Open Forum Infectious Diseases

REVIEW ARTICLE

Risk Factors for Herpes Zoster Infection: A Meta-Analysis

Fawziah Marra, Kamalpreet Parhar, Bill Huang, and Nirma Vadlamudi
Faculty of Pharmaceutical Sciences, University of British Columbia, Vancouver, British Columbia, Canada

Background.  The burden of herpes zoster (HZ) is significant worldwide, with millions affected and the incidence rising. Current
literature has identified some risk factors for this disease; however, there is yet to be a comprehensive study that pools all evidence to
provide estimates of risk. Therefore, the purpose of this study is to identify various risk factors, excluding immunosuppressive med-
ication, that may predispose an individual to developing HZ.
Methods.  The literature search was conducted in MEDLINE, EMBASE, and Cochrane Central, yielding case control, cohort,
and cross-sectional studies that were pooled from January 1966 to September 2017. Search terms included the following: zoster OR
herpe* OR postherpe* OR shingle* AND risk OR immunosupp* OR stress OR trauma OR gender OR ethnicity OR race OR age OR
diabetes OR asthma OR chronic obstructive pulmonary disease OR diabetes. Risk ratios (RRs) for key risk factors were calculated via
natural logarithms and pooled using random-effects modeling.
Results.  From a total of 4417 identified studies, 88 were included in analysis (N = 3, 768 691 HZ cases). Immunosuppression through
human immunodeficiency virus/acquired immune deficiency syndrome (RR = 3.22; 95% confidence interval [CI], 2.40–4.33) or malig-
nancy (RR = 2.17; 95% CI, 1.86–2.53) significantly increased the risk of HZ compared with controls. Family history was also associated
with a greater risk (RR = 2.48; 95% CI, 1.70–3.60), followed by physical trauma (RR = 2.01; 95% CI, 1.39–2.91) and older age (RR = 1.65;
95% CI, 1.37–1.97). A slightly smaller risk was seen those with psychological stress, females, and comorbidities such as diabetes, rheu-
matoid arthritis, cardiovascular diseases, renal disease, systemic lupus erythematosus, and inflammatory bowel disease compared with
controls (RR range, 2.08–1.23). We found that black race had lower rates of HZ development (RR = 0.69; 95% CI, 0.56–0.85).
Conclusions.  This study demonstrated a number of risk factors for development of HZ infection. However, many of these char-
acteristics are known well in advance by the patient and clinician and may be used to guide discussions with patients for prevention
by vaccination.
Keywords.  age; herpes zoster; immunocompromised; meta-analysis; risk factors.

Herpes zoster (HZ) or shingles, as its commonly known, results major complication associated with HZ is postherpetic neu-
from reactivation of the varicella zoster virus (VZV), which ralgia, pain persisting for over 90 days after shingles onset, that
lies dormant in the spinal and cranial sensory ganglia after pri- occurs within 20% of HZ patients [7] with an estimated preva-
mary infection in childhood [1–3]. Herpes zoster presents as lence of 0.5–1 million [8].
a painful, erythematous, maculopapular rash in which lesions It is clear from the literature that millions of individuals are
become fluid-filled before crusting over. Unique features that affected each year by shingles or HZ infection around the globe;
distinguish HZ from other dermatological rashes are unilateral in the United States, more than 1 million new cases of HZ are
presentation and restriction to a single dermatome [4]. Through reported every year [9]. The incidence of HZ ranges from 3 to
various mechanisms, VZV is reactivated to cause HZ. Although 5 per 100 000 in North America, Europe, and Asia, but more
treatment is available via antiviral therapy, there are many oph- importantly, the incidence seems to be increasing with time,
thalmic, vascular, visceral, and neurological complications of and it is unclear to what this may be related [10, 11]. Numerous
HZ [5, 6]. These complications lead to increased all-cause total studies have identified risk factors associated with reactivation
healthcare cost and place financial burdens on patients [6]. The of VZV, many of which are related to a decrease in T-cell im-
munity, such as aging and immunosuppression, but some are
related to family history or stress [12]. We have previously con-
 

