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Journal of Venomous Animals and Toxins including Tropical Diseases

On-line version ISSN 1678-9199

J. Venom. Anim. Toxins incl. Trop. Dis vol.25  Botucatu  2019  Epub June 10, 2019

http://dx.doi.org/10.1590/1678-9199-jvatitd-2019-0012 

Review

Is the cat an important reservoir host for visceral leishmaniasis? A systematic review with meta-analysis

Shabnam Asfaram1 

Mahdi Fakhar2   
http://orcid.org/0000-0002-4690-6938

Saeed Hosseini Teshnizi3 

1Student Research Committee, Department of Parasitology, School of Medicine, Mazandaran University of Medical Sciences, Sari, Iran.

2Toxoplasmosis Research Center, Department of Parasitology, School of Medicine, Mazandaran University of Medical Sciences, Sari, Iran.

3Infectious and Tropical Diseases Research Center, Hormozgan University of Medical Sciences, Bandar Abbas, Iran.


Abstract

In recent years feline leishmanial infections (FLI) have been studied more than ever before in various parts of the world. However, evidence-based knowledge on FLI has remained unavailable. The main objectives of this study were to investigate the status of felines infected by Leishmania spp. worldwide. Data were extracted from 10 available databases over the period of 1982 to 2017. Overall, 78 articles fulfilled the inclusion criteria and were used for data extraction in this systematic review. The overall FLI prevalence by both serological and molecular methods was estimated at 10% (95% CI: 8%-14%). In Italy, both the seroprevalence (24 %) and PCR prevalence (21 %) were found to be higher than in other countries. The most common diagnostic test used was the indirect fluorescent antibody test (38.5%). Studies on mixed-breed felines were more common than those on other breeds, while the most common parasite species was L. infantum (63%). Our findings suggest that cats act as primary and/or secondary reservoir hosts in the transmission of the Leishmania spp. to humans and also to dogs, by sandflies, at least in endemic foci. Moreover, available data confirm the enzootic stability situation of FLI in several countries including some in Europe.

Keywords: Feline leishmanial infection; Global prevalence; Diagnostic tests; Systematic review; Meta-analysis

Background

The leishmaniases are neglected protozoal diseases caused by Leishmania spp. that occur in 98 countries [1], affecting 1.2 million in the form of cutaneous leishmaniasis (CL), and 400,000 in the form of visceral leishmaniasis (VL), leading to approximately 40,000 deaths per year [2]. The main route of VL transmission is through the bite of vectors infected with Leishmania donovani (L. donovani) complex, mainly Leishmania infantum/chagasi (L. infantum/chagasi). Both domestic and wild animals may serve as host reservoirs of Leishmania spp. [3]. Dogs are the main reservoir hosts of L. infantum/chagasi but sandflies, as the natural vectors of Leishmania spp., may also feed on the blood of cats [4]. Therefore, cats infected with the L. donovani complex may be urban reservoirs of VL and transmit the protozoan to other sandflies [5, 6]; therefore, cats are potential reservoirs of this zoonotic VL disease. Studies on feline leishmanial infection (FLI) are limited and several aspects of the disease in cats are still unclear [7]. Recently, reports of FLI have increased dramatically, achieving a prevalence of up to 60% in certain cat populations [8]. The most common clinical signs reported in FLI include lymphadenomegaly, splenomegaly, weight loss, anorexia, as well as cutaneous, mucocutaneous and ocular lesions [8]. However, in endemic regions such as Mediterranean countries, the subclinical feline infection L. infantum/chagasi is common, whereas clinical illness is relatively uncommon [7-8].

Identification of Leishmania amastigotes in aspirated samples of bone marrow, spleen and lymph node is specific and considered the gold standard method for diagnosing FLI. Feline vector-borne pathogens have been increasingly recognized worldwide based on serological and/or molecular epidemiological investigations [9,10]. Most epidemiological studies demonstrated the presence of anti-Leishmania antibodies in feline sera by means of different techniques such as indirect fluorescent antibody test (IFAT), enzyme-linked immunosorbent assay (ELISA) or western blot (WB) [10-17]. Polymerase chain reaction (PCR) is recommended preferentially over other diagnostic tests, especially when blood samples and other clinical samples contain a low parasitic burden [13, 16, 18,19]. However little is known in reference to their diagnostic performance in cats with FLI.

