU/mL following receipt of one dose of tetanus-diphtheria toxoids (Td) vaccine containing 5 limits of flocculation (Lf) diphtheria toxoid per dose [8]. However, for epidemic control in Ukraine, most of the Td vaccine supplied for use in adults was formulated to contain 2 Lf diphtheria toxoid/dose; therefore, an evaluation was needed to determine if one dose of such a vaccine was sufficient to raise diphtheria immunity levels. This study evaluated the degree of diphtheria immunity conferred by one dose of adult-formulation Td vaccine containing 2 Lf diphtheria toxoid/dose among Ukrainian adults. The specific objectives of the study were (1) to determine what proportion of adults develop protective levels of DAT after one dose of Td containing 2 Lf diphtheria toxoid; (2) to determine if there were any differences in the level of protection obtained after one dose of Td by age group, sex, occupation, or military
2 S204 Golaz et al. JID 2000;181 (Suppl 1) Table Characteristics of the study population Odessa, Ukraine, Attribute No. male No. female Total no. (%) Age group, years (27) (24) (23.5) (25.5) Total Employed (50.1) Military service (39.3) service; (3) to assess the local and systemic adverse reactions following receipt of Td; and (4) to use the study findings as a basis either to reaffirm or modify the adult vaccination policy for controlling epidemic diphtheria in Ukraine, and to make the findings available to WHO for consideration when formulating epidemic-control strategies in other NIS countries. Methods The study was conducted concurrently with the implementation of a Td mass vaccination campaign in the city of Odessa in During the mass campaign, adults presenting for vaccination at Polyclinic 29 in the Sovorovski district were invited to participate in the study. A total of 400 persons were enrolled between 18 and 21 April Before vaccination, blood samples were obtained from all subjects for determination of DAT titers. Each subject received one dose of an adult-formulation Td vaccine (manufactured by Pasteur Mérieux Connaught Sérums et Vaccins, Lyon, France) containing 2 Lf diphtheria toxoid and was asked to return 30 and 180 days later. At 30 days, study participants were asked about local and systemic symptoms following Td vaccination, using a standard questionnaire. Blood samples were obtained again for determination of DAT levels. At 180 days, DAT levels were again determined, and participants who did not have protective levels of antitoxin at day 30 were given another dose of Td vaccine containing 2 Lf diphtheria toxoid. Anyone who reported that they had received any diphtheria toxoid containing vaccine in the previous 5 years was not enrolled in the study. However, because there were doubts about the vaccination status of some subjects after enrollment, a hospital chart review was done at the end of the study to assess the vaccination status of participants. Characteristics like employment and military service were also assessed. Serum antibody titers against diphtheria toxin were determined at the Virology Research Laboratory, St. Christopher s Hospital for Children, in Philadelphia, by toxin neutralization in Vero cells, using a modification of a previously described procedure [9 11]. Assays were done in 96-well microtiter plates, using doubling serum dilutions. DAT titers were converted to international units per milliliter after standardization with reference sera provided by the Center for Biologic Evaluation and Research, US Food and Drug Administration, using a standard technique [12]. The lowest limit of detection for the diphtheria assay was IU/mL. In the present study, an antibody concentration of 0.1 IU/mL was defined as the minimum protective level, providing short-term protection against disease, and a concentration of 1.0 IU/mL was defined as a protective level, conferring more certain, longer-term protection [13]. Epi Info [14] was used to calculate relative risks (RRs) and confidence intervals (CIs). Results Of 400 enrolled subjects, 5 had received diphtheria toxoid vaccine within the past 5 years, 53 missed either the 30- or 180- day visit, and 1 did not have a valid vaccination record; thus, serologic results for 341 subjects were available for analysis. Demographic characteristics of the subjects are shown in table 1. Immunogenicity. The percentages of study participants, stratified by age group, who had DAT levels 0.1 IU/mL and 1.0 IU/mL at baseline (day 0), day 30, and day 180 are shown in table 2. At baseline, 57.2% of the participants