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HIV and meningococcal disease, Page 1
Meningococcal Disease in Patients with HIV Infection—A Review of Cases Reported
Through Active Surveillance in the United States, 2000- 2008
Authors: Christine M. Harris1,2, Henry M. Wu1, Jianmin Li3, H. Irene Hall3, Adria Lee1, Elizabeth
Zell1, Lee H. Harrison4, Susan Petit5, Monica M. Farley6, Ruth Lynfield7, Lisa Miller8, Megin
Nichols9, Arthur Reingold10, William Schaffner11, Ann Thomas12, Jessica R. MacNeil1, Thomas
A. Clark1, Amanda C. Cohn1
1Division of Bacterial Diseases, National Center for Immunization and Respiratory Diseases,
Centers for Disease Control and Prevention; 2Logistics Health Inc., La Crosse, Wisconsin;
3Division of HIV/AIDS Prevention, National Center for HIV/AIDS, Viral Hepatitis, STD, and TB
Prevention, Centers for Disease Control and Prevention; 4Department of International Health,
Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland; 5Connecticut
Department of Public Health, Hartford, Connecticut; 6Department of Medicine, Emory University
School of Medicine and the Atlanta VA Medical Center, Atlanta, Georgia; 7Minnesota
Department of Health, St. Paul, Minnesota; 8Colorado Department of Public Health and
Environment, Denver, Colorado; 9New Mexico Department of Health, Sante Fe, New Mexico;
10School of Public Health, University of California, Berkeley, California; Vanderbilt University
School of Medicine, Nashville, Tennessee; 12Oregon Department of Human Services, Portland,
Oregon
Keywords: meningococcal disease; HIV; meningitis; disease surveillance
Summary: In this study of patients with meningococcal disease and HIV infection in the US,
persons living with HIV infection who met the AIDS surveillance case definition have a higher
incidence of meningococcal disease compared to the general adult population.
Corresponding Author (Current Contact Information):
Henry M. Wu, MD
Emory University
550 Peachtree Street NE, MOT 7
Atlanta, Georgia 30308
Email: hmwu@emory.edu
Phone: (404) 686-7892
Fax: (404) 686-4508
Alternative Corresponding Author:
Jessica MacNeil, MPH
Meningitis and Vaccine Preventable Diseases Branch
Centers for Disease Control and Prevention
1600 Clifton Road NE, MS C-25
Atlanta, GA 30329-4027
Email: jmacneil@cdc.gov
Phone: (404) 639-1194
Fax: (404) 315-4681
Disclaimer: The findings and conclusions in this article are those of the authors and do not
necessarily represent the views of the Centers for Disease Control and Prevention
Published by Oxford University Press on behalf of the Infectious Diseases Society of America 2016.
This work is written by (a) US Government employee(s) and is in the public domain in the US.
Open Forum Infectious Diseases Advance Access published October 24, 2016
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HIV and meningococcal disease, Page 2
Abstract
Background: Although HIV infection is an established risk factor for several bacterial infections,
the association between HIV infection and meningococcal disease remains unclear.
Methods: Expanded chart reviews were completed on persons with meningococcal disease
and HIV infection reported from 2000 through 2008 from nine US sites participating in an active
population-based surveillance system for meningococcal disease. The incidence of
meningococcal disease among patients meeting CDC AIDS surveillance criteria was estimated
using data from the National HIV Surveillance System for the participating sites.
Results: Thirty-three cases of meningococcal disease in individuals with HIV infection were
reported from participating sites, representing 2.0% of all reported meningococcal disease
cases. Most (75.8%) persons with HIV infection were adult males aged 25 to 64 years old.
Among all meningococcal disease cases aged 25 to 64 years old, case fatality ratios were
similar among HIV-infected and HIV-uninfected persons (13.3% vs. 10.6%; P =0.6). The
cumulative, mean incidence of meningococcal disease among patients aged 25 to 64 years old
with HIV infection ever classified as AIDS was 3.5 cases per 100,000 person years (95% CI 2.1-
5.6), compared to 0.3 cases per 100,000 person years (95% CI 0.3 – 0.3) for persons of the
same age group not reported to have AIDS (RR= 12.9; 95% CI 7.9- 20.9).
Conclusions: Individuals with HIV infection meeting the AIDS surveillance case definition have
a higher incidence of meningococcal disease compared to the general adult population.
