The Decline of Measles Antibody Titers in Previously Vaccinated Adults: A Cross-Sectional Analysis
The Decline of Measles Antibody Titers in Previously Vaccinated Adults: A Cross-Sectional Analysis
The Decline of Measles Antibody Titers in Previously Vaccinated Adults: A Cross-Sectional Analysis
http://doi.org/10.1590/S1678-9946202466004
Anna Carla Pinto Castiñeiras 1,2,3, Amanda Caroline Sales 1,2, Camila de
Melo Picone 1,2, Constância Lima Diogo3, Átila Duque Rossi 3, Rafael
Mello Galliez 3, Orlando da Costa Ferreira Jr. 3, Terezinha Marta Pereira
Pinto Castiñeiras 3, Marta Heloísa Lopes 1,2,4, Ana Marli Christovam Sartori
1,2,4
ABSTRACT
Rev Inst Med Trop São Paulo. 2024;66:e4 This is an open-access article distributed under the Page 1 of 10
terms of the Creative Commons Attribution License.
Castiñeiras et al.
In the year 2000, the World Health Organization (WHO) Then, 2018 and 2019 marked a global reemergence of
estimated that measles caused 535,000 deaths annually measles cases, even in regions that were previously free of
and was responsible for 5.0% of all deaths of children transmission, such as Brazil. In April 2019, following virus
under five, mainly in low- and middle-income countries. importation from Israel and Norway into the Sao Paulo
In 2001, a global partnership - the Measles and Rubella State, a new epidemic wave of measles swept the country.
Initiative - was launched to ensure that no more children die Sao Paulo’s metropolitan area was the epicenter, with
of measles or are born with congenital rubella syndrome, 17,976 confirmed cases17. During this outbreak, infants were
and to assist countries in the planning, financing, and the most affected group in absolute numbers, accounting
measurement of efforts required to eliminate these diseases4. for 18.2% of cases and one-third of hospitalizations, while
The strategy was centered on administering two doses of 43.1% of all cases affected individuals aged 15–29 years18.
measles- and rubella-containing vaccines to all children and Notably, the disease occurred among young adults with
strengthening surveillance. This collective effort resulted in prior vaccination, a phenomenon that had already been
the elimination of measles in the Americas, certified by the documented16,19-22.
Pan American Health Organization, in 20165. In July 2019, the Health Department of Sao Paulo State
The measles-mumps-rubella vaccine (MMR) is launched a campaign to intensify measles immunization in
extremely effective, resulting in seroconversion in the target population23. In this outbreak, as the demand for
approximately 98.0% of individuals following the second vaccination increased and an unexpectedly high proportion
dose6. The immune response triggered by the replication of cases affected vaccinated adults, we initiated a study to
of the vaccine virus mirrors that induced by the wild-type assess and evaluate the waning measles IgG antibodies in
virus, stimulating both humoral and cellular immunity, this vaccinated population at a vaccination reference center
as well as interferon production. After vaccination, IgM in Sao Paulo city.
antibodies can be detected in the organism for two to six
months, while IgG persists for an extended period. The MATERIALS AND METHODS
durability of the immune response following vaccination
is usually influenced by the induction of cellular memory A cross-sectional study was conducted from August 8th
and the persistence of antibodies7. to December 19th, 2019 at the Centro de Referencia para
Measles outbreaks in areas with high vaccine coverage Imunobiologicos Especiais (CRIE) of the Hospital das
tend to impact susceptible individuals. These groups Clinicas da Universidade de Sao Paulo (HC-USP). The
include unvaccinated infants, children whose parents refuse center, established in December 1993, has served as a
vaccination, adults who were neither previously infected reference for special immunobiological and also offers
by the wild-type virus nor adequately vaccinated during routine immunization for both adults and children, following
childhood, and individuals with primary or secondary the recommendations of the National Immunization
vaccine failure8. Program/Ministry of Health24. Its primary public includes
Primary vaccine failure results from an inadequate initial patients, healthcare workers, and university students.