Received 18 October 2019; editorial decision 6 January 2020; accepted 7 January 2020.
Correspondence: Fawziah Marra, BSc (Pharm), PharmD, FCSHP, Professor of Pharmacy, ducted a meta-analysis that pooled data from randomized clin-
University of British Columbia, 2405 Wesbrook Mall, Vancouver, British Columbia, Canada V6T
1Z3 ([email protected]).
ical trials and observational studies to determine the magnitude
Open Forum Infectious Diseases® of risk with different immunosuppressive regimens in patients
© The Author(s) 2020. Published by Oxford University Press on behalf of Infectious Diseases with rheumatoid arthritis (RA), systemic lupus erythematosus
Society of America. This is an Open Access article distributed under the terms of the Creative
Commons Attribution-NonCommercial-NoDerivs licence (http://creativecommons.org/licenses/
(SLE), and inflammatory bowel disease (IBD) [13]. This time,
by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any we have focused on pooling data from all studies evaluating the
medium, provided the original work is not altered or transformed in any way, and that the
risk of developing HZ infection except those studies evaluating
work is properly cited. For commercial re-use, please contact [email protected]
DOI: 10.1093/ofid/ofaa005 risk with taking immunosuppressive medications.

HZ-Related Risk Factors  •  ofid  • 1

METHODS immunosuppression (human immunodeficiency virus [HIV]/
This systematic review and meta-analysis was reported ac- acquired immune deficiency syndrome or malignancy [AIDS]);
cording to the MOOSE guidelines for the reporting of obser- (3) comorbidities including asthma, chronic obstructive pul-
vational studies, in accordance with the PRISMA guidelines for monary disease (COPD), cardiovascular diseases (CVDs), IBD,
conducting a meta-analysis [14, 15]. depression, diabetes, chronic renal disease, SLE; and (4) other
studies (physical trauma, psychological stress, smoking).
Data Sources and Search Strategy We measured heterogeneity across studies using the I2 sta-
We conducted a search of MEDLINE, EMBASE, Cochrane tistic, with higher values reflecting increasing heterogeneity
Central, Cochrane Systematic Reviews, Web of Science, and [17]. Sources of heterogeneity were assessed by subgroup anal-
CAB Direct for articles reporting on HZ infection and associ- ysis and by meta-regression [18]. Subgroup analyses included
ated risk from January 1, 1966 to January 31, 2019. Search terms disease subtypes, mean age, sex ratio, and study type. Using
as keywords, Mesh terms and subject headings included the funnel plots, publication bias was assessed, and asymmetry was
following: zoster OR herpe* OR postherpe* OR shingle* AND assessed by conducting the Egger test [19]. Statistical analyses
risk OR immunosupp* OR stress OR trauma OR gender OR were conducted in R version 3.3.2. All analyses were 2 sided
ethnicity OR race OR age OR diabetes OR asthma OR chronic with P < .05 defining statistical significance.
obstructive pulmonary disease OR diabetes. After pooling the
articles and deleting duplicates, a manual review of titles was RESULTS
conducted screening for relevant topics and keywords. Another Search Results, Trial Characteristics, and Risk of Bias
final manual review of article abstract was conducted on short- The literature and manual references search identified 4417
listed articles. The literature search was performed by an au- studies (Figure 1). The majority of these studies were excluded
