\\n\\n
Released this past November, the list is based on data collected from the Web of Science and highlights some of the world’s most influential scientific minds by naming the researchers whose publications over the previous decade have included a high number of Highly Cited Papers placing them among the top 1% most-cited.
\\n\\nWe wish to congratulate all of the researchers named and especially our authors on this amazing accomplishment! We are happy and proud to share in their success!
\\n"}]',published:!0,mainMedia:null},components:[{type:"htmlEditorComponent",content:'IntechOpen is proud to announce that 179 of our authors have made the Clarivate™ Highly Cited Researchers List for 2020, ranking them among the top 1% most-cited.
\n\nThroughout the years, the list has named a total of 252 IntechOpen authors as Highly Cited. Of those researchers, 69 have been featured on the list multiple times.
\n\n\n\nReleased this past November, the list is based on data collected from the Web of Science and highlights some of the world’s most influential scientific minds by naming the researchers whose publications over the previous decade have included a high number of Highly Cited Papers placing them among the top 1% most-cited.
\n\nWe wish to congratulate all of the researchers named and especially our authors on this amazing accomplishment! We are happy and proud to share in their success!
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He joined University of Veterinary and Animal Sciences during 2003 as Assistant Professor where he was later selected and appointed as Associate Professor and Professor, in 2006 and 2011 respectively. His research focus is on selection and breeding of large and small ruminants. He also supervises and evaluates postgraduate research to ensure successful and timely completion of the projects focusing on genetic improvement, enhancing breeding efficiency and production enhancement of farm animals. In addition, he participates and conducts trainings, workshops, conferences and seminars, and writes scientific publications to disseminate knowledge and techniques to the researchers and livestock producers about various areas of animal husbandry for improving behaviour, health, growth, fertility and production of livestock. 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Dominguez Vara"}]},{id:"66091",title:"Goat and Sheep Milk as Raw Material for Yogurt",slug:"goat-and-sheep-milk-as-raw-material-for-yogurt",totalDownloads:581,totalCrossrefCites:0,authors:[{id:"190314",title:"Prof.",name:"António",surname:"Monteiro",slug:"antonio-monteiro",fullName:"António Monteiro"},{id:"287922",title:"MSc.",name:"Susana",surname:"Matos",slug:"susana-matos",fullName:"Susana Matos"},{id:"287924",title:"MSc.",name:"Soraia",surname:"Loureiro",slug:"soraia-loureiro",fullName:"Soraia Loureiro"},{id:"294629",title:"Prof.",name:"Paula",surname:"Correia",slug:"paula-correia",fullName:"Paula Correia"}]},{id:"67758",title:"Optimal Procedures to Valorize High-Quality Traditional Dairy Products",slug:"optimal-procedures-to-valorize-high-quality-traditional-dairy-products",totalDownloads:319,totalCrossrefCites:0,authors:[{id:"83688",title:"Dr.",name:"Margherita",surname:"Caccamo",slug:"margherita-caccamo",fullName:"Margherita Caccamo"},{id:"270709",title:"BSc.",name:"Rosario",surname:"Petriglieri",slug:"rosario-petriglieri",fullName:"Rosario Petriglieri"},{id:"270710",title:"MSc.",name:"Catia",surname:"Pasta",slug:"catia-pasta",fullName:"Catia Pasta"}]}],productType:{id:"1",title:"Edited Volume",chapterContentType:"chapter",authoredCaption:"Edited by"},personalPublishingAssistant:{id:"225753",firstName:"Marina",lastName:"Dusevic",middleName:null,title:"Ms.",imageUrl:"https://mts.intechopen.com/storage/users/225753/images/7224_n.png",email:"marina.d@intechopen.com",biography:"As an Author Service Manager my responsibilities include monitoring and facilitating all publishing activities for authors and editors. 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BoHV-1 is a significant cofactor in the polymicrobial disease referred to as bovine respiratory disease complex (BRDC), which is the most important disease of cattle. BoHV-1 infection impairs cell-mediated immunity, CD8+ T cell recognition of infected cells, and induces apoptosis in CD4+ T cells [4]. Viral proteins, VP8, bICP0 and bICP27, inhibit interferon dependent transcription [4, 5, 6, 7, 8]. Infection also erodes mucosal surfaces of the upper respiratory tract, which promotes establishment of the bacterial pathogen, Mannheimia haemolytica (MH) in the lower respiratory tract [9]. BoHV-1 productive infection increases neutrophil adhesion and activation [10], thus amplifying the pathogenic potential of MH. MH, a gram negative bacterium, exists as normal flora within the upper respiratory tract of healthy ruminants [11]. Stress and/or co-infections disrupt this commensal relationship; consequently MH becomes the predominant organism that causes life-threatening bronchopneumonia in BRDC cases [9]. BRDC is the most important disease in cattle because it costs the US cattle industry more than one billion dollars in losses each year [9, 12, 13]. A BoHV-1 entry protein is a BRDC susceptibility gene for Holstein calves [14] confirming BoHV-1 is a significant BRDC cofactor.
\nLike most alpha-herpesvirinae subfamily members, including human herpes simplex virus 1 (HSV-1) and HSV2, BoHV-1 initiates acute infection on mucosal surfaces [1, 2, 3]. High levels of infectious virus are produced; consequently BoHV-1, HSV-1, or HSV-2, spread to the peripheral nervous system via cell-to-cell spread. Latency is subsequently established in sensory neurons, but periodically reactivates from latency, and thus is widespread in cattle throughout the world. Reactivation of the virus from the latent state is initiated by external stimuli (e.g. stress and immunosuppression). During reactivation, viral gene expression is stimulated and infectious virus is produced and transported back to mucosal surfaces. The ability of alpha-herpesvirinae subfamily members to reactivate from the latent state is critical for virus transmission. Regulation of the complex virus host interactions controlling the latency-reactivation cycle is not well understood, which hinders developing therapeutic strategies that prevent reactivation from latency.
