International Journal of

Environmental Research
and Public Health

Article
The Role of Age and Gender in Perceived
Vulnerability to Infectious Diseases
Amelia Díaz 1, * , Ángela Beleña 1 and Jesús Zueco 2
1 Department of Personality, Assessment and Psychological Treatment, Faculty of Psychology, University of
Valencia, 46010 Valencia, Spain; Mangeles.belena@uv.es
2 Department of Microbiology and Ecology, Faculty of Pharmacy, University of Valencia, 46010 Valencia,
Spain; Jesus.zueco@uv.es
* Correspondence: Amelia.diaz@uv.es; Tel.: +34-96-2864411




Received: 5 December 2019; Accepted: 8 January 2020; Published: 11 January 2020


Abstract: Background: The study of the immune system has been approached using two separate paths,
the biological immune system and the behavioral immune system. Recently, Gangestad and Grebe
proposed a unique integrated compensatory immune system, where both systems work together and
one of them could compensate for the other when necessary. However, few studies have confirmed
the existence of this integrated compensatory immune system. Our study represents an attempt to
explore the existence of this unique immune system, investigating if the behavioral immune system
variables increase when the biological immune system weakens with age. Material and Methods. The
cross-sectional design study was made up of a final sample of 1108 participants (45.2% men and
54.2 women) aged 18–64 years. The younger group (18–21 years) was made up of students, whilst the
older groups (22 to 64 years) were composed by their relatives and acquaintances, following the snow
ball process. The participants completed the Perceived Vulnerability to Disease Questionnaire that
assesses perceived infectability and germ aversion. Correlations, analyses of variance (ANOVAs), and
independent group comparisons were performed. These analyses showed the relationships between
the variables studied, the effects of age and gender in perceived infectability and germ aversion,
and the differences that perceived infectability and germ aversion presented in different age-groups
separated by gender. Results: A pattern emerged where germ aversion increases as both men and
women get older, but perceived infectability decreases up to the age of 50, and then it increases in
women from that age onward. Gender differences are only significant in younger participants, with
women having higher scores than men in both variables. Conclusion: The results partially support the
existence of a unique integrated compensatory biological/behavioral immune system.

Keywords: age; gender; perceived infectability; germ aversion; biological immune system; behavioral
immune system; integrated compensatory immune system

1. Introduction
The study of infectious diseases has included social, behavioral, economic, anatomical, hormonal,
and genetic variables as factors affecting these diseases. Therefore, due to the features of these factors,
researchers studying the immune system in relation to infectious diseases have taken two diverging
paths according to the importance given to the biological or behavioral variables. Both have been
relevant and complementary in the study of what protects us from these types of diseases, giving
rise to the separation of two immunological systems, a reactive biological system that works mainly
when the infection has already occurred and a behavioral system with a more proactive function:
avoiding the situations or elements that can lead to contagion or infection [1]. Throughout the history
of humankind, infectious diseases have caused serious pandemics that have killed millions of people.

Int. J. Environ. Res. Public Health 2020, 17, 485; doi:10.3390/ijerph17020485 www.mdpi.com/journal/ijerph
Int. J. Environ. Res. Public Health 2020, 17, 485 2 of 10

Examples dramatically illustrating this point are the “Pandemic Influenza” in 1918 or “Spanish Flu”
which is deemed to have killed 20–50 million people [2], or the most recent AIDS pandemic that is
estimated to have killed some 35 million people since it was first detected in 1981 [3]. Consequently,
the study of both approaches, biological and behavioral, is vital, the first to fight the infectious disease
responsible for the pandemic, and the second, to prevent and avoid contagion.
There is a trend in the study of pathogen avoidance that postulates the existence of an integrated
compensatory immune system [4], rather than two separate immune systems, biological and behavioral.
From the different arguments that justify the existence of this integrated immune system, the
compensatory process between the behavioral and the biological systems, illustrated by Fleischman
and Fessler’s study [5] could be highlighted. Fleischman and Fessler proposed “the compensatory
behavioral prophylaxis hypothesis” based on the fact that women avoid contaminants during the luteal
phase and pregnancy when progesterone modulates women´s immune response to tolerate a foreign
body. Therefore, the lower functioning of the biological immune system would be compensated by
higher levels of infection risk avoidance from the behavioral immune system.
Gender and age separately produce differences in both biological and behavioral immunological
systems. Men/women and younger/older comparisons present different prevalence in several infectious
diseases and different immunological responses to infectious diseases and vaccines. In addition, gender
and age differences happen in variables associated to the behavioral immunological system as perceived
infectability, germ aversion, and disgust. Studies performed in recent decades have found that our
biological immune system responses are impaired with age [6–12]. Elderly patients are a good example
of this, showing poor vaccine responses and general increased mortality as a consequence of influenza.
While 90% of young people respond to vaccination, only 40%–50% of people over 60 do the same [8].
Commonly, the diminished response of the biological immune system with age is attributed to thymic
involution and the ensuing decreased production of T cells (responsible for immune responses). This
leads to an increased risk of infectious diseases as we get older [9]. Evidence suggests that although
the biological immune system weakens at a constant rate with age, there is a pivotal age in the mid- to
late fifties (aged 56.3–60.5) that is crucial for screening and intervention [13].
As a general rule, women exhibit a more robust biological immune response to infection than
men [14–17]. Firstly, based on their differences in responses to vaccines, women develop higher
antibody responses and greater vaccine efficacy than men [15]. Secondly, sex hormones play a role
in the regulation of the transcription of many genes involved in the development and maturation of
immune cells, regulation of immune responses, and modulation of immune signaling pathways [16].
Nonetheless, women are not less susceptible to all infectious diseases, being more prone to infections
such as Human Immunodeficiency Virus (HIV) [18]. On the other hand, men are more susceptible to
infectious diseases, such as tuberculosis [19] or parasitic diseases [20].
In the case of the behavioral immune system, three variables are the most commonly studied:
perceived infectability, germ aversion, and pathogen disgust. Pathogen disgust and germ aversion
assess emotional responses to stimuli relevant to disease transmission, whereas perceived infectability
measures beliefs about perceived immunological functioning and susceptibility to infectious
diseases [21]. The first two variables, as affective or emotional responses, could be more specific to a
domain of disease-threat, while perceived infectability, as a self-reflective appraisal of vulnerability,
could be more general in the domains of disease-threat. Gender differences have been shown for
the three variables, with women scoring higher than men, but the effect of age has been studied in
pathogen disgust only. The influence of age over disgust sensitivity has been much more modest
than that of gender, although it has been commonly found that disgust sensitivity decreases with
age [22–24]. However, some of these studies were performed with undergraduate students whose
age range was very limited. Only specific stimuli were assessed, such as face masculinity and its
relationship to pathogen disgust exclusively in young adult women [22], or death-related disgust in
women [23]. Hence, the logical result should be the opposite: If aging is associated to a heightened
threat of disease, and the biological immune system shows a lower response rate when aging, disgust
Int. J. Environ. Res. Public Health 2020, 17, 485 3 of 10

