Documenti di Didattica
Documenti di Professioni
Documenti di Cultura
gender in epidemic-prone
infectious diseases
Addressing
sex and gender in
epidemic-prone
infectious diseases
Acknowledgements
WHO would like to thank Martha Anker for preparing this publication. Thanks
are also due to Roberta Andraghetti, Richard Anker, Pierre Formenty, Salma
Galal, Claudia Garcia-Moreno, Margaret Lamunu, Simon Mardel, Mike Nathan,
Guenael Rodier, Cathy Roth, Mike Ryan, Gail Thomson, Denise Werker, for
reviewing this document and providing valuable inputs.
This publication has been a joint effort of the Departments of Gender, Women
and Health, and Epidemic and Pandemic Alert and Response, WHO Geneva,
under the responsibility of Claudia Garcia-Moreno (GWH) and Cathy Roth (PAR).
Contents
1. Introduction
5
8
9
11
11
12
12
12
12
13
13
13
14
14
iii
14
15
15
16
16
17
17
17
18
18
19
22
23
23
23
3.2.1 Background
23
24
29
30
30
31
31
32
32
32
34
iv
18
34
37
1
Introduction
Particular attention has been paid to the interaction of communicable diseases and
pregnancy, where there may be special vulnerabilities, and restricted treatment
options, for both mother and foetus. The second is a detailed discussion and
analysis of selected examples of epidemic-prone infectious diseases (dengue,
Ebola haemorrhagic fever and severe acute respiratory syndrome (SARS)).
2
Definitions and key issues
the infectious disease process. Some diseases are particularly severe during
pregnancy, while others affect the unborn child. In addition, vaccines and other
pharmacological agents may have different effects on pregnant women than on
non-pregnant women, or harmful effects on the fetus or breastfed baby.
Examples of biological differences that influence who becomes ill and the course
and outcome of illness include:
differences in immune responses between males and females; and
anatomical differences particularly important for sexually transmitted
infections.
Examples of gender differences that affect who becomes ill and the course and
outcome of illness include differences in:
access to immunization;
exposures because of gender roles;
nutritional status;
access to, and use of preventive and curative health care, including differences
in the speed with which males and females get treatment outside the home.
In addition, the social and economic consequences of illness are often different
for males and females. For example, the disfigurement that results from some
infectious diseases (such as leprosy and onchocerciasis) affects marriage prospects
for females more severely than for males (Vlassoff & Bonilla, 1994; Vlassoff et al.,
2000). The level and types of stigma associated with some infectious diseases,
such as onchocerciasis and Ebola haemorrhagic fever, also differ for males and
females (Vlassoff et al., 2000; Hewlett & Amola, 2003).
Differences between males and females related to infectious diseases change
over the life-cycle. For this reason, the current paper uses a life-cycle approach with
separate sections for infants, children, adults, pregnant women and the elderly.
Infancy. Infants are particularly vulnerable to some infectious diseases (although
maternal antibodies have an important protective role for specific diseases).
Mortality rates for male infants are generally higher for than female infants.
Childhood. The biological differences between male and female children are
diverse and disease-specific. Gender-related factors vary from country to country.
Adulthood. As with children, differences between male and female adults are
diverse, vary from place to place, and are often disease-specific.
Pregnancy. Pregnancy induces many changes to the immune system, and
for some diseases, pregnancy is a risk factor for a more serious course and
outcome. In addition, the effects of infection of the mother, and/or preventive
measures taken or treatment given to the mother, on the fetus or breastfed child
are important considerations.
Old age. The elderly are also particularly vulnerable to infectious diseases. In
most societies this group has more women than men.
Table 1 presents typical similarities and differences between males and females
in disease incidence, course and outcome, and in health-seeking behaviour and
6
TABLE 1
Typical differences between males and females in the infectious disease process
WHO BECOMES ILL?
Life-cycle
Susceptibility
and immunity
Exposure
Treatment
Morbidity and
mortality
Infants
Males have
naturally weaker
immune systems.
Exposure is similar
for male and
female infants.
In some countries
boys are more
often taken for
treatment outside
the home.
Children
In some societies
there are mobility
differences (boys
spend more time
outside the home),
which may account
for differences in
incidence and
mortality for some
diseases.
In some countries
boys are more
often and/or more
quickly taken for
treatment outside
the home.
Adults
In some societies
women have poorer
access to health
care outside the
home; access to
outside care is controlled by males or
other family members. Research
on treatment often
uses males so
there is less evidence for results
for females.
Pregnant
and
lactating
women
Important changes
in the immune
system occur
during pregnancy.
Large knowledge
gaps exist about
the specific
changes.