Although an effective treatment for symptomatic cats has not yet been established, oral allopurinol administration followed by subcutaneous glucantime has been frequently used as chemotherapy regimens in cats affected by FLI [7, 8, 20].

However, there is still no available evidence-based knowledge about various epidemiological aspects of FLI. Therefore, the purpose of this study was to determine the global status of the infection in cats and introduce currently used diagnostic laboratory methods.

Methods

Searching strategy

This systematic review was performed according to the guidelines of the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) [21]. To determine the prevalence of FLI, 10 English and Iranian databases including Google Scholar, Pub Med, Science Direct, Web of Science, Scopus, Elm net, Magiran, Barakatkns (formerly Iran medex), Iran doc, and Scientific Information Database (SID) were searched from 1982 to 2017 (36 years). The relevant keywords including “Leishmania spp.”, “Leishmania donovani”, “Leishmania infantum”, “feline leishmaniasis”, “feline leishmaniosis”, “cat”, “molecular”, “PCR” , “serology”, “ELISA”, “IFAT” were chosen using medical subject headings terms (MESH).

Inclusion and exclusion criteria

Data were extracted from studies with at least one of the following inclusion criteria: cross-sectional and case-control studies corresponding to determining prevalence of leishmanial infections that evaluated the presence of FLI based on serological and molecular tests among all types of cats. Also, summaries of articles presented as proceedings at conferences, studies that contained no qualified data, experimental studies, review articles, duplicates, and case reports were excluded. The PRISMA flowchart of the study plan is shown in Figure 1. Out of the retrieved articles, 78 papers were eligible for inclusion in this systematic review and meta-analysis. The recorded data included author name, year of publication, country, type of cat, sample size, Lieshmania species, laboratory method, seroprevalence (%) and PCR prevalence and quality assessment. The above details were extracted separately by two researchers (SA and MF).

Figure 1. PRISMA flowchart showing the study design process. 

Meta-analysis

For each study, the prevalence and standard error (SE= P(1−P) n ) were determined. We used forest plots to estimate pooled effect sizes and the effect of each study with 95% confidence intervals. The Cochran Q-test (p-value<0.1) and the I-squared index were employed to evaluate heterogeneity , with I 2 values between 25% and 50% as thresholds for low , between 50% and 75% for moderate, and above 75% for high heterogeneity. When heterogeneity was found, a random-effects model (Dersimonian-Laird model) was applied; if not, a fixed effects model (Mantel-Haenszel) was utilized to calculate overall effects.

Quality assessment

The quality of meta-analysis was evaluated with the STROBE checklist. A checklist including 22 items was considered for adequate reporting of observational studies. These items related to the article’s title, abstract, introduction, methods, results, and discussion sections. A score under 7 was defined as poor quality, 8 to 17 low, 18 to 28 moderate and more than more 28 high quality [22]. The mean score obtained via the STROBE checklist for 78 analyzed articles was 31, whereas 28 is considered high quality. Possible publication bias was explored using a funnel plot and Egger’s test, which evaluated whether the precision of studies was appropriate for the scale of their effect size. All data analyses were performed using the software Stata, v. 14 (Stata Corp LP, College Station, Texas, USA).

Results

Seventy-eight (78) cross-sectional studies published from 1982 to 2017 (36 years) were included in this meta-analysis. Most studies (30.8%) were performed in Brazil (Table 1). The total number of cases was 12,635 (ranging from 8 to 1,101). In Italy, both the prevalence by seropositivity (24 %) and PCR positivity (21%) were found to be higher than in other countries. The overall seropraevalence of FLI in 4 European countries including Italy, Spain, Portugal, and Greece was estimated at 12.2% (see Table 2).

The most common diagnostic test was IFAT, used in 38.5% of studies. Among serological methods, WB and indirect hemagglutination test (IHT), being the least common diagnostic tests, were used in only 3.8 % of studies (see Table 1).

The seroprevalence (15%) and PCR prevalence (23%) of FLI in mixed-type/ breed cats (defined as cats descending from two or more breeds) were higher than in other cat types/ breeds. Approximately 63% of Leishmania species were L. infantum, while the remainder frequently included Leishmania spp. (Table 2).