sensitivity should be higher. The “unexpected” downward trend of disgust sensitivity with age can be
explained—firstly, based on the more extensive exposure to experiences of disgust in older people,
leading to habituation [24], and secondly given the amount of energy required for the elderly to
maintain a high defensive behavior [25].
Gender as a demographic variable has a strong effect on disgust sensitivity in several studies, with
women showing more disgust than men [22,26–28]. A similar pattern has been shown by perceived
infectability and germ aversion, from the Perceived Vulnerability to Disease Questionnaire (PVDQ),
with higher scores presented by women rather than men [22,29,30]. The reason for these gender
differences has been attributed to at least two reasons. The first is related to fitness shown by men, and
higher risk behaviors undertaken, with the subsequent indifference for disease signaling cues that
would explain the lower disgust sensitivity in males [25,31]. The second reason is that women would
be more prepared to avoid disease threats than men because of the higher investment of energy in
raising children. This leads women to take on the role of infectious disease protectors, for themselves
and their offspring [23,32].
From the background presented above, it can be assumed that age and gender have an important
role in both biological and behavioral immune systems, or alternatively in the integrated compensatory
immunological system. Therefore, gender differences are only clear in undergraduates or young people
in perceived infectability and germ aversion; and few studies associated age with pathogen disgust. To
our knowledge, there are no studies measuring the effect of age separately, or combined with gender,
on the specific perceived vulnerability to disease variables, perceived infectability and germ aversion.
Thus, there seems to be a significant gap in research on the role of gender in older aged samples, and
the effect that age could have on these variables.
Accordingly, it could be hypothesized that the effect of gender on older aged samples would
be similar to that presented in undergraduates, with women showing higher perceived infectability
and germ aversion than men. On the other hand, based on the compensatory behavioral prophylaxis
hypothesis” [5], we could hypothesize that perceived infectability and germ aversion would be higher
in older age samples in order to compensate for the natural decrease of efficiency in the biological
immune system; thus proving the existence of an integrated compensatory immune system.

2. Materials and Methods

2.1. Participants
The initial sample consisted of 1135 participants. From these, 27 (2.38%) were excluded from
further analyses because of incomplete or insufficient information. The final sample consisted of 1108
participants with an age range of 18 to 64 years (mean age = 33.80 ± 13.65 years), 501 men (45.2%;
mean age = 35.18 ± 13.72) and 607 women (54.8%; mean age = 32.65 ± 13.50). It was made up of
undergraduate students in the younger group and their relatives and acquaintances, following the
snow ball process, in the older groups. Participants were given the scale and clear instructions on how
to fill it out. They completed the scale individually or in small groups. Following previous procedures
on the PVDQ, the data collection was performed in the Spring and Autumn of 2018. This was, in an
attempt to avoid winter, a period with a higher prevalence of colds, flu, pharyngitis, bronchitis, and
other more serious respiratory infections such as pneumonia, which could affect the results. These
respiratory infections are more common in winter due to several factors, highlighting the contact with
other people in closed spaces, less ventilation of homes or sudden changes in temperature [33]. All
participants signed informed consent documents, and feedback was given to the participants after
correcting the scale. Participants completed the scale voluntarily, and no money or credits were given
in exchange for their collaboration. The study was conducted in accordance with the Declaration
of Helsinki, and the protocol was approved by the Ethics Committee of the University of Valencia
(20160202).
Int. J. Environ. Res. Public Health 2020, 17, 485 4 of 10

2.2. Inclusion and Exclusion Criteria for Participation

The participants included in the study were aged between 18 and 64 years. Participants were
excluded for participation when they reported symptoms that could be attributed to an infectious
disease at the time of data collection, since this attribution could affect the participants´ responses to
the PVDQ, even in the cases where symptoms could be derived from a non-infectious disease.