Exposures to some
diseases may
change during
pregnancy.
Pregnant women
have more exposure to health care
settings, so may be
at greater risk for
some nosocomial
infections.
Some treatments
and control measures are harmful to
pregnant women or
to fetus or breastfeeding baby.
Pregnant women
are excluded from
research on treatment. Some treatments not given to
pregnant women
because of insufficient evidence of
their safety.
Coninued page 8
Table 1 continued
WHO BECOMES ILL?
Life-cycle
Susceptibility
and immunity
Exposure
Treatment
Morbidity and
mortality
The
elderly
Lack of evidence.
Diagnosis is more
difficult in the
elderly for both
males and females
due to atypical
presentations.
TABLE 2
INFANTS
YOUNG CHILDREN
(AGE 15 YEARS)
POSSIBLE REASONS
FOR MALE FEMALE
DIFFERENCES
SUGGESTED BY
INVESTIGATORS
Diarrhoeal disease
Incidence higher
for males
Acute lower
respiratory
infections and
pneumonia
Mortality rates
higher for males
Sex differences in
mortality for young
children vary.
Generally only small
differences in
incidence rates.
Neonatal tetanus
Mortality rates
higher for males
Measles
Dengue
Some evidence to
suggest that girls are
more likely to have
dengue shock
syndrome than boys.
Biological reasons,
related to a more
aggressive immune
system response have
been cited as possible
causes of more severe
illness in girls.
10
However, in south-central Asia, one of the areas where excess female mortality has
been consistently observed, evidence points to better immunization status for boys
than for girls (Population Division, 1998).
11
in childhood. A modest curative care advantage for male children was also found in
northern Africa, western Asia, and Latin America. In contrast, in most countries in
sub-Saharan Africa boys and girls received similar levels and types of curative care
(Population Division, 1998).
12
members in the home. For example, nurses as well as others who cared for the sick
have been heavily infected in several outbreaks of Ebola haemorrhagic fever, and
nurses were heavily infected during the SARS outbreak of 2003 (see section 3.2).
13
between males and females in the consequences of disabilities that arise from
infectious diseases.
14
For some epidemics that are spread nosocomially, pregnancy can be a period
of increased exposure because pregnant women have more contact than
usual with health care settings. For example, it has been found that SARS
(Zhang et al., 2003) and Ebola haemorrhagic fever have been transmitted in
obstetric care settings. In these settings, there may be a low level of suspicion
of the epidemic disease, because the women are coming for pregnancy-related
reasons. Furthermore, because infectious diseases sometimes have atypical
presentations during pregnancy, they may be more difficult to diagnose during
this time. If maternal care or obstetrical procedures are performed on infected
mothers without adequate infection control measures (which may be more likely
if the infectious disease is not diagnosed), this could increase the risk of the
disease spreading in the maternal care or obstetrical setting.
As all obstetric procedures carry a risk of infection, pregnant women are at an
increased risk of infection when undergoing them. Consequently infection control
needs to be a high priority of antenatal and obstetric care systems.
Some women change their activity pattern during pregnancy in ways that either
increase or decrease their risk of exposure to infections. For example, in some
societies women may have lighter workloads during pregnancy. Furthermore,
sexual activity patterns sometimes change during pregnancy, thereby changing
exposures to sexually transmitted infections.
15
For dengue, the effect of transmission of maternal antibodies is more complex. Dengue antibodies
protect the baby from infection with the same strain of dengue, but may be detrimental if the
infant is exposed to a different dengue strain.
16
The relationship of sex and gender with differences in infectious disease patterns
in the elderly are poorly understood and have been little studied (Liang et al. 2003).
This is surprising in view of the large sex differentials in mortality seen in the elderly,
and the high mortality rates at this time of life.
17
3
How sex and gender
affect outbreaks of specific
epidemic-prone diseases
This section focuses on the relationships between sex and gender and three
specific epidemic-prone diseases: dengue, Ebola haemorrhagic fever and SARS.
In addition to describing in more detail the role of specific sex and gender factors in
disease transmission, the implications of such factors for outbreak surveillance and
response are also presented.
All three of these diseases have caused outbreaks of public health importance
during recent years. The number of cases of dengue fever, which is a vector-borne
disease, has increased dramatically during the last decade, particularly in Asia and
South America. Ebola haemorrhagic fever was first identified in 1976 and occurs
only in Africa, whereas SARS was first identified in 2003, when it caused outbreaks
in Asia and North America. Both Ebola haemorrhagic fever and SARS are spread
directly from person to person.