Table 1 Baseline characteristics of studies included in the meta-analysis of feline leishmanial infection 

Author Year of publication Country Type of cat Sample size Leishmania species Lab test Seropositive (%) PCR positive (%)
Michael. SA [43] 1982 Egypt stray 80 Leishmania spp. IHAT 3.8 .
Morsy. TA [44] 1988 Egypt stray 28 Leishmania spp. IHAT 3.6 .
Bez. M [45] 1992 France . 174 Leishmania spp. IFAT 0.6 .
Morsy. TA [46] 1994 Egypt mixed 60 Leishmania spp. IHAT 10 .
Sherlock. IA [47] 1996 Brazil . 53 Leishmania spp. IFAT 0 .
Pennisi. MG [48] 1998 Italy mixed 93 Leishmania spp. IFAT 59.1 .
Ozon. C [29] 1998 France stray 97 L. infantum WB 12.4 .
Pennisi. MG [8] 2000 Italy mixed 89 Leishmania spp. IFAT, PCR 68.5 60.7
Simões-Mattos. L [49] 2001 Brazil stray 84 Leishmania spp. ELISA 10.7 .
Poli. A [31] 2002 Italy domestic 110 Leishmania spp. IFAT 0.9 .
Portús. M [50] 2002 Spain domestic 117 L. infantum ELISA 1.7 .
Zárate-Ramos. JJ [51] 2002 Spain domestic 50 L. infantum DAT 42 .
Vita. S [52] 2005 Italy mixed 203 Leishmania spp. IFAT, PCR 16.3 100
Solano-Gallego. L [37] 2007 Spain mixed 445 L. infantum ELISA 6.3 .
Martín-Sánchez. J [36] 2007 Spain domestic 183 L. infantum IFAT, PCR 70.5 25.7
Nasereddin. A [53] 2008 Israel stray 104 Leishmania spp. ELISA 6.7 .
Huebner. J [54] 2008 Greece mixed 389 Leishmania spp. IFAT 21.6 .
Tabar. MD [55] 2008 Spain domestic 100 L. infantum PCR . 3
Ayllon. T [40] 2008 Spain domestic 233 L. infantum IFAT, PCR 4.29 0.4
Maia. C [56] 2008 Portugal stray 23 L. infantum IFAT, PCR 17.4 30.4
Da Silva. AV [42] 2008 Brazil domestic 8 L. infantum IFAT 25 .
Sarkari. B [57] 2009 Iran stray 40 L. infantum IFAT, DAT 27.5 .
Diakou. A [58] 2009 Greece stray 284 Leishmania spp. ELISA 3.9 .
Figueiredo. FB [11] 2009 Brazil . 43 Leishmania spp. IFAT, ELISA 2.4 .
Hatam. GR [59] 2010 Iran domestic 40 L. infantum PCR . 7.5
Veronesi. F [60] 2010 Italy mixed 95 Leishmania spp. IFAT, PCR 9.5 5.3
Cardoso. L [35] 2010 Portugal domestic 316 L. infantum ELISA, DAT 2.8 .
Duarte. A [61] 2010 Portugal stray 180 L. infantum IFAT 0.6 .
Maia. C [62] 2010 Portugal domestic 142 L. infantum IFAT, PCR 1.3 20.4
Costa. TA [63] 2010 Brazil . 200 L. infantum ELISA 11.5 .
Dahroug. MA [64] 2010 Brazil Puma concolor, Panthera onca, Leopardus pardalis 16 L. infantum PCR . 37.5
Bresciani. KD [65] 2010 Brazil domestic 283 Leishmania spp. IFAT 0 .
Sherry. K [36] 2011 Spain mixed 105 L. infantum ELISA, PCR 12.4 8.6
Millán. J [66] 2011 Spain mixed 86 L. infantum WB, PCR 15.7 25.6
Miró. G [67] 2011 Spain . 20 L. infantum IFAT 15 .
Vides. JP [12] 2011 Brazil . 55 L. infantum IFAT, ELISA 27.3 .
Da Silveira Neto. L [ 68] 2011 Brazil . 113 L. infantum ELISA 34.5 .
Coelho. WM [13] 2011 Brazil . 70 Leishmania spp. IFAT, ELISA 4.2 .
