Geographic distribution and spatial analysis of Leishmania ... · The domestic and wild dogs are...
Transcript of Geographic distribution and spatial analysis of Leishmania ... · The domestic and wild dogs are...
INTRODUCTION
Leishmaniasis, one of the most important parasitic disease transmitted by Phlebotominae vectors is wide-spread, and has different epidemiological and clinical fea-tures. The disease is endemic in more than 98 countries on four continents, and an estimated 700,000 to 1 million new cases and 20,000 to 30,000 deaths occur annually across the world1–2. Visceral leishmaniasis (VL) is one of the most important clinical form of leishmaniasis in humans as well as canines2. The causal agent of the disease belongs to the group of Leishmania donovani complex (Order Ki-netoplastida), which is transmitted by different species of female sandflies2–5. The disease can be fatal if left untreat-ed, and even with the availability of treatment, the mor-tality rate reported6 varies from 10 to 20%. Leishmania infantum is the main causative agent of VL in humans and dogs in Mediterranean region2. Recently, L. tropica and
L. major have been reported in some cases, as principal agents of VL in human8–10 and domestic dogs11–12. Visceral leishmaniasis is endemic in several parts of Iran includ-ing Ardabil, East Azerbayjan, Fars, Bushehr, Kerman and Qom and North Khorasan provinces12–13. Though, it has been reported to exist in sporadic form in other areas of Iran14–15. The domestic and wild dogs are the most impor-tant reservoirs for VL in Iran12–16. Domestic dogs and wild canines such as foxes, jackals and wolves are infected with L. infantum, which seem to play an important role in the wild cycle of the disease in mountainous areas14–17.
Determining the prevalence of canine VL (CVL) in endemic areas is necessary for controlling zoonotic vis-ceral leishmaniasis (ZVL)17–18. The prevalence of L. in-fantum infection varies from 2.6 to 26.6% in different parts of the world17. The clinical symptoms of CVL vary from asymptomatic forms to restricted and deadly infec-tion16, 18. Moreover, the incubation period lasts from sev-
J Vector Borne Dis 55, September 2018, pp. 173–183
Review Article
Geographic distribution and spatial analysis of Leishmania infantum infection in domestic and wild animal reservoir hosts of zoonotic visceral leishmaniasis in Iran: A systematic review
M. Mohebali1–2, E. Moradi-Asl3 & Y. Rassi4
1Department of Medical Parasitology and Mycology, School of Public Health, 2Center for Research of Endemic Parasites of Iran, Tehran University of Medical Sciences, Tehran; 3Department of Public Health, School of Public Health, Ardabil University of Medical Sciences, Ardabil; 4Department of Medical Entomology, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran
ABSTRACT
Visceral leishmaniasis (VL) is an important parasitic disease which is endemic in different parts of Iran; and domestic and wild canines are principal reservoir hosts of the disease. The objective of this study was to review the spatial distribution of canine VL (CVL) caused by Leishmania infantum in domestic and wild canines in different geographical areas of Iran. An extensive literature search was conducted in different international and national databases, including Cochrane, MEDLINE/PubMed, Scopus, Web of Science and Iran Medex to find articles with the words “visceral leishmaniasis in Iran” in their titles and “canine visceral leishmaniasis in Iran” or “feline visceral leishmaniasis in Iran” or “accidental reservoir hosts of visceral leishmaniasis in Iran” in their subtitles, irrespective of the type and duration of study. Screening of the irrelevant articles from total 36,342, yielded 61 eligible articles. More than 93% of the studies were carried out on domestic dogs (Canis familiaris, n = 57) and the remaining were on other carnivores such as wild canines including foxes (Vulpes vulpes, n = 4), jackals (C. aureus, n = 6) and wolves (C. lupus, n = 6); while studies on domestic cats (Felis catus, n = 3) as well as desert rodents (n = 2) were rare. The average rate of L. infantum infections reported among domestic dogs using direct agglutination test (DAT) in Iran was 12.5%. The highest prevalence rate (14%) was reported from the northwest regions of the country where VL is endemic. The review indicates that CVL is endemic in various parts of Iran and domestic dogs are the main and potential reservoir hosts of the disease. Other carnivores, such as domestic cats and some species of desert rodents (Cricetulus migratorius, Mesocricetus auratus and Meriones persicus) seem to be playing a role in the maintenance of transmission cycle of L. infantum in the endemic areas of the disease.
Key words Domestic canines; Iran; reservoirs; visceral leishmaniasis
[Downloaded free from http://www.jvbd.org on Friday, January 4, 2019, IP: 5.122.114.141]
J Vector Borne Dis 55, September 2018174
eral months to several years, depending on the virulence of the parasite and host genetic characteristics19. Differ-ent serological and molecular methods are used to detect L. infantum in humans and reservoirs19–20. The easiest and most cost-effective detection method in this regard is direct agglutination test (DAT) which has high sensi-tivity and specificity and is widely used in developing countries19–20. Domestic dogs are most important reser-voirs of the disease, which might not show any symp-toms for a long time and relative resistance to antileish-manial treatments can easily distribute VL in different regions17, 20–21.
Therefore, one of the best ways of preventing infec-tion to humans is rapid identification and control of the reservoir population, including infected domestic dogs and wild canines17. Hence, determining the disease status in animal reservoirs and their control can play a significant role in preventing VL spread to humans19, 22. Given the plethora of studies conducted on domestic and wildlife reservoirs in different areas of Iran, it is necessary to es-timate the prevalence of L. infantum infections in differ-ent reservoirs in endemic and non-endemic areas of Iran. This study was an attempt to review the earlier studies of VL caused by L. infantum carried out on animal reservoir hosts using different methods in Iran.
Study designThis study systematically searched all the earlier pub-
lished studies, reports and documentations related to VL that used parasitological (microscopy and culture), sero-logical (DAT) and molecular methods for its identifica-tion/diagnosis. International databases such as Cochrane, MEDLINE/PubMed, Google Scholar, Science Direct, Scopus, Web of Science, Veterinary information net-work, VetMed Resource, Zoological Records, Biological Abstracts, CAB Abstracts as well Iran’s databases (for Persian articles) including Iran Medex, Scientific Infor-mation Database (SID ) and Magiran were searched with no time limitation. The results were qualitatively summa-rized in order to find out any precise information relating to the purpose of the study.
Quality assessment and data extractionInitially, all the article titles were entered into a ref-
erence manager software, namely End Note. After dele-tion of the duplicate cases, they were assorted for initial screening. In the first stage, these article titles were re-viewed. Afterward, all the articles that were irrelevant to the objectives of the study were removed from the prima-ry databank. Next, two persons scrutinized the titles and abstracts; and the articles that were selected by both the
Fig. 1: Flow chart demonstrating database search, screening and selection of studies.
persons were finalized for subsequent analysis (Fig. 1).