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Introduction
Although it is well-established that individuals with HIV infection are at increased risk of
several bacterial infections, including invasive pneumococcal disease [1], the association
between Neisseria meningitidis infection and HIV infection is less clear. Like Streptococcus
pneumoniae and Haemophilus influenzae, N. meningitidis is an encapsulated bacterial
pathogen that is normally an upper airway commensal, and systemic infections with these
bacteria are associated with asplenia and complement deficiencies [2, 3]. Individuals with
terminal complement deficiencies are at particularly elevated risk of invasive meningococcal
infection [3].
Previous studies examining the association between HIV infection and meningococcal
disease have produced conflicting results. While some case series and studies from
industrialized countries have suggested an increased risk of meningococcal infection in persons
with HIV, early studies were limited by small numbers of patients [4-6]. In contrast, most reports
from Africa have not shown an association [7-10]. Most recently, studies from South Africa [11],
New York City [12], and England [13] with larger case numbers have reported elevated relative
risks of meningococcal disease among HIV-infected individuals. Clinical data describing
meningococcal disease in HIV-infected patients are also limited, though the South African study
found HIV infection to be a risk factor for meningococcal bacteremia [11].
A better understanding of the association between HIV infection and meningococcal disease
is important to inform prevention strategies. In this study, we reviewed cases of meningococcal
disease in patients with diagnosed HIV infection reported through a population-based
surveillance system for meningococcal disease [14, 15] and estimated the incidence of
meningococcal disease in persons with HIV ever classified as stage 3, AIDS.
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Methods
Meningococcal Disease Surveillance
Surveillance of N. meningitidis invasive infection was conducted through the Active
Bacterial Core surveillance system (ABCs), part of CDC’s Emerging Infections Program [14, 15].
ABCs is an active, laboratory and population-based surveillance system with sites in ten states.
The surveillance area included California (3 San Francisco Bay area counties), Colorado (5
Denver area counties), Connecticut, Georgia, Maryland, Minnesota, New Mexico (2004-2008),
New York (15 Rochester and Albany area counties), Oregon, and Tennessee (11 Nashville,
Chattanooga, and Knoxville counties). The population under surveillance was approximately
35,559,550 in 2008, representing 11.7% of the US population in 2008. A case of
meningococcal disease was defined as the isolation of Neisseria meningitidis from a normally
sterile site such as blood, cerebrospinal fluid (CSF), pleural fluid, or joint fluid in a resident of an
ABCs catchment area. N. meningitidis isolates were sent to state public health laboratories for
serogroup determination and to the CDC Meningitis Laboratory for testing with serogroup-
specific real-time polymerase chain reaction assays [16].
Chart Review
Chart reviews are routinely performed on all meningococcal disease cases to collect
demographic and clinical data. Surveillance officers record HIV infection as a comorbid
condition on the case report form if it is reported in the hospital record. For this study,
meningococcal disease cases with onset dates from January 1, 2000 until December 31, 2008
in ABCs sites were included. Cases reported from the New York ABCs site were excluded due
to local health information disclosure policies pertaining to HIV infection. Cases were also
excluded from the Colorado site if reported from 2000 (due to incomplete data for that year
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HIV and meningococcal disease, Page 5
since this site began participation in ABCs during 2000) and the Maryland site if reported from
2000 (since data on comorbid medical conditions were not reported by this site until after that
year).
Expanded chart reviews were performed on persons with diagnosed HIV infection using
a supplemental case report form, that included information on HIV disease-related data (e.g.,
CD4 cell counts, AIDS defining conditions, medications to treat HIV and for opportunistic
infection chemoprophylaxis), meningococcal disease risk factors, comorbid conditions,
meningococcal vaccination history, physical examination at presentation, hospital course, and
complications. Data for the expanded chart reviews were abstracted from the inpatient hospital
record for the episode of meningococcal disease; data from the patient’s primary care clinic
records also were included if available. HIV infection was classified as meeting the CDC AIDS
surveillance case definition if data from the expanded chart review indicated a CD4 count ever
less than 200 cells/µL and/or a history of an AIDS-defining condition [17]. A concurrent CD4 cell
count was defined as a CD4 count dated within three months prior to the date of meningococcal
disease presentation, performed during the hospitalization, or reported in the chart as current.
Analysis
Among meningococcal disease cases ages 25 to 64 years, clinical and microbiologic
characteristics of those with diagnosed HIV infection were compared with those without HIV
infection using the Fisher’s Exact test for categorical data and the Wilcoxon-Mann-Whitney test
for continuous variables. Analyses of younger and older age groups were not possible due to
the paucity of HIV-infected patients outside this age range.