18
19
infection rates in boys and girls. Furthermore, Halstead cited Ministry of Health data
for Bangkok for 19681977 showing greater numbers of deaths from dengue in
female children from 4 to 14 years of age. A large prospective study of 712 children
admitted with dengue to the Dong Nai Pediatric Center in southern Viet Nam from
June 1996 to June 1998, found significantly more females requiring treatment for
DSS than males (Phuong et al., 2004). However, a study of infants admitted to a
hospital in Ho Chi Minh City, Viet Nam found no differences in DSS between males
and females in this age group (Hung et al). Two explanations for the apparently
greater severity of dengue in female children have been proposed:
females may have increased immune responses (the more serious forms of
disease are associated with an immune response to cross-reactive yet nonneutralizing antibodies); or
female capillary systems may be more prone to permeability than those of
males and this may put them at great risk of DHF and DSS (Halsted, 1997).
More work to quantify and understand differences between symptoms and severity
in males and females is required.
Although the causes of possible male-female differences in severity and mortality
may be biological, a greater awareness of a potentially higher risk to girls could lead
to more girls being taken for treatment outside the home, or to girls being taken for
treatment outside the home sooner. This would be particularly important in areas
where gender norms such as son preference have created barriers to health care
outside the home for females.
Adults
Wide variations in symptoms of dengue between male and female adults have not
been suggested in the literature, although one study in Puerto Rico, which presented
combined results for children and adults, found that among serologically confirmed
cases, females reported body pain, joint pain and rash significantly more often than
males (Cobra et al., 1995). In addition, female patients with dengue commonly
experience vaginal bleeding, during both dengue fever and DHF/DSS (Gubler and
Kuno, 1997). There are a number of clinical reports of patients with dengue fever
experiencing severe vaginal bleeding during menstruation.
Severe menorrhagia has been described in women during dengue infections.
Individuals with open mucosal lesions, whether pathologic (peptic ulcer) or
physiologic (menstruation), who suffer dengue infections may bleed. Blood loss
may be catastrophic and life threatening (Halstead, 1997).
However, the level of risk of severe blood loss posed by dengue fever for menstruating as opposed to non-menstruating women has not been quantified (Gubler
D, personal communication, 2003). If there is an increased risk of severe blood
loss for menstruating women during dengue infections, this would be of potential
importance because of the large number of menstruating women in the population.
20
(At any point in time menstruating women make up approximately 15% of women of
childbearing age.)
The frequency of vaginal bleeding among female patients with dengue fever
or DHF/DSS is seldom reported because male and female symptom profiles
are combined and because vaginal bleeding is typically grouped with other
haemorrhages. For example, a clinical review of dengue in China reports severe
haemorrhage occurring in 5% of patients, and includes the uterus as one of the
common sites of bleeding but does not make specific reference to the proportion
of women who experienced severe bleeding of the uterus (Qui et al., 1993). The
importance of vaginal bleeding is also often masked by the tendency to list symptoms
in order of frequency among all patients. For example, in a study of dengue in Cuba
(Guzman, 1984a), vaginal bleeding was listed as a symptom that occurred in 23% of
patients (24/103), which made it appear much less frequent than the most common
symptom petechiae (which occurred in 39% of cases) and haematemesis (which
occurred in 30% of cases). If only female patients had been considered, vaginal
bleeding would have ranked as being of equal importance to petechiae, because
it occurred in 39% of female patients. Similarly, in China, uterine bleeding tied with
gum bleeding as the fourth most common haemorrhagic symptom affecting 17.5%
of patients. However, it was the second most prevalent symptom in females affecting
35% of female dengue patients (Qui et al., 1993).
The failure to study the symptom profiles of males and females separately is not
limited to dengue fever, but has also hampered the understanding of sex differences
in symptoms for other diseases (particularly diseases that affect males in greater
numbers than females). For example, because of the failure to look at male and
female symptom profiles separately, and because in the early days of the HIV/AIDS
epidemic most cases studied were among males, it took many years to recognize
that vaginal thrush is a typical opportunistic infection associated with HIV/AIDS in
females.
Inconsistent patterns of incidence rates of dengue fever in males and females
have been found. Some studies report similar incidence rates for males and females
(Thaung et al., 1975, Halstead, 1980), some have found higher incidence rates in
females (Kaplan et al., 1983; Guzman et al., 1984a; da Cunha et al., 1997), whereas
others have found higher incidence rates in males (Goh & Yamazaki, 1987; Ooi,
2001). When differences in incidence rates between males and females have been
found, they have often been attributed to differences in exposure. For example, the
authors of some studies which found higher rates of dengue infection among adult
females than adult males hypothesized that women have greater exposure to the
bites of dengue-infected mosquitoes because they spend more time during the
day (when the mosquitoes are most likely to bite) in the home (Kaplan et al., 1983:
Guzman et al., 1984). Ooi attributed the higher incidence rates in males to greater
exposure of males of working age outside the home.