Search methodologyThe following words and phrases were used in or-
der to search the articles: “visceral leishmaniasis in Iran” in the titles and “canine visceral leishmaniasis in Iran” or “feline visceral leishmaniasis” or “acciden-tal reservoir hosts of visceral leishmaniasis in Iran” in subtitles. Other key words included visceral leishmani-asis, kala-azar, canine visceral leishmaniasis, leishmani-asis in domestic and wild canine, leishmaniasis in dogs, foxes, wolves, jackals, and rodents, L. infantum in dogs and canines.
Analyzed methods All the studies were in the form of a M.Sc., or Ph.D.
theses and research projects, whose results had been pub-lished as research articles in prestigious journals. All of the compiled articles in this review study had met the rules of publishing a scientific article in the journals. The exclu-sion criteria consisted of the absence of the issue number and approval letter by the university. Data were summa-rized based on individual provinces, endemic and non-endemic areas, as well as two groups of wild and domestic reservoirs. The prevalence of the CVL disease, based on the years and different regions at the provincial level, was developed using the Arc GIS 10.4.1 software, and dis-tribution maps were generated based on the type of res-ervoirs (Fig. 2). SPSS ver. 23 and quantitative statistical
[Downloaded free from http://www.jvbd.org on Friday, January 4, 2019, IP: 5.122.114.141]
175Mohebali et al: Distribution and spatial analysis of L. infantum infection in Iran
Fig. 3: Frequency of studies carried out on CVL in Iran (1982–2017).
Fig. 2: Distribution and prevalence rate of CVL in provinces of Iran (1982–2017).
tests, such as chi-square analysis and correlation analysis were used in order to investigate the status of CVL among different reservoirs as well as the relationship between age and gender. Moreover, all the diagnostic methods (molec-ular, serological and parasitological) were used in order to analyze the infection of the reservoirs.
Out of all the databases searched from 1982 to 2017, only 61 articles/studies were found eligible for inclusion in this systematic review. These studies were carried out in 20 of the 31 provinces, and >38% of them were conducted in northwest of Iran (Ardabil province). The highest num-ber of studies, i.e. 10 and 9 were conducted in 2011 and 2013, respectively (Fig. 3). The first study was conducted in 1982 in Mazandaran province (non-endemic area of VL) and the latest study was reported from Kerman prov-ince (endemic area) in 2017 (Table 1).
In these studies, a total of 24,884 animals were exam-ined, of which 94.23% were the owned pets and stray dogs and the remainders were other wild animals. Of all the dogs investigated, 90% were pets and sheep dogs and 10% of those were stray dogs. The infection rate with Leishma-nia parasites was 14.18% in the domestic dogs and 6.35% in wild canines (Table 2).
In total, 1434 cases of wildlife as reservoir hosts for VL have been investigated, in which the highest number of examined animals were rodents (48%) and the low-est were wolves (~3%) (Fig. 4). Analysis of L. infantum infection frequency in dogs according to different re-gions of the country shows that it was distributed mainly in 20 provinces of Iran, viz. Alborz, Ardabil, Bushehr, East Azarbaijan, Razavi Khorasan, Chaharmahal and Fig. 4: The percentage share of wildlife reservoirs in terms of CVL
in Iran (1982–2017).
Fig. 5: Geographical distribution of L. infantum infections in dogs, Iran 1982–2017.
Bakhtiari, Isfahan, Fars, Qom, Golestan, Hamadan, Ker-man, Khuzestan, Kohgiluyeh and Boyer-Ahmad, Lores-tan, Mazandaran, North Khorasan, Semnan, Sistan and Baluchestan and Tehran (Fig. 5).
Infection with L. infantum in domestic cats (by DAT method) was reported from three provinces of Iran,
[Downloaded free from http://www.jvbd.org on Friday, January 4, 2019, IP: 5.122.114.141]
J Vector Borne Dis 55, September 2018176 Ta
ble
1. T
he st
udie
s con
duct
ed o
n V
L ca
used
by
L. in
fant
um in
Iran
(198
2–20
17)
Aut
hors
Prov
ince
Year
Tota
l an
imal
s in
clud
ed
No.
of
posi
tive
case
s
Sero
logi
cal m
etho
ds p
erfo
rmed
(%)
Para
sito
logi
cal
met
hod
perf
orm
ed
(%)
IFA
DAT
PCR
ELIS
A
Ham
idi e
t al22
M
azan
dara
n19
8234
617
.60
NP*
NP*
NP
NP
Bok
ai e
t al23
A
rdab
il19
9330
345
14.8
214
.82
NP
NP
NP
Moh
ebal
i et a
l24
Ard
abil,
Bus
hehr
2001
613
41N
P 6
.76
NP
NP
1.95
Gav
gani
et a
l21
Ard
abil
2002
199
43N
P21
.65
NP
NP
6Sa
degh
i and
Ars
hi25
Ard
abil
2003
458
34N
P 7
.48
NP
NP
NP
Moh
ebal
i et a
l26A
rdab
il20
0426
810
6N
P39
.55
NP
NP
NP
Moh
ebal
i et a
l27A
rdab
il20
0430
323
NP
7.6
NP
6.93
NP
Fakh
ar e
t al28
Qom
2004
328
NP
25N
PN
PN
PM
osal
lane
jad
et a
l29Se
mna
n20
0412
06
NP
4.1
7N
PN
PN
PM
oheb
ali e
t al17
Nor
thw
est,
Sout
hwes
t, C
entra
l20
0515
6822
2N
P14
.22
NP
NP
4.50
Mah
ami e
t al30
Ard
abil
2006
223
NP
13.7
2N
PN
P4.
56Ze
bard
ast
et a
l31C
haha
rmah
al-v
a-B
akht
iari
2005
492
NP
4N
P4
NP
Fakh
ar e
t al32
Fars
2006
196
NP
26.3
331
.57
NP
NP
Moh
ebal
i et a
l20N
orth
east
, Nor
thw
est,
Sout
h, C
entra
l20
0613
8315
2N
P11
NP
NP
NP
Aviz
eh e
t al33
Khu
zest
an20
0721
029
NP
13.8
NP
NP
NP
Ras
si e
t al34
Fars
2007
206
NP
NP
30N
PN
PTa
ran
et a
l35A
rdab
il20
0712
655
NP
43.6
NP
NP
NP
Farz
am e
t al36
Fars
2008
431
33N
P 7
.62
NP
NP
NP
Mos
hfe
et a
l37A
rdab
il20
0838
467
NP
17.4
5N
PN
P0.