\nBoHV-1 is an excellent model to study these events because the natural host can be used and the synthetic corticosteroid dexamethasone (DEX) consistently initiates reactivation from latency in infected calves [2]. We have used experimentally infected calves treated with DEX to initiate reactivation from latency in order to identify virus-host interactions important for the latency-reactivation cycle. These studies identified host cellular factors and pathways that may be crucial for latency maintenance [15] and reactivation [16]. The following discussion focuses on the mechanisms by which BoHV-1 “escapes” a latent infection following a stressful stimulus and subsequently successfully reactivates from latency. Certain steps during BoHV-1 reactivation from latency are likely to be similar during reactivation of latency of other alpha-herpesvirinae subfamily members.
\nAcute infection of calves induces programmed cell death, inflammation and high levels of virus production [1, 2, 3]. BoHV-1 genes are expressed in three distinct phases during acute infection or productive infection of cultured cells: immediate early (IE), early (E), or late (L) [1, 2, 3]. IE gene expression is specifically stimulated by viral protein 16 (VP16), a tegument protein. IE transcription unit 1 (IEtu1) encodes two transcriptional regulatory proteins, BoHV-1 infected cell protein 0 (bICP0) and bICP4, because a single IE transcript is differentially spliced and subsequently translated into bICP0 or bICP4 (Figure 1). The bICP0 protein is also translated from an E mRNA (E2.6) because a separate E promoter drives expression of the bICP0 E transcript.
\nLocation of IE transcripts and promoters actively expressed during productive infection. The mRNA IE/4.2 encodes the bICP4 protein and IE/2.9 encodes the bICP0 protein [58, 59, 72]. A single IE promoter activates expression of IE/4.2 and IE/2.9 and is designated IEtu1 (black rectangle). E/2.6 is the early transcript that encodes bICP0 and an early promoter activates expression of this transcript (bICP0 E pro; gray rectangle). All bICP0 protein-coding sequences are contained in Exon 2 (e2). The origin of replication (ORI) separates IEtu1 from IEtu2. The IEtu2 promoter (IEtu2 pro) regulates expression of the IE1.7 mRNA that is translated into the bICP22 protein. Solid lines in the transcript position map represent exons (e1, e2, or e3) and dashed lines denote introns.
During acute infection of calves, infectious virus particles enter the peripheral nervous system via cell–cell spread. If infection is initiated within the oral, nasal, or ocular cavity, the primary site for latency is sensory neurons located in trigeminal ganglia (TG) [1, 2, 3]. Viral gene expression and infectious virus are detected in TG from 2 to 6 days after infection. Lytic cycle viral gene expression is then extinguished, a significant number of infected neurons survive, and these neurons harbor viral genomes, which is operationally defined as the establishment of latency. Abundant expression of the BoHV-1 encoded latency related (LR) gene occurs in latently infected neurons, but infectious virus is not detected (maintenance of latency) [1, 2, 3]. LR-RNA is anti-sense to and overlaps the BoHV-1 infected cell protein 0 (bICP0) gene. The LR gene has two open reading frames (ORF1 and ORF2), and two reading frames lacking an initiating methionine (RF-B and RF-C). In addition, the LR gene encodes two micro-RNAs that interfere with bICP0 expression in transfected cells [17]. A LR mutant virus strain with three stop codons at the N-terminus of ORF2 exhibits diminished clinical symptoms, and reduced virus shedding from the eye, TG, or tonsils of infected calves [1, 2, 3]. ORF1, ORF2, and RF-C are expressed when bovine cells are infected with wild-type or the LR-rescued virus, but these proteins have reduced or no expression following infection with the LR mutant virus [1, 2, 3]. Wild-type (wt) BoHV-1, but not the LR mutant virus, reactivates from latency after treatment with the synthetic corticosteroid DEX. The anti-apoptosis activity of ORF2 is predicted to increase the survival of infected neurons and thus would be important for the latency-reactivation cycle [1, 2, 3].
\nRecent studies demonstrated that during latency, the canonical Wnt/β-catenin signaling is active and ORF2 appears to be important for maintaining this important signaling pathway [15, 18]. Although dysregulation of the Wnt/β-catenin signaling is frequently associated with many types of cancer [19, 20], this signaling pathway has the potential to promote the establishment and maintenance of latency in sensory neurons because it enhances cell survival, axonal growth, and directs axons to their proper synaptic targets [21, 22, 23, 24, 25].
\nIncreased corticosteroid levels, due to increased stress, correlates with increasing the incidence of BoHV-1 reactivation from latency [1, 2, 3]. DEX can also stimulate productive infection [26], and initiate reactivation from latency in calves or rabbits latently infected with BoHV-1 [1, 2, 3]. Six hours after DEX treatment lytic cycle viral RNA expression is detected in neurons of latently infected calves [27, 28]. Certain lytic cycle viral proteins, bICP0 and VP16 for example, are readily detected in TG neurons within hours after DEX treatment [29, 30]. The glucocorticoid receptor (GR) and mineralocorticoid receptor (MR), which are present in sub-populations of sensory neurons [31, 32], are activated by interacting with corticosteroids. The GR is frequently detected in TG neurons that express bICP0 or VP16 [31, 32]. IEtu1 promoter activity is stimulated by the GR and the synthetic corticosteroid DEX because there are two consensus GREs in the promoter [26] suggesting this promoter is activated by the GR and/or MR following stressful stimuli. Since the IEtu1 promoter drives expression of two viral transcriptional regulatory proteins (bICP0 and bICP4; Figure 1), activation of this promoter may stimulate productive infection in certain latently infected neurons.