2.3. Instruments
The Spanish validated version of the PVDQ [34] was completed—a 13-item self-report on a 7-point
scale response (with endpoints labelled as “strongly disagree” and “strongly agree”) that measures
two factors: perceived infectability, assessed by 7 items (example: “In general, I am very susceptible to
colds, flu and other infectious diseases”), and germ aversion, assessed by 6 items (example: “It really
bothers me when people sneeze without covering their mouths”). The internal consistency (Cronbach´s
alpha) of these subscales in this study was 0.79 for perceived infectability and 0.59 for germ aversion.
The germ aversion variable is composed of a list of threatening infectious situations, and the subscale´s
internal consistency obtained here is similar to that presented in previous studies: α = 0.61 in Duncan
et al. [21]; α = 0.56 in Prokop and Fančovičová [35]; and α = 0.55 in Wu and Chang [36]. Additionally,
participants completed a sociodemographic record including age and gender information.

2.4. Research Design and Statistical Analyses

The study presents a cross-sectional design [37] that includes age-groups from 18 to 64 years
taking into account gender.
Data were analyzed using IBM Corp. Released 2015. IBM SPSS Statistics for Windows, Version
23.0. Armonk, NY: IBM Corp. Frequencies, percentages, mean age, and standard deviation age were
obtained for the whole sample, and separately for men and women. Correlations, two-way ANOVAs,
and Chi-square tests were performed to find out the relationship between all variables studied and
the effects of age and gender on perceived infectability and germ aversion, respectively. To analyze
differences between groups in a more detailed way, Bonferroni correction, Student´s t, and Cohen´s d
were performed using independent gender and age-groups. As stated in the introduction, the first
age-group should correspond to undergraduates, since most of the studies performed on perceived
infectability and germ aversion have been carried out on this segment, so the age-range for this group
was 18 to 21. However, the question is how to split the remaining participants into different age-groups
in the absence of clear theoretical or biological criteria. Statistical considerations point towards groups
of a minimum of 100 participants and a similar number of years in the interval. Furthermore, clarity
in the interpretation of results, in order to confirm that they are not the consequence of the grouping
chosen in the study, point toward the presentation of different bundles of participants. Following
these considerations, the remaining participants were bundled in different ways: as a single group
age-ranged 22 to 64; in two groups, age-ranged 22 to 43 and 44 to 64; or three groups age-ranged 22 to
35, 36 to 49, and 50 to 64.