thor (B.H.) and a university librarian, the article review was based on the title and/or abstract screening and removal of du-
conducted by 2 authors (B.H. and N.V.), and uncertainty and plicate records (N = 4192). Two hundred twenty-five studies
revisions were resolved by consensus. were included for a full article review and 88 studies were in-
cluded, corresponding to 68 cohort studies [20–87], and 20
Inclusion and Exclusion Criteria case-control studies [88–107]. Reasons for exclusion were
We included all English studies that evaluated the risk factors as- mainly irrelevant topic, immunosuppressive therapy focus,
sociated with HZ in the population. We excluded cases and case study design, studies were evaluating herpes treatment and vac-
series reports and literature reviews. We also excluded all studies cine effect rather than risk factors, complications associated
that used immunosuppressive medications, including biologics, with HZ infection, or lack of quantitative data on the incidence
disease-modifying antirheumatic drugs, and/or corticosteroids. of HZ associated with individual risk factors. One percent of
the studies were published between 1965 and 1969, 5% were
Data Extraction, Study Verification, and Quality Assessment published from 1990 to 1999, 17% were published from 2000 to
Data were extracted independently by 2 authors using a stand- 2009, and 77% were published from 2010 to 2018.
ardized abstraction form, with discrepancies being resolved A summary of the baseline characteristics of patients included
through consensus. Data extracted from the studies included for analysis are presented in Supplementary eTable 1. A  total
the author, date of the study, type of study, inclusion and ex- study population of 198 751 846 was included, with 3 768 691
clusion criteria, risk factor, number of patients, confounders HZ cases reported in the included studies. The age ranged from
adjusted for, demographics, and study outcome data. Quality 3 months to 104 years, the percentage of women in studies ranged
assessment of the studies was conducted by 2 authors independ- from 0% to 100%, and the follow-up duration ranged from 1
ently using the Newcastle-Ottawa quality assessment scale [16]. to 62  years. Most studies were conducted in North America
(Canada and United States; N = 35), followed by Asia (China,
Statistical Analysis Iran, Israel, Japan, South Korea, and Taiwan; N = 31), and Europe
Pooled risk ratios (RRs) with 95% confidence intervals (CI) (Belgium, Denmark, France, Germany, Italy, Spain, Netherlands,
were calculated for the risk of HZ associated with key risk fac- and United Kingdom; N = 20). Overall quality of the included
tors, using natural logarithm of reported effect estimates, and studies ranged from fair to good, based on the Newcastle Ottawa
their corresponding CI. Because these observational studies scale assessment, ranging from 6 to 9 for cohort studies and 4 to 9
were conducted in different geographic locations, the true effect for case-control studies (Supplemental eTables 2 and 3).
estimate will likely vary and represent a random sample of ef-
fect estimates; therefore, pooled estimates were obtained using Risk of Herpes Zoster
a random-effects model. The estimates are presented in (Figure 2), and detailed forest plots
We compared the risk of HZ in those with the following: (1) for each outcome can be found in Supplemental eFigure 1–18).
innate risk factors, such as race, sex, age, and family history; (2) Within our categorization of innate characteristics, 56 studies