\nDEX treatment of latently infected calves induces apoptosis of T cells that persist in TG after infection [27]. T cells also persist in TG of humans or mice latently infected with HSV-1 and may promote maintenance of latency [33, 34, 35, 36, 37]. Within 3 h after DEX treatment, 11 cellular genes are induced more than ten fold in TG [16]. Pentraxin 3, a regulator of innate immunity and neuro-degeneration, is stimulated 35–63 fold at 3 or 6 h after DEX treatment. Furthermore, expression of a soluble Wnt antagonist, Dickkopf-1 is induced more than 10 fold [15, 16]. Dickkopf-1 is responsible for stress-induced neuronal death [38, 39] indicating there is a correlation between disrupting the Wnt signaling pathway and activation of lytic cycle viral gene expression during reactivation. Two transcription factors, promyelocytic leukemia zinc finger (PLZF) and Slug are induced more than 15-fold 3 h after DEX treatment. PLZF or Slug stimulates BoHV-1 productive infection 20-fold or 5-fold respectively, and Slug stimulates the late glycoprotein C promoter more than 10-fold. Additional DEX induced transcription factors, SPDEF (Sam-pointed domain containing Ets transcription factor), Kruppel-like transcription factor 15 (KLF15), KLF4, KLF6, and GATA6, stimulate productive infection and certain key viral promoters.
\nThe finding that four KLF family members (KLF4, KLF6, KLF15, and PLZF) are stimulated during DEX induced reactivation from latency is intriguing because KLF family members resemble the SP1 transcription factor family and both family of transcription factors interact with guanine-cytosine (GC) rich motifs, reviewed in [40, 41]. Genomes of alpha-herpesvirinae subfamily members, including BoHV-1, are GC rich and many viral promoters contain Sp1 consensus binding sites as well as other GC rich motifs [40]. In fact, HSV-1 gene expression is activated by Sp1 [42]. HSV-1 and probably BoHV-1 genomes exist as silent chromatin during latency, [43]: however, HSV-1 DNA is associated with unstable chromatin during productive infection [44, 45, 46]. Regardless of the stimulus that initiates reactivation from latency, silent viral heterochromatin must be converted into an actively transcribing template for reactivation from latency to be successful suggesting cellular transcription factors initially stimulate lytic cycle viral gene expression.
\nTo test whether the GR and certain stress-induced transcription factors can cooperate to stimulate viral transcription, the IEtu1 promoter and BoHV-1 DNA fragments (less than 400 bp) containing potential GR and KLF binding sites were identified and examined for transcriptional activation by stress-induced transcription factors. The rational for testing intergenic regions of the BoHV-1 genome is the viral genome contains more than 100 putative GRE binding sites [26] and a subset of GREs in cellular chromatin can activate transcription from greater than 5 kb to the nearest promoter [47]. KLF15 cooperated with the GR to stimulate the IEtu1 promoter activity and productive infection [48]. Furthermore, intergenic regions within the unique long 52 gene (UL-52; component of DNA primase/helicase complex), bICP4, IEtu2 that expresses the regulatory protein (bICP22), and unique short region were stimulated by KLF15 and the GR. In contrast to KLF15, the other stress-induced transcription factors only have a modest effect on IEtu1 promoter activity. The GR and KLF15 interact with sequences within wild-type IEtu1 GREs and UL-52 fragment, but not GRE mutants. Co-immunoprecipitation studies indicated that KLF15 and the GR are stably associated with each other. Interestingly, the GR and KLF15 can synergistically regulate gene expression by a feed-forward transcription loop [49, 50, 51]. Hallmarks of a feed-forward loop are a primary factor (GR in this example) induces expression of a second factor, KLF15 [16, 49, 50, 51, 52, 53, 54], and the two factors synergistically activate expression of genes in a specific pathway. Adipogenesis [55] and amino acid metabolizing enzymes are also synergistically regulated by the GR and KLF15 [50, 51]. In summary, these studies suggest that activation of BoHV-1 gene expression during DEX induced reactivation from latency is, in part, regulated by a feed-forward transcription loop containing the GR and KLF15.
\nTo test whether KLF6 and the activated GR have a cooperative effect on productive infection, a mouse neuroblastoma cell line (Neuro-2A) was cotransfected with gCblue genomic DNA and KLF6 and/or the GR. The gCblue virus grows to similar titers as the wt parental virus and expresses the Lac Z gene from the gC locus during productive infection (Figure 2A). Neuro-2A cells were used for these studies because they have neuronal like properties [56], can be readily transfected, and are semi-permissive for BoHV-1 [57]. Neuro-2A cells were transfected with gCblue DNA instead of infecting cells because VP16 and other viral regulatory proteins in the virion particle can diminish the stimulatory effects of DEX on productive infection (data not shown). KLF6 and the GR plus DEX treatment increased the number of β-Gal+ Neuro-2A cells more than 4-fold, which was significantly higher than GR + DEX and the GR or KLF6 alone (Figure 2A and B). Cotransfection of gCblue and the GR + KLF6 stimulated productive infection 2-fold even when cultures were not treated with DEX, which was similar to the effects observed when gCblue genomic DNA was cotransfected with the GR and DEX treatment.