3. Results
Pearson correlations were performed for all variables except gender where, due to the categorical
nature of the variable, Spearman correlations were obtained. The results show that perceived
infectability was significantly related with germ aversion (r = 0.15; p < 0.001), age (r = -0.21; p < 0.001),
and gender (r = 0.17; p < 0.001). Germ aversion was also significantly related to age (r = 0.30: p < 0.001)
and gender (r = 0.06; p < 0.05). Accordingly, perceived infectability and germ aversion were positive
and significantly related, whilst perceived infectability showed a negative relationship with age but
positive with gender. Germ aversion was positively associated with both gender and age.
In the next stage of the analysis, two-way ANOVAs were performed to examine the effects of
gender and age on perceived infectability and germ aversion. The analysis showed significant effects of
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the twogerm
lowest
age-groups aversion
age-groups
values,
comparison,with (M = 18.22 Student’s
comparison,
Student’s ±t test
6.02) than the
t test
infectability
.ngvalues
The three (Mgroup
progressively
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the ± 8.06)
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was and
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older
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the
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group For (M
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the
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7.69),
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differences
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6.02)
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perceived
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4tps.
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the = 20.50
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being (M
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perceived
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again
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perceived infectability (M = 24.24 ± 8.06) and lower germ aversion (M = 18.22 ± 6.02) than the older than the
the younger more perceived
group p
(18–21 < 0.001;
infectability d = ± 0.001;
8.06)
one
values, d =
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and
thatwith 0.048
lower
presented for germ
germ aversion.
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significantly (M = 18.22 ± 6.02)
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perceived
being
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the
one p(22–64
< 0.001;
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that
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d presented
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years)
± significantly
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20.50 aversion.
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7.69), =t(1106)
lower 20.50 germ±=7.69),aversion
Student’s
7.11, t(1106)
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=d18.22 p <±0.001;
= 0.48 6.02)
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= 0.48
perceived thefor perceivedand
infectability, infectability,
older
6)younger
and loweronegroup (22–64
germ (M212213
years)
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(18–21 (Mand
years)
= 21.21 =(M
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being
6.33), =±21.217.69),
again Table
±t(1106)
± 6.02)
t(1106)= 6.33),
the 1.
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−7.07, Bonferroni
t(1106)=
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p7.11,
that correction
p-7.07,
< 0.001;
presented
< 0.001; d= p <0.048
d0.001;with 4
fordgerm
= 0.48
significantly age-groups
= 0.048
for perceived (left)
for germ
aversion. and 3 age-groups
aversion.
infectability, (right).
able
and1.
106)
ectabilityBonferroni
= (M = 21.21
7.11,
(M correction
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p =< 24.24
0.001; withfor4 lower
= t(1106)=
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0.48 and age-groups
-7.07, pgerm
perceived (left)
< 0.001; and 3 age-groups
d = 0.048
infectability,
aversion (M for germ
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Age-groups Mean Age-groups Mean
1; d =(M
ars) 0.048
=
Age-groupsfor
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± 213
aversion.
7.69), t(1106)
Mean = 7.11,
Table p <
1. Table
0.001; d 1.
Bonferroni= Bonferroni
0.48 for
Comparison
Age-groups
correction
perceived
correction with 4
Mean D
SE4 age-groups
with
infectability,
age-groups (left) p 3(left)
and and 3 age-groups
age-groups (right).
Comparison (right).
D
SE p
Table 1. SE p SE p
3), t(1106)=
Comparison -7.07, D Bonferroni
p < 0.001; d = 0.048correction
for germ with 4 age-groups
aversion.
18–21
Comparison
Age-groups22–35 (left)
D
Mean
and 3 age-groups
2.76 0.58 (right).
