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Real-Time RT-PCR Assay to Detect Granada Virus and the Related

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Real-Time RT-PCR Assay to Detect Granada Virus and the Related Davó et al. Parasites Vectors (2020) 13:270 https://doi.org/10.1186/s13071-020-04110-5 Parasites & Vectors METHODOLOGY Open Access Real-time RT-PCR assay to detect Granada virus and the related Massilia and Arrabida phleboviruses Laura Davó1,2, Laura Herrero1, Maria Paz Sánchez‑Seco1, Nuria Labiod1, David Roiz3,6, Elena Gómez‑Díaz3,4, Lourdes Hernandez1, Jordi Figuerola3,5 and Ana Vázquez1,5* Abstract Background: Granada virus belongs to the genus Phlebovirus within the Naples serocomplex and was detected for the frst time in sand fies from Spain in 2003. Seroprevalence studies have revealed that Granada virus may infect humans with most cases being asymptomatic. Moreover, recent studies in vector samples revealed that the related Massilia and Arrabida phleboviruses could be also circulating in Spain. The objective of this study was to develop and assess a new sensitive real‑time RT‑PCR assay for Granada virus diagnosis able to detect the related phleboviruses Massilia and Arrabida. Methods: Two specifc primers and one unique probe to detect Granada, Massilia and Arrabida viruses, without diferentiating between them, were designed targeting the conserved L‑segment of their genome. Sensitivity was assessed using 10‑fold serial dilutions of quantifed in vitro DNA samples. Specifcity was evaluated by testing diferent genomic RNA extracted from other representative phleboviruses. The new assay was used for virus detection in sand fies collected in 2012 from the Balearic Archipelago, a touristic hotspot in the Mediterranean. Results: The real‑time RT‑PCR assay exhibited a sensitivity per reaction of 19 copies for Granada and Arrabida, and 16 copies for Massilia. No other related phleboviruses were detected. From the 37 pools of sand fy samples studied from four diferent Balearic Islands, we detected one positive in the island of Cabrera. Conclusions: To our knowledge, the method described here is the frst real‑time RT‑PCR designed to detect Granada virus and the related Massilia and Arrabida phleboviruses. The study demonstrated that this is a rapid, robust and reli‑ able assay for the accurate diagnosis of human infections as well as for virus surveillance in vectors. Keywords: Real‑time RT‑PCR, Granada virus, Massilia virus, Arrabida virus, Diagnosis, Surveillance Background protein (N) and non-structural proteins (NSs); the M Sand fy-borne viruses of the genus Phlebovirus (fam- segment encodes two surface glycoproteins (G1 and G2) ily Phenuiviridae) are important emerging pathogens in and non-structural proteins (NSm), and the L segment Europe and are widely distributed [1]. All members of encodes the RNA-dependent RNA polymerase. Te cod- this genus are enveloped and the genome is composed ing strategy seems to be common to all members of the of three negative RNA segments, S (small), M (medium) family [2]. Until now, ten viral species defned by the and L (large). Te S segment encodes the nucleocapsid sero-neutralization tests as well as several tentative spe- cies have been described [3], although their real medical *Correspondence: [email protected] 1 Centro Nacional de Microbiología, Instituto de Salud Carlos III, importance has not been fully addressed yet. Te sand fy 28220 Madrid, Spain fever Naples (SFNV) and Sicilian (SFSV) viruses, cause Full list of author information is available at the end of the article a “3-day fever”, characterized by fu-like symptoms, and © The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Davó et al. Parasites Vectors (2020) 13:270 Page 2 of 7 Toscana virus (TOSV) may produce neuroinvasive infec- B genotype, three isolates strongly related to Italian Arbia tion (encephalitis and meningoencephalitis) [1]. TOSV is virus (ARBV), and one isolate of a novel putative phlebo- endemic in the Mediterranean countries, where the Phle- virus related to the recently characterized ARRV in South botomus vectors are present. Most TOSV infections have Portugal, tentatively named Arrabida-like virus. been reported in Italy, France and Spain and sporadically Despite the increasing evidence that these viruses cir- in Portugal, Greece, Cyprus, Turkey and Tunisia. culate in Spain, only human disease has been directly Recent reports suggest that other sand fy-transmitted associated with TOSV in diferent regions (Murcia, phleboviruses may