Lower Rate of Seropositivity to Measles Among Young Healthcare Personnel in New York City

Abstract

We examined the prevalence of measles antibody among 12 349 newly hired HCP between 2009 and 2019. Younger HCP were significantly more likely to have no immunity. Compared with a 92.2% seropositive rate among 1057 persons hired at age >50 years, only 84.4% of approximately 10 000 HCP aged <40 years had protective antibody.

Since indigenous measles was eliminated from the United States 2 decades ago, limited outbreaks have occurred in undervaccinated populations. In 2019, the largest number of annual cases of measles were reported in the United States since 2000 [1]. The extraordinary scale and geographic spread of the 2018–2019 outbreak has prompted nationwide intensification of measles-specific prevention measures in the healthcare setting.

From 2001–2014, 78 nosocomial cases of measles were reported in US healthcare facilities. This includes 29 healthcare personnel (HCP), 19 (65.5%) of whom had presumptive evidence of immunity by the Centers for Disease Control and Prevention (CDC) criteria [2]. Illness in fully vaccinated individuals is less severe, and onward transmission to other HCP or patients is rare [3, 4]. Undervaccination and immunization failure in HCP has important implications for measles prevention efforts in healthcare settings.

According to the CDC, only 10 states have enacted laws to ensure immunity to measles-mumps-rubella (MMR) among hospital employees. Among vaccinated HCP, approximately 3% develop primary vaccine failure to measles. Risk of secondary vaccine failure due to a fall in antibody levels or affinity is challenging to determine. Furthermore, there is discrepancy between vaccination coverage and seroprotection due to variable performance of commercially available assays to measure measles antibody [5]. Despite these limitations, serosurveillance for measles antibody is an important tool for estimating and monitoring HCP susceptibility to measles [6, 7]. Previous large seroprevalence studies among US HCP were conducted in the 1990s, including a single study from our institution [6, 8]. These reports collectively showed that approximately 6.5% of HCP lack measurable measles antibodies. Only a few similar assessments are available in the recent literature for US HCP born after 1985, birth cohorts that would have received 2 MMR doses in childhood [7].

In this study, we describe the age-specific seroprevalence of measles antibody in a large cohort of newly employed HCP at a tertiary care cancer center in New York City.

METHODS

Memorial Sloan Kettering is a 484-bed tertiary care center in New York City. Prescreening for vaccine-preventable illness is routinely done at the time of employment regardless of job duties. New York State law mandates proof of immunity for measles for all healthcare workers at the time of hire [6]. Presumptive evidence of immunity is based on the following CDC criteria: 2 doses of MMR vaccine for HCP born in 1957 or later or positive measles immunoglobulin G (IgG) antibody. At Memorial Sloan Kettering Cancer Center (MSKCC), serological assessment is performed for all new hires regardless of documentation or history of adequate vaccination. History of clinical measles infection is not used as proof of immunity to measles. HCP who lack immunization records or have negative titers and have no contraindications to MMR vaccine must be vaccinated before their official start date.

Study Design

In September 2019, measles serostatus was assessed for all MSKCC employees hired between 1 January 2009 and 30 September 2019, including those with and without direct patient contact. Only employees tested for measles antibody (IgG) at MSKCC as part of pre-employment clearance were included. Outside laboratory results were not included in the study. Serological immunity testing at the study institution is performed using the Vitek Immunodiagnostic Assay System Measles IgG Assay. This is an automated enzyme-linked fluorescent immunoassay for the qualitative detection of IgG antibodies to measles (rubeola) virus in human serum.

Statistical Analyses

Data were stratified based on positive and negative + equivocal immunity to measles by age cohort. Significant differences between each age cohort and the reference group were determined using Pearson χ² analyses. The Fisher exact test was used where cell counts were <5. Odds ratios (ORs) and 95% confidence intervals (CIs) were calculated to quantify strengths in association. Data were analyzed using IBM SPSS Statistics version 25.

The MSKCC institutional review board granted a Health Insurance Portability and Accountability Act waiver to conduct this study.

