Public Health Nursing Vol. 31 No. 3, pp. 206–214 0737-1209/© 2013 Wiley Periodicals, Inc. doi: 10.1111/phn.12073

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Gender Differences in Immediate Hypersensitivity Reactions to Vaccines: A Review of the Literature Mari Griffioen, M.S., R.N.1 and Neal Halsey, M.D.2 1

School of Nursing, University of Maryland, Baltimore, Maryland; and 2Institute for Vaccine Safety, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland Correspondence to: Mari Griffioen, University of Maryland School of Nursing, 655 West Lombard Street, Baltimore, MD 21201. E-mail: [email protected]

ABSTRACT Objective: To examine published studies of immediate hypersensitivity reactions (IHS) following vaccination and to determine whether women are at an increased risk of developing IHS after vaccination. Design and Sample: PubMed was reviewed for vaccine articles reporting IHS by gender through June 2012. Data were abstracted on type of study, vaccine, hypersensitivity reaction, and statistic reported. Measures: Articles were included if they described experimental, quasi-experimental, correlational or descriptive studies and IHS was reported by gender. Results: Of 847 articles found in PubMed, 11 met the inclusion criteria. In eight studies, more women than men reported IHS, in two studies more men than women reported IHS and in one study the count was even. Conclusion: Limited data from these studies suggest that women may have higher rates of IHS reactions following vaccination than men. Limitations to the available data include the lack of denominator data and that the definition of IHS was not consistent across the studies. Large-scale populationbased studies are indicated to determine if there are differences in rates by gender and biologic basis for these differences. Key words: gender, immediate hypersensitivity, review, vaccine, women.

Background The most common adverse events following vaccines are fevers, local reactions, pain and allergic reactions (Zhou et al., 2003). Immediate hypersensitivity reaction (IHS), a form of allergic reaction, usually develops in minutes, but can occur as late as 8–12 hr after initial exposure (Lieberman et al., 2005). IHS can range in severity from very mild urticaria to severe anaphylaxis. Evidence exists to support causal relationships between anaphylaxis, a potentially lethal IHS, and MMR, varicella, influenza, HPV, tetanus toxoid, meningococcal, hepatitis B, and other vaccines (Institute of Medicine, 2011). Women may be at an increased risk of IHS following vaccines as anaphylaxis has been observed in higher frequencies among women than men in several studies. Two studies reviewing anaphylaxis in emergency rooms found 58% (Harduar-

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Morano, Simon, Watkins, & Blackmore, 2010) and 60% (Brown, McKinnon, & Chu, 2001) of anaphylaxis cases reported in women. A population-based incidence study over 10 years reported 56% of anaphylaxis cases to be in women (Decker et al., 2008) and a study of nonfood-related anaphylaxis hospitalizations found 57% of cases to be in women (Poulos, Waters, Correll, Loblay, & Marks, 2007). Women have been found at an increased risk of €gren’s synimmune system illnesses including Sjo drome, systemic lupus erythematosus, and rheumatoid arthritis; 78% of autoimmune diseases occur in women (Fairweather & Rose, 2004). Asthma has been reported to be 20% more frequent in women older than 35 years than men (Leynaert et al., 2012) and for food allergies, 65% occur in women (Kelly & Gangur, 2009). The Vaccine Adverse Event Reporting System (VAERS) has more reports on

Griffioen and Halsey: Gender Differences in Vaccine Reactions women compared to men in all adult age groups (Zhou et al., 2003), which could indicate that women either experience more adverse events or are more likely to report adverse events than men. Vaccination rates by genders were similar as during 2010/2011 influenza season; 31.8% of men and 37.5% of women received the vaccine (Centers for Disease Control and Prevention [CDC], 2011b). Immunization programs have been and continue to be one of the most successful public health interventions implemented to date. Adverse events following vaccines are rare; serious adverse events such as anaphylaxis are very rare, occurring at a rate of about 1 per million for most vaccines (Kelso, Greenhawt, & Li, 2012). As the threat of infectious diseases has diminished, so has the population’s acceptance of side effects from immunizations (Chen et al., 1994). CDC (2011a) recommends infants, children, adolescents, and adults be vaccinated for 17 vaccine-preventable illnesses. Many vaccines are recommended as 2 or up to 5-dose regimens in a lifetime (i.e., varicella, MMR, hepatitis B, DTP) or every 10 years (Td); influenza vaccine is the only one recommended annually. Since 2010, the Advisory Committee on Immunization Practices has recommended that everyone 6 months of age and older receive influenza vaccine every year (CDC, 2012). An increase in influenza vaccination rates in adults can be expected as more than 200 organizations in several states have instituted mandatory influenza vaccination policies for health care employees (Immunization Action Coalition, 2012). Health care organizations with mandatory seasonal influenza vaccination policies, have seen an increase in vaccinated employees from 50% to over 98% (Karanfil, Bahner, Hovatter, & Thomas, 2012; Rakita, Hagar, Crome, & Lemmert, 2010). In the United States, 74% of health care practitioners and technical occupations (requiring a postsecondary education) are women and, of the almost 3 million registered nurses, 91% are women (Bureau of Labor Statistics, 2010), therefore it can be anticipated that an increased number of women will be vaccinated. Concerns about side effects has been stated as the most common reason for health care workers not getting vaccinated (Aguilar-Dıaz, Jimenez-Corona, n-Rosales, 2011; Hollmeyer, Hay& Ponce-de-Leo den, Poland, & Buchholz, 2009) and as a concern among parents vaccinating their children (Salmon