Determination of meningococcal disease incidence among all HIV-infected individuals
was not possible due to the absence of name-based HIV reporting in all states during the study
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HIV and meningococcal disease, Page 6
years. Therefore, the cumulative, annual incidence of meningococcal disease among
individuals aged 25 to 64 years with HIV infection that met the CDC AIDS surveillance case
definition [17] was estimated. The number of persons with meningococcal disease and a history
of a CD4 count less than 200 cells/µL or a history of an AIDS-defining condition was used as the
numerator, and end-year AIDS case counts reported to CDC’s National HIV Surveillance
System for ABCs counties were used as the denominator. Because of increased levels of
AIDS-defining condition ascertainment resulting from our chart review when compared to
routine HIV surveillance (where most cases meet AIDS surveillance criteria with CD4 count
criteria [17, 18]), a second incidence estimate was made including only HIV-infected
meningococcal disease patients aged 25 to 64 years with a CD4 count ever < 200 cells/µL in
the numerator (excluding patients staged with only a history of an AIDS defining condition). The
cumulative annual incidence of meningococcal disease among patients aged 25 to 64 years that
did not meet AIDS surveillance criteria was also estimated. For this calculation, the number of
meningococcal disease cases with no HIV-infection reported to ABCs or HIV-infection reported
but data from expanded chart review did not fulfill CDC AIDS surveillance criteria was used as
the numerator. The denominator was the population of the study area that was not reported
with AIDS, which was calculated by subtracting the number of end-year AIDS case counts
reported to CDC from the total population for the ABCs counties based on US census data.
Confidence intervals were calculated based on Jeffreys Prior method for incidence estimates
and Mantel-Haenszel interval estimates for rate ratios.
All statistical analyses were conducted using SAS 9.3 (SAS Institute Inc., Cary, NC).
Two-sided p-values less than 0.05 were considered significant. This study was determined to
be non-human subjects research, exempt from human subjects regulations by the CDC Human
Research Protection Office. The study was also determined exempt from human subjects
regulations by the participating ABCs surveillance sites except for the Georgia Metropolitan
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HIV and meningococcal disease, Page 7
Statistical Area (MSA) and Maryland sites. The study was approved by the investigational
review boards of the Georgia MSA, Maryland Department of Health and Mental Hygiene, and
Johns Hopkins School of Public Health.
Results
During the study period, 1,613 cases of meningococcal disease were reported. Thirty-
three (2.0%) of these patients had a reported diagnosis of HIV-infection. The median ages of
HIV-infected patients and those without HIV infection were 41 years (range 15-60) and 20.5
years (range 0-98), respectively. Among patients aged 25 to 64 years, there were 491
meningococcal disease cases, of whom 30 (6.1%) had HIV infection reported (Table 1). In this
age group, case fatality ratios were similar among HIV-infected and HIV-uninfected persons
(13.3% vs. 10.6%; P =0.6). Other clinical characteristics, including meningococcal disease
syndrome, and N. meningitidis serogroups were similar among those with and without reported
HIV infection, except a higher proportion of HIV-infected persons were male compared to
persons without HIV infection (83.3% vs. 51.4%, P =0.0007).
Expanded chart reviews were completed for 32 of the 33 persons with HIV infection
(97.0%). Comorbid conditions, physical examination findings, complications, and HIV-related
clinical data are summarized in Table 2. Two patients had initially been suspected to have
disseminated Neisseria gonorrhoeae infection based on clinical findings, including one with
septic arthritis. Eighteen patients had infection that met the AIDS surveillance case definition,
including ten (55.6%) that had a history of a CD4 count <200 cells per µL found on chart review
and eight (44.4%) who met surveillance criteria based on a reported AIDS-defining condition
alone. Twenty-two persons with HIV had a concurrent CD4 count available, with six persons
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(27.3%) having a CD4 count less than 200 cells per µL. Data on HIV viral loads, CD4
percentages, and CD4 count nadir history were limited (data not shown). The case fatality
ratios were similar among HIV-infected patients who met the CDC AIDS surveillance criteria and
those who did not (11.1% vs. 14.3%; P =0.8).
A total of 491 cases of meningococcal disease among persons aged 25 to 64 were
reported to ABCs from study sites, 17 of whom had HIV infection that met the CDC AIDS
surveillance case definition. The mean number of persons living with HIV infection ever
classified as AIDS in this age group each year during 2000 to 2008 in the included ABCs sites
was 53,212, resulting in a cumulative, mean incidence of 3.5 cases per 100,000 person years
(95% CI 2.1- 5.6) for meningococcal disease among persons reported with AIDS. The
incidence of meningococcal disease among the population not reported with AIDS (i.e., patients
with meningococcal disease without HIV reported or patients with HIV infection that did not meet
the AIDS surveillance case definition based on chart review) was 0.3 cases per 100,000 person
years (95% CI 0.3- 0.3), resulting in a rate ratio of 12.9 (95% CI 7.9- 20.9) of meningococcal
disease among persons with infection meeting the AIDS surveillance case definition. The rate
ratio among men (11.8; 95% CI 6.7- 20.6) was not significantly different from that among
women (15.1; 95% CI 5.6- 40.6; P >0.05 for the comparison). The rate ratio among persons
aged 25-44 years (12.5; 95% CI 6.8-25.6) was similar to that among those aged 45-64 (13.2;
95% CI 6.2-25.2).