52K
hanm
oham
mad
i et a
l38Ea
st A
zerb
aija
n20
0815
14
2.66
NP
NP
2.66
NP
Mos
hfe
et a
l39A
rdab
il20
0966
16N
P24
.22
33.3
3N
P10
.60
Kha
nmoh
amm
adi e
t al40
East
Aze
rbai
jan
2010
102
10N
PN
P10
NP
Sala
hi-M
ogha
ddam
et a
l41A
rdab
il20
1038
435
NP
9.1
1N
PN
PN
PFa
khar
et a
l42M
azan
dara
n20
1149
17N
P34
.63
4.1
NP
NP
Falla
h et
al43
East
Aze
rbai
jan
2011
384
35N
PN
P11
.81
9.15
NP
Falla
h et
al44
East
Aze
rbai
jan
2011
120
23N
P19
NP
NP
16.6
6Fa
llah
and
Kha
nmoh
amm
adi45
East
Aze
rbai
jan
2011
521
1.92
NP
1.92
2.12
1.92
Shar
ifdin
i et a
l46A
rdab
il20
1117
127
NP
15.8
0N
PN
PN
PM
oham
mad
i-Gha
lehb
in e
t al47
Ard
abil
2011
607
NP
NP
NP
11.6
NP
Ans
ari e
t al48
Koh
gilu
yeh
and
Boy
er-A
hmad
2011
1514
NP
93.3
793
.37
NP
73.3
3 (con
td...
)
[Downloaded free from http://www.jvbd.org on Friday, January 4, 2019, IP: 5.122.114.141]
177
Aut
hors
Prov
ince
Year
Tota
l an
imal
s in
clud
ed
No.
of
posi
tive
case
s
Sero
logi
cal m
etho
ds p
erfo
rmed
(%)
Para
sito
logi
cal
met
hod
perf
orm
ed
(%)
IFA
DAT
PCR
ELIS
A
Mah
mou
dvan
d et
al49
Ker
man
2011
307
NP
23.3
3N
PN
P16
.67
Moh
ebal
i et a
l16N
orth
east
and
Wes
t, So
uth,
Sou
thea
st
2011
2559
212
NP
8.3
8N
PN
P1.
32Fa
khar
et a
l50Fa
rs20
1211
025
NP
5.5
22.7
0N
PN
PH
osse
inin
ejad
et a
l51C
haha
rmah
al-v
a-B
akht
iari
Khu
zest
an, T
ehra
n20
1254
853
NP
9.6
6N
PN
PN
PR
azza
ghi e
t al52
Isfa
han
2012
184
20N
P10
.82
NP
NP
NP
Afla
toon
ian
et a
l53K
erm
an20
1212
89
NP
NP
NP
7.03
NP
Moh
amm
adih
a et
al54
Ard
abil
2012
168
125
NP
7970
NP
0M
oshf
e et
al55
Koh
gilu
yeh
and
Boy
er-A
hmad
2012
170
17N
P10
NP
NP
NP
Hei
darp
our e
t al56
Raz
avi K
hora
san
2012
300
268.
66N
PN
PN
PN
PH
adda
dzad
e et
al57
Alb
orz
2013
337
12N
P 3
.6N
PN
PN
PM
oheb
ali e
t al13
Nor
thea
st a
nd W
est,
Sout
hwes
t, C
entra
l20
1372
0487
9N
P12
.2N
PN
P1.
02H
ajja
ran
et a
l58A
rdab
il,Te
hran
, Nor
th K
hora
san
2013
8056
NP
7058
/75
NP
68/7
5A
dine
zade
h et
al59
Raz
avi p
rovi
nce
2013
100
8N
P 8
NP
NP
NP
Sabz
evar
i et a
l60R
azav
i pro
vinc
e20
1320
916
7.6
NP
NP
NP
NP
Shab
esta
ri et
al61
Ard
abil
2013
100
45N
P45
NP
25N
PM
alm
asi e
t al62
Tehr
an, A
lbor
z20
1460
230
NP
4.9
8N
PN
PN
PM
osta
favi
et a
l63K
erm
an, S
ista
n-B
aluc
hest
an20
1420
131
NP
NP
NP
15.4
NP
Fakh
ar e
t al64
Gol
esta
n20
1450
16N
P32
30N
PN
PG
hare
khan
i et a
l65H
amad
an20
1438
015
NP
NP
NP
3.9
NP
Fato
llahz
adeh
et a
l66Ea
st A
zerb
aija
n20
1465
15N
P23
NP
NP
NP
Nam
rood
i et a
l67M
azan
dara
n20
1460
5N
PN
PN
P8.
33N
PB
amor
ovat
et a
l68K
erm
an20
1480
9N
P12
.25
1.25
NP
NP
Bam
orov
at e
t al69
Ker
man
2015
471
2N
PN
P0.
42N
PN
PFa
rahm
and
et a
l70A
rdab
il20
1535
091
NP
26.9
NP
49.7
NP
Gha
ffarin
ejad
et a
l71A
rdab
il20
1520
049
NP
24.5
NP
NP
NP
Bar
ati e
t al72
Ard
abil
2015
508
119
NP
23.4
NP
NP
NP
Ara
inne
jad
et a
l73R
azav
i pro
vinc
e20
1660
4N
PN
P6.
67N
PN
PM
olae
i et a
l74A
rdab
il20
1611
036
NP
NP
32.7
2N
P17
.27
Jalil
nava
z et
al75
A
rdab
il20
1611
820
NP
15.8
NP
NP
NP
Moh
ebal
i et a
l15N
orth
Kho
rasa
n20
1684
11N
P13
NP
NP
NP
Akh
tard
anes
h et
al76
Ker
man
2017
6010
NP
NP
16.7
06.
70N
PN
P—N
ot p
erfo
rmed
.
Tabl
e 1.
(con
td...
)Mohebali et al: Distribution and spatial analysis of L. infantum infection in Iran
[Downloaded free from http://www.jvbd.org on Friday, January 4, 2019, IP: 5.122.114.141]
J Vector Borne Dis 55, September 2018178
namely Ardabil, East Azarbaijan, and Kerman, with the infection rates of 24.27, 23 and 6.70%, respectively66, 76, 91. Fox infection was reported from four provinces of Iran—North Khorasan, Ardabil, East Azerbaijan and Bush-ehr. The mean infection rate reported (using serological and parasitological methods) was 20.5, 10.71, 5.2 and 15.55%, respectively in these provinces (Fig. 6). The infection in jackals (identified via serological methods) was reported from six provinces namely, East Azerbaijan (20%), Ardabil (23%), Mazandaran (5.5%), North Kho-rasan (11.66%), Chahar Mahal and Bakhtiari (5.26%) and Bushehr (15%). The infection rate was 7.70% in Ardabil province using parasitological method. Infection with L. infantum in rodents was only reported from northwest of Iran (Ardabil and East Azerbaijan provinces) (Fig. 5). Among the five species of rodents investigated, infection share/frequency was highest for Meriones persicus (69%) and lowest for Mesocricetus auratus (0.5%). The infec-tion rate reported for Meriones persicus by using parasi-tological methods was 14.7%, for Cricetulus migratorius it was 7.2%, and for Mesocricetus auratus it was 75%; while no reports were observed for Mus musculus and Rattus norvegicus.