\nKLF6 and the GR cooperate to stimulate productive infection. Neuro-2A cells were transfected with 2 ug BoHV-1 gCblue genomic DNA and where indicated a plasmid that expresses the mouse GR protein (1.0 ug DNA) and/or KLF6 (0.5 ug DNA) using Lipofectamine 3000 (catalog no. L3000075; Invitrogen). A mouse GR expression vector was obtained from Dr. Joseph Cidlowski, NIH and the KLF6 expression vector was obtained from Bin Guo (North Dakota State University). Neuro-2A cells were grown in Eagle’s minimal essential medium (EMEM) supplemented with 10% FCS, penicillin (10 U/ml), and streptomycin (100 μg/ml). The BoHV-1 mutant containing the β-Gal gene in place of the viral gC gene was obtained from S. Chowdury (LSU School of Veterinary Medicine) (gCblue virus) and stocks of this virus grown in bovine kidney cells (CRIB). The gCblue virus grows to similar titers as the wt parental virus and expresses the Lac Z gene. Procedures for preparing genomic DNA were described previously [73]. To maintain the same amount of DNA in each sample, empty vector was included in samples. Cells were incubated with stripped fetal calf serum 24 h after transfection and then treated with water soluble DEX (10 μM; Sigma, D2915). At 40 h after transfection, cells were fixed and stained for counting the number of β-Gal+ cells as previously described [48]. Representative cultures stained for Lac Z expression are shown in (Panel A). The value for the control (gCblue virus DNA treated with PBS after transfection) was set at 1. The results from DEX treated cultures were compared to the control and are an average of three independent studies (Panel B). The asterisk denotes a significant difference between the control and samples transfected with the GR or KLF6 and treated with DEX (P < 0.05) using the student’s T test.
Transient transfection studies were performed in Neuro-2A cells to test whether KLF6 and the GR synergistically trans-activate the IEtu1 promoter because this promoter contains two consensus GR binding sites (Figure 3A) required for DEX mediated transactivation [26]. The IEtu1 promoter drives IE expression of bICP0 and bICP4, the most important viral transcriptional regulatory proteins encoded by BoHV-1 [58, 59, 60] (Figure 1). The IEtu1 collapsed promoter construct (Figure 3A) was initially used to test whether sequences adjacent to the GREs were trans-activated by KLF6 and the GR. The full-length IEtu1 promoter construct contains extensive sequences downstream from the start site of transcription and has sequences between the TATA box and the GREs that are important for KLF trans-activation [16]: consequently the collapsed IEtu1 collapsed promoter construct was used for these studies. We have consistently found that the GR+ DEX stimulated promoter activity more than 15 fold and GR + KLF6 + DEX stimulated promoter activity more than 50 fold (Figure 3B). RU486 antagonizes corticosteroid/GR signaling [61, 62] and as expected RU486 significantly reduced the ability of KLF6 and GR to transactivate the IEtu1 collapsed construct.
\nKLF6 and the GR cooperatively transactivate the IEtu1 promoter. Panel A: The full length IEtu1 promoter was cloned as an XhoI-SphI restriction site. Start site of transcription (arrow), TATA box, binding site for VP16/Oct1 complex is denoted as TAATGARAT [74], and location of GRE#1 and GRE#2 (black and grey rectangles) are shown. Numbers are genomic coordinates of the first nucleotide of each respective motif or restriction enzyme site. GenScript synthesized the IEtu1 collapsed promoter construct and genomic coordinates are included: this fragment is inserted at KpnI and HindIII restriction sites of pGL3-Basic Vector. A 280 bp fragment (IEtu1 GREs) was cloned into the pGL3-Promoter Vector at unique KpnI and XhoI restriction sites [48]. Panel B: Neuro-2A cells were transfected with 0.5 ug DNA of the IEtu1 collapsed promoter (Collapsed) or IEtu1 GREs plasmid (GREs) and where indicated a plasmid that expresses the mouse GR protein (1.0 ug DNA) and/or KLF6 (0.5 ug DNA). To maintain equal plasmid amounts in the transfection mixtures, the empty expression vector was added as needed. Designated cultures were treated with water-soluble DEX (10 uM; Sigma) or DEX + RU486 (10 uM; Sigma) at 24 h after transfection. At 48 h after transfection, cells were harvested, and protein lysate subjected to dual-luciferase assay using a commercially available kit (E1910; Promega). Luminescence was measured by using a GloMax 20/20 luminometer (E5331; Promega). All transfections contained a plasmid encoding Renilla luciferase under the control of a minimal herpesvirus thymidine kinase (TK) promoter (0.050 ug DNA) as an internal control. Promoter activity in the empty luciferase vector (pGL3-Promoter Vector) was normalized to a value of 1 and fold activation for other samples presented. The results are the average of three independent experiments and error bars denote the standard error. A single asterisk denotes a significant difference (P < 0.05) between the IEtu1 collapsed or IEtu1 GREs when cotransfected with GR and KLF6 plus DEX treatment when compared to promoter activity of the respective promoter construct cotransfected with GR plus DEX treatment. Two asterisks denote a significant difference (P < 0.05) between the IEtu1 collapsed or IEtu1 GREs when cotransfected with GR and KLF6 and DEX treatment versus the same study conducted but treated with DEX+ RU486 or no DEX. A (#) denotes a significant difference between IEtu1 collapsed or IEtu1 GREs cotransfected with the GR and treated with DEX when compared to the same luciferase reporter cotransfected with GR and treated with DEX+ RU486 or no DEX. Statistical analysis was performed using the Student t test.
A 280 bp fragment containing both GREs within the IEtu1 promoter and flanking sequences was cloned upstream of the minimal SV40 early promoter and designated IEtu1 GREs [48] (Figure 3A). This construct was examined for its ability to be activated by KLF6 and the GRE as a comparison to the IEtu1 collapsed promoter construct. KLF6 and the GR consistently stimulated the IEtu1 GREs construct approximately 16-fold whereas the GR + DEX stimulated this construct only 6-fold (Figure 3B). RU486 also significantly reduced the ability of KLF6 and GR to transactivate the IEtu1 GREs construct. Although the IEtu1 collapsed construct was trans-activated more by the GR + KLF6+ DEX relative to the IEtu1 GREs construct, the overall trends were similar.