2 • ofid  •  Marra et al

 Records identified (N = 4417)
Embase, N = 1476
MEDLINE, N = 2600

Identification
COCHRANE, N = 341

Duplicates excluded (N = 776)

Records after duplicates

removed (N = 3641) Records excluded (N = 3416)
Different topic, N = 922
Immunosuppressive therapies, N = 620
Review/ Guideline, N = 524
Ineligible study design (Case Brief, Case
series, letter to editor, cross-sectional,
ecological), N = 431
HZ treatment, N = 260
Screening

HZ vaccination, N = 236
Records after title/abstract Complications of HZ, N = 226
screened (N = 225) Post Herpetic Neuralgia, N = 197

Full-text articles excluded (N = 137)

HZ Epidemiology, N = 104
Abstracts only, N = 28
Commentary, N = 4
Articles included in the Not English, N = 1
Included

review (N = 88)

Figure 1.  Screening of studies for inclusion into the study.

evaluated gender and 39 studies looked at age as potential risk fac- Other nonmedical factors evaluated in studies included psy-
tors for development of HZ. A smaller number of studies evalu- chological stress (N = 8), physical trauma (N = 6), and smoking
ated race (N = 17) and family history of zoster (N = 9). Family (N = 8); HZ was strongly associated with physical trauma
history was strongly associated with an increased risk of HZ than (RR  =  2.01; 95% CI, 1.39–2.91; I2  =  92.5%), but the rest were
controls (RR = 2.48, 95% CI, 1.70–3.60; I2 = 94.4%) (Figure 2). not significant.
Both older age (RR  =  1.65, 95% CI, 1.37–1.97; I2  =  100%) and A considerable amount of heterogeneity was found through
gender (odds ratio [OR] = 1.19, 95% CI, 1.14–1.24; I2  = 99.4%) visual inspection of funnel plot assessment (data not shown),
were associated with an increased HZ risk, but less so than family but after evaluation with Egger’s test only a handful of the risk
history. Of note, a lower risk of HZ was associated with black race factors (family history, SLE, psychological stress, and depres-
(RR = 0.69, 95% CI, 0.56–0.85; I2 = 97.2%). sion) were found to possess statistically significant heteroge-
We found 40 studies that reported risk of HZ from malignan- neity. Most of the heterogeneity was found to be associated with
cies and 18 studies on HIV/AIDS. Human immunodeficiency study design, population, and geographic location.
virus/AIDS was strongly associated with an increased risk of
HZ compared with controls (RR  =  3.22; 95% CI, 2.40–4.33;
DISCUSSION
I2  =  98.1%). Malignancies, such as lymphoma and leukemia,
were also strongly associated with risk of HZ (RR = 2.17; 95% CI, This is the most comprehensive systematic review assessing
1.86–2.53; I2  = 99.6%). Numerous studies evaluated risk of HZ risk factors for HZ infection. Our meta-analysis indicates that
with various concurrent illnesses including diabetes (N = 34), immunosuppression through HIV/AIDS or malignancy places
chronic renal disease (N = 18), CVD (N = 16), depression individuals at significant risk of reactivating the latent viral
(N = 14), COPD (N = 13), SLE (N = 13), asthma (N = 12), suppression. Family history of zoster, physical trauma, and
RA (N = 12), and IBD (N = 8). Most of these comorbidities older age also significantly increased risk. Although the risk is
increased risk of HZ, RR ranging from 2.08 to 1.23, particu- present with female gender, psychological stress, or presence of
larly SLE (RR = 2.08; 95% CI, 1.56–2.78; I2 = 98.00%) and RA comorbidities, such as diabetes, RA, CVDs, renal disease, SLE,
(RR = 1.51; 95% CI, 1.31–1.75; I2 = 99.10%). and IBD, it was slightly less than the former risk factors.

HZ-Related Risk Factors  •  ofid • 3

 Risk Factor No. of Studies Effect Estimate Pooled Effect Estimate with 95% Cl I2 P Value

Innate Characteristics
Family History 9 OR: 2.48 (1.70–3.60) 94.40% <0.0001
Age 39 RR: 1.65 (1.37–1.97) 100.00% <0.0001
Sex (Women) 56* RR: 1.19 (1.14–1.24) 99.40% <0.0001
Race (Black) 17* RR: 0.69 (0.56–0.85) 97.90% <0.0001

Immunosuppression
HIV/AIDS 16* RR: 3.22 (2.40–4.33) 98.10% <0.0001
Malignancies 40* RR: 2.17 (1.86–2.53) 99.60% <0.0001

Co-morbidities
Systemic Lupus Erythematosus 13 RR: 2.08 (1.56–2.78) 98.00% <0.0001
Rheumatoid Arthritis 12 RR: 1.51 (1.31–1.75) 99.10% <0.0001
Chronic Obstructive Pulmonary Disease 12 RR: 1.41 (1.28–1.55) 99.10% <0.0001
Cardiovascular conditions 16 RR: 1.34 (1.17–1.54) 97.50% <0.0001
Inflammatory Bowel Disoder 8 RR: 1.32 (1.24–1.40) 83.00% <0.0001
Chronic Renal Disease 18 RR: 1.29 (1.10–1.51) 99.50% <0.0001
Asthma 12* RR: 1.24 (1.16–1.31) 97.30% <0.0001
Diabetes 32* RR: 1.24 (1.14–1.35) 99.50% <0.0001
Depression 14* RR: 1.23 (1.11–1.36) 98.40% <0.0001

Other Studies
Physical Trauma 6 RR: 2.01 (1.39–2.91) 92.50% <0.0001
Psychological Stress 8* RR: 1.47 (1.03–2.10) 99.50% <0.0001
Smoking 8 RR: 0.96 (0.95–0.97) 36.40% 0.0057

0.5 1 1.5 2 2.5 3 3.5 4 4.5

<---Reduced HZ Risk--- ---Increased HZ Risk--->

Figure 2.  Pooled analysis of the risk of herpes zoster.