Of the all domestic and wild reservoirs that were studied, L. infantum parasite was reported in 12.33% hosts using the molecular, serological and parasitological methods. The major diagnostic methods used in these studies included DAT (12.5%), ELISA (6.1%), PCR (1.7%), DIPESTIC rK39 (0.8%), IFA (0.1%) and parasi-tology (0.5 %).
The infection rate of L. infantum in different res-ervoirs examined by serological and parasitological methods was 23% for cats, 12.52% for domestic dogs, 11.33% for rodents, 10.2% for wolves, 9.9% for foxes and 6.36% for jackals. Other than L. infantum parasite, L. tropica and L. donovani were also isolated from the reservoirs. Leishmania tropica has been isolated from
dogs in the northwest, center, and northeast of Iran; from the jackals in northeastern Iran, and from foxes and wolves in northwest of Iran while L. donovani has been only reported in desert rodents in northwestern of Iran by using both serological and parasitological methods.
Among endemic areas, the highest infection rate was reported from the Ardabil province (24%) and the low-est infection rate was reported from Bushehr province (9%), using all diagnostic methods. In non-endemic ar-eas, the highest and lowest infection rates were report-ed from Golestan (32%) and Hamadan (4%) provinces, respectively. According to the included studies, the in-fection rate in CVL reservoirs varied from 6 to 24% in endemic areas and from 4 to 32% in non-endemic areas of Iran.
Each year, >20,000 to 30,000 human deaths occur from VL in the world7. The dogs and wild canines consti-tute the most important reservoirs for L. infantum in the old and new worlds14, 17, 37. Determining the prevalence and rate of infection in different reservoirs can help in controlling ZVL18. Various studies have shown that in the past decade, L. infantum was the most predominant Leish-mania species for both VL and CVL in different parts of Iran14, 24. It has been reported that dogs and wild canines in-cluding jackals, foxes and wolves are frequently infected with L. infantum in Iran13, 17, 20, 77.
Over the past 35 yr, about 61 studies have been car-ried out on domestic and wildlife reservoirs in different regions of Iran, especially endemic areas, all those point to the indispensable role of reservoirs in epidemiological as-pects of VL. The first study in non-endemic areas of Iran was conducted in 1982 in Mazandaran province22 where the reported infection rate was 3%, while the most recent one was conducted in Sistan and Baluchestan province in 2014, with the reported infection rate of 15.4%, indicat-ing the variability of the infection rate in different parts of the country.
Among the endemic regions of Iran, the first study was conducted in 1993 in Ardabil province23, where the infection rate was 14.8% by serological method. The most recent study was conducted in 2016, in the same province, and infection rate in dogs was found to be 32.6%, which represents an increase of reservoirs in this province74. The comparison of the results of the infection prevalence in reservoirs, in both endemic and non-endemic regions shows that the percentage of reservoir infection is high in both the regions. Findings pertaining to the prevalence of VL in humans also show that >50% of human cases occur in the endemic areas of the northwest of Iran, which is consistent with the prevalence of reservoirs infection in
Table 2. Prevalence of VL infections caused by L. infantum in different animal reservoir hosts in Iran (1982–2017)
%No. of positive
cases
Total examined
cases
Animal hosts
12.52293723450Domestic dog ( Canis familiaris) 9.913131Foxes (Vulpes vulpes) 6.3622346Jackals (Canis aureus)10.2549Wolves (Canis lupus)19.2944228Domestic cats (Felis catus)11.3277680Desert rodents (Cricetulus
migratorius, Mesocricetus auratus and Meriones persicus)
12.45309824884Total
[Downloaded free from http://www.jvbd.org on Friday, January 4, 2019, IP: 5.122.114.141]
179
Fig. 6: Distribution of L. infantum infections among the studied animals, Iran 1982–2017—(a) Fox; (b) Cats; (c) Rodents; and (d) Jackals.
Mohebali et al: Distribution and spatial analysis of L. infantum infection in Iran
(a) (c)
(b) (d)
northwest of Iran13–14, 78–80.The prevalence rate of CVL in Iran is higher in en-
demic areas than in non-endemic ones and varies from 4–32%. In northeastern Brazil81, the infection rate of CVL was reported to be 3.95–5.31% in 2014; and in north Spain it was reported to be 28% by PCR method6. Among vari-ous reservoirs in Iran, domestic dogs and jackals showed the highest rate of infection with L. infantum implying that dogs and jackals are respectively their main domestic and wild reservoir in Iran. Leishmania infantum was isolated from Cricetulus migratorius and Mesocricetus auratus, Two species of parasites, i.e. L. infantum and L. donovani were isolated and reported from the Meriones persicus. These results indicate that rodents should be considered in devising strategies for epidemiological control of VL
in Iran. In a study conducted in Brazil, three parasites namely, L. donovani complex, L. mexicana complex and L. braziliensis were isolated and reported using molecular method81–82. In other areas, like Italy, Saudi Arabia and Venezuela, where human VL is active, natural infection of black rats with L. infantum and L. donovani and their role in preserving the disease has been reported in many studies83–85.
So far, three species of Leishmania parasites have been isolated and reported from wild and domestic res-ervoirs in Iran, 98% of which constitute/include L. infan-tum and L. tropica while L. donovani is rarely reported. This result shows that L. infantum is the main agent of CVL in Iran. In a WHO report also, L. infantum has been introduced as the main cause of Mediterranean VL in hu-
[Downloaded free from http://www.jvbd.org on Friday, January 4, 2019, IP: 5.122.114.141]
J Vector Borne Dis 55, September 2018180
mans and reservoirs 2, 16. Leishmania parasites have also been isolated from domestic and wildlife reservoirs in other parts of the world. For instance, in Mexico, three species of parasites including L. mexicana (20.63%), L. infantum (6%) and L. braziliensis (7.52%) were isolated from the blood serum of dogs by ELISA method86. The frequency of L. infantum infections in Mexico was less than that reported in Iran. In Spain, 28% of the studied animals were found to be infected with L. infantum by us-ing PCR method. The infection rate was found to be 29% in foxes, 25% in wild cats, 50% in weasels, 30% in sages and 26% in gravels87. As in Madrid, the L. infantum was isolated from 22.9% rabbits under investigation by rK39 method88. These results indicate that L. infantum infection has a wide distribution in domestic and wild reservoirs in most of the regions of Iran.
The first study in Iran was conducted on cats in 2010 in Fars and East Azerbaijan provinces and L. infantum was isolated from cats by molecular and parasitological meth-ods89. In Sao Paulo and Rio de Janeiro, Brazil L. infan-tum/chagasi was reported in domestic and wild cats5, 90. In an another study, high seroprevalence rates have been reported in domestic cats (Felis catus) based on detection of anti-L. infantum antibodies, indicating that infected cats might play a potential role in the maintenance of L. infantum in the endemic areas of ZVL91. This finding sug-gests that cats could play an important role in preserving VL in natural environments.