21
22
families to bring females for treatment as well as males especially because females
are more likely to have severe disease and to die than males.
23
24
TABLE 3
CASES
CASE
FATALITY
RATE
(%)
FEMALE
CASES
(%)
CASES IN
HEALTH
CARE
WORKERS
(%)
Yambuku,
Zaire, 1976
318a
88
56
13 of 17
82
health
workers in
Yambuku
mission
hospital
Nzara and
Maridi area,
Sudan, 1976
284a
53
NAa
26 (34%
in Maridi;
3% in
Nzara)
NAb
Began in small
town of Nzara
among employees
of a cotton factory,
spread to city of
Maridi, amplified in
Maridi Hospital.
Nzara and
Maridi area,
Sudan, 1979
34a
65
62
5.9
NA
Same site as
previous outbreak.
61
47
NA
NA
Minkebe,
51
Ogooue-Ivindo
Province,
Gabon, 1994
NUMBER
COMMENTS
OF CASES
AMONG
PREGNANT
WOMEN
First recognition of
EHF.
Amplification by
contaminated
needles used for
vitamin injections to
pregnant women.
Rural area.
Kikwit area,
DRC, 1995
315a
81
53
25
15/105
cases in
Kikwit
General
Hospital
Index cases in
charcoal worker
and farmer.
Nosocomial spread
in Kikwit II Maternity
and in Kikwit
General Hospital.
Mayibout,
Gabon,
Spring 1996
31a
68
45
0.0
Booue,
Gabon,
Autumn 1996
60a
75
43
3.3
NA
Outbreak most
likely began with a
hunter in a logging
camp near Booue.
Continued
25
Table 3 continued
PLACE
AND YEAR
CASES
CASE
FATALITY
RATE
(%)
FEMALE
CASES
(%)
CASES IN
HEALTH
CARE
WORKERS
(%)
NUMBER
COMMENTS
OF CASES
AMONG
PREGNANT
WOMEN
53
63
7.3
NA
Amplification by
nosocomial spread
in hospitals, caring
for sick relatives and
traditional burial
practices.
Zadie district
Gabon and
Mbomo and
Kelle districts,
Congo,
October 2001
July 2002
124
79
50
1.6
NA
Olloba,
Congo, 2002
16
63
31
0.0
NA
Mbomo and
Kelle districts,
Congo,
JanuaryApril
2003
143
89
49
2.1
NA
Three independent
introductions linked
to hunting.
Congo
October
December
2003
35
83
54
NA
26
FIG 1
Four-week moving average of number of EHF cases by sex and week (n = 404),
Uganda, week 35, 2000 week 2, 2001
45
40
4 per moving average (female)
Number of cases
35
30
25
20
15
10
5
0
35 36 37
38 39
40 41 42
43 44
45 46 47
48 49
50 51 52
Week of onset
EHF, Ebola haemorrhagic fever.
Source: World Health Organization, Department of Communicable Disease Surveillance and Response,
unpublished data, 20002001.
to predominately female. If only the cumulative distribution had been plotted for the
outbreak in Gabon, the switch in incidence from an excess of male cases to an
excess of female cases would not have been seen until later in the outbreak when
the total number of females infected was greater than the total number of males
infected.
Figure 3 is a scatter plot of the proportion of female cases according to the size of
the outbreak. There is a general tendency for the larger outbreaks to include a larger
proportion of female cases, although the relationship is not strong and is statistically
significant only at the 10% level (P = 0.09). The female excess may be explained
by the fact that the transmission of the Ebola virus often occurs while caring for the
sick, a role that is more likely to be played by women than men.
Interestingly, the outbreaks in Sudan are notable exceptions. Although no
published data are available on the proportion of female cases in a relatively large
Table 3 sources continued
Pierre Formenty, personal communication for percentage of cases in females, Booue, Gabon, 1996; all
data for Olloba, Congo, 2002, and percentage of cases in females and percentage of cases in health care
workers, Congo, 2003.
Hwelett B, Amola R, 2003 for percentage of cases in females Gulu, Masindi and Mbarara districts, Uganda,
20002001.
Omaswa F et al., 2002 for percentage of cases in health care workers, Gulu, Masindi and Mbarara districts,
Uganda, 20002001.
Formenty P, Libama F, et al, 2003 for number of cases, percentage of cases in females, and percentage of
cases in health care workers, Zadie district, Gabon, and Mbomo and Kelle districts, Congo, 20012002.
