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Cost-Effectiveness of Meningococcal Vaccination Among Men Who Have Sex With Men in New York City

Simon, Matthew S. MD, MS*,†; Weiss, Don MD, MPH; Geevarughese, Anita MD, MPH; Kratz, Molly M. MPH; Cutler, Blayne MD, PhD‡,§; Gulick, Roy M. MD, MPH*; Zucker, Jane R. MD, MSc‡,‖; Varma, Jay K. MD; Schackman, Bruce R. PhD*,†

Author Information
JAIDS Journal of Acquired Immune Deficiency Syndromes: February 1, 2016 - Volume 71 - Issue 2 - p 146-154
doi: 10.1097/QAI.0000000000000822

Abstract

INTRODUCTION

In September 2012, an outbreak of invasive meningococcal disease (IMD) was identified among men who have sex with men (MSM) in New York City (NYC).1 From August 2010 through February 2013, 22 cases of IMD among NYC MSM were reported to the NYC Department of Health and Mental Hygiene (DOHMH).2 Cases were due to a distinct strain of Neisseria meningitidis serogroup C, sequence-type (ST-11), and affected both human immunodeficiency virus (HIV) infected and HIV-uninfected MSM. No IMD cases due to the outbreak strain were recognized among non-MSM. The outbreak was associated with a case fatality of 32% and age-adjusted IMD incidence among NYC MSM was more than 50-fold greater than non-MSM NYC males.1,2

In response, the NYC DOHMH recommended vaccination of all HIV-infected MSM and HIV-uninfected MSM “who had intimate contact with any man met online, through a smartphone application, or at a bar or party.”3 The Advisory Committee on Immunization Practices (ACIP) recommends meningococcal vaccination to control outbreaks when the attack rate exceeds 10 per 100,000 persons compared with a national incidence of IMD of 0.3 IMD cases per 100,000 persons in the United States.4 Routine meningococcal vaccination is recommended for adolescents aged 11–12, with a booster dose at age 16. Vaccine effectiveness in adolescents is estimated to be 80%–85% over 5 years with waning immunity over time.5 ACIP also recommends routine meningococcal vaccination for persons aged >2 months at increased risk for IMD.4 High-risk populations include persons with asplenia or complement component deficiency, military personnel, microbiologists with occupational exposure, and travelers to countries in which IMD is hyperendemic. HIV-infected adolescents are recommended to receive a 2-dose primary series 12 weeks apart based on immunogenicity data suggesting improved response rates compared with a single dose, but response rates were poor regardless of dosing when CD4% was less than 15.6 Several observational studies in the US4,7,8 and South Africa9 have found at least a 10-fold increase in relative risk of IMD in HIV-infected adults compared with age-matched HIV-uninfected adults. However, HIV infection is not currently a recommended indication for routine meningococcal vaccination due to limited data on vaccine efficacy, durability, and cost.

After recognition of the NYC outbreak, additional IMD clusters among MSM have been reported in Los Angeles,10 Chicago,11 France,12 and Germany13 prompting health officials in these locations to issue vaccination recommendations. Past IMD outbreaks among MSM in Toronto (2001) and Chicago (2003) also prompted targeted vaccination efforts.14,15 Such community-based IMD outbreaks, affecting individuals who are linked through a social network, pose unique challenges for public health decision makers who must determine the at-risk population, consider the costs of mass vaccination, and implement an effective and timely response to prevent further morbidity and mortality.16

With the seemingly high likelihood of future IMD outbreaks in MSM populations, we sought to estimate the cost-effectiveness of meningococcal vaccination among HIV-infected and HIV-uninfected MSM based on the NYC experience to inform public health decision making.