RESULTS

Between 1 January 2009 and 30 September 2019, 12 349 individuals entered the MSKCC workforce and are included in the analysis. The age distribution at the time of employment is shown in Table 1. The majority of individuals were aged between 20 and 39 years (78%). The overall seroprevalence for measles was 85.7%. Among newly hired HCP aged <60 (n = 231), 98% were seropositive for measles antibody. Serological evidence of immunity was statistically different across all age groups, with reduced odds for all other age cohorts when compared with the reference group of 60+ years (seropositive rates: 20–29 [83.2%], 30–39 [86.5%], 40–49 [89.6%], and 50–59 [90.7%]; Table 1]. Employees aged 20–29 years had significantly higher odds of negative measles immunity compared with those aged 30–39 years (OR = 1.29; 95% CI, 1.15–1.45; P < .0001). Employees aged 30–39 years had significantly higher odds of negative immunity compared with those aged 40–49 years (OR = 1.35; 95% CI, 1.12–1.64; P = .002). A significant difference was not found in the odds of negative immunity when comparing employees aged 40–49 years with those aged 50–59 years (P = .419).

DISCUSSION

The results of this age-based serosurveillance study demonstrate that young HCP cohorts are less likely to have detectable measles antibodies, suggesting declining rates of vaccination among younger employees or significant waning of vaccine-induced immunity below the threshold of clinical protection, despite vaccination, due to fewer opportunities of natural boosting from wild-type virus. The lowest seroprotection (83.2%) was observed in the those aged 20–29 years that also comprised the largest group of newly employed HCP (approximately 48% of all new hires). This age cohort includes individuals born after 1985, representing the first generation immunized with 2-dose MMR as opposed to the single-dose MMR for the generation before. While the clinical implications of waning antibodies in young HCP are not completely understood, our study results offer important considerations for prevention and management of measles exposure in HCP. This is especially relevant as policies and practices related to occupational exposures are revisited with the unprecedented worldwide resurgence of measles.

HCP are at a higher risk of measles [9]; 5%–22% of cases in recent outbreaks from Europe and North America have occurred in HCP [6, 10, 11]. Those affected in the workplace are primarily unvaccinated, although reports of measles in HCP vaccinated with 2-dose MMR, including some with baseline evidence of serological immunity, are well described [4, 6, 7, 11]. This raises concern around consequences of waning immunity for measles transmission in the healthcare setting. Notably, in a 2014 outbreak among vaccinated HCP in the Netherlands (n = 6; median age, 27), the attack rate among 2 dose–vaccinated HCPs was 12% [12].

Our findings are similar to those from recent seroprevalence surveys from the general population and among non-US healthcare workers. A UK-based survey performed in 2010–2012 describes measles seropositivity among HCP born after 1980 and 1990 at 88.2% and 73.4%, respectively [13]. The most recent survey from the National Health and Nutrition Examination Survey in 2009–2010 shows the lowest seropositivity rate of 87.9% among the general population aged 30–39 years. Additionally, a serial decline in seropositivity is noted between the ages of 6 and 39, presumably an effect of interval after vaccination [14].

The strength of our study is the large sample size, broader inclusion of HCP born after 1985, and representation of an HCP population from a region that experienced the largest US measles outbreak in the postelimination era. There are several limitations in our data, most notable among these is nonavailability of immunization records, particularly among foreign-born HCP, and lack of information about history of wild-type measles infection. This is a common challenge for pre-employment clearance that necessitates reliance on serological assessments. Second, enzyme immunoassay (EIA)–based testing has the following limitations: EIA assays have lower sensitivity compared with the gold standard plaque reduction neutralization test [5] and EIA does not measure avidity (affinity) of measles antibodies. However, EIA has been used at our institution since 2001, thus offering the same standard of serological assessment for all newly hired employees included in the current study. Some vaccinated HCP with negative or equivocal titers may have detectable measles antibodies on more sensitive assays or can potentially mount an anamnestic response upon measles exposure; however, this is not easily discerned from primary and secondary vaccine failure to enable timely decisions in the postexposure setting [15]. During the 2019 New York City outbreak, public health authorities recommended that HCP with 2 documented MMRs found to have negative IgG in the setting of a measles exposure be considered nonimmune and furloughed for 21 days [16]. With an expanding pool of vaccinated HCP with negative measles titers, a large-scale exposure during an outbreak could pose workforce challenges.

In conclusion, HCP are at a higher risk of acquiring and transmitting measles to vulnerable patients. Our findings demonstrate a fall in the measles seropositivity rate among young HCP entering the workforce possibly due to undervaccination. The gradual increase in the pool of serosusceptible HCP and their management in the event of a workplace measles exposure should be formally addressed in national guidelines. Wider adoption of requirements to increase MMR vaccination rates for healthcare workers is necessary.

Notes

Financial support. This work was supported by a Center Support Grant funded by the National Cancer Institute, National Institutes of Health (P30 CA008748).

Potential conflicts of interest. The authors: No reported conflicts of interest. All authors have submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest.

References