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et al., 2005, 2009). Health care workers who do not receive influenza vaccine often have misconceptions that influenza illness is not a serious illness and that the vaccine is not effective (Hollmeyer et al., 2009). Protective antibody responses usually involve the production of immunoglobulin G (IgG) antibodies, but vaccines also induce the production of other antibodies including IgA, IgD, IgE, and IgM (Nairn & Helbert, 2007). Immediate hypersensitivity reactions occur in persons who have developed IgE antibodies in response to an earlier antigen exposure. These antibodies are often bound to the surface of mast cells. Following a repeat encounter with the antigen, the antigen binds to the IgE and results in the release of histamine and other inflammatory mediators (Nairn & Helbert, 2007). These chemicals stimulate vasodilation, vascular leakage, smooth-muscle spasms, increased mucus secretion, edema, bronchospasms, and epithelial damage (Castillo, 2005). IHS can manifest as urticaria, angioedema, flushing, pruritus without rash, dyspnea, wheezing, rhinitis, dizziness, syncope, hypotension, nausea, vomiting, and/or diarrhea (Lieberman et al., 2005). Anaphylaxis is a severe form of IHS and the most common triggers are drugs, food, insect stings, and latex (Matasar & Neugut, 2003). Estimated population rates of severe anaphylaxis reactions range from 1 to 3 per 10,000 persons (Moneret-Vautrin, Morisset, Flabbee, Beaudouin, & Kanny, 2005) to 49.8 per 100,000 person/year (Decker et al., 2008). Vaccine components including the vaccine agent, preservatives (i.e., thimerosal), antimicrobials (i.e., Streptomycin), stabilizers (i.e., sucrose, gelatin), adjuvants (i.e., aluminum), and residual media from production (i.e., egg protein) can trigger IHS reactions (Halsey, 2002; Institute for Vaccine Safety, 2011). Rates of anaphylaxis following vaccines have been estimated at 0.65 cases per million doses for children and adolescents (Bohlke et al., 2003), 0.5 cases per 100,000 following MMR for persons aged 13 months to 23 years (Patja et al., 2000) and 1 in 131,000 following yellow fever vaccine (Kelso, Mootrey, & Tsai, 1999). The terms “sex” and “gender” are sometimes used indiscriminately resulting in confusion about biologic or cultural determinants. The ambiguous terminology reflects the confusion about whether

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the gender differences in adverse events following vaccines are biologic, environmental or a mix of both. Authors should strive to use the terms “sex” and “gender” conforming to the Institute of Medicine (2001) definition where “women” and “men” relate to societal function and are rooted in biology and shaped by environment and experience; female and male are defined according to reproductive organs and chromosomal functions in an effort to clarify whether they are examining biologic or cultural determinants. In this review, the terms women and men are used in general terms, while female and male are used when discussing the articles.

Research question The objective of this review was to examine published studies of IHS following any vaccine to determine if there is evidence of women being at increased risk of developing IHSs following vaccines. If a true gender difference exists, health care professionals, such as public health nurses, who often are involved in vaccination programs, should be aware that women could be at a higher risk and be prepared to treat these reactions.

Methods Design and sample PubMed was queried for articles describing IHS by gender following vaccination through June 2012. The search strategy included MeSH, text words and asterisk (*) as a wildcard. The following terms were included: vaccine(s), adverse effect(s), adverse event, hypersensitivit*, allerg*, anaphylact*, gender, sex, x chromosome, y chromosome, and sex characteristic. In addition, a search was conducted with each U.S. licensed vaccine and hypersensitivit*; for example “influenza vaccine AND hypersensitivit*. Articles were included if they described experimental, quasi-experimental, correlational or descriptive studies for currently licensed vaccines in the United States; age limits on study participants were not imposed. The search was limited to articles in English and humans. Case studies or case series, practice guidelines, review articles, letters to the editor, and experimental vaccines (HIV, malaria, cancer) were excluded as the focus was on primary studies examining IHS following currently licensed vaccines.