< 0.001 Age-groups 3.39
Mean
Age-Groups Mean Age-Groups 18–21 Mean
22–43 0.57 < p0.001
h 4 18–21
age-groups (left) and
22–35 3 age-groups
2.76 0.58
Age-groups
(right).
< 0.001
Mean 18–21 Comparison 36–49 SE3.39 5.45 pSE
D
Age-groups0.69 p0.001
<Mean Comparison SE D 4.29 pSE
Comparison D
22–43 0.57 < Comparison
0.001 D
44–64 0.63 < 0.001
1. Bonferroni correction
36–49 with 40.69
5.45 age-groups (left) and
< 0.001 SE 3 age-groups
p
50–64 (right).3,86 0.58
4.29 0.67 < <0.001 0.001 SE p
Comparison
Age-groups Mean D 18–21 22–35 2.76
Comparison D 3.39
E p 50–64 18–21 SE 22–35 p 2.76
Perceived
44–64 0.58 < 0.001
0.63 < 0.001
18–21 22–43 3.39
18–21 22–43 0.57 < 0.001
0.57 < 0.001
3,86
18–21
Comparison 0.67
22–35 < 0.001
D 2.76 Age-groups
0.58 < 36–49
0.001Mean5.45 0.69 < 0.001
3.39 4.29
Age-groups Mean 44–64 0.63
SE 36–49 Infectability
p 22–35< 5.45
36–49 50–64
18–21
36–49 0.693,862.69
SE 22–43
< 0.001
0.62p < <0.001
0.67
0.57
0.001 44–64 < 0.001
22-43 44–64
4.29 0.56 < 0.001
0.63 0.90< 0.001 0.326
58 < 0.001
Comparison D Perceived 3.39 5.45 Comparison
0.69 0.001 D 4.29
22–35 36–49 18–21 22–43
2.69 0.62 < 0.001 0.57 <
22-43 0.001
44–6450–64 1.10
0.90 44–64
0.64
0.56 0.326 0.510 0.63 < 0.001
69
8–21 < 22–35
0.001 2.76 InfectabilityPerceived
0.58 50–64 4.29 3,86 50–64
< 0.001 0.67 < 3.86
0.001 3.390.67 < 0.001
50–64 44–64 0.64
1.10 0.5100.63 <22–43
18–2122–35 0.001 36–49 0.57 0.62
< 0.001< 0.001
67 Perceived
<36–49
0.001 5.45 0.69 Infectability
< 0.001
22–35 36–49 2.69 4.29
0.62
2.69
< 0.001
22-43 44–64 0.90 0.56 0.326
Infectability 44–64 50–64 1.100.63 <
0.64 0.001 0.510
50–64 3,86 22–35
0.67 36–49
< 0.001 2.69 0.6236–49< 0.001
50–64 22-43 -1.60 44–64
0.73 0.90
0.177 0.56 0.326
62 36–49< 0.00150–6422-43-1.60 1.100.5650–64
50–64 0.900.177
44–640.73 0.640.326 1.100.510 0.64 0.510 22-43 44–64 0.90 0.56 0.326
18-21 22–35 -1.54 0.47 0.006 < 0.001
64
2–35 36–490.510 2.69 0.62 36–49 22-43
< 0.001 44–64−1.60
50–64
36–49 50–64
0.73 0.56
0.90 -1.60
0.177 0.326 18–21 22–43 -1.94 0.45
18-21 22–35 -1.54 0.47 0.006 36–49 -3.36 0.73 <0.177
0.56 < 0.001 0.001 < 0.001
50–64 1.10 36–49
0.64 50–640.510 18-21
-1.60 22–3518–21 22–43
0.73 −1.54
0.177 0.47
-1.94 0.006
0.45 18–21 22–43 44–64 0.45 -4.61
−1.94 < 0.001
0.49
36–49 -3.36 0.56 < 0.001 18-21 22–35 50–64 -5.10
-1.54 0.47 0.54 < <
0.0010.001
0.006 < 0.001
73 0.177
50–64 -5.10 36–49 44–64 −3.36 -4.61 < 0.001
0.56 0.49 18–21 22–43
44–64 −4.61 0.49-1.94< 0.001
0.45
Germ0.54
18-21 22–35 < 0.001
-1.54
Germ Aversion 0.47 36–49
0.006 -3.36 0.56 < 0.001 < 0.001 < 0.001
6–49 50–64 -1.60 Aversion
0.73 36–490.177 -3.36 50–64 0.5622-35 36–49 0.54
<−5.10
50–64
0.001
18–21
-1.81< 22–43
-5.10 0.53 < 0.001
0.54
0.001
-1.94 0.45
0.004 22–43<44–64
44–64
0.001
-4.61 0.49
47 0.006 < 0.001 -2.67 0.44 < 0.001
36–4918–21-1.81
22-350.001 22–430.53 -1.94 0.004 0.45 22–43 44–64 50–64 -3.54 44–64
0.51 <-4.61
0.001 0.49
56
8-21 <22–35 -1.54 0.47 50–64Germ 0.006 -5.10 36–49
22-35
Aversion
0.54< 0.001<−1.81
0.001 0.53
-2.67 0.004
0.44 <22–43
< 0.001 0.001 44–64 −2.67 0.44 < 0.001
50–64 44–640.51 -4.61
-3.54 < 0.0010.49 22–43 36–49-1.94 -1.81
18–21 22-35 0.45 0.53 0.004 22–43 44–64
54 <36–49
0.001 -3.36 0.56 < 0.001 < 0.001
Germ Aversion 50–6444–64−3.54
36–49 50–64 0.51-1.74
-4.61 < 0.001
0.49 0.59 < 0.001
0.002 -2.67 0.44 < 0.001
50–64 -5.1022-350.54 36–49
< 0.001 -1.81 0.53 50–64
0.004 -3.54
22–43 0.51
44–64
SE = Standard -2.67 0.44 < 0.001
53 36–49 0.00450–6422–43-1.74 44–640.59
50–64 -3.54 Error;
36–49
0.002 0.51 D = Difference.
50–64 <−1.74
0.001 0.59 0.002
rror; -2.67 0.44 < 0.001
2-35 D<=36–49
51 Difference.
0.001 -1.81 0.53 0.004 22–4336–4944–64 SE = Standard
50–64 -1.74 = Difference.
0.59
Error; D 0.002
50–64 214
36–49
-3.54 0.51 SE =
50–64 Student´s
Standard
< 0.001 -1.74 t and
Error;
0.59D Cohen´s
= d
Difference.
0.002 -2.67
were 0.44 < 0.001
performed, taking into account the gender variable first in the
and Cohen´s
59 SE =0.002 d were 215
Standard Error; DStudent´s whole
performed, t and Cohen´s d were performed, taking into account theshowed
= Difference. sample
taking intoand then
account in
theeach age-group.
gender variable Men and
first in women
the gender significant
variable firstdifferences
in the in both
nd
6–49then50–64in each -1.74 2160.59
214
age-group.
whole sample perceived
Men andthen
Student´s
and
0.002 infectability
women t and
in showed
each andsignificant
Cohen´s
age-group. germ
d were aversion
Men andin
differences
performed, the taking
women whole
in showed sample.
bothinto Perceived
account
significant infectability
thedifferences
gender variable was
in both higher
first in thein
ability and germt aversion
Student´s
D = Difference. and217
215 in
Cohen´s women
the
whole d whole (M
sample
were = 22.79
sample.
and
performed, ±
then 8.40)
Perceived
in
takingthan
each in men
infectability
age-group.
into account(M = 19.98
was
Men
the
perceived infectability and germ aversion in the whole sample. Perceived infectability was higher in ±
higher
and