Anonymous, 2003 for number of cases and case fatality rate, Congo, 0ctoberDecember 2003.
27
FIG 2
Four-week moving average of number of EHF cases by sex and week (n = 119),
Gabon Congo, week 43, 2001 week 11, 2002
9
8
Number of cases
7
6
5
4
3
2
4 per moving average (female)
1
0
43 44 45 46 47 48 49 50 51 52
10 11
Week of onset
EHF, Ebola haemorrhagic fever.
Source: World Health Organization, Department of Communicable Disease Surveillance and Response,
unpublished data, 20012002.
FIG 3
Scatter plot of the proportion of EHF cases among females to the toal
number of cases
80
70
60
50
40
30
20
10
0
0
10
28
outbreak that occurred in 1976, it has been reported that males predominated
because 75% of the medical staff in the main hospital was male (WHO International
Study Team, 1976). The 1979 outbreak in Nzara and Yambio, Sudan was also
unusual, in that despite its small size, a large proportion of those infected were
female (69%). Baron et al. suggested that the transmission of cases was almost
exclusively from providing nursing care for sick relatives; 24 of 29 secondary cases
had provided such care.
There is anecdotal evidence that the increased burden for females caring for
the sick has been well understood by some populations, and that females are
deliberately asked to care for the sick to protect males from becoming sick. For
example, during a recent outbreak in the Congo in October 2003, an international
investigator asked a group of men how they avoided contracting EHF, and they
responded that they made sure that women cared for the sick thus protecting
males from infection (P. Formenty, personal communication, 2003).
The preparation of bodies for burial has been found to play a role in the
transmission of EHF. In some societies this activity is heavily influenced by gender
norms. In Gulu, Uganda, for example, the paternal aunt of the deceased or another
female relative on the fathers side is responsible for washing the body of the
deceased, a practice that is likely to have contributed to the high proportion of
female cases in the 20002001 outbreak (Figure 1). Communal washing of hands
and touching the body of the deceased during burial traditional practices in which
both males and females participate also contributed to the transmission of EHF
during this particular outbreak.
There is no indication of differences between males and females in symptoms of
or mortality from Ebola, apart from the effects of Ebola during pregnancy, which are
discussed below. Because Ebola is a haemorrhagic disease, in which bleeding can
occur from all orifices, vaginal bleeding does occur. However, this does not appear
to be of particular clinical significance.
29
30
among elderly women. In Uganda, among the Acholi it is customary for the paternal
aunt or an older woman in the paternal line to prepare bodies for burial. In addition,
local customs call for either a survivor of disease or an elderly woman to care for the
sick during outbreaks of very severe disease (Hewlett & Amola, 2003).
3.2.6 The impact of EHF on the lives of male and female survivors
Because of the fear engendered by outbreaks of EHF, many survivors experience
difficulties in reintegrating into their families and the community after recovery. An
anthropological study in Gulu, Uganda revealed a wide range of problems of this
nature, which included not being able to return home and abandonment by a spouse
(for example, wives were told to return to their home villages). Stigmatization was
also frequently reported; some children were told not to touch survivors (Hewlett
& Amola, 2003). Females reported stigmatization somewhat more frequently than
males (although the sample size was small and the differences were not statistically
significant). This included being feared when they returned to the community, and
experiencing rejection in localities around the village such as markets, wells and
boreholes, and when walking through the neighbourhood.
Some of the survivors of the 20002001 outbreak in Gulu told investigators
that the resumption of sexual relations was problematic (M. Lamuru, personal
communication, 2003). Possible reasons for these problems include weakness
after the illness, and the fact that males were told to use condoms or to avoid sex
for a period after recovery because of the possibility of the virus still being present in
semen after recovery but they were not necessarily told for how long they should
continue to take such precautions.
31
The sex of 46 cases from China was not determined. These cases were not considered when
calculating the percentage of SARS cases that occurred in females.
32
21% (World Health Organization, 2003). Gender roles are such that health care
workers tend to be predominantly female, a factor that would have contributed to
higher infection rates for females than males in most countries.
Pregnancy and SARS
The SARS epidemic provides important insights into the extent to which the
surveillance and response system for serious new diseases takes sex and gender
considerations into account. During the SARS outbreak, pregnancy status was
generally ignored by the surveillance and response system, and pregnancy was
treated like any other concomitant condition. Thus, pregnancy status was not
systematically established and recorded in several of the countries with sizeable
numbers of SARS cases. Nor was pregnancy data included in line-listings of cases
provided to WHO. This has made it difficult to identify pregnant cases and hampered
our understanding of the clinical manifestations of pregnancies complicated by
SARS.