be involved in human disease [1, 4, Madrid, Catalonia, Andalusia and the Mediterranean 5]. Tis is the case for Granada virus (GRV), a phlebo- coast) [12–14]. Two human serological studies carried virus detected for the frst time in sand fies captured in out in Granada (Spain) have reported the GRV infective 2003 and 2004 in the province of Granada (southeast capacity. Collao et al. [6] revealed the presence of spe- Spain). Phylogenetic analysis of the complete genome cifc GRV-neutralizing antibodies in sera from healthy revealed that GRV belongs to the Sand fy fever Naples individuals collected in 2003 (10.8% of IFA positives, Complex (SFNC) and it is probably a natural reassor- 1.8% of the total analyzed samples). In a diferent study, tant of the Massilia virus (MASV), donor of the L and S GRV seroprevalence was found to be 15.8% by IFA with GRV genome segments, with a yet unidentifed phlebovi- 2.8% of neutralizing antibodies (18% of IFA positives). rus as donor of the M segment [6]. MASV was detected Moreover, anti-GRV IgM antibodies were detected and isolated for the frst time from Phlebotomus perni- (6.6%) in sera from patients with symptoms of unknown cious captured in 2005 in Marseille and Nice [7] and later etiology [5]. Terefore, the authors concluded that GRV from P. perniciosus captured in 2007–2008 in Portugal may infect humans but that most cases would prob- (Arrabida region) [8]. In the same study carried out in ably be asymptomatic. Occasionally, mild GRV infec- Portugal, a new phlebovirus named Arrabida (ARRV) tions may occur, usually as self-limited febrile illnesses was described [9]. ARRV was also phylogenetically clas- accompanied by other signs and symptoms (exanthema sifed as member of the SFNC showing a high nucleotide and/or acute respiratory infection) [5]. Tese infections identity with MASV, GRV and Punique virus (PUNV). most probably take place during the warm months of Whereas the sequences on the L and S segments of the year, which occurs with infections caused by other ARRV were closely related to MASV and GRV, the glyco- phleboviruses in Mediterranean countries. Whether proteins (M segment) were most closely related to PUNV, GRV or the related MASV and ARRV could be circu- detected in sand fies from Tunisia in 2008, opening the lating in other areas or countries and/or causing mild question whether ARRV can be considered as a reassor- febrile diseases needs to be determined. Until now only tant between MASV/GRV and PUNV [9]. Terefore, the a real-time RT-PCR designed in the nucleoprotein gene closely related MASV, GRV and ARRV shared the L and (S segment) has been published to detect MASV spe- S segments but difered for the M segment due to a reas- cifcally [7]. sortment process with diferent phleboviruses. All these data strongly support the need for new In Spain, a few studies conducted in sand fies have molecular assays that allow the specifc detection of GRV, revealed the presence and co-circulation of several MASV and ARRV to improve current diagnostic meth- phleboviruses belonging to the SFNC (such as TOSV, ods and to be used in vector-borne diseases surveillance GRV and ARRV) and Salehabad virus species Complex programmes for these phleboviruses. Terefore, the main (such as Arbia virus). As mentioned above, GRV has objective of this study was to develop the frst real-time been detected in Granada but sequences resembling RT-PCR assay able to detect GRV with high sensitivity, the L-segment of GRV and MASV have been reported that at the same time might also detect the related phle- in other areas of Spain such as the Balearic Archipelago boviruses MASV and ARRV. Tis assay will be very useful (Ibiza island) and Catalonia. However, without further in studies about the possible implications of these viruses sequence information for the M segment, they cannot be in human disease and in virus surveillance programmes. unequivocally assigned to GRV or MASV strains. Fur- thermore, similar sequences of viruses belonging to the Methods Salehabad virus species Complex have been described Primer and probe design in sand fies from Granada [6]. TOSV has also been Representative sequences from the three phleboviruses detected in sand fies in Barcelona and Granada [6, 10]. genomic segments (S, M and L) were obtained from In a recent study carried out in Madrid, six viral isolates the NCBI GenBank database and were aligned using were obtained from P. perniciosus captured in 2012 and the Clustal W program [15].
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