Ten of the seventeen meningococcal disease patients aged 25 to 64 with HIV infection
meeting the AIDS surveillance case definition had a report of a CD4 count <200 cells/µL. When
including only these patients as cases of meningococcal disease among persons reported to
have AIDS (and considering the excluded seven cases as cases of meningococcal disease
among those not reported with AIDS), the mean incidence of meningococcal disease among
persons reported with AIDS was 2.1 cases per 100,000 person years (95% CI 1.1- 3.7),
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resulting in a rate ratio of 7.5 (95% CI 4.0- 14.0) when compared to the incidence of
meningococcal disease among the population aged 25 to 64 years that were not reported with
AIDS.
Discussion
We found a substantially increased risk of meningococcal disease among adults with
HIV infection that met AIDS surveillance criteria, compared with all other individuals not reported
with AIDS. The clinical presentations and outcomes of meningococcal disease in these patients
were generally similar to those in patients without HIV infection, and patients presented with a
wide range of CD4 counts. Because the incidence of meningococcal disease in the US has
decreased significantly over the past decade [19], and the prevalence of HIV infection in the US
in recent years is estimated to be less than 500 per 100,000 persons [20], the total number of
meningococcal disease cases among persons living with HIV is likely low. Because not all ABCs
sites had name-based HIV case reporting during the period considered for this evaluation and
not all persons with HIV have been diagnosed and reported, we were not able to estimate an
incidence of meningococcal disease among all persons with HIV infection. For our calculation
of incidence, we included those living with HIV infection ever classified as AIDS, which includes
persons with immune reconstitution; therefore, it is important to emphasize that our incidence
estimate applies to a patient population with variable levels of immunocompetence. Although
this population is not necessarily representative of the larger population of persons living with
HIV infection, the increased relative risk we observed for meningococcal disease is similar to
those observed for HIV-infected individuals in New York City, South Africa, and England [11-13].
In this study, almost half of the patients with meningococcal disease and HIV infection
that met AIDS surveillance criteria did not have a CD4 cell count history available and were
staged only with a history of an AIDS-defining condition. Because the majority of persons
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included in the US HIV surveillance system are staged with immunologic (CD4 count) criteria
rather than an AIDS-defining condition history [18], we considered the possibility that our
meningococcal disease incidence calculation might be inflated by the incongruous patterns of
criteria used in staging. To address this possibility, we calculated the incidence of
meningococcal disease among those reported with AIDS including only patients with HIV
infection and a history of a CD4 cell count <200 cells/µL in the numerator. Although the
incidence calculated was lower, the rate ratio was still elevated (7.5) when compared with the
incidence of meningococcal disease in the population not reported with AIDS.
Our study is subject to other limitations. A patient’s HIV status may not have been
known to the treating physician. Among the patients with HIV infection reported in ABCs, many
inpatient medical records had incomplete CD4 count histories (i.e., current counts or nadir
count), and the history of previous opportunistic infections is likely also incomplete. Therefore,
our ascertainment of patients with HIV infection meeting CDC AIDS surveillance criteria is
presumably incomplete. It should also be noted that the AIDS surveillance case definition used
by CDC during the period of this study included a subset of cases without laboratory-confirmed
HIV infection [21]. The above factors would bias our estimates towards an underestimate of
meningococcal disease risk in persons with HIV meeting AIDS surveillance criteria. On the
other hand, any incomplete ascertainment of persons with HIV infection meeting the AIDS
surveillance criteria in the general population would bias our estimates of meningococcal
disease risk in this population towards an overestimate.
We were unable to control for possible confounding due to smoking, which is an
established risk factor for meningococcal disease, due to limited tobacco use history reported in
the ABCs surveillance system during the study period. Smoking prevalence among HIV-
infected individuals has been described to be as much as three times the prevalence in the
general population [22]. The risk of meningococcal disease among smokers is 2-3 times the
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HIV and meningococcal disease, Page 11
risk among non-smokers [23]. Further study may help elucidate the portion of the increased risk
for meningococcal disease among HIV-infected persons that might be attributable to smoking or
other risk factors associated with meningococcal disease.