response to the vaccine, which negatively affects antibody A convenience sample of participants was recruited
neutralization capacity and avidity9. Secondary vaccine for the study. It included individuals aged over 18 years
failure happens due to a progressive loss of immunity over who had visited the center for vaccine updates and had
the years following vaccination, and is particularly notable documentation proving that they had received two or more
in regions with low circulation of the wild-type virus8. This doses of the MMR vaccine, either on a physical card or
failure has been documented in cases of measles occurring electronic medical records. Those meeting these criteria
in individuals with prior evidence of immunity10-15. Cases were invited to participate and, upon providing written
resulting from secondary failure tend to be milder but can informed consent, underwent an interview and had a blood
still be potentially transmissible16. sample collected.
Over the years, antibodies induced by vaccination Data collection included information on age, gender,
decrease and may become undetectable8. This decline in profession, comorbidities, medications, history of measles
antibodies does not necessarily indicate susceptibility to disease, and records of measles-containing vaccines. Each
the virus, as an anamnestic immune response may still participant was assigned a protocol number to protect their
occur upon revaccination. However, for some individuals, personal information. Individuals with clinical conditions
this response is partial, resulting in low antibody titers, and that could affect their immune response to vaccination,
the disease may develop. This underscores the need for such as immunosuppression and uncontrolled diseases,
surveillance during periods of viral circulation7. were excluded.
Table 2 presents the results of ELISA and CLIA. The positive by ELISA but negative by CLIA. Figure 1 illustrates
seropositivity rates were 32.7% by ELISA and 75.3% the dispersion of antibody titers in both methods. Kendall’s
by CLIA. There were 20 samples (12.3%) that were test revealed a strong positive correlation between ELISA
inconclusive by ELISA and five (3.1%) by CLIA. and CLIA (tau coefficient 0.73; p <0.001).
Figure 2 shows the distribution of antibody titers. The
Table 2 - Measles IgG antibody rates (%) and titers, determined overall mean measles antibody titer was 182.8 IU/L (IQR
by the enzyme-linked immunosorbent assay (ELISA) and 92.3-422.6) by ELISA and 68.9 AU/mL (IQR 17.2–190.5)
chemiluminescence assay (CLIA) test in 162 adults with two
or more MMR vaccine doses. Sao Paulo, 2019. by CLIA. Three samples exceeded the upper limit of 5,000
IU/L in ELISA, while six negative samples had undetectable
Serologic test ELISA CLIA titers—and in the association analyses, the values of 5,000
Seroprevalence, IU/L and 8 IU/L were attributed to them, respectively.
n (%) Thirty-one samples exceeded the upper limit of CLIA
Positive 53 (32.7%) 122 (75.3%) (300 AU/mL), whereas 20 had undetectable titers, and the
Inconclusive 20 (12.3%) 5 (3.1%) values of 300 AU/mL and 5 AU/mL titers, respectively,
Negative 89 (54.9%) 35 (21.6%)
were assigned to them.
IgG antibodies titers
Table 3 shows the associations between measles
Median (IQR)* 182.8 (92.3-422.6) 68.9 (17.2-190.5) positivity rates and IgG titers with the variables of interest.
IU/L** AU/mL***
In the bivariate analyses, the variables age, time elapsed
*IQR = Interquartile range (25-75%); **IU/L: International Units/
Liter; ***AU/mL: Arbritary Units/milliliter
since the last MMR dose, and history of measles showed
a statistically significant association with both positivity
and titers (p<0.05).
Among the samples, 52 were positive and 34 were Logistic and linear regression models were conducted
negative in both tests. The 20 inconclusive and 50 to identify factors independently associated with measles
negative samples by ELISA were all positive by CLIA. seropositivity and IgG titers, respectively (Table 4).
Additionally, five samples that were negative by ELISA had Age was independently associated with seropositivity
an inconclusive result by CLIA, and only one sample was (OR=1.0725; 95% CI 1.024–1.1234; p=0.0031), indicating
Figure 1 - Measles IgG antibody titers measured by enzyme-linked immunosorbent assay (ELISA) and chemiluminescence assay
(CLIA) tests in 162 adults with two MMR vaccine doses. Sao Paulo, 2019. Red lines represent the negative cutoff; blue lines represent
the positive cutoff; black lines represent the median and IQR (25-75%).
