Journal of Infection and Public Health (2017) 10, 59—63

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Seroprevalence of sandfly virus

infection in military personnel

on the western border of

a,c,∗ b a

Ramin Shiraly , Afra Khosravi , Saman Farahangiz

a

Department of Community Medicine, Shiraz University of Medical Sciences, Shiraz, Iran

b

Department of Immunology, Ilam University of Medical Sciences, Ilam, Iran

c

Psychosocial Injuries Research Center, Ilam University of Medical Sciences, Ilam, Iran

Received 17 November 2015; received in revised form 22 January 2016; accepted 20 February 2016

KEYWORDS Summary Military troops deployed to endemic areas are at risk of contracting

Sandfly fever; sandfly fever, an arthropod-borne viral infection. Although typically a self-limited

Virus; disease, sandfly fever can cause significant morbidity and loss of function among

Past infection; soldiers. We conducted this study to determine the extent of past SFV infection in a

group of healthy Iranian military personnel in Ilam province on the western border of

Military personnel

Iran. A total of 201 serum samples were tested by indirect immunofluorescence assay

(IFA) to detect four common sandfly fever virus serotypes. Demographic data were

also collected. Overall, 37 samples (18.4%) were positive for specific IgG antibodies

to sandfly viruses. Sandfly fever Sicilian virus (SFSV) and sandfly fever Naples virus

(SFNV) were the most common serotypes. A positive test was inversely related to

nativity (P < 0.01) but was not associated with age (P = 0.163), duration of presence

in the border region (P = 0.08) or employment status (P = 0.179).

Our findings indicate that past SFV infection is common among military personnel

in the western border region of Iran, a Leishmania-endemic region. Therefore, it

should be considered in the differential diagnosis of troops presenting with acute

febrile illness in similar settings.

© 2016 King Saud Bin Abdulaziz University for Health Sciences. Published by Elsevier

Limited. All rights reserved.

∗

Corresponding author at: Department of Community Medicine, Shiraz University of Medical Sciences, Shiraz, Iran.

Tel.: +98 711 234 7977.

E-mail address: [email protected] (R. Shiraly).

http://dx.doi.org/10.1016/j.jiph.2016.02.014

1876-0341/© 2016 King Saud Bin Abdulaziz University for Health Sciences. Published by Elsevier Limited. All rights reserved.

60 R. Shiraly et al.

Introduction of sandfly fever in troops serving in the border

area during the autumn of 2013. The population of

Sandfly fever, also called phlebotomus fever, the study consisted of all military forces deployed

three-day fever or Pappataci fever, is an acute along the western border of Mehran, Ilam province.

mosquito-borne infection caused by Inclusion criteria included being a member of the

(family Bunyaviridae). The virus is transmitted armed forces (conscripted or staff) and having

to humans by the bite of infected female phle- been in the area for at least 1 year, including

botomine sandflies, which are also the vectors of a summer season (the period of intense sandfly

the protozoan parasite Leishmania [1]. Although activity). Voluntary informed consent was required

the genus comprises over 60 antigeni- for participation in the study. Demographic data

cally distinct serotypes, only eight serotypes are including age, place of birth, employment status

known to cause disease in humans. The four most and duration of presence in the border region were

common serotypes associated with human infec- collected and blood samples were taken by trained

tions include sandfly fever Sicilian virus (SFSV), technicians.

sandfly fever Naples virus (SFNV), sandfly fever Indirect fluorescent antibody test (IFA) was used

Cyprus virus (SFCV), and Toscana virus (TOSV) [2]. to detect specific immunoglobulin G (IgG) antibod-

Clinical disease usually presents as an acute ies to four common strains of the virus (SFSV, SFNV,

febrile illness that lasts 3 to 5 days, characterized SFCV and TOSV) in serum samples. Using the mosaic

by fever, myalgia and headache. In most cases, a IgG SFV kits enables us to recognize all 4 serotypes

disease follows a self-limiting course [3]. TOSV is of the virus. The laboratory kits were com-

the only serotype that has been associated with mercially available from EUROIMMUN, a German

acute meningitis and encephalitis [4]. company.