gender 7.11),
in
women t(1106)
variable =
showed
first6.04,
in p < 0.001;
significant
the d = 0.36.
differences In ainsimilar
both
79whole
med, ± taking
8.40) than
sample and 218
216
intoinaccount
men (Mthe
then
women in
(M = 22.79
way,
=perceived
19.98
each
gender ±germ
7.11),
age-group. aversion
variable t(1106)
±infectability
8.40) Men
first
than =wasand
and
inin higher
6.04,
the
men p(M =in
< 0.001;
germ
women women in(M
d =±0.36.
aversion
showed
19.98 =t(1106)
In
the 20.74
a similar
whole
significant
7.11), ±=sample.
6.59) p <Perceived
6.04,than
differences menin both
0.001; d ==infectability
(M 19.67±
0.36. In 6.11), t(1106)
was
a similar higher= 2.01,
in
dsion
Men was women
perceived
and
Cohen´s higher 219
217
wereinshowed
women
d infectability
performed,
way, and(M paversion
women=< 20.74
germ
significant
germ 0.05;
taking (Md±was
=6.59)
aversion= 0.17.
22.79
differences
into inHowever,
than
account
higher ±the men
8.40)
in
in whole
both
the (Mthese
than =in
19.67±
sample.
gender
women (M men= 20.74
significant
6.11),
(M =±
Perceived
variable differences
t(1106)
19.98
first
6.59) = 2.01,
±than
7.11),
ininfectability
the menwere
t(1106)
(Mwas==19.67±
not present
6.04,
higher < in
p6.11),
in all
0.001; = 2.01,
age-groups,
d = 0.36.
t(1106) In aassimilar
shown
.hen
theHowever,
women
whole
in each(M these
= 22.79
sample. <220
218
significant
± 0.05;
8.40)
pPerceived
age-group. Men =infectability
in
dway,
than Table
differences
and germ
in
0.17. men
women 2,aversion
where
However,were
(Mwas only
not
= 19.98
showed was
higher
these ±women
present
higher
7.11),
significant
significant between
in int(1106)
inallwomen 18(Mand
age-groups,
= 6.04,
differences
differences p=in 21
as
<20.74
were 0.001;
both years
shown
not =old
± 6.59)
dpresent
0.36.presented
than Inmen
in aall (Mhigher
similar = 19.67±
age-groups, perceived
6.11),
as shown infectability
t(1106) = 2.01,
eway,
9.98
ity only women
germ
± 7.11),
and aversion
germt(1106)
aversion=221
in219
between in18
was
6.04,
Table <and
2,pand
phigher
the 21
whole
where germ
<0.001;
0.05;inyears = aversion
women
dsample.
only old
0.17.
0.36.
women (M
In a=than
presented
However,
Perceived20.74
similar
betweenmen. Perceived
higher
these
±infectability
6.59)
18 perceived
significant
than
and men
21 wasinfectability
years(M
higher= 19.67±
old in was
infectability
differences were also
6.11),
presented nothigher
present
t(1106)
higher in women
=perceived
2.01, than men as
in all age-groups,
infectability in the age-
shown
on <than
p20.74
=8.40) ±men.
0.05;
than d in
= 0.17.
6.59) than
men (M222
220
Perceived
However,
men= (M
19.98 in
=groups
infectability
Table
these
19.67±
± 7.11), 22–64,
2, was
where
significant
6.11),
t(1106) 22–43,
also
t(1106)
= higher
only
6.04, and
= women
differences2.01,
p < 22–35,
in women
0.001; but
between
were d from
than
not
= 0.36.
and germ aversion than men. Perceived infectability was also higher in women than men in 18 the
men
present
Inand
a four
in 21
in
similar age-groups
the
all age-
years old
age-groups, comparison,
presented
as shown higherit seems that
perceived the difference
infectability
2–43,
was and 22–35,
in Table
differences
higher 2, in but
where
were not
women 223
221
from
only
present
age-groups the
= and
(Mwomen was
infour
20.74 ±found
germ
all
22–64, age-groups
between
age-groups,
6.59) in
aversion18
than
22–43, theandlast
menthan
as 21group,
comparison,
shown
(M men.
years
22–35, 22 to
it seems
Perceived
= 19.67±old
but 35 years.
that
presented
6.11),
from theThe
infectability
t(1106)
the fourhigher difference
=difference
2.01, between
was alsocomparison,
perceived
age-groups higher men
in
infectability itand
women seemswomen
than men
that is
thenoteworthy
in the age-
nde and
last group,
germ
21 years
wever, theseold to 222
22presented
aversion 35than
significant years.men.
higherThePerceived
groups
differences difference
22–64,
perceived
were not between
22–43,
infectability
infectability
present men
and 22–35,
inwasalland
butwomen
also from
higher
age-groups, theis
in noteworthy
four
as women
shown age-groups
than men comparison,
in the age-it seems that the difference
nly groups
tability
women 22–64,
was 223
also22–43,
between 18and
higher was
in 22–35,
and women
21 yearsfound
butthan inmen
from
old the last
thein
presented fourthe age- 22perceived
group,
age-groups
higher to 35 years.
comparison, Theitdifference
infectability seems thatbetween men and women is noteworthy
the difference
hanwasage-groups
our found
men. in the
Perceived last
comparison,group,it 22
infectability seems to 35
was thatyears.
also the Theindifference
difference
higher women than between
men men in theand age-women is noteworthy
The
, and difference
22–35, butbetween
from themen fourand women comparison,
age-groups is noteworthy it seems that the difference
st group, 22 to 35 years. The difference between men and women is noteworthy
 Int. J. Environ. Res. Public Health 2019, 16, x FOR PEER REVIEW 6 of 10