METHODS

Model Overview

We developed a decision analytic model (see Appendix, Supplemental Digital Content, https://links.lww.com/QAI/A740) to simulate the health and economic consequences of quadrivalent meningococcal conjugate vaccination (MCV4) in a hypothetical cohort of MSM, with and without HIV infection. MSM in the model are assigned probabilities of developing IMD based on their vaccination and HIV status. Because of uncertainty regarding the indirect protection impact of MCV4 vaccination, we considered scenarios with and without herd immunity. Under the herd immunity scenario, unvaccinated MSM have a reduced risk of IMD due to greater vaccine-induced immunity in the MSM population as a whole. MSM in the model who experience IMD may fully recover, recover with long-term disease sequelae, or die of IMD. Model inputs and sensitivity analysis ranges are reported in Table 1. The model was programmed in TreeAge Pro 2013 (TreeAge Software Inc., Williamstown, MA).

T1-4
TABLE 1-a:
Model Inputs
T2-4
TABLE 1-b:
Model Inputs

The model calculates the number of IMD cases averted, IMD deaths averted, quality-adjusted life-years (QALYs) gained, and costs associated with IMD and vaccination. We adopted a 1-year time frame to account for IMD cases and vaccination costs. The health and economic benefits of preventing IMD-related morbidity and mortality were calculated over a lifetime horizon with future health costs and consequences discounted at 3% annually.17 The analysis was conducted from a healthcare system perspective.

Target Population

The MSM cohort had a mean age of 35 based on the age of IMD cases during the outbreak. We estimated approximately 60,000 NYC MSM to be targeted through DOHMH vaccine recommendations. This estimate was derived using data from the NYC Community Health Survey,18 the NYC HIV/AIDS surveillance registry,19 and the National HIV Behavioral Surveillance system (unpublished data, Kathleen H. Reilly, PhD, MPH, October 2012) (see Appendix, Supplemental Digital Content, https://links.lww.com/QAI/A740).

Vaccine Coverage

Vaccine coverage was based on provider reporting to DOHMH (see Appendix, Supplemental Digital Content, https://links.lww.com/QAI/A740). The number of individuals reported to DOHMH who had received at least 1 dose was 4300 at 4 months, 12,400 at 8 months, and 17,800 at 12 months. The first dose vaccine coverage (17%) was the weighted average over this time period (see Appendix, Supplemental Digital Content, https://links.lww.com/QAI/A740). We assumed HIV-infected and HIV-uninfected individuals did not differ in their likelihood of receiving vaccination. HIV-infected individuals were recommended to receive 2 doses of vaccine 8 weeks apart, and we used data from the HIV clinic at New York Presbyterian Hospital/Weill Cornell Medical Center to estimate the probability of receiving both doses (56% conditional on receiving 1 dose).

Vaccine Effectiveness

Vaccine effectiveness in HIV-uninfected individuals (90%) was estimated from the literature.5 Vaccine effectiveness in HIV-infected adults was based on available data from HIV-infected adolescents and was stratified by CD4 cell count (above or below 200) and receipt of 1 versus 2 doses of vaccine (see Appendix, Supplemental Digital Content, https://links.lww.com/QAI/A740).6,20 We assumed no previous immunity to meningococcal disease (ie, from previous adolescent vaccination or meningococcal carriage) and that immunity did not wane throughout the 1-year time frame.

Herd Immunity

To estimate the indirect effects of vaccination, we incorporated data from a previously published dynamic transmission model of serogroup C Neisseria meningitides.21 The value of Ro, defined as the average number of secondary infections generated by a primary case, reported in that model was 1.36. To model herd immunity, we used this value to calculate a critical vaccination threshold (37%), representing the proportion of immune individuals in the population required to eliminate transmission of the outbreak strain (see Appendix, Supplemental Digital Content, https://links.lww.com/QAI/A740).22 The risk of IMD in unvaccinated MSM was assumed to decline exponentially as a function of vaccination coverage until reaching the critical vaccination threshold based on published functions of herd immunity described by a susceptible-infected-recovered model of infectious disease transmission.22,23 The average relative risk reduction of IMD among unvaccinated MSM calculated during the 1-year time period was approximately 20% using this herd immunity assumption and was varied between 0% and 63% in sensitivity analysis (see Appendix, Supplemental Digital Content, https://links.lww.com/QAI/A740).