Figure 2 - Comparison between Measles IgG antibody titers measured by enzyme-linked immunosorbent assay (ELISA) and
chemiluminescence assay (CLIA) tests in 162 adults with two MMR vaccine doses. Sao Paulo, 2019. Blue lines represent the
positive cutoff by ELISA; green lines represent the positive cutoff by CLIA.
Table 3 - Bivariate analyses of the association of measles IgG antibody rates and titers (ELISA) with variables of interest in 162
adults with ≥2 previous MMR vaccine doses. Sao Paulo, 2019.
Median (IQR)** 10.4 (3.6-14.1) 6.2 (2.3–1.4) 11.2 (5.6-15.0) 0.0006 - 0.1998 0.0002
Femaleab
n (%) 113 42 (37.2) 71 (628) 0.0715 - 0.1551
Healthcare workerab
n (%) 100 32 (32.0) 68 (68.0) 0.8683 - 0.3861
History of measlesab
n (%) 13 9 (69.2) 4 (30.8) 0.0102 - 0.0176
a
Mann-Whitney U test; bFisher test; cKendall test; *included both negative and inconclusive samples; **median [IQR: Interquartile
range (25-75%)]
that older individuals were more likely to be seropositive since the last MMR vaccine was negatively associated
for measles and to have higher antibody titers (OR=1.0216; with seropositivity (OR=0.9421; 95% CI 0.8885–0.9989;
95% CI 1.0048–1.0629; p=0.0216). The time elapsed p=0.0458), suggesting that antibody titers wane over time
Table 4 - Regression analysis of the association of measles IgG antibody seropositivity and titers (ELISA) with variables of interest
in 162 adults with two MMR vaccine doses. Sao Paulo, 2019.
after vaccination. Only age was correlated with IgG titers trend was partially attributed to the collinear relationship
in the multiple analyses. A history of previous measles was between increasing age and the absence of vaccine records
not associated with positivity or IgG titers. among participants.
Another study compared CLIA (LIAISON XL®) with
DISCUSSION PRNT26. CLIA exhibited a 90.2% sensitivity rate (95% CI
82.7–79.2) and a 75.0% specificity (95% CI 59.7-86.8).
This study was conducted during a measles outbreak in The comparison revealed a disagreement of 14.4% between
the Sao Paulo State in 2019 and aimed to assess measles IgG the tests, which was more frequent near the lower cutoff.
antibody titers among adults who had previously received The authors noted that CLIA may yield false-negative
at least two MMR vaccine doses after one year of age. Two results in the vaccinated population, which leads to an
widely distributed commercial serological tests, ELISA underestimation of protection against measles.
and CLIA, were employed. ELISA identified 32.7% of the An American study aimed to validate commercial
samples as positive (≥275 IU/L), 12.3% as inconclusive (≥200 immunoassays and employed ELISA (Euroimmun®) and
to <275 IU/L), and 54.9% as negative (<200 IU/L). On the CLIA (LIAISON XL®) to evaluate measles antibodies
other hand, CLIA indicated that 75.3% of the samples were titers compared to neutralization tests 27 . Both tests
positive (≥16.5 AU/mL), 3.1% were inconclusive (≥13.5 to showed a positive correlation with neutralization, but
<16.5 AU/mL), and 21.6% were negative (<13.5 AU/mL). ELISA demonstrated a stronger correlation (R=0.71–0.79;
Notably, these two tests showed a strong positive correlation p<0.0001) than CLIA (R=0.40–0.55; p<0.05) and yielded
with a tau coefficient=0.73 (p<0.001). more precise results.