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Measures The authors reviewed titles, abstracts, and articles for eligibility. Articles included were reviewed in detail during face-to-face meetings. The outcomes provided in the articles were reviewed for type of hypersensitivity reaction, that is, allergic reaction, anaphylaxis, anaphylaxis like reaction, hypersensitivity, immediate hypersensitivity, delayed hypersensitivity, urticaria, rash, hives or angioedema. Data were abstracted on type of study, source of data, type of vaccine, gender, type of hypersensitivity, and statistics reported. To compare IHS women to men, the authors calculated incidence ratios for studies with denominator data and ratios for those without.

Results Of 847 articles found in PubMed, 434 were excluded at title level, 248 at abstract level and of 99 articles reviewed, 11 met the inclusion criteria (Figure 1). Reasons for exclusion included the following: description of illness not vaccine, no monitoring of adverse events or hypersensitivity reactions following vaccines, article was not available electronically, the study only included women or hypersensitivity reactions were not reported by gender. Articles not available electronically were not in English or were excluded at title level for not relating to vaccines. The vaccines of interest in the 11 studies were as follows: anthrax (2), 2009 Influenza A (H1N1) monovalent vaccine (2), Japanese encephalitis (2), measles, mumps, rubella (MMR) (1), rabies (2), yellow fever (1) and one study combined results from 10 different vaccines. The definition of IHS varied across the studies with five studies reporting anaphylaxis and the others reported anaphylactic-like reaction, allergic reaction, immediate allergic reaction, hives or urticaria and/or edema. Seven of the studies reported data from passive surveillance systems, two were prospective studies, one reviewed medical records and one relied on vaccine recipient self-report. The studies providing information on IHS by gender are shown in Table 1. In the four studies that provided denominator data, Sever et al. (2004) reported data from the military where females constituted only 15% of the population vaccinated (Department of Defense,

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rou, Tumsah, Al-Jeffri, and Meshkas (2003) followed 44,900 children following MMR and reported two females and no males with allergic reactions. Suwansrinon et al. (2007) reviewed medical records on 72,132 persons and found only one case of anaphylaxis in a female.

Discussion

Figure 1. Flow Diagram Showing Article Review Process 2002). Although many more males than females received the anthrax vaccine, the female/male incidence ratio for IHS was 2.17. The second article examining anthrax vaccine reported four females and no males with hives (Pittman, Gibbs, Cannon, & Friedlander, 2002). Fishbein et al. (1993) found a female/male incidence ratio of 1.90 following rabies vaccine, but Lindsey et al. (2008) reported an estimated female to male incidence ratio of .61 following yellow fever vaccine. The remaining studies only reported frequencies of IHS without denominator data, so no conclusions about population rates could be determined. For Japanese encephalitis vaccine one study reported a female/male ratio of 10:1 (Lindsey et al., 2011) and another did not find a difference by gender (Plesner & Ronne, 1997). Plesner, Ronne, and Wachmann (2000) conducted a case–control study during the same time period and reported a female/male ratio of 1.8:1. Both studies of adverse events following H1N1 vaccine (Tavares et al., 2011; Vellozzi et al., 2010) and a study reporting on multiple vaccines (Zent, Arras-Reiter, Broeker, & Henning, 2002) reported more females than males with IHS. As the information on the number of vaccinees by gender was missing, no conclusions could be drawn from these three studies. Khalil, Al-Maz-

The limited data from these studies suggest that women have higher rates of IHS reactions following vaccination than men; however, few studies included denominator data and the definition of IHS was not consistent across the studies, which prevented the measurement of true risk. While the differences between women and men in immune response to vaccines have been reported (Cook, 2008; Klein, Jedlicka, & Pekosz, 2010), the magnitude of the difference has not been reported. Engler et al. (2008) did report that women who received a half dose of trivalent inactivated influenza vaccine had similar or higher antibody responses compared to men who received a full dose. Although a review of various vaccines (Cook, 2009) and a meta-analysis of inactivated influenza vaccine (Beyer, Palache, Kerstens, & Masurel, 1996) found that women reported more injection site pain than men, neither article reported percentages by gender. The reasons for gender differences in the immune response and adverse events following vaccines have not been determined, but sex hormones have been considered a factor in autoimmunity and hypersensitivity reactions. A review by Chen, Mempel, Schober, Behrendt, and Ring (2008) found that, before puberty, boys were more likely to develop asthma than girls, but after puberty, reports were more prevalent in women. This pattern has also been noted for food allergies in Norway (Namork, Faeste, Stensby, Egaas, & Lovik, 2011) and for anaphylaxis in England (Sheikh & Alves, 2001) and Canada (Simons, Peterson, & Black, 2002). The exact role of sex hormones in immune responses is not clear. Further studies are needed on this issue including levels of reproductive hormones at the time of immunization. A limitation found in the review of the literature was that a majority of the studies used passive surveillance systems, such as VAERS to collect data. These systems have several limitations including underreporting, selective reporting, lack of a control