Partly because information on pregnancy status was not systematically collected,
there is very little information on the outcome of SARS infection during pregnancy
for the women or for the fetuses. However, other causes of pneumonia have been
associated with increased complications and hazards for the fetus, and greater
mortality during pregnancy (Dumont, 1989; Rodrigues & Niederman, 1992; Ie et
al., 2002), so one could reasonably also expect SARS to be associated with poor
outcomes.
To date, there are published reviews of the clinical course and outcome of SARScomplicated pregnancies from five cases in China (Zhang et al., 2003), 12 cases in
Hong Kong SAR (Shek et al., 2003; Wong et al., 2004; Lam 2004), two cases from
the USA (Robertson et al., 2004; Stockman et al., 2004) and one case from Canada
(Yudin et al., 2005). These reports provide an indication of the ranges of outcomes
that have occurred following pregnancies complicated by SARS. However, they
cover a total of only 20 cases.
Despite the small number of cases, there is some evidence from Hong Kong
SAR and China that SARS had a more severe course in pregnant women than in
non-pregnant women. In addition, mortality rates were greater in pregnant SARS
patients in Hong Kong SAR than non-pregnant female patients of childbearing age.
Furthermore, pregnant women who recovered from SARS, and remained pregnant,
faced psychological problems. Indeed in China, two pregnant SARS patients developed mental disorders attributed by the authors to the psychological stress of
being pregnant and contracting a new infectious disease whose potential effects on
the fetus are unknown.
The limited evidence available also raises concerns about the outcome of SARS
for the fetus. In Hong Kong SAR, there was a high incidence of spontaneous
abortion involving four of seven women presenting with SARS during their first
trimester, and a high incidence of pre-term delivery involving four of five patients
who presented after 24 weeks of gestation in Hong Kong SAR (Wong et al., 2004).
33
In addition two of the five infants born in Hong Kong SAR to mothers who had SARS
developed severe gastrointestinal complications. In China, one twin was lost from
a twin-pregnancy. There was one pre-term delivery at 31 weeks, and fetal distress
occurred in two deliveries (Zhang et al., 2003). In the USA and Canada, all mothers
delivered healthy babies with no apparent effect from the mothers having SARS
(Robertson 2004; Stockman 2004; Yudin et al., 2005).
There is no evidence of SARS transmission to health care staff during obstetrical
procedures, but it is highly unlikely that all pregnancies complicated by SARS
have been identified. Because the modes of transmission of SARS were not fully
understood, stringent infection control measures were used for deliveries following
pregnancies complicated by SARS and described in the literature on Hong Kong
SAR (Ng et al., 2003), China (Zhang et al., 2003) and on the USA (Robertson et al.,
2004). Descriptions of the infection control methods used during these deliveries
may become important should there be another outbreak of SARS, or an outbreak
of another new infectious disease with unknown routes of transmission.
34
2. Despite the scarcity of information, there are strong indications that sex and
gender are important for transmission and control of epidemic-prone diseases.
3. The ways in which sex and gender affect outbreaks of epidemic-prone diseases
are complex and disease-specific. For example, there are indications that
severity may be greater for female children with dengue, and for males with
SARS. Exposure to EHF is sometimes greater for male hunters at the onset of the
outbreak and for female caregivers later on.
4. There need to be changes in the information that is routinely collected during
outbreaks because information on sex, occupational status and pregnancy
status cannot easily be collected retrospectively. This is particularly important for
outbreaks of new diseases.
Some other general conclusions and suggestions are provided below to help improve
surveillance and control of outbreaks of epidemic-prone infectious diseases.
35
36
References
37
Chong K, Lin K (1989) [A preliminary report of the fetal effects of dengue infection in
pregnancy.] Kaohsiung Journal of Medical Sciences, 1:3134 [in Chinese].
Cobra C et al. (1995). Symptoms of dengue fever in relation to host immunologic response
and virus serotype, Puerto Rico, 19901991. American Journal of Epidemiology,
142:12041211.
da Cunha R et al. (1997). Dengue infection in Paracambi, State of Rio de Janeiro, 1990
1995. Revista da Sociedade Brasileira de Medicina Tropical, 30:379383.
Dumont M (1989). Influenza and pregnancy. Revue Francaise de Gynecologie et d
Obstetrique, 84:605607.
Formenty P, Libama F, Epelboin A et al Outbreak, of Ebola hemorrhagic fever in the
Republic of the Congo, 2003: a new strategy?, Med Trop (Mars). 2003;63(3):291295
Francesconi P et al. (2003). Ebola Hemorrhagic fever transmission and risk factors of
contacts, Uganda, Emerging Infectious Diseases, [serial online] 2003 Nov. Available
from: URL: http://www.cdc.gov/ncidod/EID/vol9no11/03-0339.htm .