CONCLUSION
The review indicates that CVL is endemic in various parts of Iran and domestic dogs are the main and potential reservoir hosts of the disease. Other carnivores, such as domestic cats and some species of desert rodents (Cri-cetulus migratorius, Mesocricetus auratus and Meriones persicus) seem to be playing a role in the maintenance of transmission cycle of L. infantum in the endemic areas of the disease. High infection rates of CVL among domestic dogs compared to other canines pose a potential transmis-sion of the disease to humans. The status of other reservoir hosts, including domestic cats as well as domestic and wild rodents particularly in endemic areas could be help-ful in controlling the expansion of the disease. Moreover, the status estimation of sandflies that feed on the blood from these infected reservoir—Hosts is also necessary to prevent the disease transmission. Due to the increas-ing trend of CVL in Iran, it is strongly recommended that comprehensive plans should be implemented in order to prevent and control this disease, especially in endemic areas.
Conflict of interest: None.
ACKNOWLEDGEMENTS
This study was approved and financially supported by the Tehran University of Medical Sciences (Project Nos: 96-01-160-34180; 94-02-27-29919; and 97-01-160-37931).
REFERENCES
1. Alvar J, Velez ID, Bern C, Herrero M, Desjeux P, Cano J, et al. WHO leishmaniasis control team. Leishmaniasis worldwide and global estimates of its incidence. PloS One 2012; 7(5): e35671.
2. Control of leishmaniases. WHO Tech Rep Ser No. 793. Geneva: World Health Organization 2010.
3. Collin S, Davidson R, Ritmeijer K, Keus K, Melaku Y, Kipn-getich S, et al. Conflict and kala-azar: Determinants of adverse outcomes of kala-azar among patients in southern Sudan. Clin Infect Dis 2004; 38(5): 612–9.
4. Cortes S, Vaz Y, Neves R, Maia C, Cardoso L, Campino L. Risk factors for canine leishmaniasis in an endemic Mediterranean region. Vet Parasitol 2012; 189(2–4): 189–96.
5. da Silva AV, de Souza Cândido CD, de Pita Pereira D, Brazil RP, Carreira JC. The first record of American visceral leishmaniasis in domestic cats from Rio de Janeiro, Brazil. Acta Trop 2008; 105(1): 92–4.
6. Del Río L, Chitimia L, Cubas A, Victoriano I, De la Rúa P, Ger-rikagoitia X, et al. Evidence for widespread Leishmania infan-tum infection among wild carnivores in L. infantum periendemic northern Spain. Prev Vet Med 2014; 113(4): 430–5.
7. Desjeux P. Leishmaniasis: Current situation and new perspec-tives. Comp Immunol Microbiol Infect Dis 2004; 27(5): 305–18.
8. Jafari S, Hajiabdolbaghi M, Mohebali M, Hajjaran H, Hashemi-an H. Disseminated leishmaniasis caused by Leishmania tropica in HIV-positive patients in the Islamic Republic of Iran. East Mediterr Health J 2010; 16(3): 340–3.
9. Alborzi A, Rasouli M, Shamsizadeh A. Leishmania tropica-isolated patient with visceral leishmaniasis in southern Iran. Am J Trop Med Hyg 2006; 74: 306–7.
10. Shafiei R, Mohebali M, Akhoundi B, Galian MS, Kalantar F, Ashkan S, et al. Emergence of coinfection of visceral leishman-iasis in HIV-positive patients in northeast Iran: A preliminary study. Travel Med Infect Dis 2014; 12(2): 173–8.
11. Badirzadeh A, Mohebali M, Sabzevari S, Ghafoori M, Arza-mani K, Seyyedin M, et al. Case report: First coinfection report of mixed Leishmania infantum/Leishmania major and human immunodeficiency virus—Acquired immune deficiency syn-drome: Report of a case of disseminated cutaneous leishmani-asis in Iran. Am J Trop Med Hyg 2018; 98(1): 122–5.
12. Hajjaran H, Mohebali M, Zarei Z, Edrissian G. Leishmania tropica: Another etiological agent of canine visceral leishmani-asis in Iran. Iran J Public Health 2007; 36(1): 85–8.
13. Mohebali M. Visceral leishmaniasis in Iran: Review of the epi-demiological and clinical features. Iran J Parasitol 2013; 8(3): 348–58.
14. Edrissian GH, Nadim A, Alborzi AV, Ardehali S. Visceral leish-maniasis: The Iranian experience. Arch Iran Med 1998; 1(1): 22–6.
[Downloaded free from http://www.jvbd.org on Friday, January 4, 2019, IP: 5.122.114.141]
181
15. Mohebali M, Arzamani K, Zarei Z, Akhoundi B, Hajjaran H, Raeghi S, et al. Canine visceral leishmaniasis in wild canines (fox, jackal and wolf) in northeastern Iran using parasitologi-cal, serological, and molecular methods. J Arthropod Borne Dis 2016; 10(4): 538–45.
16. Mohebali M, Edrissian GH, Shirzadi MR, Akhoundi B, Haj-jaran H, Zarei Z, et al. An observational study on the current distribution of visceral leishmaniasis in different geographical zones of Iran and implication to health policy. Travel Med Infect Dis 2011; 9(2): 67–74.
17. Mohebali M, Hajjaran H, Hamzavi Y, Mobedi I, Arshi S, Zarei Z, et al. Epidemiological aspects of canine visceral leishmani-osis in the Islamic Republic of Iran. Vet Parasitol 2005; 129(3–4): 243–51.
18. Tesh RB. Control of zoonotic visceral leishmaniasis: Is it time to change strategies? Am J Trop Med Hyg 1995; 52(3): 287–92.
19. Reiner SL, Locksley RM. The regulation of immunity to Leish-mania major. Annu Rev Immunol 1995; 13(1): 151–77.
20. Mohebali M, Edrissian GH, Nadim A, Hajjaran H, Akhoundi B, Hooshmand B, et al. Application of direct agglutination test (DAT) for the diagnosis and seroepidemiological studies of vis-ceral leishmaniasis in Iran. Iran J Parasitol 2006; 1(1): 15–25.
21. Gavgani AS, Mohite H, Edrissian GH, Mohebali M, Davies CR. Domestic dog ownership in Iran is a risk factor for human in-fection with Leishmania infantum. Am J Trop Med Hyg 2002; 67(5): 511–5.
22. Hamidi AN, Nadim A, Edrissian GH, Tahvildar-Bidruni GH, Ja-vadian E. Visceral leishmaniasis of jackals and dogs in northern Iran. Trans R Soc Trop Med Hyg 1982; 76(6): 756–7.