had DAT levels 0.1 IU/mL, and 25.2% had levels 1.0 IU/mL. Thirty days after receiving one dose of Td vaccine with 2 Lf diphtheria toxoid, 91.5% of subjects had DAT levels 0.1 IU/mL, and 73.9% had levels 1.0 IU/mL. Six months after receiving one dose of the Td vaccine, 84.5% of subjects still had DAT levels 0.1 IU/mL, and 49.6% had levels 1.0 IU/mL. At baseline, the youngest age group (17 29 years of age) had the highest proportion of participants with DAT levels 0.1 IU/mL and 1.0 IU/mL (87.0% and 48.9%, respectively), whereas the 40- to 49-year-old age group had the lowest proportion of participants with DAT levels 0.1 IU/mL and 1.0 IU/mL (33.8% and 10.0%, respectively) (table 2). Thirty and 180 days after receiving one dose of Td vaccine, participants in the youngest age group had the highest proportion of participants with antitoxin levels 0.1 IU/mL, whereas participants in the 30- to 39-year-old and 40- to 49-year-old age groups had the lowest proportion of participants with antitoxin levels 0.1 IU/mL. Figure 1 shows median levels of DAT by age group at baseline and 30 and 180 days later. The 17- to 29-year-old age group had the highest baseline median levels (0.7 IU/mL), which raised to 4 IU/mL 30 days after one dose of Td and remained at 2.8 IU/mL 6 months after vaccination. Those in the 50- to Table 2. Seroprevalence of protective diphtheria antitoxin (DAT) titers ( 0.1 and 1.0 IU/mL) at baseline and 30 and 180 days after immunization among 341 study participants, by age group Odessa, Ukraine, Age group, years DAT titers 0.1 IU/mL (%) DAT titers 1.0 IU/mL (%) Day 0 Day 30 Day 180 Day 0 Day 30 Day Total
3 JID 2000;181 (Suppl 1) Immunogenicity of One Dose of Diphtheria Toxoid S year-old age group also responded well to one dose of Td vaccine, with a median 30-day titer of 4.0 IU/mL and a median 180-day titer of 1.0 IU/mL. The 30- to 39-year-old age group responded relatively well to the vaccination, with a median 30- day DAT level of 1.4 IU/mL and a median 180-day level of 0.7 IU/mL. The 40- to 49-year-old age group had the lowest median levels of antitoxin at baseline and at 30 days and 180 days; however, they responded relatively well to the vaccination, with a median DAT level of 1.4 IU/mL at 30 days and 0.5 IU/ ml at 6 months. At 30 days, subjects years old were significantly more likely than those 50 years old to remain unprotected (i.e., to have DAT levels!0.1 IU/mL) after one dose of Td with 2 Lf diphtheria toxin ( RR = 2.64; 95% CI = ) (table 3). Subjects in the 30- to 39-year-old age group were no more likely to be unprotected at 30 days or 180 days than those 50 years old. There were no differences in DAT levels by sex except in the 40- to 49-year-old age group. In this group, men were significantly more likely than women to be unprotected (at 30 days, RR = 3.6 and 95% CI = ; at 180 days, RR = 2.44 and 95% CI = ). There were no significant differences in DAT levels after vaccination by employment or past military service. Adverse events. After Td vaccination, local reactions at the injection site included pain (17.9%), local swelling (17.3%), induration (12.8%), and redness (11.3%). Systemic reactions were rare, with 1.5% of participants reporting fever 138 C. However, none of these adverse events were severe enough to render participants unable to work. Table 3. Predictors of failure among study participants to achieve a diphtheria antitoxin level 0.1 IU/mL at 30 and 180 days following one dose of 2 limit of flocculation units of diphtheria toxoid in a tetanus-diphtheria toxoid (Td) vaccine Odessa, Ukraine, Factor RR (95% CI) at 30 days P RR (95% CI) at 180 days Age group, years ( ) ( ) ( ) ( ).10 Sex a Female Male 1.67 ( ) ( ).33 Employed Yes No 1.24 ( ) ( ).64 Military service Yes No 1.54 ( ) ( ).33 NOTE. RR, relative risk; CI, confidence interval. a For 40- to 49-year-old age group only, RR = 3.6 ( CI = ) at 30 days ( P=.003) and RR = 2.44 ( CI = ) at 180 days ( P=.01). Discussion These findings confirm the excellent potency of the adultformulation Td vaccine containing 2 Lf diphtheria toxoid. This lower-potency Td vaccine performed well, raising immunity among all age groups. Results with this vaccine were similar to those reported in studies using the higher-potency Td vaccine containing 5 Lf diphtheria toxoid [15]. Age was the only sociodemographic variable associated with differences in diphtheria immunity. Participants years of P Figure 1. Median diphtheria antitoxin titers during study period, by subject age group Odessa, Ukraine, yrs, years.