Garca-Rivera EJ, Rigau-Prez JG (2003). Dengue severity in the elderly in Puerto Rico.
Pan American Journal of Public Health, 13:362368.
Garenne M (2003). Sex differences in health indicators among children in African DHS
surveys. Journal of Biosocial Science, 35:601614.
George A-J et al. (1999). Ebola hemorrhagic fever outbreaks in Gabon, 1994-1997:
Epidemiological and health control issues. Journal of Infectious Diseases, 179 (Suppl 1):
S6575.
Goh K, Yamazaki S (1987). Serological survey on dengue virus infection in Singapore.
Transactions of the Royal Society of Tropical Medicine and Hygiene, 81:687689.
Gubler D (2002). Epidemic dengue/dengue haemorrhagic fever as a public health, social
and economic problem in the 21st century. Trends in Microbiology, 10:100103.
Gubler D, Kuno G, eds (1997). Dengue and dengue hemorrhagic fever. London, CAB
International.
Gubler D (2002). Epidemic dengue/dengue haemorrhagic fevers as a public health,
social and economic problem in the 21st century. Trends in Microbiology, 10.
Guha-Sapir D, Schimmer B (2005). Dengue fever: New paradigms for a changing
epidemiology. Emerging Themes in Epidemiology, 2:1.
Guzman M, Kouri G (2002). Dengue: an update. Lancet Infectious Diseases, 2:3342.
Guzman M et al. (1984a). Dengue haemorrhagic fever in Cuba I. Serological confirmation
of clinical diagnosis. Transactions of the Royal Society of Tropical Medicine and Hygiene,
78:235238.
Guzman M et al. (1984b). Dengue haemorrhagic fever in Cuba II. Clinical investigations.
Transactions of the Royal Society of Tropical Medicine and Hygiene, 78:239241.
Hall A, Clemens J (2000). Adverse reactions to vaccines in the tropics. Tropical Medicine
and International Health, 5:229230.
Halstead SB (1997). Epidemiology. In: Gubler DJ, Kuno G, eds. Dengue and dengue
haemorrhagic fever. London, CAB International:3738.
Hewlett BS, Amola RP (2003). Cultural contexts of Ebola in Northern Uganda. Emerging
Infectious Diseases 9;(10):12421248.
Hung N et al. (2005). Association between sex, nutritional status, severity of dengue
hemorrhagic fever, and immune status in infants with dengue hemorrhagic fever,
American Journal of Tropical Medicine and Hygiene, 72:370374.
38
Ie S et al. (2002). Respiratory complications of pregnancy. Obstetrical and Gynaecological Survey, 57:3946.
Institute of Medicine, Committee on Understanding the Biology of Sex and Gender
Differences. (2001). Exploring the biological contributions to human health. Does sex
matter? National Academy Press, Washington, DC.
Kabra S et al. (1999). Dengue haemorrhagic fever in children in the 1996 Delhi epidemic.
Transactions of the Royal Society of Tropical Medicine and Hygiene, 93:294298.
Kaplan J et al. (1983). Epidemiologic investigations of dengue infection in Mexico, 1980.
American Journal of Epidemiology, 117:335343.
Khan A et al. (1999). The reemergence of Ebola hemorrhagic fever. Democratic Republic
of the Congo. Journal of Infectious Diseases, 179 (Suppl 1):S7686.
Lam CM et al. (2004). A case-controlled study comparing clinical course and outcomes
of pregnant and non-pregnant women with severe acute respiratory syndrome. British
Journal of Obstetrics & Gynaecology, 111:771774.
Liang J et al. (2003). Gender differences in old age mortality: Roles of health behavior
and baseline health status. Journal of Clinical Epidemiology, 56:572582.
Mitra A, Rahman M, Fuchs G (2000). Risk factors and gender differentials for death
among children hospitalized with diarrhoea in Bangladesh. Journal of Health Population
and Nutrition, Dec 18(3):151156
Mupapa K et al. (1999). Ebola hemorrhagic fever and pregnancy. Journal of Infectious
Diseases, 179(Suppl 1):S1112.
Nielsen N et al. (2002). Does cross-sex transmission increase the severity of polio
infection? Journal of Infectious Diseases, 34:273277.
Ng P et al. (2003). Infection control for SARS in a tertiary neonatal centre. Archives of
Disease in Childhood: Fetal and Neonatal Edition, 88(5):F405409
Omaswa F et al. (2002). An outbreak of Ebola in Uganda. Tropical Medicine and
International Health, 7:10681075.