IMD Incidence, Mortality, and Impact on Quality of Life

IMD incidence (Table 1) was the incidence of serogroup C IMD in HIV-infected and HIV-uninfected NYC MSM from August 2010 to October 2012, before the initiation of the vaccination recommendations. Risk of IMD was assumed to be independent of CD4 cell count. Case fatality rates were derived from mortality in HIV-infected and HIV-uninfected MSM during the outbreak. We used published sources for the probability and quality-of-life impact of long-term sequelae for IMD survivors including amputation, neurological disability, seizures, and hearing loss (Table 1).24–31 Life expectancy for a 35-year-old HIV-uninfected MSM (42.6 years) was from standard life table mortality data,32 and life expectancy for HIV-infected MSM was from US national HIV surveillance data (28.3 years if CD4 count was above 200 cells/mm3 and 19.4 years if CD4 count was below 200 cells/mm3).33 Additional details are in the Appendix (see Supplemental Digital Content, https://links.lww.com/QAI/A740).

Costs

IMD treatment costs were based on a detailed analysis of US insurance claims data.24 Lifetime health care costs associated with IMD sequelae were derived from the literature.24,34–36 Vaccine program costs included the cost of vaccination ($68 at public sector price and $110 at private sector price) and an additional cost ($25) for staff time to administer vaccine and counsel patients.37 The proportion of vaccinations administered in the public versus private sector was from DOHMH data. Fixed costs ($577,000) were considered separately and included DOHMH expenditures on vaccine promotion and labor (see Appendix, Supplemental Digital Content, https://links.lww.com/QAI/A740). All costs are reported in 2012 US dollars.

Analysis

To project the overall costs and health effects of the vaccination intervention, individual-level outcomes were multiplied by the estimated size of the population (60,000 MSM) targeted by the DOHMH vaccine recommendations. Lifetime costs and QALYs for each strategy were used to calculate incremental cost-effectiveness ratios (ICERs). ICERs were calculated excluding fixed costs, consistent with US guidelines38 and including fixed and variable costs. ICERs were compared with a threshold of $100,000/QALY based on the literature.39,40 Since no universally agreed upon threshold for cost-effectiveness exists in the US,40,41 in a sensitivity analysis, we also considered a higher willingness to pay threshold of $220,000/QALY. This was based on cost-effectiveness of adopted meningococcal vaccination recommendations for US adolescents4 and evidence that societal willingness to pay is higher for life-saving interventions compared with those that reduce relatively mild, chronic symptoms.41 Parameters were varied individually in one-way sensitivity analyses across plausible ranges (Table 1). Overall model uncertainty was evaluated in probabilistic sensitivity analysis by simultaneously conducting 1000 random draws from probability distributions specified for each variable (see Appendix, Supplemental Digital Content, https://links.lww.com/QAI/A740). One-way and probabilistic sensitivity analyses included variable costs only.

RESULTS

Figure 1 displays the modeled reduction in IMD incidence, with and without herd immunity, compared with the number of cases that occurred in NYC in the year after the vaccination recommendations. With herd immunity, the meningococcal vaccination campaign targeting 60,000 NYC MSM was estimated to avert 2.7 IMD cases, 1.0 IMD deaths and to result in a gain of 33.4 life-years. Without herd immunity, vaccination was estimated to avert 1.1 IMD cases, 0.4 deaths and result in a gain of 13.6 life-years (see Appendix, Supplemental Digital Content, https://links.lww.com/QAI/A740).

F1-4
FIGURE 1:
Observed versus predicted IMD cases per month with and without herd immunity.