According to the manufacturer’s instructions, the Antibody titers tend to decline over the years after
CLIA positive cutoff (16.5AU/mL) is equivalent to 175 vaccination. In 2011, a study evaluated 764 adolescents and
IU/L (as per the WHO Third International Standard for young adults aged 11–22 years who had received two doses
Anti-Measles). This suggests that the CLIA seropositivity of the MMR vaccine using an automated plaque reduction
cutoff is lower than that of ELISA (≥275 IU/L), which partly microneutralization (PRMN) assay. The study revealed that
explains the higher proportion of seropositivity indicated 8.9% of participants had non-protective neutralizing antibody
by CLIA. This hypothesis is further supported by the fact titers (titers <120 mIU/mL). This percentage was interpreted
that all samples classified as inconclusive by ELISA tested as indicating potential susceptibility to symptomatic
positive by CLIA. disease28. Furthermore, a 2020 meta-analysis estimated an
A Thai study 25 compared ELISA antibody titers annual antibody decline rate of 0.009 in a similar population,
with protective neutralizing antibodies (>120 mIU/mL) implying that 8.6% of initially positive individuals would
in children and adolescents aged 3 to 18 years. They transition to a negative status over 10 years8. Another study
found a 100% correlation when the ELISA cutoff was from the US revealed an even more pronounced decrease in
set at ≥275 IU/L, an 85.7% correlation when it was set neutralizing antibodies, projecting a 33.0% seronegative rate
at ≥200 IU/L, and a 72.2% correlation when it was set after 20 years of MMR immunization29.
at >120 IU/L. When using the cutoff recommended by As vaccination coverage expands and the number of
Euroimmun® (≥275 IU/L), they found a positivity rate of unvaccinated individuals decreases, the proportion of
46.3%, which is more similar to our findings. In the Thay vaccinated individuals among those with confirmed measles
study, an inverse correlation was observed between antibody cases is expected to rise30. In fact, approximately 40.0% of
titers and age, with protection declining with aging. This people infected with measles in the 2019 Sao Paulo outbreak
had a history of previous vaccination20. Those aged 20 to to decrease in the coming years, due to the systematic
35 years were the most affected, accounting for 40.2% of recommendation of two MMR doses in childhood.
cases31. This age group, born after the implementation of In contrast, the time elapsed since the last MMR
systematic measles vaccination, observed multiple changes dose did emerge as a negative independent predictor
in the vaccination schedule and comprised the majority of for seropositivity (OR=0.9421, 95% CI 0.8885–0.9989,
participants in our study (median 30; IIQ 26–36 years). p=0.0458). The median time since vaccination was greater
In our study, the variable age was independent and in seronegative individuals than in seropositive ones:
positively associated with seropositivity (p=0.0024) 11.2 (IQR 5.62–15.0) and 6.15 years (IQR 2.29–11.4)
and higher IgG titers (p=0,0014). This result can be (p=0.0006), respectively. A previous German study36 also
partly attributed to underreported infections and higher observed this association, indicating that individuals with
immunogenic stimulus due to repeated wild virus exposure more than eight years elapsed since the last dose were 4.59
in older individuals. A meta-analysis examining the times more likely to be seronegative than those vaccinated
effects of age and gender on measles susceptibility found within the last two years.
that individuals born before 1980 had a 2.78 relative risk The high rate of seronegative individuals in adequately
(RR) (95% CI 2.18–3.50; p<0.0001) of being seropositive vaccinated populations raises concerns about the potential
compared to younger individuals. No significant association role of a third dose of the MMR vaccine, particularly during
with gender was found (RR=0.92, 95% CI 0.83–1.03, outbreaks. An American study37 observed a significant
p=0.02)32. increase in neutralizing antibodies after a booster dose in
Healthcare professionals did not show a significant young adults. Most individuals with non-protective baseline
association with seropositivity (p=0.8683). Note that, in titers (<120 mIU/mL) seroconverted after a third dose, but
addition to having an individual risk of infection, these returned to near-baseline titers after one year.
professionals can become a source of nosocomial infection The booster effect may help disrupt the transmission
themselves, potentially exposing a population that lacks chain and achieve disease control, albeit temporarily.
immunity, making them vulnerable to severe disease. This Therefore, while periodic boosters of measles-containing
may lead to increased measles morbidity and mortality33-35. vaccines may not be justified, they may be valuable during
In South Korea, a study conducted during an outbreak in outbreaks.