224 in perceived infectability in the age range of 18 to 21 years old, highly significant and with a large
Int. J. Environ. Res. Public Health 2020, 17, 485 6 of 10
225 effect size.

226 difference was found Table

in2.the
Mean
lastdifferences
group, 22between men and
to 35 years. women
The in eachbetween
difference age-group.
men and women is
noteworthy in perceived infectability in thePerceived
age range of 18 to 21 years old, highlyGerm
significant and with
a large effect size. Infectability Aversion
Age-groups n M SD t d M SD t d
18–21 ♂ 2. Mean20.35
Table 121 differences between men and women in17.11
6.87 each age-group.
5.20
♀ 181 26.83 7.76 -7.44*** -0.88 18.97 6.42 -2.77** -0.32
Perceived Germ
Infectability Aversion
22–35 ♂ 168 20.36 7.42 19.76 5.86
Age-Groups ♀n M
213 SD
22.36 8.65 t -2.43* d -0.25 M 19.77 SD 6.25 t0.02 d
0.00
18–21 ♂ 121 20.35 6.87 17.11 5.20
36–49 ♀ ♂
181 100
26.83 19.12
7.76 7.70
−7.44 *** −0.88 18.9720.83 6.42 6.26 −2.77 ** −0.32
♀ 101 18.44 6.59 0.67 0.10 22.32 6.28 -1.68 -0.24
22–35 ♂ 168 20.36 7.42 19.76 5.86
♀ 213 22.36 8.65 −2.43 * −0.25 19.77 6.25 0.02 0.00
50–64 ♂ 112 19.76 6.34 22.61 5.97
36–49 ♂ 100
♀ 19.12
112 7.70
21.00 7.62 -1.33 -0.1820.8324.04 6.26 6.34 -1.74 -0.23
♀ 101 18.44 6.59 0.67 0.10 22.32 6.28 −1.68 −0.24
22–43 ♂
50–64 112
♂ 19.76
224 6.34
20.01 7.59 22.6119.88 5.97 5.97
♀ 112
♀ 21.00
267 7.62
21.56 8.49−1.33 -2.14* −0.18 -0.1924.0420.40 6.34 6.47 −1.74
-0.91 −0.23
-0.08
22–43 ♂ 224 20.01 7.59 19.88 5.97
44–64 ♀ ♂
267 156
21.56 19.64
8.49 6.59
−2.14 * −0.19 20.4022.31 6.47 6.02 −0.91 −0.08
44–64 ♂ ♀
156 159
19.64 20.25
6.59 7.26 -0.78 -0.0922.3123.34 6.02 6.22 -1.50 -0.17
♀ 159 20.25 7.26 −0.78 −0.09 23.34 6.22 −1.50 −0.17
22–64 ♂ 380 19.86 7.19 20.88 6.10
22–64 ♂ 380 19.86 7.19 20.88 6.10
♀ 426 21.07 8.07 -2.25* -0.16 21.50 6.53 -1.38 -0.10
♀ 426 21.07 8.07 −2.25 * −0.16 21.50 6.53 −1.38 −0.10
♂ =Men; ♀= Women; M = Mean; SD = Standard Deviation; t = Student´s t-test; d = Cohen´s d; * p < 0.05; ** p < 0.01;
♂ =Men; ♀= Women; M = Mean; SD = Standard Deviation; t = Student´s t-test; d = Cohen´s d; * p < 0.05; ** p <
*** p < 0.001.
0.01; *** p < 0.001.

227 The representation of the mean in the four age-groups in men and women in Figure 1 clearly
228 differences at
shows the important gender differences at the
the ages
ages of 18 to 35 in
in perceived
perceived infectability.
infectability. Similar scores
229 are shown at the ages of 36 to 49, 49, where
where both
both men
men and
and women
women get the the lowest
lowest value,
value, their perceived
230 infectability increasing again at the age of 50–64. At this stage, women present more extreme values
231 than men, whose representation
representation line is flatter.
flatter. Germ aversion shows a similar similar pattern
pattern in
in both
both genders.
genders.
232 only peculiarity
The only peculiarityisisthat
thatwomen
womenpresent
present higher
higher values
values than
than menmen in age-groups
in all all age-groups except
except at age
at the the
233 age22ofto22
of 35,towhere
35, where their values
their values are similar.
are similar. At aspecific
At a more more specific
level, whenlevel,looking
when atlooking
the germat the germ
aversion
234 aversion
items, items,
there there is aincrease
is a constant constant
inincrease
the four inagethe four age
groups groups
in the in the
six items six items or
or behaviors behaviors
that made upthatthe
235 made up
factor, withthethe
factor,
lowestwith the in
scores lowest scoresage-group
the 18–21 in the 18–21
andage-group
the highestand the 50–64
in the highest in the 50–64 age-
age-group.
236 group.

237
238 Figure 1. Perceived infectability and germ aversion for the four age-groups (18–21; 22–35; 36–49; and
239 50–64) in men and women separately.
separately.
Int. J. Environ. Res. Public Health 2020, 17, 485 7 of 10