In the absence of vaccination, the expected cost of IMD in NYC MSM was $793,800. The expected cost of vaccination with herd immunity was approximately $2.2 million with variable costs only and $2.8 million including variable and fixed costs. Depending on inclusion of herd immunity, the cost to avert 1 IMD case was between $520,000 to $1.4 million and the cost to avert 1 IMD death was between $1.4 million to $3.8 million. With inclusion of fixed costs, the cost to avert 1 IMD case increased to between $740,000 to $1.9 million, and the cost to avert 1 IMD death increased to $1.9 million to $5.2 million, with and without herd immunity respectively. In the hypothetical cohort of 60,000 MSM, with herd immunity, vaccination resulted in a gain of 22 QALYs. Without herd immunity, there was a gain of only 9 QALYs. Considering only variable costs, the ICER for vaccination was $66,000/QALY in the herd immunity scenario and the ICER was $177,000/QALY in the no herd immunity scenario. Considering both variable and fixed costs, the respective ICERs were $93,000/QALY and $243,000/QALY (Table 2).

T3-4
TABLE 2:
Projected Cost-Effectiveness of Meningococcal Vaccination in 60,000 NYC MSM

In one-way sensitivity analyses, variables that exerted the greatest influence on results under the herd immunity scenario were the magnitude of herd immunity, IMD case fatality ratio, and IMD incidence (Fig. 2). At a $100,000/QALY threshold, when herd protection reduced the relative risk of IMD in unvaccinated individuals by less than 10% (as compared with 20% in the base case), vaccination was no longer cost-effective. The same result would occur if vaccine coverage was reduced from 17% to less than 9% with the herd immunity assumption. If the IMD case fatality ratio was <18% for either HIV-infected or HIV-uninfected MSM (compared with 40% for HIV-infected and 20% for HIV-uninfected MSM in the base case), the ICER exceeded $100,000/QALY. When IMD incidence was less than 12 per 100,000 persons, vaccination was no longer cost-effective at a 100,000/QALY threshold (Fig. 3). If willingness to pay was $220,000/QALY, vaccination was favorable at IMD incidence as low as 6 cases per 100,000. In the no herd immunity scenario, vaccination at current effectiveness was not cost-effective at $100,000/QALY threshold, unless vaccine cost was reduced to less than $45 (as compared with the base case costs of $68 in the public sector and $113 in the private sector). When vaccination effectiveness was improved to 100%, it was still not cost-effective unless private sector vaccine costs less than $85. In the no herd immunity scenario, varying vaccine coverage had no impact on cost-effectiveness results.

F2-4
FIGURE 2:
Tornado analysis depicting results of one-way sensitivity analysis of key variables. The horizontal bars represent the change in the ICER across plausible ranges. ICERs include variable costs only and with herd immunity fixed at 20% (except for first bar). The vertical line represents the ICER in the base case analysis ($66,000/QALY). aRelative risk of IMD in unvaccinated MSM is varied between 0% and 67%. bCase fatality ratio range for HIV-infected MSM (10%–60%) and HIV-uninfected MSM (5%–40%) is varied simultaneously. cIncidence range for HIV-infected MSM (13–25 per 100,000 persons) and HIV-uninfected MSM (4–24 per 100,000 persons) is both varied simultaneously. dRanges for public sector vaccine cost ($34–$102) and private sector cost ($55–$160) are varied simultaneously with the percentage of public sector vaccine fixed at 42%. eRanges for permanent neurological disability (5%–40%), hearing loss (1%–20%), seizures (1%–10%), and amputation (0%–5%) were varied simultaneously. fValues for vaccine effectiveness in HIV-uninfected (75%–95%), HIV-infected with CD4 >200 after 1 dose (30%–90%) and after 2 doses (35%–95%) were varied simultaneously. gProportion of HIV-infected MSM in the target population was varied from 30% to 90%.
F3-4
FIGURE 3:
Cost-effectiveness ratio ($/QALY) varying IMD incidence with and without herd immunity. ICERs include variable costs only. ACIP recommends vaccination to control an IMD outbreak when incidence exceeds 10 cases per 100,000 persons over a 3-month period. $100,000/QALY is a commonly used standard for cost-effectiveness analyses in the US.39,40

In probabilistic sensitivity analyses, at a cost-effectiveness threshold of $100,000/QALY, vaccination was preferred in 97% of simulations with herd immunity and 20% of simulations without herd immunity (see Appendix, Supplemental Digital Content, https://links.lww.com/QAI/A740).