\nTo identify sequences in the IEtu1 GREs that mediate transactivation by KLF6 and the GR, constructs containing site-specific mutations in GRE#1, GRE#2, and KLF like binding sites were compared to the wt IEtu1 GREs (Figure 4A–C) [48]. Mutagenesis of GRE1 (∆GRE1) or both GREs and the KLF binding sites (∆2xGRE∆KLF) significantly reduced cooperative activation by KLF6 and the GR when DEX was added to the cultures (Figure 4D). Mutagenesis of the 2 putative KLF sites (∆KLF) had no effect on trans-activation by KLF6 and the GR when cultures were treated with DEX. As previously reported [48] and shown in Figure 4D, the effect of DEX and the GR was significantly reduced when GRE#1 (∆GRE1) was mutated and abolished when both GREs and putative KLF sites (∆2xGRE∆KLF) were mutated. In summary, mutagenesis of the GRE#1 significantly reduced synergistic transactivation by KLF6 and the GR when cultures were treated with DEX.
\nIdentification of sequences in the IEtu1 GREs that are responsive to KLF6 and the GR. Panel A: Schematic of IEtu1 promoter and location of TATA box, TAATGARAT motif, and the two GREs. Numbers denote the genomic location of the first nucleotide of each motif. Panel B: Schematic of 280 bp fragment that contains the IEtu1 GREs and putative KLF-binding sites. Panel C: Nucleotide sequence of motifs in the IEtu1 GREs and mutations that were prepared. Mutations in GRE#1 and GRE#2 were previously described and were shown to disrupt trans-activation by the GR in transient transfection studies [26, 48]. Panel D: Neuro-2A cells were transfected with the designated luciferase plasmid (0.5 ug DNA) and where indicated a plasmid that expresses the mouse GR protein (1.0 ug DNA) and/or KLF6 (0.5 ug DNA). To maintain the same amount of DNA in each sample, empty vector was included in certain samples. Cultures were then treated with 2% “stripped” fetal calf serum and then water soluble DEX (10 uM; Sigma) at 24 h after transfection. At 48 h after transfection, cells were harvested, and protein lysate was subjected to dual-luciferase assay as described in Figure 3B. The level of promoter activity in the empty luciferase vector (pGL3-Promoter Vector) was normalized to a value of 1 and the fold activation values for other samples are presented. The results are the average of three independent experiments and error bars denote the standard error. The asterisks denote a significant difference (P < 0.05) between IEtu1 GREs (wt) and the ∆KLF mutant when compared to the other mutants (∆GRE1, ∆GRE1∆KLF and ∆2XGRE∆KLF) after cotransfection with GR + KLF6 and treated with DEX, as determined by the Student t test.
To test whether KLF6 and the GR interact with sequences located in the IEtu1 GREs, chromatin immuno-precipitation (ChIP) studies were performed in Neuro-2A cells. Cells were transfected with the promoter construct containing the IEtu1 GREs followed by treatment with Vehicle or DEX. As shown in Figure 5A, ChIP studies demonstrated that the GR and KLF6 occupied the GRE region of the IEtu1 GREs (lanes 2–4). No specific PCR product was amplified from ChIPs of cells transfected with the IEtu1 GREs from IPs using the control IgG (IgG C Panel) or cells transfected with the ∆2XGRE∆KLF construct (Figure 5C and D). Treatment with DEX had little effect on the levels of GR bound to IEtu1 GRE sequences (Figure 5A and B); however, we detected an increase in KLF6 bound to the IEtu1 GREs when cotransfected with KLF6 and GR in the absence of DEX when compared to DEX treatment. At least three reasons may have led to this unexpected result. First, we suggest that low levels of corticosteroids in media containing 2% stripped fetal bovine serum may be a reason why the GR was associated with the IEtu1 GREs in the absence of DEX. Secondly, independent studies concluded that the GR can be associated with GREs in the absence of corticosteroids [61, 63]. Thirdly, treatment of cells with DEX reduces GR levels and the availability of GR to bind to DNA [26, 64]. All input samples (whole lysate prior to IP) yielded the specific 107 bp PCR product except Neuro-2A cells not transfected with the IEtu1 GREs construct (Figure 5A, Input panel, lane 1). In summary, the GR and KLF6 were specifically recruited to IEtu1 GRE sequences when the GREs were intact.
\nInteraction between GR and KLF6 with IEtu1 GREs. Neuro-2A cells were cotransfected with the IEtu1 GREs construct (Panel A; 4 ug DNA) or ∆2XGRE∆KLF fragment (Panel C; 4 ug DNA), KLF6 expression plasmid (1.5 ug DNA) and/or the GR plasmid (2 ug DNA). Empty vector was added to maintain the same concentration of DNA in each transfection assay. Designated cultures were treated with DEX (10 uM; Sigma) 4 h before cells were harvested. ChIP studies were performed as previously described in Neuro-2A cells [48]. Polymerase chain reaction (PCR) was performed using primers that amplify the IEtu1 GREs and ∆2XGRE∆KLF: forward primer is 5′- CCCACTTTTGCCTGTGTG-3′ and reverse primer is 5’-TTTTCCTCCTCCTTCCCC-3′. These primers yield a product of 107 base pairs. Input was 10% of the total DNA: protein complexes that used for IP and then PCR performed using PCR primers described in the materials and methods. Arrows denote the specific PCR product, 107 bp for IEtu1 GREs or for ∆2XGRE∆KLF, and the circle denotes the position of primer dimers. Estimation of the level of binding to wild-type IEtu1 GREs sequences (Panel B) or ∆2XGRE∆KLF (Panel D) is shown. The results are representative of three independent studies.