4. Discussion
Taking our sample as a whole, our results present a picture where women obtained higher
perceived infectability and germ aversion scores than men, confirming previous studies with these
variables [21,29,30] and with disgust variables [22,26–28]. However, a closer look at the results obtained
with the sample divided by age-groups reduces these similarities concerning previous results to
younger age groups, especially those including undergraduates. Men and women aged over 35 years
did not present significant differences in perceived infectability and germ aversion.
The explanation for these gender differences also applies better to younger age-groups than older
ones. In a behavioral context, men are more into fitness, health risk activities, and sensation seeking,
being more indifferent to infectious and contagion signs than women [25,31]. The peak point in health
risk behaviors, such as extreme sport, alcohol and drug consumption, driving, and sexual activities
undertaken by men has been suggested to correspond to an age of 35 [38], whilst sensation seeking has
been suggested to peak in the twenties [39]. On the other hand, women are more concerned about
infectious or contagious clues when they are of child-bearing age, pregnant or raising young children,
which occurs in younger women [23,30]. The fact that most studies about gender differences have
been performed on samples of young adults may explain why these differences were not so obvious in
studies where the sample included a wider range of ages [33].
The results from this study are also more coherent with the biological immune system responses
than previous studies using disgust variables in relation to age [22–24]. In general, women and young
people present a stronger immune response than men and older people [14–17], but the inflexion
point in the biological immune system seems to occur in the fifties, where the necessity for health
assessment and screening is especially relevant [13]. Therefore, it may explain why people up to the
age of 49 perceive that their immune systems are protecting them, but this perception changes from
the ages of 50 to 64 where it goes in the opposite direction. Our results show that this is exactly the
evolution that perceived infectability follows in women, dropping until they reach the age of 50, only
to increase again from this point onward while the biological immune system is weakening. The
differences between men and women in perceived infectability could be tentatively explained by sex
hormones. Menopause in women produces an increment in the risk of several diseases, including
coronary heart disease [40], osteoporosis [41], and type 2 diabetes [42]. Although all the diseases cited
are not infectious, women’s health after menopause seems to be poorer, so they could perceive that
their immune system is weaker than before menopause.
The role played by germ aversion in our study is totally concordant with what could be expected
from the evolution of the biological immune system, showing an increasing aversion to germs as our
own biological immune system weakens with age. Accordingly, germ aversion may be an adequate
variable for the study of the integrated compensatory immune system response, as it seems to work in
a logical manner: increasing with age to compensate for the progressive weakening of the biological
immune system in both genders. Therefore, our study suggests a link between the biological and the
behavioral immune systems, where germ aversion in both men and women, and perceived infectability
in women over 50 years of age confirm “the compensatory behavioral prophylaxis hypothesis” [5] and
partially support the existence of an integrated immune system [4]. Furthermore, our results represent
a significant step forward in two of the main issues in the study of the behavioral immune system
proposed by Ackeman et al. [43], namely, the linking the biological and behavioral immune systems
and the study of the evolution of the behavioral immune system throughout life.
The PVDQ used in this study [34] includes both statements on the resistance or weakness of our
immune system, together with others on avoidance or non-avoidance behavior towards germ-risk
situations, placing the person being assessed in a situation that goes beyond simple disgust, where
the risk of contagion could be high. Sentences related to the participants’ history of susceptibility to
infectious diseases, and more specifically, being more likely to catch a cold, flu or other infectious
diseases, are combined with sentences on avoiding people sneezing without covering their mouths
or washing their hands after touching something that could be contaminated. This combination of
Int. J. Environ. Res. Public Health 2020, 17, 485 8 of 10

statements assumes an awareness of the diversity of bacteria, viruses, and parasites and their possible
transmission, in any of the situations listed as items on the scale. Likewise, the relationship between
the two PVDQ variables, perceived infectability and germ aversion, significant but low in the studies
published [21,34], does not allow us to conclude that a high perceived infectability directly implies a
high germ aversion. Mediational variables may affect this relationship in the same way that they could
have an important role in the differences presented by men and women in the younger groups in both
variables, perceived infectability and germ aversion. Sensation seeking and risky sexual behavior in
men, or child bearing age in women may mediate/modulate these differences, and they should be
taken into account in future research on the subject. The interpretation of the results of this study is
partially limited by the possibility of unmeasured variables having an effect on the results we have
found. Cohort/generational effects due to cross-sectional method; demographic variables such as
parenthood; and psychological variables such as anxiety and physiological variables such as estrogen
levels could all have a role in explaining gender and age effects in perceived infectability and germ
aversion. Future research should include these variables in order to discard or confirm this possibility.
Finally, the results should be placed in the specific context from where the sample has been
obtained, Spain. Vaccination coverage is 97% (poliomyelitis, diphtheria, tetanus and pertussis, hepatitis
B, meningococcal group B and C, pneumococcus, Haemophilus influenzae type b, measles, rubella,
mumps, and human papillomaviruses) although vaccination is not mandatory. This percentage
decreases to 92% in booster doses. It is also significant that some 54% of adults over 64 years were
vaccinated against influenza in the winter of 2018–2019 [44]. Therefore, we could conclude that
awareness of infectious diseases and confidence on the preventive value of vaccination is relatively
high in the Spanish population.

5. Conclusions
Our results on the effect of gender and age in perceived vulnerability to infectious diseases
variables suggest that gender plays a role in young people only, where women presented higher
perceived infectability and germ aversion than men. Germ aversion increased with age in both men and
women; however, perceived infectability did not change with age in men, whilst in women, it decreased
up to the age of 50 to increase again from this point onward. Overall, the lowered effectiveness of the
biological immune system with age seems to be compensated by behavioral variables, mainly germ
aversion in men and women, and perceived infectability in women. Accordingly, this study represents
a contribution supporting the existence of a unique integrated compensatory biological/behavioral
immune system.

Author Contributions: Conceptualization: A.D., Á.B., and J.Z.; Methodology: A.D., Á.B., and J.Z.; Formal
Analyses: A.D. and Á.B.; Investigation: A.D., Á.B., and J.Z.: Supervision: A.D., Á.B., and J.Z; Writing—Original
Draft Preparation: A.D.; Writing—Review and Editing: A.D., Á.B., and J.Z. All authors have read and agreed to
the published version of the manuscript.
Funding: This research received no external funding.
Acknowledgments: The authors thank all of the participants in the study.
Conflicts of Interest: The authors declare no conflict of interest.

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