23. Bokai S, Mobedi I, Edrissian GH, Nadim A. Seroepidemiologi-cal study of canine visceral leishmaniasis in Meshkin-Shahr, northwest of Iran. Arch Inst RAZI 1998; 48–49: 41–6.
24. Mohebali M, Hamzavi Y, Edrissian GH, Forouzani A. Seroepi-demiological study of visceral leishmaniasis among humans and animal reservoirs in Bushehr province, Islamic Republic of Iran. East Mediterr Health J 2001; 7(6): 912–7.
25. Sadeghi H, Arshi SH. The prevalence of serologic leishmani-asis in flock and domestic dogs of nomads in Ardebil province in 2002 by using DAT method. J Ardabil Uni Med 2003; 3(2): 25–40.
26. Mohebali M, Khamesipour A, Mobedi I, Zarei Z, Hashemi-Fe-sharki R. Double-blind randomized efficacy field trial of alum precipitated autoclaved Leishmania major vaccine mixed with BCG against canine visceral leishmaniasis in Meshkin-Shahr district, IR Iran. Vaccine 2004; 22(29–30): 4097–100.
27. Mohebali M, Taran M, Zarei Z. Rapid detection of Leishmania infantum infection in dogs: Comparative study using an immu-nochromatographic dipstick rk39 test and direct agglutination. Vet Parasitol 2004; 121(3–4): 239–45.
28. Fakhar M, Mohebali M, Barani M. Identification of endemic fo-cus of kala-azar and seroepidemiologcial study of visceral leish-mania infection in human and canine in Qom province, Iran. Armaghane Danesh 2004; 9(1): 43–52.
29. Mosallanejad B, Ranjbar SH, Moradi B. Seroepidemiological investigation of visceral leishmaniasis in local dogs of Garmsar. Vet Microbiol 2004; 3(2): 60–5.
30. Mahami M, Moheb Ali M, Keshavarz H, Hajjaran H, Akhoondi B, Zarei Z, et al. A seroepidemiological survey of visceral leish-maniasis (kala-azar) in Germi district, Ardabil Province. Sjsph 2006; 4(1): 45–55.
31. Zebardast N. The identification of canine, reservoirs of visceral leishmaniasis (VL) in Chaharmahal and Bakhteyari provinces
of Iran. Iran J Parasitol 2005; 2(1): 35–45.32. Fakhar M, Motazedian MH, Asgari Q, Mohebali M, Mehrabani
D. A new endemic focus of visceral leishmaniosis in southeren Iran. Armaghane Danesh 2006; 11(2): 103–13.
33. Avizeh R, Mohebali M, Sheikholslami M. Seroepidemiological investigation of visceral leishmaniasis in dogs of Ahvaz district, Iran. Arch Razi Inst 2007; 62(1): 31–7.
34. Rassi Y, Gassemi MM, Javadian E, Rafizadeh S, Motazedian H, Vatandoost H. Vectors and reservoirs of cutaneous leishmani-asis in Marvdasht district, southern Islamic Republic of Iran. Iranian J Arthropod-Borne Dis 2007; 1(2): 14–8.
35. Taran M, Mohebali M, Modaresi MH, Mamishi S, Mahmoudi M, Mojarad M. Diagnosis of canine visceral leishmaniasis by ELISA using K39 subrecombinant antigen. Iran J Public Health 2007; 36(2): 1–6.
36. Farzam M, Changizi E, Mohebali M, Akhoundi B, Salimi BM. Seroepidemiological survey of canine visceral leishmaniasis in Jahrom City, Fars province. Iran J Vet Res 2008; 4(3): 58–67.
37. Moshfe A, Mohebali M, Edrissian G, Zarei Z, Akhoundi B, Kazemi B, et al. Seroepidemiological study on canine viscer-al leishmaniasis in Meshkin-Shahr district, Ardabil province, northwest of Iran during 2006–2007. Iran J Parasitol 2008; 3(3): 1–10.
38. Khanmohammadi M, Fallah E, Rahbari S, Hesaraki S. Study of seroprevalence of visceral leishmaniasis in wild canines in Sar-ab region (East Azarbaijan province). J Vet Diagn Invest 2008; 4(4): 997–1005.
39. Moshfe A, Mohebali M, Edrissian G, Zarei Z, Akhoundi B, Ka-zemi B, et al. Canine visceral leishmaniasis: Asymptomatic in-fected dogs as a source of L. infantum infection. Acta Trop 2009; 112(2): 101–5.
40. Khanmohammadi M, Fallah E, Rahbari S, Sohrabi I, Farsh-chian M, Hamzavi F, et al. Study on seroprevalence of ca-nine visceral leishmaniasis (CVL) in ownership dogs of Sar-ab, East Azerbaijan province, northwest of Iran with indirect immunofluorescence antibody test (IFAT) and its health impor-tance in 2008–2009. Asian J Anim Vet Adv 2010; 9(1): 139–43.
41. Salahi-Moghaddam A, Mohebali M, Moshfae A, Habibi M, Za-rei Z. Ecological study and risk mapping of visceral leishmani-asis in an endemic area of Iran based on a geographical informa-tion systems approach. Geospat Health J 2010; 5(1): 71–7.
42. Fakhar M, Rahmati B, Gohardehi S, Mohebali M, Akhoundi B, Sharif M, et al. Molecular and seroepidemiological survey of visceral leishmaniasis among humans and domestic dogs in Mazandaran province, north of Iran. Iran J Parasitol 2011; 6(4): 51.
43. Fallah E, Farshchian M, Khanmohammadi M. Molecular and seroepidemiological study of Leishmania infantum infection among humans, dogs and wild canines from Azarshahr (new endemic focus), Iran. Afr J Microbial Res 2011; 5(10): 1237–42.
44. Fallah E, Khanmohammadi M, Rahbari S, Farshchian M, Far-ajnia S, Hamzavi F, et al. Serological survey and comparison of two polymerase chain reaction (PCR) assays with enzyme-linked immunosorbent assay (ELISA) for the diagnosis of canine visceral leishmaniasis in dogs. Afr J Biotechnol 2011; 10(4): 648–56.
45. Fallah E, Khanmohammadi M. A case report of visceral leish-maniasis in red fox (Vulpes vulpes). Afr J Biotechnol 2011; 10(86): 19941–6.
46. Sharifdini M, Mohebali ME, Keshavarz H, Hosseininejad M, Hajjaran H, Akhoundi B, et al. Neospora caninum and Leishma-nia infantum co-infection in domestic dogs (Canis familiaris)
Mohebali et al: Distribution and spatial analysis of L. infantum infection in Iran
[Downloaded free from http://www.jvbd.org on Friday, January 4, 2019, IP: 5.122.114.141]
J Vector Borne Dis 55, September 2018182
in Meshkin-Shahr district, northwestern Iran. Iran J Arthropod Borne Dis 2011; 5(2): 60–8.