Co-immunoprecipitation (co-IP) studies were used to test whether GR and KLF6 physically interact. Neuro-2A cells were cotransfected with plasmids that express KLF6 and the GR. Following IP with the GR antibody, we were unable to detect KLF6 in the immunoprecipitate regardless of DEX treatment (Figure 6). As expected, both proteins were detected in whole cell lysate (input). Furthermore, the GR was detected in the immunoprecipitate after IP was performed with the GR antibody. When KLF6 was used to IP whole cell lysate, the GR was not detected in the immunoprecipitate (data not shown). The same experimental conditions revealed that KLF15 and the GR were stably associated in transfected Neuro-2A cells [48]. In summary, co-IP studies suggested KLF6 and the GR were not stably associated with each other.
\nThe GR does not physically interact with KLF6. Neuro-2A cells were grown to confluence on 100 mm dishes. Cells were cotransfected with plasmids that express KLF6 (1.5 μg) and the GR (2 μg). Cultures were treated with DEX (10 μM) in 2% stripped serum medium for 4 h before harvesting of transfected cells and other cultures were not treated DEX. Whole cell lysate was prepared with RIPA lysis buffer with 1× Protease Inhibitor cocktail (Thermo-scientific, cat. No: 78430) and protein concentration quantified. Protein extracts (500 μg) were combined with anti-GR (Cell Signaling; 3660) and /or anti-KLF6 (5 μg) antibodies (Thermo Fisher Scientific, 39–6900) and reactions were incubated for overnight at 4°C on rotator. Co-IP and Western blot studies were performed as described previously [48]. The secondary donkey anti-rabbit antibody (NA9340V) was purchased from GE Healthcare and secondary sheep anti-mouse antibody was purchased from GE Healthcare. Following immunoprecipitation with the GR antibody, KLF6 was not detected in the immune-precipitate by western blotting in samples treated with or without DEX. Input lanes are (whole cell lysate) used as positive controls for expression of the both proteins. Molecular weight markers (lane M) are shown to the left of the panels.
In this study, we provided evidence that KLF6 and the GR synergistically stimulate productive infection and IEtu1 promoter activity. The IEtu1 promoter must be activated for productive infection because it encodes two viral transcriptional regulators, bICP0 and bICP4 (Figure 7A) [2]. During reactivation from latency, stress, as mimicked by the synthetic corticosteroid DEX, activates the GR and induces expression of several KLF family members (KLF4, KLF6, KLF15, and PLZF) [16]. A previous study demonstrated that KLF15, but not KLF4, and the GR synergistically stimulate IEtu1 promoter activity [48]. In contrast to KLF6, KLF15 stably interacts with the GR to establish a feed-forward transcriptional loop [48, 51, 53, 65, 66] (Figure 7B). Although KLF6 and KLF15 can both positively regulate promoter activity, they also can repress transcription in a promoter-specific manner [67, 68]. One study concluded there is a synergistic effect between the GR and transcriptional factors that recognize CACCC motifs [69], a known KLF6 binding site [70, 71]. There are no CACCC motifs on the positive strand of the IEtu1 GREs fragment; however, there are 2 CACCC motifs on the negative strand (KLF-1 like; Figure 7B). When these motifs were mutated (∆KLF mutant), there was no difference in KLF6 and GR mediated trans-activation suggesting there may be KLF binding sites located between GRE#2 and GRE#1.
\nThe GR and certain KLF family members stimulate BoHV-1 replication and IEtu1 promoter activity. Panel A: Stress activates the GR, which in turn stimulates expression of four stress-induced KLF family members in TG neurons [16]. Recent studies demonstrated that stress, as mimicked by DEX plus the GR, activates IEtu1 promoter activity because two GREs are located in the promoter [26]. KLF6 and KLF15 cooperate with the GR to activate IEtu1 promoter activity. Stress mediated activation of the IEtu1 promoter is crucial for productive infection because this promoter drives expression of two viral regulatory proteins (bIC0 and bICP4). Panel B: KLF15 stably interacts with the GR: consequently, this complex synergistically stimulates IEtu1 promoter activity by binding to the GREs [48]. Panel C: KLF6 and the GR cooperate to stimulate expression of IEtu1 promoter activity and productive infection. In contrast, to KLF15, KLF6 did not stably interact with the GR. Consequently, we propose that a KLF6 indirectly interacts with the GR via an unknown GR coactivator (X) or binding of the GR to a GRE promotes KLF6 interactions with sequences between GRE#1 and GRE#2. This schematic does not suggest that the interactions occur at independent GREs within the IEtu1 promoter; it merely suggests that these are the two likely mechanisms by which KLF6 cooperates with the GR to stimulate IEtu1 promoter activity.
Relative to GRE#2, mutating GRE#1 was more important for GR mediated trans-activation [26, 48]. To ablate DEX induction of the IEtu1 promoter or the IEtu1 GREs, both GREs must be mutated [26, 48]. This is consistent with the results demonstrating there are cooperative effects between KLF15 [48] or KLF6 and the GR. ChIP results demonstrated that mutagenesis of both GREs interfered with KLF6 binding to sequences spanning the IEtu1 GREs, suggesting: 1) an unknown GR or KLF6 coactivator functions as a bridge between the GR and KLF6, which allows interactions between these two transcription factors (Figure 7C; left scenario at GRE#2), or 2) GR interactions with GRE#1 and/or GRE#2 influence adjacent sequences that are necessary for KLF6 to bind DNA Figure 7B; right scenario at GRE#1). Since KLF family members can bind to several GC or CA rich motifs, it is difficult to predict which sequences adjacent to GRE#1 or GRE#2 are important for interacting with KLF6 and/or KLF15.