The elevated risk in the older patients is likely due to stimulation and immunoglobulin G-mediated B-cell prolifera-
immunosenescence, in which the immune system progres- tion [113]. In elderly patients with reduced immune function,
sively deteriorates as individuals age [108]. Varicella zoster- VZV- specific T-cell immunity (CD4, CD8, and memory T cells)
virus is normally kept dormant in dorsal root sensory ganglia is below the clinical threshold of maintaining virus latency, thus
via specific cell-mediated immunity (CMI) [109, 110]. Cell- placing this population at elevated risk of developing HZ [114].
mediated immunity naturally declines over time, but it is nor- In our meta-analysis, most of the studies were conducted in the
mally boosted by exogenous and endogenous methods, thereby population aged 60 years and over (N = 36), with only 1 study
limiting VZV’s ability to reactivate and cause HZ. Exogenous reporting HZ risk in those aged 40 years and over [29] and 2
boosting occurs through repeated exposures to wild-type VZV studies reporting risk in individuals aged 50  years and above
causing subclinical infections that are immediately mediated by [22, 35]; the lack of data in these at-risk individuals meant we
cellular processes [110]. Endogenously, subclinical reactivation were unable to further characterize risk in these age groups.
of VZV stimulates CD4+ cells to release cytokines, including It is well known that immunosuppressive conditions such
tumor necrosis factor (TNF)-alpha, interferon-gamma, and in- as HIV/AIDS and malignancies [115] result in decreased CMI
terleukin-2 (IL-2) [111, 112]. The latter agent enables T-helper that increases the risk of viral infections, such as zoster. In
cells to stimulate neutrophils and macrophages that phago- general, these individuals have low CD4+ and CD8+ cells and
cytize the zoster virus. In addition, IL-2 promotes CD8+ cells impaired lymphocyte proliferation. We were not able to do a
to release proteases, interferon-gamma, and lysins to destroy separate analysis according to CD4 count because most studies
viral cells. Finally, CD4+ cells also play a role in memory B-cells reported HZ in HIV patients with >350 CD4 cell count and at