Sandfly fever virus (SFV) infections have been The test was conducted as follows: first, cells

reported from endemic regions of certain Mediter- infected with sandfly fever virus were incubated

ranean and Middle Eastern countries; Phleboviruses with the patient’s diluted sera. In the case of

appear to be responsible for many outbreaks of a positive reaction, specific IgG antibodies bind

febrile illness among susceptible groups in these to the antigens. Next, the antibodies attached to

areas [5—10]. As most native adults in endemic the antigens in the previous stage were stained

regions are immune, there are few reports of clin- by a fluorescein antibody (fluorescein-labeled anti-

ical cases among indigenous people [2]; therefore, human antibodies); they would be visible under a

many studies have focused on SFV infection in fluorescent microscope. According to the manufac-

high risk groups such as travelers to endemic areas turer’s instructions, a positive IFA test indicates

and armed forces [11—13]. The disease is of par- previous (past) or acute infection with SFV.

ticular importance to the military and was first Data were statistically analyzed using SPSS soft-

described during World War II when nonimmune sol- ware; descriptive statistics, t-test and chi square

diers entered Mediterranean regions [2,5]. test were performed.

Leishmaniasis is endemic in different parts of

Iran. Sandflies are vectors of both leishmaniasis and

sandfly fever viruses. Therefore, it is assumed that Results

SFVs are present in Leishmania-endemic areas of

the country. The only published study pertaining We visited all military posts along Mehran’s west-

to SFV infection in Iran was published more than ern border with . Approximately 220 military

35 years ago when Saidi et al. [14] assessed the personnel were eligible to participate in the study,

prevalence of SFV infection in Isfahan province, of which 201 agreed to take part. Overall, 58% of

a well-known endemic area of zoonotic cutaneous the troops were indigenous people living in Ilam

leishmaniasis in central Iran [14,15]. province. The mean age of participants was 24 years

The aim of this study was to assess the extent of (SD: 5.5) with a range from 19 to 46 years. Military

past SFV infection in a group of military personnel in personnel included 56 (27.9%) staff officers and 145

Mehran, a small city on the western border of Iran, (72.1%) conscripted soldiers. Deployment duration

which is also an endemic area of zoonotic cutaneous ranged from 12 to 156 months, with a mean of 18

leishmaniasis. months (SD: 21.1) (Table 1).

Among 201 samples tested, 37 (18.4%) sera were

Materials and methods found positive for phlebovirus-specific antibody by

indirect immunofluorescence assay. The most com-

This cross-sectional study was conducted in Ilam, mon serotype was SFSV (10.9%), followed by SFNV

a province of Iran, to assess the seroepidemiology (5%), SFCV (1.5%) and TOSV (1%) (Table 2).

Seroprevalence of sandfly fever virus infection in military personnel 61

residual sequelae, it may incapacitate a large

Table 1 Characteristics of military personnel who

number of troops and, in certain cases, require hos-

participated in the study.

pitalization [13]. Tests to diagnose sandfly fever are

Characteristic Value

not routine and efforts to diagnose the cause of

Male/female: n (%) 201/0 (100/0) acute undifferentiated febrile illnesses may result

Age (years): mean (SD) 24 (5.5)

in further unnecessary workup and increased costs.

Staff/conscripted soldiers: n (%) 56/145 (28/72)

As leishmaniasis is a highly focal disease and its

Duration of deployment (months): 18.1 (21.1)

distribution depends on sandfly habitat [21], it is

mean (SD)

expected that SFVs also have a focal geographic

Native/non-native: n (%) 24/177 (12/88)

distribution that parallels leishmaniasis.