Coelho. WM [13] 2011 Brazil . 52 L. infantum PCR . 5.8
Pennisi. MG [69] 2012 Italy mixed 431 Leishmania spp. IFAT, PCR 6.9 18.3
Ayllon. T [70] 2012 Spain mixed 680 L. infantum IFAT, PCR 3.7 0.6
Sobrinho. LS [14] 2012 Brazil stray 302 L. infantum IFAT, ELISA 15.23 .
Longoni. SS [17] 2012 Mexico stray 95 L. infantum, L. braziliensis ELISA, WB 31.6 .
Spada. E [71] 2013 Italy stray 233 Leishmania spp. IFAT, PCR 25.3 0
Vilhena. H [9] 2013 Portugal domestic 320 L. infantum PCR . 0.3
Cardia. DF [72] 2013 Brazil stray 386 Leishmania spp. IFAT 0.5 .
Silva. RD [73] 2013 Brazil . 153 L. infantum ELISA 3.9 .
Chatzis. MK [10] 2014 Greece domestic 100 L. infantum IFAT, ELISA, PCR 11 41
Silaghi. C [74] 2014 Albania stray 146 Leishmania spp. IFAT, PCR 0.7 0
Miró. G [75] 2014 Spain stray 346 L. infantum IFAT, PCR 3.2 0
Maia. C [76] 2014 Portugal mixed 649 L. infantum PCR . 9.9
Maia. C [76] 2014 Portugal mixed 271 L. infantum DAT 3.7 .
Nimsuphan. B [77] 2014 Bangkok pet 237 L. donovani DAT 0.8 .
Moreno.I [78] 2014 Spain stray 43 L. infantum IFAT 9.3 .
Dorbadam. SM [79] 2014 Iran stray 50 L. infantum DAT 2 .
Sousa. KC [80] 2014 Brazil domestic 151 L. infantum IFAT 6.6 .
Fatollahzadeh. M [81] 2014 Iran . 65 L. infantum DAT, PCR 23.0 0
Braga. AR [82] 2014 Brazil domestic 50 Leishmania spp. IFAT 4 .
Costa. AP [83] 2014 Brazil domestic 52 L. infantum IFAT 3.8 .
Braga. AR [84] 2014 Brazil . 100 Leishmania spp. IFAT, PCR 15 0
Nemati. T [85] 2015 Iran . 65 Leishmania spp. DAT 27.7 .
Maia. C [86] 2015 Portugal mixed 271 L. infantum DAT 3.7 .
Dincer. E [87] 2015 Turkey . 22 L. infantum PCR . 4.5
Oliveira. TM [88] 2015 Brazil . 52 Leishmania spp. PCR . 13.5
Spada. E [89] 2016 Italy stray 90 L. infantum IFAT, PCR 30 2.2
Figueiredo. FB [90] 2016 Brazil domestic 34 L. braziliensis ELISA 20.6 .
Persichetti. MF [91] 2016 Spain . 42 L. infantum IFAT, PCR 2.4 7.1
Can. H [16] 2016 Turkey stray 1101 L. infantum, L. tropica IFAT, ELISA, PCR 10.5 0.54
Persichetti. MF [15] 2017 Italy . 161 L. infantum ELISA, IFAT, WB 29.2 .
Otranto. D [92] 2017 Italy . 330 L. infantum IFAT, PCR 25.8 3.9
Mylonakis. ME [93] 2017 Greece . 100 L. infantum PCR . 41
Mohebali. M [94] 2017 Iran stray 103 L. infantum DAT 24.3 .
Metzdorf. IP [95] 2017 Brazil domestic 100 L. infantum PCR . 6
De Mendonça. IL [96] 2017 Brazil domestic 83 L. infantum ELISA 4 .
Lopes. AP [97] 2017 Portugal domestic 102 Leishmania spp. DAT 0 .
Poffo. D [98] 2017 Brazil domestic 88 Leishmania spp. PCR . 0
Akhtardanesh. B [99] 2017 Iran stray 60 L. infantum, L. tropica ELISA, PCR 6.7 16.7
Benassi. JC [100] 2017 Brazil mixed 108 L. infantum PCR . 1.85

Table 2 Subgroup meta-analysis for seroprevalence and PCR prevalence of Leishmania infection in cats 