Owolabi T, Kwolek S (2004). Managing obstetrical patients during severe acute
respiratory syndrome outbreak. Journal of Obstetrics and Gynaecology Canada, 26:35
41.
Ooi E (2001). Changing pattern of dengue transmission in Singapore. Dengue Bulletin,
25: 4044
Pandey A et al. (2002). Gender differences in healthcare-seeking during common
illnesses in a rural community of West Bengal, India. Journal of Health Population and
Nutrition, 20:306311.
Phuong C et al. (2004). Clinical diagnosis and assessment of severity of confirmed
dengue infections in Vietnamese children: Is the World Health Organization Classification
system helpful? American Journal of Tropical Medicine and Hygiene, 70:172179.
Population Division (1998). Too young to die. Genes or gender? New York, NY,
Department of Economic and Social Affairs, United Nations.
Qui F-X et al. (1993). Dengue in China: a clinical review, 1993. Bulletin of the World Health
Organization, 71:349359.
Rahman M et al. (2002). The first outbreak of dengue haemorrhagic fever, Bangladesh.
Emerging Infectious Diseases, 8 738740.
Rathgerber E, Manderson L, Vlassoff C (1993). Gender and tropical diseases: a new
research focus. Social Science and Medicine, 37:513520.
REFERENCES
39
Robertson C et al. (2004). SARS and pregnancy: a case report. Emerging Infectious
Diseases, 10 (2);345347.
Rodrigues J, Neiderman M (1992). Pneumonia complicating pregnancy. Clinics in Chest
Medicine, 13:679691.
Sheck C et al. (2003). Infants born to mothers with severe acute respiratory syndrome.
Pediatrics, 112:e254e256.
Shohat T et al. (2000). Gender differences in the reactogenicity of measles-mumpsrubella vaccine. Israel Medical Association Journal, 2:192195.
Stockman L et al. (2004). SARS during pregnancy, United States. Emerging Infectious
Diseases, 10 (9): 1689
Thaung U et al. (1975) Epidemiological features of dengue and chikungunya infections in
Burma. Southeast Asian Journal of Tropical medicine and Public Health, 6:276283.
UNICEF (2004). Integrated management of childhood illness. New York, NY, United
Nations Childrens Fund (http://www.childinfo.org, accessed 12 September 2004).
Vlassoff C, Bonilla E (1994). Gender-related differences in the impact of tropical diseases
on women: What do we know? Journal of Biosocial Science, 26:3753.
Vlassoff C, Garcia-Moreno C (2001). Placing gender at the centre of health programming:
challenges and limitations. Social Science and Medicine, 54: 17131723.
Vlassoff C et al. (2000). Gender and the stigma of onchocercal skin disease in Africa.
Social Science and Medicine, 50:13531368.
Whiteford L (1997). The ethnoecology of dengue fever. Medical Anthropology Quarterly,
11:202223.
Wong SF et al. (2004). Pregnancy and perinatal outcomes of women with severe acute
respiratory syndrome. American Journal of Obstetrics & Gynaecology, 191: 292297.
WHO International Study Team (1978). Ebola haemorrhagic fever in Sudan, 1976.
Report of a WHO/International Study Team, Bulletin of the World Health Organization
1978;56(2):24770
WHO International Commission, (1978). Ebola haemorrhagic fever in Zaire, 1976. Bulletin
of the World Health Organization, 56 (2):271293.
WHO SEARO (1999). Prevention and control of dengue and dengue haemorrhagic fever.
Comprehensive guidelines. New Delhi, World Health Organization Regional Office for
South-east Asia. WHO Regional Publication, No. 29.
WHO (2000). Fact Sheet No. 242. Geneva, World Health Organization.
WHO (2002). Future trends in veterinary public health. Report of a WHO study group.
Geneva, World Health Organization (WHO Technical Report Series, No. 907).
WHO (2003). Summary table of SARS by country 1 November 20027 August 2003
(http://www.who.int/entity/csr/sars/country/country2003_08_15.pdf, accessed Sept 23,
2003).
WHO (1998). Gender and health. Geneva, World Health Organization (document
WHD/1998/16) (http://www.who.int/reproductive-health/publications, accessed 9 September 2004).
Yudin M et al. (2005). Severe acute respiratory syndrome in pregnancy. Obstetrics &
Gynecology. 105:124127.
Zhang J et al. (2003). Clinical analysis of pregnancy in second and third trimesters complicated severe acute respiratory syndrome. Chinese Journal of Obstetrics & Gynaecology, 38:516520.
40