DISCUSSION

Our study is the first to evaluate the cost-effectiveness of meningococcal vaccination in the context of an IMD outbreak among MSM. Vaccination averted IMD cases and deaths and had an ICER less than $100,000/QALY when including herd immunity but did not meet this threshold without herd immunity. Cost-effectiveness results also depended on IMD incidence and the case fatality ratio.

There are conflicting data on herd immunity protection associated with meningococcal conjugate vaccines, serogroup C meningococcal conjugate vaccine (MCC). Since adoption of qudarivalent meningococcal conjugate (MCV-4) vaccination in adolescents in the US, a reduced risk of IMD has not been observed in unvaccinated groups such as infants or the elderly.4 In contrast, in the United Kingdom (UK), after mass vaccination of infants and adolescents with serogroup C MCC, there was a 67% reduction in risk of IMD in unvaccinated populations.42 A similar indirect benefit occurred in Canada after mass vaccination with MCC.43 Greater impact of MCC on N. meningitidis carriage compared with MCV4 may account for the discrepancy. Although indirect protection with MCV4 has not been established for endemic IMD in the US, such protection is biologically plausible in the context of an IMD outbreak, where a reduction in carriage of only the specific outbreak strain would be required to confer indirect protection. Our model's predicted decline in IMD cases when herd immunity was assumed was similar to observed data in NYC in the year after the vaccination campaign (Fig. 1). However, a formal study of meningococcal carriage would be required to definitively establish the role of herd immunity in halting this outbreak.

From March 2013 to June 2014 no serogroup C IMD cases due to the outbreak strain occurred in NYC compared with 16 cases among NYC MSM in the previous year. Targeted vaccination at MSM bars and sex clubs throughout NYC combined with efforts to promote vaccination on popular MSM mobile phone dating applications may have contributed to interrupting the outbreak.44 Such venue-based vaccination likely enabled the campaign to reach high-risk MSM at the center of transmission, providing individual level immunity, and a sufficient level of protection within the NYC MSM community to prevent additional cases. From June 2014 to December 2014, 5 cases of IMD due to the serogroup C outbreak strain occurred in MSM.45 Three of the cases were linked by person-to-person contact and 2 occurred in HIV-infected MSM who were vaccinated with 2 doses of MCV4. Although vaccination did not prevent IMD in these cases, it may have attenuated illness and prevented death. MCV4 vaccine failures have previously been reported in immunocompromised adolescents5 and our model accounted for diminished vaccine effectiveness due to varying degrees of immunosuppression.

The US ACIP recommends vaccination to control an IMD outbreak when incidence exceeds 10 cases per 100,000 persons over a 3-month period.4 In practice, this recommendation can be challenging to implement because the at-risk population can be difficult to precisely define.16 To our knowledge, this is the first study to evaluate the cost-effectiveness of different incidence thresholds for meningococcal vaccination during an outbreak. We found an ICER of $102,000/QALY at an IMD incidence of 11 per 100,000 persons in a model that assumed herd immunity, consistent with the ACIP recommendation. At a higher willingness to pay threshold ($220,000/QALY), corresponding with the MCV4 adolescent vaccination recommendations, MCV4 vaccination during a community outbreak is economically appropriate at an even lower incidence (6 per 100,000 persons) when herd immunity is assumed. The lower incidence threshold is congruent with the response of public health authorities in Berlin, who recommended vaccination of all MSM at an incidence of 6.3 per 100,000, despite the recommendation of the German Standing Committee on Vaccination (also 10 cases per 100,000 persons).46,47