\nThe BoHV-1 genome contains approximately 100 putative GREs [26]. We identified 13 intergenic regions in the viral genome that contain at least 2 putative GREs and potential KLF binding sites within 400 base pairs. KLF15 and the GR significantly transactivate fragments present in unique long (UL)-52, bICP4, IEtu2, and Us fragments when DEX was added to cultures [48]. In contrast, KLF6 and the GR were unable to transactivate these intergenic fragments in the presence or absence of DEX (data not shown) confirming KLF15 has novel properties relative to KLF6.
\nKLF4, KLF6, and KLF15 expression are induced in TG neurons of calves that are latently infected with BoHV-1 during early stages of DEX induced reactivation from latency [16]. Cellular, not viral encoded, transcription factors are predicted to be crucial for initiating viral transcription during initial stages of reactivation from latency because lytic cycle viral gene expression is not readily detected in TG of latently infected calves [29, 30]. Thus, activation of the IEtu1 promoter by the GR and DEX-induced transcription factors, KLF6 and KLF15 for example, may be sufficient to trigger lytic cycle viral gene expression in a subset of latently infected neurons following a stressful stimulus, as shown in Figure 7B and C.
\nThis research was supported by grants from the USDA-NIFA Competitive Grants Program (13-01041 and 16-09370), funds derived from the Sitlington Endowment, and support from the Oklahoma Center for Respiratory and Infectious Diseases (National Institutes of Health Centers for Biomedical Research Excellence Grant # P20GM103648). Research reported in this publication was also partially supported by the National Institute Of Neurological Disorders And Stroke of the National Institutes of Health under Award Number R21NS102290. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. Fouad S. El-mayet was supported by a fellowship from the Egyptian Ministry of Higher Education, Mission Sector (JS-3541).
\nEchinococcus granulosus is one of cestodes that caused cystic hydatid disease (Echinococcosis), and this parasite is transmitted from carnivores (dogs, foxes, leopards, lions, and hyenas), which are the definitive hosts of E. granulosus and the parasite (the adult stages) lives in their intestines, to herbivores (sheep, goats, camels, cows, buffaloes, horses, donkeys, pigs, rabbits, and humans), which are intermediate hosts of the parasite where the larvae (hydatid cyst) live [1].
E. granulosus has three different stages of development: eggs, larvae, and adult worms, which are small and do not exceed 7 mm in length as shown in Figure 1 and live adjacent to the mucous layer of the small intestine of the definitive hosts until they reach the adult phases of sexual maturity in about 5–4 weeks [2, 3]. The adult worm has a spherical head of 0.3 mm diameter with a short neck and three types of connected segments, and the head contains a sucker surrounded by two rows of spines ranging from 50 to 28 forks, with four side suckers. The segment that follows the head is immature and contains immature genitals, while the middle segment is mature and contains the testes and ovaries and is located in the middle of the genital opening [4, 5]. The third segment is called gravid segment and contains a branched uterus and has 15–12 branches containing 1000–500 eggs [6].
E. granulosus adult.
The eggs are spherical in shape (Figure 2) and have a diameter of about 40–30 μm and are similar in appearance to the eggs of other tapeworms, containing a hexacanth or oncosphere embryo because the embryo has sixth-hooks lets. The eggs are surrounded by clear coatings [8] and the eggs contain a sticky layer that adheres to the fur of animals and other things, which helps them to spread, as well as insects such as flies, beetles, and birds that play the role of mechanical carrier of eggs, in case of optimal conditions, the eggs remain viable for weeks or months in pastures and gardens as well as they remain viable with the right humidity and moderate temperatures, and the eggs are found in water and wet sand for 3 weeks at 30°C and 225 days at 6°C and 32 days at 10–21°C, also the eggs remain for a short time when exposed to sunlight and dry conditions and kill eggs when exposed to 3.75% of sodium hypochlorite for 10 minutes as well as killed when frozen at −70°C for 4 days or −80°C for 2 days or by heat larger from 60°C for 3 minutes [9].
E. granulosus egg in feces [7].
When intermediate hosts (farm animals) or humans (accidental host) ingest the eggs, the embryo (oncospheres) hatches and becomes active, transmitted by the bloodstream to the liver or any other organ. As soon as the hexacanth embryo reaches its definitive position, it develops into unilocular hydatid cyst that enlarges and produces daughter cysts or protoscoleces inside the inner layer of the hydatid cyst [10, 11].
Transmission to humans is caused by fecal-oral route while eating food and water contaminated with parasite eggs, and these eggs are thrown out with feces of the definitive hosts such as dogs or through contamination of hands with eggs found in contaminated soil or sand or in the hair of infected dogs. The definitive hosts become infected with the adult worm when they feed on the hydatid cysts, which are found in the organs of the intermediate host, such as infected sheep [9, 11].
Species of E. granulosus is divided into several strains such as G1–G10 and these strains have a high degree of adaptation to their hosts, as these strains are named according to the names of their intermediate hosts that play an important role in the continuity of the life cycle of these strains. These strains vary in shape, rate of development, pathogenicity, and geographical extent of their presence: G1 is found in sheep, G2 in Tasmania sheep, and G3 in buffalo. These strains all fall within the E. granulosus species, and G4 strain in equine is therefore called E. equinus; G5 in cows is called E. ortleppi; G6 in camels; G7 in pigs; G9, which is characterized weak, has been isolated from cystic disease in human cases in Poland; G7, G8, and G9 may fall into E. canadensis, and some researchers consider the G9 strain a type of G7 strain in pigs [12].