47. Mohammadi-Ghalehbin B, Hatam GR, Sarkari B, Mohebali M, Zarei Z, Jaberipour M, et al. A Leishmania infantum FML-ELI-SA for the detection of symptomatic and asymptomatic canine visceral leishmaniasis in an endemic area of Iran. Iran J Immu-nol 2011; 8(4): 244–50.
48. Ansari H, Moshfe AA, Solhjoo K, Khodadadi P, Kalantari M, Afshoon E, et al. Characterization of visceral leishmaniasis in reservoir host (dogs) and determination of agent by PCR in Boyer-Ahmad district, Iran. Armaghane Danesh 2012; 16(6): 537–44.
49. Mahmoudvand H, Mohebali M, Sharifi I, Keshavarz H, Haj-jaran H, Akhoundi B, et al. Epidemiological aspects of visceral leishmaniasis in Baft district, Kerman province, southeast of Iran. Iran J Parasitol 2011; 6(1): 1–11.
50. Fakhar M, Motazedian MH, Asgari Q, Kalantari M. Asymptom-atic domestic dogs are carriers of Leishmania infantum: Possi-ble reservoirs host for human visceral leishmaniasis in southern Iran. Comp Clin Path 2012; 21(5): 801–7.
51. Hosseininejad M, Mohebali M, Hosseini F, Karimi S, Sharifzad S, Akhoundi B. Seroprevalence of canine visceral leishmaniasis in asymptomatic dogs in Iran. Iran J Vet Res 2012; 13(1): 54–7.
52. Razzaghi Manesh M, Mahabadi S, Ghamesi A, Namjoo AR. Seroprevalence of canine visceral leishmaniasis in dogs at Ard-estan district detected by PCR. Vet Res 2012; 5(2): 22–5.
53. Aflatoonian MR, Akhtardanesh B, Sharifi I, Mostafavi M. Sero-epidemiology of canine visceral leishmaniosis in Kerman City, 2011. J Kerman Uni Med 2012; 19(6): 531–9.
54. Mohammadiha A, Haghighi A, Mohebali M, Mahdian R, Abadi AR, Zarei Z, et al. Canine visceral leishmaniasis: A comparative study of real-time PCR, conventional PCR, and direct aggluti-nation on sera for the detection of Leishmania infantum infec-tion. Vet Parasitol 2013; 192(1–3): 83–90.
55. Moshfe A, Mohebali M, Afshoun E, Mousavizadeh A, Zarei Z, Abidi H, et al. Canine visceral leishmaniasis in Boyer Ahmad district, Kohgiluyeh and Boyer Ahmad province, southwest of Iran. Iran J Parasitol 2012; 7(4): 75–81.
56. Heidarpour M, Pourtaghi M, Khoshnegah J. Prevalence and risk factors for canine leishmaniasis in Mashhad, northeast of Iran. Iran J Vet Tech 2012; 4(1): 37–46.
57. Haddadzade HR, Fattahi R, Mohebali M, Akhoundi B, Ebra-himzade E. Seroepidemiologcal investigation of visceral leish-maniasis in stray and owned dogs in Alborz province, central Iran using direct agglutination test. Iran J Parasitol 2013; 8(1): 152–7.
58. Hajjaran H, Mohebali M, Mamishi S, Vasigheh F, Oshaghi MA, Naddaf SR, et al. Molecular identification and polymorphism determination of cutaneous and visceral leishmaniasis agents isolated from human and animal hosts in Iran. Biomed Res Int 2013; 2013: 789326.
59. Adinezadeh A, Eshrat Beigom KI, Mohebali M, Shojaee S, Rokni MB, Zarei Z, et al. Endoparasites of stray dogs in Mash-had, Khorasan-Razavi province, northeast Iran with special reference to zoonotic parasites. Iran J Parasitol 2013; 8(3): 459–66.
60. Sabzevari S, Razmi GR, Naghibi A, Khoshnegah J. A serologi-cal study of Leishmania infantum in dogs of Khorasan Razavi province, Iran. J Parasit Dis 2013; 37(2): 189–91.
61. Shabestari-Asl A, Sharifi M, Mohebali M, Zarei Z, Babaloo Z, Akhoundi B. Evaluation of canine anti-Leishmania IgG sub-classes and their relation with skin signs in naturally infected
dogs in the northwest of Iran. Turk J Vet Anim Sci 2013; 37(5): 512–5.
62. Malmasi A, Janitabar S, Mohebali M, Akhoundi B, Maazi N, Aramoon M, et al. Seroepidemiologic survey of canine visceral leishmaniasis in Tehran and Alborz provinces of Iran. J Arthro-pod Borne Dis 2014; 8(2): 132–8.
63. Mostafavi M, Baharak A, Iraj S, Sina K, Javad K, Mehdi B. Seroprevalence of canine visceral leishmaniasis in southeast of Iran. J Parasit Dis 2014; 38(2): 218–22.
64. Fakhar M, Kia AA, Gohardehi S, Sharif M, Mohebali M, Ak-houndi B, et al. Emergence of a new focus of visceral leishmani-asis due to Leishmania infantum in Golestan province, north-eastern of Iran. J Parasit Dis 2014; 38(3): 255–9.
65. Gharekhani J, Heidari H, Hajian-Bidar H, Abbasi-Doulatshahi E, Edalati-Shokat H. Prevalence of anti-Leishmania infantum antibodies in dogs from west of Iran. J Parasit Dis 2014; 40(3): 964–7.
66. Fatollahzadeh M, Khanmohammadi M, Bazmani A, Mirsamadi N, Jafari R, Mohebali M, et al. Survey of feline visceral leish-maniasis in Azarshahr area, northwest of Iran, 2013. J Parasit Dis 2016; 40(3): 683–7.
67. Namroodi S. Serological survey of Leishmania infantum in jackals in Golestan province, Iran (2011–2013). J Mazandaran Med 2015; 24(120): 25–9.
68. Bamorovat M, Sharifi I, Mohammadi MA, Harandi MF, Mo-hebali M, Afshar RM, et al. Canine visceral leishmaniasis in Kerman, southeast of Iran: A seroepidemiological, histopatho-logical and molecular study. Iran J Parasitol 2014; 9(3): 342.
69. Bamorovat M, Sharifi I, Dabiri S, Mohammadi MA, Harandi MF, Mohebali M, et al. Leishmania tropica in stray dogs in southeast Iran. Iran J Public Health 2015; 44(10): 1359–66.
70. Farahmand M, Khalaj V, Mohebali M, Khalili G, Naderi S, Ghaffarinejad P, et al. Comparison of recombinant A2-ELISA with rKE16 dipstick and direct agglutination tests for diagnosis of visceral leishmaniasis in dogs in northwestern Iran. Rev Soc Bras Med Trop 2015; 48(2): 188–93.