Characteristics Factors Seropositive PCR positive
n Prevalence (%) (95%CI) I-square (%) p n Prevalence (%) (95%CI) I-square (%) P<0.001
Country Iran 6 17.0 (8.0-28.0) 83.8 0.06 3 6.0 (0.0-21.0) - P<0.001
Egypt 3 6.0 (2.0-10.0) 98.3 NR -
Greece 3 11.0 (2.0-26.0) 95.2 NE -
Italy 10 24.0 (13.0-37.0) 97.1 7 21.0 (10.0-61.0) 99.5
Spain 12 12.0 (4.0-23.0) 97.7 8 6.0 (1.0-14.0) 96.7
Portugal 7 2.0 (1.0-4.0) 70.1 4 11.0 (2.0-26.0) 96.7
Brazil 17 8.0 (3.0-13.0) 93.7 7 5.0 (1.0-11.0) 85.3
Diagnostic test ELISA 12 9.0 (5.0-13.0) 87.8 P<0.001 - - - -
IHAT 3 6.0 (2.0-10.0) 97.5 - - -
IFAT 30 11.0 (6.0-17.0) 97.7 - - -
IFAT, ELISA 6 11.0 (7.0-16.0) 97.5 - - -
WB 3 14.0 (9.0-20.0) 96.6 - - -
DAT 9 10.0 (3.0-19.0) 94.9 - - -
PCR 12 7.0 (3.0-14.0) 93.5 - - -
Breed of cat Stray 22 10.0 (6.0-14.0) 95.2 0.46 7 2.0 (0.0-5.0) 90.5 P<0.001
Domestic 17 7.0 (2.0-16.0) 97.6 9 8.0 (1.0-19.0) 96.8
Mixed 13 15.0 (8.0-24.0) 95.6 16 23.0 (4.0-50.0) 99.4
Leishmania species L. infantum 36 12.0 (8.0-17.0) 95.4 0.09 23 8.0 (4.0-14.0) 95.9 P<0.001
Leishmania spp. 25 8.0 (4.0- 14.0) 96.7 9 15.0 (.5.0-48.0) 99.4
L. infantum, L. tropica 2 10.0 (8.0-12.0) 97.1 2 1.0 (0.0-1.0) -

NR=not reported, NE= not enough studies

The pooled prevalence of FLI based on a random effect meta-analysis ( 𝐼 2 =97.54 , 𝑃<0.001) was estimated at 10% (95% CI: 8%-14%). The estimate of prevalence based on seropositivity (11%), was significantly higher than PCR positivity (10%) (z=0.01, p=0.92) (Figure 2).

Not only funnel plot but also Egger's test found no evidence a heterogeneity among effect size of studies for seroprevalence (b=1.36, p= 0.180 ) and PCR prevalence (b= 0.16 , p= 0.875) (see Figure 3).

Figure 2. Forest plot for the prevalence of Leishmania infection in cats by PCR and serology tests. 

Figure 3. Funnel plot for seroprevalence (a) and PCR prevalence (b) of Leishmania infection in cats. 

Discussion

Zoonotic VL (ZVL) is a zoonosis that occurs in the Old and New World. Research studies on FLI are limited but have become more numerous internationally in recent years, especially in Brazil [23]. In this study the highest numbers of reported studies (30.8%) were found in Brazil, where leishmaniasis is a major public health problem. Brazil is one of the countries with the highest prevalence and widest geographical distribution of the disease [2, 24].

In the current study, the overall prevalence of FLI was estimated to be 10%. The relatively high prevalence of infection in cats demonstrates a similarity with dogs exposed to the leishmanial infections in some endemic areas [25-28 ]. A larger prevalence of L. infantum infection in dogs compared to cats is related to the immune-system differences in these two species and a more efficient Th1 immune response in cats compared to dogs [25,28]. The different FLI reports and the increased cat populations in diverse areas highlight the ability of these animals to maintain and spread the infection in natural and urban environments [28]. Overall, little information is available on the adaptive immune response of cats naturally exposed to L. infantum infection and mechanisms responsible for susceptibility or resistance of feline hosts. However, some evidence suggests that large numbers of clinical cases of FLI are reported in cats that are probably immunocompromised [8], although it seems that asymptomatic cases have an immunocompetent condition and act as cryptic reservoir hosts.