4 • ofid  •  Marra et al

the beginning of antiretroviral therapy. Immunosuppression Zostavax is less effective in older individuals and is contraindi-
also impacts recovery of CMI posttherapy, specifically towards cated in immunosuppressive conditions (HIV/AIDs, malignan-
IL-2 and CD4+, which play a significant role in limiting VZV cies), during immunosuppressive drug therapy and pregnancy
reactivation to cause HZ [116]. Autoimmune diseases such as [127]. Shingrix contains a recombinant VZV glycoprotein E
RA, IBD, and SLE also cause impaired CMI [115]. A study by and an adjuvant component that increase VZV-specific CMI
Park et al [112] found lower CD4+ cell counts (including TNF- and enhances specific humoral immunity, respectively [128,
alpha and interferon-gamma) in patients with SLE, which they 129]. Shingrix is recommended to all adults ≥50 years old, in
stated may place individuals at higher risk of HZ. Furthermore, 2 separate intramuscular injections 2–6  months apart [130].
a study conducted by Nagasawa et al [117] also discussed that However, vaccination rates are still low and substantial efforts
SLE patients show altered immune function via tests for delayed by healthcare professionals are required to increase uptake.
hypersensitivity reactions, CD8+ activity, interferon produc- Our study was not without limitations. Most studies selected
tion, and T-cell transformations. Elevated risk factors for both were observational (cohort or case-control studies) and, due to
immunosuppressive conditions and autoimmune diseases were design, have a higher likelihood of bias. The potential for recall
identified in our meta-analysis. bias is possible in the studies that reported on family history and
Only 1 other meta-analysis studied the impact of family his- physical trauma [131]. Family history may have differential re-
tory on developing HZ. Lai and Yew [118] evaluated this re- call depending on various factors, such as the number of years
lationship, as well as dose-response relationships and whether since HZ events, variations in awareness of family history, or the
the number of relatives affected HZ rates. They included 5 strength of the relationships between families. Physical trauma
case-control studies (N = 4169) and identified a statistically sig- can either impair patient’s ability to recall events or strengthen
nificant increase in the risk of family history with first-degree their memory of coinciding events. Finally, selection bias may
relatives (OR = 3.03; 95% CI, 1.86–4.94) [118]. One proposed also be present in studies that collected HZ cases from specialist
genetic mechanism, discussed by Lai and Yew [118], involves clinics such as those from dermatologists [131]. However, bias
human leukocyte antigens (HLAs), specifically HLA-A, which was accounted for via risk of bias assessment, in which all studies
is responsible for presenting peptides to CD8+ receptors to elicit scored low. Due to study design, studies were also at risk of con-
an immune response. IE6862 is a VZV transcription factor founding, although most studies minimized the risk by adjusting
protein and one of the main peptides responsible for eliciting for some of the variables such as age, sex, or other comorbidities.
CD8+ response; a study conducted by Meysman et  al [119] It is likely that a patient with multiple risk factors is at higher
found that patients in Belgium who had lower HLA-A presen- risk for HZ compared with someone with single risk factor;
tation ability of IE62 protein had a 60% greater risk of HZ. however, because of the differences in study design and popula-
Our meta-analysis found female gender places individuals at tion, we were not able to determine cumulative risk in our study.
a slightly higher risk of HZ, but there is no definite explanation Administrative data was the preferred method of data collection
for this difference. However, a review conducted by Fleming by a majority of the studies selected. This form of data can be
et al [34] proposed that gender biases during diagnosis may be miscoded, incorrect, or vary between practitioners [132]. Most
a factor; another probable cause may be due to hormonal or bi- studies accounted for the possible error through various methods
ological differences between genders [120]. such as the following: only including patients with first diagnosis
Black race was seen to be protective against HZ in comparison of HZ, selecting databases that were validated for correctness
to white individuals. There are few documented reasons for this and accuracy, or incorporating various sources to confirm di-
occurrence. A possible explanation is due to differences in house- agnosis (International Classification of Diseases codes + antiviral
hold composition; black individuals may have elevated exposure prescriptions) [89, 90, 103]. Heterogenicity was high, which may
to varicella, which boosts CMI [121]. Other explanations may lie be attributed to variations in study design, differences in out-
in genetic variations, racial differences in reporting disease or the come ascertainment (record linkage, hospital records, diagnosis
frequency of medical interactions [122]. Finally, it may also be re- by physician), characteristics of populations (age, gender, size),
lated to lower rates of healthcare access among black individuals, and countries in which studies were conducted.
which may be due to mistrust or lack of a consistent healthcare
source, and this may contribute to lower numbers of patients seen
CONCLUSIONS
with HZ by a healthcare professional [123, 124].
Currently, there are 2 vaccines on the market, Zostavax (a In conclusion, HIV/AIDS, immunosuppression, family his-
live vaccine) and Shingrix (a recombinant zoster vaccine) [125]. tory, older age, trauma, females, and presence of comorbid
Both vaccines increase cellular mediated immunity. Zostavax is conditions place individuals at an increased risk of HZ. With
no longer the recommended vaccination for HZ because vac- 2 vaccinations available on the market, physicians and other
cine effectiveness after 3  years is only slightly above 50% and healthcare providers can target patient education based on their
is further diminished to ≤24% after 4 years [126]. In addition, risk factors and improve the uptake of zoster vaccination.

HZ-Related Risk Factors  •  ofid • 5

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