71. Ghaffarinejad P, Farahmand M, Nahrevanian H, Mohebali M, Zaboli F, Zarei Z, et al. Diagnosis of Leishmania infantum us-ing direct agglutination test and rKE16 dipstick rapid test in do-mestic dogs from Ardabil province, Iran. J Parasitol Res 2015; 10(3): 102–10.
72. Barati M, Mohebali M, Alimohammadian MH, Khamesipour A, Akhoundi B, Zarei Z. Canine visceral leishmaniasis: Sero-prevalence survey of asymptomatic dogs in an endemic area of northwestern Iran. J Parasit Dis 2015; 39(2): 221–4.
73. Arainnejad M, Razmi G, Khoshnegah J. Molecular detection of canine leishmaniasis using conjunctival swab and buffy coat samples. Vet Clin Pathol 2016; 9(36): 275–84.
74. Molaei S, Dalimi A, Mohamadi B, Akhondi B, Azarm A. Study of canine visceral leishmaniasis in symptomatic and asymptom-atic domestic dogs in Meshkinshahr City, Iran. J Ardabil Med 2016; 16(1): 105–15.
75. Jalilnavaz MR, Abai MR, Vatandoost H, Mohebali M, Akhavan AA, Zarei Z, et al. Application of flumethrin pour-on on res-ervoir dogs and its efficacy against sandflies in endemic focus of visceral leishmaniasis, Meshkinshahr, Iran. Iran J Arthropod Borne Dis 2016; 10(1): 78–86.
76. Akhtardanesh B, Sharifi I, Mohammadi A, Mostafavi M, Ha-kimmipour M, Pourafshar NG. Feline visceral leishmaniasis in Kerman, southeast of Iran: Serological and molecular study. J Vector Borne Dis 2017; 54(1): 96–102.
77. Nadim A, Navid-Hamidid A, Javadian E, Bidruni GT, Amini H.
[Downloaded free from http://www.jvbd.org on Friday, January 4, 2019, IP: 5.122.114.141]
183
Present status of kala-azar in Iran. Am J Trop Med Hyg 1978; 27(1): 25–8.
78. Moradi-Asl E, Mohebali M, Mohammadi-Ghalehbin B, Ganji A, Molaei S, Mehrivar R, et al. Study on changes in epidemio-logical patterns and parameters of visceral leishmaniasis in pa-tients referred to health care centers of Meshkin Shahr during 2001–2012: A retrospective study. J Ardabil Med 2014; 14(1): 63–70.
79. Moradi-Asl E, Hanafi-Bojd AA, Rassi Y, Vatandoost H, Mo-hebali M, Yaghoobi-Ershadi MR, et al. Situational analysis of visceral leishmaniasis in the most important endemic area of the disease in Iran. J Arthropod Borne Dis 2017; 11(4): 482–96.
80. Moradi-Asl E, Rassi Y, Hanafi-Bojd AA, Vatandoost H, Sa-ghafipour A, Adham Davoud, et al. The relationship between climatic factors and the prevalence of visceral leishmaniasis in northwest of Iran. Int J Pediatr 2018; 6(2): 7169–78.
81. Oliveira FS, Pirmez C, Pires MQ, Brazil RP, Pacheco RS. PCR-based diagnosis for detection of Leishmania in skin and blood of rodents from an endemic area of cutaneous and visceral leish-maniasis in Brazil. Vet Parasitol 2005; 129(3–4): 219–27.
82. Marcelino AP, Ferreira EC, Avendanha JS, Costa CF, Chi-arelli D, Almeida G, et al. Molecular detection of Leish-mania braziliensis in Rattus norvegicus in an area endemic for cutaneous leishmaniasis in Brazil. Vet Parasitol 2011; 183: 54–8.
83. Gradoni L, Pozio E, Gramiccia M, Maroli M, Bettini S. Leish-maniasis in Tuscany (Italy): VII. Studies on the role of the black rat, Rattus rattus, in the epidemiology of visceral leishmaniasis. Trans R Soc Trop Med Hyg 1983; 77(4): 427–31.
84. Ibrahim EA, al-Zahrani MA, al-Tuwaigri AS, al-Shammary FJ, Evans DA. Leishmania infecting man and wild animals in Saudi Arabia. 9. The black rat (Rattus rattus) a probable reservoir of
visceral leishmaniasis in Gizan province, southwest Saudi Ara-bia. Trans R Soc Trop Med Hyg 1992; 86: 513–4.
85. Zulueta AM, Villarroel E, Rodriguez N, Feliciangeli MD, Maz-zarri MI, Reyes O, et al. Epidemiologic aspects of American visceral leishmaniasis in an endemic focus in eastern Venezuela. Trans R Soc Trop Med Hyg 1999; 61(6): 945–50.
86. López-Céspedes A, Longoni SS, Sauri-Arceo CH, Sánchez-Moreno M, Rodríguez-Vivas RI, Escobedo-Ortegón FJ, et al. Leishmania spp epidemiology of canine leishmani-asis in the Yucatan Peninsula. Scientific World J 2012; 2012: 945871.
87. Rosypal AC, Tidwell RR, Lindsay DS. Prevalence of antibodies to Leishmania infantum and Trypanosoma cruzi in wild canids from South Carolina. J Parasitol 2007; 93(4): 955–7.
88. Jiménez M, González E, Martín-Martín I, Hernández S, Molina R. Could wild rabbits (Oryctolagus cuniculus) be reservoirs for Leishmania infantum in the focus of Madrid, Spain? Vet Parasi-tol 2014; 202(3–4): 296–300.
89. Hatam GR, Adnani SJ, Asgari Q, Fallah E, Motazedian MH, Sadjjadi SM, et al. First report of natural infection in cats with Leishmania infantum in Iran. Vector Borne Zoonotic Dis 2010; 10(3): 313–6.
90. Savani ES, de Oliveira Camargo MC, de Carvalho MR, Zamp-ieri RA, dos Santos MG, D’Áuria SR, et al. The first record in the Americas of an autochthonous case of Leishmania (Leish-mania) infantum chagasi in a domestic cat (Felix catus) from Cotia County, São Paulo State, Brazil. Vet Parasitol 2004; 120(3): 229–33.
91. Mohebali M, Malmasi A, Khodabakhsh M, Zarei Z, Akhoundi B, Hajjaran H, et al. Feline leishmaniosis due to Leishmania infantum in northwest Iran: The role of cats in endemic areas of visceral leishmaniosis. Vet Parasitol 2017; 9: 13–6.
Correspondence to: Dr E. Moradi-Asl, Department of Public Health, School of Public Health, Ardabil University of Medical Sciences, Ardabil, Iran.
E-mail: [email protected]
Received: 13 May 2018 Accepted in revised form: 1 August 2018
Mohebali et al: Distribution and spatial analysis of L. infantum infection in Iran
[Downloaded free from http://www.jvbd.org on Friday, January 4, 2019, IP: 5.122.114.141]