Our analysis has important limitations. First, we used a static model and made the simplifying assumption that IMD risk depended only on HIV and vaccination status. Similar to previously published cost-effectiveness analyses of pneumococcal and meningococcal vaccination,29,48 we used this static model to incorporate the indirect effects of vaccination. Because of considerable uncertainty regarding specific behavioral risk factors and transmission dynamics of N. meningitidis infection in MSM, using dynamic transmission modeling would have been unlikely to further clarify indirect vaccination effects. Second, we used a hypothetical relationship between vaccine coverage and reduced risk of IMD in unvaccinated MSM incorporating data from a transmission model of serogroup C N. meningitidis in the United Kingdom. This relationship assumes that the risk of disease is homogenous within a randomly mixing population, which is a common limitation of infectious disease models.49 The UK model was not specifically validated for IMD among NYC MSM, and the MCC vaccine used in the United Kingdom has different immunologic characteristics than the MCV4 vaccine used during the NYC outbreak. To account for these uncertainties, we considered a varied impact of herd immunity and presented results using scenarios with and without herd immunity. Third, the effect of fixed costs, such as vaccine promotion, on vaccination uptake and IMD prevention is unknown. Such efforts increased awareness but other unaccounted factors, such as increased media attention, undoubtedly also had a significant impact on vaccination rates. However, assuming the remaining costs were variable likely underestimates the additional costs associated with increasing coverage beyond levels achieved in this outbreak. Fourth, we did not consider patient time or transportation costs and thus did not technically capture a societal perspective. However, we did account for long-term direct healthcare costs of IMD sequelae and incorporating additional indirect costs would not likely have impacted results. Fifth, our estimates of vaccine effectiveness in HIV-infected adults are extrapolated from immunogenicity data in HIV-infected adolescents. We incorporated a wide range of plausible values for vaccine effectiveness to account for this uncertainty, but MCV4 immunogenicity and carriage studies in HIV-infected MSM are needed. Sixth, we did not address the cost-effectiveness of routine vaccination of MSM with or without HIV in a nonoutbreak setting. Several observational studies in the US and South Africa have demonstrated an elevated risk of IMD in HIV infected adults, but not specifically MSM.7,9 Considering the potential for future IMD outbreaks in this population, routine vaccination of high-risk MSM warrants further investigation.2 Lastly, we did not consider vaccination effects beyond 1 year because of limited data on key inputs, such as vaccine coverage, vaccine effectiveness, and IMD incidence. In healthy adolescents, circulating meningococcal antibody levels decline 3–5 years after vaccination and for persons at persistently increased IMD risk, such as those with asplenia and complement deficiency, booster dosing is recommended every 5 years.4 If we had incorporated health effects in subsequent years, cost-effectiveness could have been further improved due to continued, albeit reduced, protection against IMD. However, waning immunity, particularly in HIV-infected MSM, would likely necessitate booster vaccination for sustained IMD protection, incurring additional costs. Revaccination of MSM in NYC is an important policy question because carriage of the outbreak strain in NYC MSM has been observed (NYC DOHMH unpublished data) and could pose a risk for future outbreaks if sufficient population level immunity is not maintained.

In summary, recent IMD outbreaks and case clusters among MSM in the US, Canada, and Europe have created new challenges for prevention and control of IMD. During a large IMD outbreak affecting MSM in NYC, we found a targeted vaccination campaign likely averted IMD cases, deaths and had a favorable cost-effectiveness ratio, but cost-effectiveness results depended heavily on herd immunity in this population.

ACKNOWLEDGMENTS

The authors thank Ismael Ortega Sanchez of the Centers for Disease Control and Prevention for providing expert opinion and feedback.

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Keywords:

Neisseria meningitidis; cost-effectiveness; men who have sex with men; invasive meningococcal disease; meningococcal vaccination

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