4 S206 Golaz et al. JID 2000;181 (Suppl 1) age were less likely than younger and older participants to have protective levels of DAT. All 17- to 29-year-old participants had protective DAT levels 30 days after vaccination, and participants in the 30- to 39-year-old and 50- to 63-year-old age groups were highly protected. Before receiving the Td vaccine with 2 Lf diphtheria toxoid, about three-quarters of the participants in the 40- to 49-yearold age group and half of those in the 30- to 39-year-old age group were unprotected. One month after receiving the vaccine, about one-quarter of those years of age did not develop short-term protection, and about half of them did not develop long-term protection. The reason for the poor response among 40- to 49-year-old subjects may be that many in this age group have not been immunologically primed to diphtheria toxin. This cohort was born between 1945 and 1955, when immunization against diphtheria had not yet begun and the incidence of diphtheria was falling, thus preventing them from acquiring immunity through infection with the organism. In contrast, most persons born before 1945 developed natural immunity by exposure to diphtheria in childhood, and most persons born after 1955 were vaccinated. When vaccination against diphtheria began in the late 1950s and early 1960s, diphtheria toxoid administration was targeted to persons!15 years of age, and coverage was suboptimal. This is consistent with the finding of a larger proportion of diphtheria-immune persons among the 30- to 39-year-old age group than among the 40- to 49-yearold age group and the finding of a still larger proportion among those years of age. There were no differences in DAT levels by past military service following vaccination. Diphtheria toxoid was not administered routinely to recruits or at any time during the military service prior to the 1980s. There were no differences in DAT levels following immunization according to sex except among those years of age. In this age group, men, compared with women, had almost four times the risk of being unprotected 30 days after immunization, and they had two and one-half times the risk after 180 days. In this age group, men who had served in the military probably did so before the 1980s, but they were too young to have been exposed to natural infection, whereas women probably had had more exposure to diphtheria because of their roles in child care and health care. Six months after immunization, the proportion of subjects who were protected had decreased, suggesting waning immunity and the need for more doses of diphtheria toxoid or higher potency toxoid to achieve more permanent immunity against diphtheria. This study did not assess immunity beyond 6 months after immunization, but other studies show a continuing, progressive decrease in antitoxin titers over the years after vaccination. The relatively small proportion of subjects presenting with adverse effects after vaccination and the absence of severe adverse reactions show that the 2-Lf content of diphtheria toxoid in the vaccine is safe and has a similar safety profile to other Td vaccines. Our study did have limitations: It was not population-based; the adult outpatients of Odessa s Polyclinic 29 may not have been representative of all persons in Ukraine or of the general population in other countries; and we only evaluated an urban population, which may have had relatively better immunity levels than rural populations because of easier access to care or because of different exposure to the organism. Our study showed that high adult coverage with one dose of 2 Lf containing Td might have been an effective short-term strategy to protect adults of all ages except those years of age. Our findings are consistent with those of others who suggested that people years of age in Ukraine required additional doses or even a complete three-dose primary vaccination series for optimal individual protection against diphtheria. In Ukraine, and probably in other countries with a similar age distribution of diphtheria cases, adults years old should receive a three-dose primary series with diphtheria toxoid. This immunogenicity trial provided support for the WHO/ UNICEF adult vaccination strategy during the diphtheria epidemic, which consisted of high routine coverage, mass campaigns targeting diphtheria toxoid vaccination to the entire adult population, and more doses of vaccine to selected cohorts in order to control the diphtheria epidemic. References 1. Hardy IRB, Dittmann S, Sutter RW. Current situation and control strategies for resurgence of diphtheria in the New Independent States of the former Soviet Union. Lancet 1996;347: Galazka AM, Robertson SE, Oblapenko GP. Resurgence of diphtheria. Eur J Epidemiol 1995;11: Galazka AM, Robertson SE. Diphtheria: changing patterns in the developing world and the industrialized world. Eur J Epidemiol 1995;11: CDC. Diphtheria epidemic New Independent States of the former Soviet Union, MMWR Morb Mortal Wkly Rep 1995;44: Nekrassova LS, Chudnaya LM, Marievski VF, et al. Epidemic diphtheria in Ukraine, J Infect Dis 2000;181(suppl 1):S Feldblium IV, Basova NN, Koza NM. Immunological structure of the population in the system of epidemiological surveillance of diphtheria. Zh Mikrobiol Epidemiol Immunobiol 1986;63: Shvarts SA, Bukova VE, Pichushkov AV. Dynamics of diphtheria morbidity and population immunity [in Russian]. Zh Mikrobiol Epidemiol Immunobiol 1987;64: Hardy IRB, Kozlova IA, Tchoudnaia LM, et al. Immunogenicity of Td vaccine in Ukrainian adults (abstract G25). In: Abstracts of 35th Interscience Conference on Antimicrobial Agents and Chemotherapy (San Francisco). Washington, DC: American Society for Microbiology, Miyamura K, Nishio S, Ito A, et al. Micro cell culture method for determination of diphtheria toxin and antitoxin titres using VERO cells. I. Studies on factors affecting the toxin and antitoxin titration. J Biol Stand 1974;2: Miyamura K, Tajiri E, Ito A, et al. Micro cell culture method for determination of diphtheria toxin and antitoxin titres using VERO cells. II. Comparison with the rabbit skin method and practical application for seroepidemiological studies. J Biol Stand 1974;2:203 9.
5 JID 2000;181 (Suppl 1) Immunogenicity of One Dose of Diphtheria Toxoid S Deforest A, Long SS, Lischner HW, et al. Simultaneous administration of measles-mumps-rubella vaccine with booster doses of diphtheria-tetanuspertussis and poliovirus vaccines. Pediatrics 1988;81: Ipsen J. Circulating antitoxin at the onset of diphtheria in 425 patients. J Immunol 1946;54: Ipsen J. Immunization of adults against diphtheria and tetanus. N Engl J Med 1954;251: Dean AG, Coulombier D, Brendel KA, et al. Epi Info, version 6: a word processing, database, and statistics program for epidemiology on microcomputers. Atlanta: Centers for Disease Control and Prevention, Sutter RW, Hardy IR, Kozlova IA, et al. Immunogenicity of tetanus-diphtheria toxoids (Td) among Ukrainian adults: implications for diphtheria control in the Newly Independent States of the former Soviet Union. J Infect Dis 2000;181(suppl 1):S
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