Based on our findings, FLI in the mixed-type /breed cats were higher than in other feline types/-breeds. The role of domestic cats has been controversial in leishmaniasis epidemiology because they live in close contact with humans. Domestic cats can act as primary, secondary or accidental hosts [7, 28].

Seroprevalence rates from 0.9% to 28.5% and PCR detection rates between 0.43% and 30% have been reported in some regions and countries such as Spain, Portugal , France, and Italy in Southern Europe, as well as in North Africa, Iraq, Iran, Turkey and Central and South America, where canine leishmaniasis is endemic [29-36].

In our study, both seroprevalence (24%) and PCR prevalence (21%) of FLI were found higher in Italy than in other countries. Moreover, our data show the high seropraevalence rate (12.2%) of FLI in Southern European countries including Italy, Spain, Portugal, and Greece. However, this could be justified by the increased finding of active cases in cats, development of simple and rapid diagnostic tests and elevated rate of disease prevalence in these countries.

Diagnosis is usually based on the results of cytology, histopathology, immunohistochemistry (IHC), culture, serology and PCR. Apart from the advantages and limitations inherent to each of these methods, their diagnostic value depends on many factors, including the biological sample being used, the reagents and the particular technique employed.

In our study the most common diagnostic laboratory method was IFAT (38.5%). IFAT and ELISA are the most common serological techniques used for diagnosis and for clinical and research studies on canine and feline leishmanial infections [10-16]. In areas endemic for Trypanosoma spp. or other Leishmania spp., cross reactions with L. infantum must be taken into account for interpretation of serological tests [16]. However, some attention is needed before confirming leishmaniasis with IFAT in cats, whereas cats that present clinical symptoms for leishmaniasis but are found negative by IFAT should be subjected to other serological tests or complementary diagnostic tools such as WB and PCR [7]. WB analysis, a qualitative serological method, distinguishes the molecular weight of the L. infantum antigens stimulating antibody production, but is less frequently used for the diagnosis of leishmaniasis [37]. One potential application of the WB method is the discrimination between subclinical and clinical infections [38].

Three different species of Leishmania have been found in cats in Brazil: L. amazonensis [39], L. braziliensis [40] and L. infantum [34, 41]. Five Leishmania species have been reported in cats worldwide, although most cases involved L. infantum [8]. This is in agreement with our findings in the current study in which approximately 63% of species were L. infantum.

In conclusion, our data provide substantial evidence that cats can be considered sentinel reservoir hosts at least in endemic foci of zoonotic visceral leishmaniasis. Moreover, the current data demonstrate enzootic stability of FLI in several countries of the world particularly in some European countries. Furthermore, our results show the most common lab method for diagnosing FVL is the IFA test. In general, control of cat populations is recommended to reduce the transmission of Leishmania spp. among human populations in the endemic areas especially among nomadic tribes [42].

Abbreviations

Not applicable.

Acknowledgments

The authors are grateful to the vice Chancellor of Research and Technology, Mazandaran University of Medical Sciences.

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Availability of data and material All data extracted and or analyzed during this study are included in this published article.

Funding This publication was supported in part by the Coordination for the Improvement of Higher Education Personnel (CAPES) through “Programa Editoração CAPES” - call No. 13/2016, grant No. 0722/2017, record No. 88881.142062/2017-01 and by the National Council for Scientific and Technological Development (CNPq) and Coordination for the Improvement of Higher Education Personnel (CAPES) through “Programa Editorial CNPq/CAPES” call No. 18/2018, grant No. 404770/2018-5. Funding for this systematic review was provided by the vice Chancellor of Research and Technology, Mazandaran University of Medical Sciences (grant number: 2794).

Ethics approval and consent to participate Not applicable.

Consent for publication Not applicable.

Received: February 27, 2019; Accepted: May 08, 2019

*Correspondence: mahdifakhar53@gmail.com

Competing interests

The authors declare that they have no competing interests.

Authors’ contributions

SA wrote the preliminary draft of the manuscript and extracted all data. MF designed all steps of the study and contributed to writing and revising of the final manuscript. SHT contributed to meta-analysis of the extracted data. All authors read and approved the final manuscript.

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