2007 found that nearly half of cases occurred in a hospital This study aimed to expand the knowledge about
environment34. The authors also noted that nosocomial measles susceptibility in Sao Paulo City, potentially guiding
spread preceded the peak of the community outbreak by measures to control outbreaks and effectively eliminate the
approximately two weeks. Notably, 23.0% of the healthcare disease. However, it is essential to acknowledge certain
professionals affected during the South Korea outbreak had limitations that may have partially compromised the
previously received two MMR doses, which emphasizes the accuracy of the results. The study population was selected
need to assess their measles immunological status. by convenience sampling, and the sample size may be
Surprisingly, in our study, prior measles infection insufficient to identify some associations.
was not independently associated with seropositivity The reported cases of measles were not laboratory-
(p=0.0828) or antibody titers (p=0.1359) by the ELISA confirmed, and precise dates of illness onset were
method. However, only one participant out of the four who undocumented. However, none of the patients had contracted
had a history of measles and a negative antibody titer in the illness during the most recent outbreak. Antibody
ELISA was also negative in CLIA. It is also noteworthy measurements were conducted using immunoassay
that since measles mainly affects children, recall bias may tests rather than the gold standard (PRNT). In addition,
affect the reliability of information on cases, and measles the laboratory variation in test procedures can make it
may be misdiagnosed with other childhood exanthematous challenging to compare the results.
diseases. Similarly, the number of measles vaccine doses Data on measles seroprevalence during periods of viral
was subject to measurement bias. While some participants circulation may be relevant for estimating the impact of
had proof of vaccination since childhood, others only had the outbreak7,29. Our data revealed that 67.3% of young
adult life records. adults considered adequately vaccinated had apparently
The interval between MMR doses was relatively long non-protective IgG antibody titers, which may render
(median 13.2, IQR 5.6–18.5 years) and did not differ them susceptible to measles. Nonetheless, it is important
significantly between seropositive and seronegative to emphasize that a low number of IgG titers or even the
individuals (p=0.9105). This extended interval may be related absence of them do not necessarily imply a lack of protection
to changes in vaccination schedules over time and is expected upon virus exposure. Vaccines can also stimulate cellular
immune responses similar to, albeit less pronounced than, methodology; ADR, RMG, and ODCJ: formal analysis,
the wild-type virus7. Although not currently detectable with methodology; TMPPC: formal analysis, Methodology,
available tests, this response may still provide protection Writing – review and editing; MHL: conceptualization,
against the disease. data curation, formal analysis, funding acquisition,
Future studies could expand the knowledge on measles investigation, methodology; AMCS: conceptualization, data
protection in the general population and specific groups. curation, formal analysis, funding acquisition, investigation,
Employing the gold standard measles neutralization test methodology, project administration, writing – original
would validate the results obtained with immunoassay draft, writing – review and editing.
tests. The long-term persistence of antibodies should be
evaluated, especially in cohorts exclusively vaccinated CONFLICT OF INTERESTS
during early childhood. Furthermore, the immunological,
epidemiological, and financial aspects of a potential third All authors declare no commercial or other conflict of
measles-containing vaccine dose need to be studied, interests.
particularly during outbreaks.
Lastly, the elimination of regional measles must be seen FUNDING
as a fundamental step toward global eradication. However,
it is crucial to recognize its fragility. Sustaining elimination This research received financial support from the
requires maintaining high and homogeneous vaccination Programa de Apoio a Pos-Graduacao of the Coordenacao
coverage and improving surveillance to prevent virus de Aperfeicoamento de Pessoal de Nivel Superior (CAPES),
importation and a subsequent measles spread38. the Laboratorio de Investigacao Medica em Imunologia
(LIM-48), and the Instituto de Avaliacao de Tecnologias
CONCLUSION em Saude (IATS).
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