This study is limited to patients reported during 2000 through 2008; therefore, our
findings do not reflect any changes in disease epidemiology since 2008. Notably, since 2012
there have been multiple reports of meningococcal disease clusters among men who have sex
with men (MSM) [24, 25]. Among cases in MSM where HIV status was known, as many as 59%
of patients were HIV-infected [24]. In our study, data on MSM status were not collected in our
expanded chart review or the standard ABCs case report form.
In summary, we observed an increased incidence of meningococcal disease among
patients with HIV ever classified as AIDS in the United States. Our findings are consistent with
those of other population-based studies that have shown an increased incidence of
meningococcal disease among HIV-infected persons [11-13]. Considering these studies, in
June 2016 the US Advisory Committee on Immunization Practices (ACIP) approved a
recommendation for routine vaccination of HIV-infected persons aged ≥2 months [26].
Funding
This work was supported by the Centers for Disease Control and Prevention Emerging
Infections Program cooperative agreement CI05-026, which funded Active Bacterial Core
surveillance system sites.
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Acknowledgements
We thank the ABCs surveillance officers of the CDC Emerging Infections Program; Tracy Pondo
of the Division of Bacterial Diseases, National Center for Immunization and Respiratory
Diseases (CDC); and David Stephens of the Division of Infectious Diseases, Emory University
School of Medicine.
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Table 1: Clinical and microbiologic characteristics of patients with and without reported HIV
infection, aged 25-64, 2000-2008, in Active Bacterial Core surveillance sitesa. P values for all
comparisons >0.05 unless otherwise noted.
HIV-infected
(N=30)
No HIV infection
reported
(N=461)
Male, n (%)b
25 (83.3)
237 (51.4)
Median age (years)
44.5
44.0
Case fatality ratio (%)
13.3
10.6
Syndrome
Meningitis, n (%)
11 (36.7)
238 (52.8)
Bacteremia, n (%)
11 (36.7)
140 (31.0)
Bacteremic pneumonia, n (%)
7 (23.3)
51 (11.3)
Other, n (%)
1 (3.3)c
22 (4.9)
N. meningitidis serogroup
B, n (%)
7 (25.0)
142 (33.3)
C, n (%)
11 (39.3)
134 (31.5)
Y, n (%)
8 (28.6)
139 (32.6)
W, n (%)
2 (7.1)
11 (2.6)
aDenominators may vary due to missing data.
bFisher’s exact P =.0007
cSeptic arthritis.
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Table 2: Clinical data of HIV-infected persons with meningococcal disease reported by Active
Bacterial Core surveillance sites, 2000-2008 (n =32) a.
N (%)
Past medical history, physical exam on admission, and
complications
History
Previous meningococcal vaccination
0
Tobacco use
11 (35.5)
Asplenia
1 (3.1)
Complement deficiency
0
Diabetes mellitus
3 (9.7)
Liver disease
5 (16.1)
Chronic renal disease
3 (9.7)
Exam
Cachexia, malnourishment, or wasting
5 (18.5)
Fever ≥100.5° F (38° C)
25 (80.6)
Rash
13 (41.9)
Altered mental status or comatose
9 (31.0)
Complications
ICU admission
16 (55.2)
Respiratory failure requiring intubation
8 (25.0)
Purpura fulminans
1 (3.1)
Waterhouse-Friederichsen syndrome
1 (3.1)
Death
4 (12.1)
HIV related clinical datab
CDC AIDS surveillance case definition met
18 (56.3)
History of AIDS defining condition only
8 (44.4)
History of CD4 ever <200 cells/µL only
6 (33.3)
Both AIDS defining condition and CD4 criteria met
4 (22.2)
Concurrent CD4 count available
22 (68.8)
≥500 cells/µL
7 (31.8)
200-499 cells/µL
9 (40.9)
<200 cells/µL
6 (27.3)
History of HAARTc use ascertainable
25 (78.1)
Currently taking at time of presentation
16 (64.0)
Previous use
7 (28.0)
Never used
2 (8.0)
Currently taking opportunistic infection prophylaxis at time of
presentationd
7 (22.6)
aDenominators may vary due to missing data.
bReported data on CD4 percentages and HIV viral load testing was limited and are not shown.
cHAART, highly active antiretroviral therapy
dDefined as taking trimethoprim-sulfamethoxazole, azithromycin, dapsone, or other medication
specifically for prophylaxis against Pneumocystis pneumonia or Mycobacteriam avium complex
infection.
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