The only previous study investigating sandfly

virus infection in Iran was conducted in northeast-

A positive test was inversely related to nativ-

ern Isfahan, an area endemic to zoonotic cutaneous

ity (P < 0.01), but was not associated with age

leishmaniasis (ZCL). In this study, antibodies to

(P = 0.163), duration of presence in the border

SFSV and SFNV were found in 25% and 17% of the

region (P = 0.08) or employment status (P = 0.179)

rural population living in the area, respectively.

(Table 3).

The viruses were also isolated from sandflies (pre-

dominantly Phlebotomus papatasi) and gerbils in

this endemic region in central Iran [14]. Zoonotic

Discussion cutaneous leishmaniasis (ZCL) accounts for 80% of

reported cases of leishmaniasis in Iran and there are

Arboviral infections remain a major health problem endemic foci of the disease, especially in the cen-

for troops deployed to endemic foci in the Middle tral, western and southwestern parts of the country

East and Mediterranean basin [16]. Acute febrile [19,22].

illness associated with SFVs has been reported The results of the present study and the study

among Western military forces in Middle Eastern by Saidi et al. [14] suggest that SFSV and SFNV are

countries affected by war, such as Afghanistan and probably present in rural areas of central and west-

Iraq [12,13]. Outbreaks of undiagnosed febrile ill- ern Iran where ZCL is endemic. Saidi et al. [14]

nesses among military forces can be a challenging also identified some other phlebovirus serotypes

health issue as it may elicit anxious reactions in (e.g., Salehabad & Karimabad) that have not been

soldiers and necessitate a thorough investigation described as human pathogenic strains [17]. How-

into the causes of disease. Although sandfly fever ever, significant doubt remains over the presence

is not usually associated with a fatal outcome or of TOSV and SFCV in Iran, as TOSV has never been

Table 2 Summary of IFA test results for serotype-specific IgG antibodies to four common sandfly fever viruses.

Total number Positive Positive Positive Positive Negative

of samples results for results for results for results for results

SFSV SFNV SFCV TOSV

201 22 (10.9%) 10 (5%) 3 (1.5%) 2 (1%) 164 (81.6%)

Table 3 Demographic and IFA test characteristics of 201 military personnel participants.

Characteristic Positive Negative All P value

Age, years: mean (SD) 23 (4.6) 24.2 (4.7) 24 (5.5) 0.163

Deployment duration, months: mean (SD) 14 (13) 18.9 (16) 18.1 (21.1) 0.08

Nativity [n (%)]

*

Native 0 (0) 24 (100) 24 (100) <0.01

Non-native 37 (20.9) 140 (79.1) 177 (100)

Employment status [n (%)]

Conscripted soldiers 30 (20.7) 115 (79.3) 145 (100) 0.179

Army staff 7 (12.5) 49 (87.5) 56 (100)

*

Statistically significant.

62 R. Shiraly et al.

isolated from P. papatasi, the predominant phle- Funding

botomus species in the country [6]. In the present

study, TOSV and SFCV were detected IFA test in only No.

a few cases; this may be due to cross-reactivity

between viral serotypes [6,18].

Mehran is a small city on the western border

Competing interests

of Iran. Due to its strategic location, there are

many military posts along the border with Iraq. This

None declared.

region has a warm climate with hot, dry summers —

an ideal environment for sandflies to breed — and is

endemic to ZCL [19,22]. The results of the present

Ethical approval

study suggest that exposure to sandfly fever viruses

can be a possible cause of acute febrile episodes

Not required.

among military personnel in ZCL-endemic areas in

Iran. Phlebovirus infection can produce a very mild

or subclinical infection and many patients do not

seek medical attention, so the study of healthy indi- Acknowledgments

viduals may better reflect the actual prevalence of

We gratefully acknowledge the support given to our

the infection.

effort by the Vice Chancellor for Research and Tech-

A noteworthy limitation of the study is that

nology, Ilam University of Medical Sciences.

we only investigated specific IgG antibodies; this

merely indicates past exposure to the virus and is

not necessarily associated with current or recent

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