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TABLE 1. Immediate Hypersensitivity Reactions Following Vaccines by Gender

Author Anthrax vaccine Sever et al. (2004)

Pittman et al. (2002)

Source VAERSa 1998–2001

Self-report 1973–1999

2009 Influenza A (H1N1) monovalent vaccine Tavares et al. (2011) Pharmaceutical safety database 2010 Vellozzi et al. (2010) VAERS 2010 Japanese encephalitis vaccine Lindsey et al. (2011) VAERS 1999–2009 Plesner and Ronne (1997) Pharmacovigilance 1983–1995 MMR vaccine Khalil et al. (2003) Prospective study 2000 Rabies vaccine Suwansrinon et al. (2007) Medical records 1987–2005 Fishbein et al. (1993)

Yellow fever vaccine Lindsey et al. (2008)

Multiple vaccines Zent et al. (2002)

Prospective study 1990–1991

VAERS 2000–2006

Population

Outcomes

Gender specific incidence

N = 2 million doses in 500,000 vaccinees F  51,546b M  448,454b N = 10,722 doses in 1,583 vaccinees F = 332 M = 1,249

Anaphylactic-like reaction

F = 1, M = 4 F/M incidence ratio: 2.17

Hives

F = 4, M = 0

N = 30.8 million vaccinees

Anaphylaxis

F = 81, M = 16 F/M ratio: 5.1:1

N = 82.4 million vaccinees

Anaphylaxis

F = 80, M = 36 F/M ratio: 2.2:1

N = 1.26 million doses distributed N = 350,000 doses distributed

Anaphylaxis Urticaria and/or angioedema

F = 10, M = 1 F/M ratio: 10:1 F = 3, M = 3 F/M ratio: 1:1

N = 44,904 children

Allergic reaction

F = 2, M = 0

N = 72,132 vaccinees F = 35,893 M = 36,239 N = 98 vaccinees F = 50 M = 48

Anaphylaxis

F = 1, M = 0

Immediate systemic F = 2, M = 1 hypersensitivity F/M incidence ratio: 1.90

N = 1,534,170 vaccineesc Anaphylaxis F = 790,865d M = 743,305d

Pharmacovigilance N = 80 million doses 1994–1998

Immediate allergic reaction

F = 1.3, M = 2.3 per 100,000 dosese F/M incidence ratio: 0.61 F = 107, M = 47 F/M ratio: 2.3:1

Note. aVaccine Adverse Event Reporting System. bEstimated from reported 8.7:1 M/F ratio for approximately 2 million doses. cEstimated from years 2000–2006 number of doses distributed. dEstimated from a 2006 survey of clinics. eReporting rate for 100,000 doses administered.

group, inadequate denominator data to calculate event rates, and difficulty in determining causality (Varricchio et al., 2004). Reporting bias might exist in passive systems such as VAERS as women may be more likely to report adverse events than men (Durbin et al., 2009; Hazell, Morris, Linehan, Frank, & Frank, 2009; Kaboli et al., 2010). In passive surveillance systems, the denominator often has to be estimated as few agencies collect centralized data on persons receiving the vaccine; as a consequence it is difficult know the true rates of adverse

events. Another major limitation was the variety of populations observed and methods of data collection make it difficult to compare studies as well generalize to the population at large. Although the information obtained from this review suggests that women have higher rates of IHS reactions following vaccination than men, there are important limitations to the available data. The use of passive surveillance systems with no denominator data makes it difficult to calculate true incidence rates. As adverse events and IHS are

Griffioen and Halsey: Gender Differences in Vaccine Reactions rare, all vaccine studies, regardless of focus, should report results by gender and therefore add to the growing literature about sex differences in general and following vaccines. By recognizing IHS and other adverse events following vaccines, public health nurses are in a position to notify authorities of potentially increased occurrences. Large-scale population-based studies are indicated to determine if there are differences in rates by gender and biologic basis for these differences.

Acknowledgments This study was supported by independent funds without any external support. Neal Halsey has served on safety monitoring committees for Novartis for meningococcal vaccines and from Merck for HPV vaccines. Dr. Halsey also is being compensated for participation in the legal defense over patent lawsuits from Glaxo Smith Kline. Authors wish to thank Tina Proveaux for editorial support.

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Gender differences in immediate hypersensitivity reactions to vaccines: a review of the literature.

To examine published studies of immediate hypersensitivity reactions (IHS) following vaccination and to determine whether women are at an increased ri...
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