The classification of Echinococcus genus has been controversial for a long time, and 16 species and 13 subspecies of this genus have been described, based on the difference in the structural and phenotypic properties of the parasite and the characteristics of the host and its type, but only 4 of them are taxonomically adopted: E. granulosus, E. multilocularis, E. oligarthrus, and E. vogeli [13]. According to [14], the classification system of granulocytic parasitic parasite is as follows:
Kingdom: Animalia
Phylum: Platyhelminthes
Superclass: Eucestoda
Class: Cestoda
Subclass: Cestoda
Order: Cyclophyllidea (Ben; Braun, 1900)
Family: Taeniidae (Ludwig, 1886)
Genus: Echinococcus (Rud, 1801)
Species: granulosus (Batsch, 1786)
The adult phases of the E. granulosus lives in the mucous layer of the definitive host’s small intestine, and the eggs are highly resistant to harsh environmental conditions for several months or even a year depending on environmental conditions [15]. Therefore, it remains a source of infection to the intermediate hosts during drinking contaminated water and food, including humans that may also be infected by contact with infected dogs, especially in children, whereas eggs adhere to dog hair around the anus [16, 17].
The eggs reach the stomach of the intermediate host and then decompose the chitinous cortex by digestive juices and release the embryo (oncospheres) of the sixth-hooks, and the oncospheres penetrate the intestine and reach the liver, lungs, and other organs including the brain and muscles to develop into hydatid cysts at the end of about 5 months [18].
When the definitive host feeds on infected organs of the intermediate host, the parasite will reach its small intestine, where the primary heads grow into adult worms within 7–4 weeks, and each worm produces thousands of eggs per day, starting the cycle again [15] (Figure 3).
The adult E. granulosus (sensu lato) (2–7 mm long) resides in the small intestine of the definitive host. Gravid proglottids release eggs that are passed in the feces and are immediately infectious. After ingestion by a suitable intermediate host, eggs hatch in the small intestine and release six-hooked oncospheres that penetrate the intestinal wall and migrate through the circulatory system into various organs, especially the liver and lungs. In these organs, the oncosphere develops into a thick-walled hydatid cyst that enlarges gradually, producing protoscolices and daughter cysts that fill the cyst interior. The definitive host becomes infected by ingesting the cyst-containing organs of the infected intermediate host. After ingestion, the protoscolices evaginate, attach to the intestinal mucosa, and develop into adult stages in 32–80 days. Humans are aberrant intermediate hosts and become infected by ingesting eggs . Oncospheres are released in the intestine , and hydatid cysts develop in a variety of organs . If cysts rupture, the liberated protoscolices may create secondary cysts in other sites within the body (secondary echinococcosis) [19].
The hydatid cysts (Figure 4) of E. granulosus are often spherical or semispherical if not compressed by adjacent organs. The size of the hydatid cysts varies with age, approximately 15–1 cm3 [21].
Cross section in the hydatid cyst [20].
The outer layer is also called adventitia or ectocyst that encases the hydatid cyst, and this layer is produced by the host cells (modified dense fibrous protective tissue) as the host’s response to the infection. There is a close interaction between the host tissue and the parasite, and this layer plays an important role in the development and survival of the cyst. Any degradation of the outer layer leads to the degeneration or explosion of the hydatid cyst; the diameters of a pericyst layer vary depending on the host organ where the hydatid is present, but in general, the diameters are about a few millimeters [22].
It is a solid, noncellular chitinous layer, white in color, consisting of microfibers fibers and dense granules rich in amino carbohydrates observed under electron microscopy [23]. It plays a role in protecting the parasite from the immune response of host and providing the suitable environment for its continued growth in addition to its role in reducing the effect of drugs used in the treatment of the disease [6].
This is the inner layer of hydatid cyst, a cellular living layer containing nuclei and associated with the lamellar layer by fingerprints formed by the germinal layer [20, 24]. It acts to protect components of the cyst and controls the osmotic pressure of the cyst wall [25]. The buds are formed from the germinal layer and grow toward the cavity of the cyst, and after the buds become vacuolated and stalked, the process of forming buds from the inner layer of cells begins from those cavities that lead to the formation of protoscolices [26]. The fertility of the aqueous cyst is determined by the presence of protoscolices, their increasing growth, and their association with the germinal layer, as well as other criteria for determining the cyst fertility through the white color and thickness of the germinal layer [27].
These capsules consist of the generated layer by several endogenous budding, which are small buds formed from the germinal layer toward the cavity of the cyst [15]. These buds enlarge, and each capsule is connected to the germinal layer of the parental cyst by the stem. The process of budding is repeated, and each capsule contains large numbers of protoscolices, which have about 30–10 heads per capsule [28]; capsules are gradually separated from the germinal layer and float in the cyst fluid. These capsules are similar in their structure to the parental cyst [29].
The capsules may rupture and protoscolices may be released together with the free capsules, and this is the so-called hydatid sand. Occasionally, cysts are free from brood capsules when they grow in an inappropriate medium or due to bacterial invasion or calcification. The capsules are formed but do not produce protoscolices, and these are called sterile cysts, whereas capsules that produce protoscolices are called fertile cysts [14].
A term of hydatid sand refers to the contents of the hydatid cyst, which includes the daughter cysts, brood capsules, and protoscolices that present in the hydatid fluid of the E. granulosus [30].
It is a clear colorless or yellowish liquid with a specific weight of 1.005–1.009, a pH of 7.2–6.7, and inorganic substances such as iron, chlorine, magnesium, sodium, calcium, cadmium, nickel, chromium, copper, and some enzymes such as glutamic pyruvic transaminase (GTP), glutamic oxaloacetic transaminase (GOT), Acid phosphatase with lipase, oxidase, phosphatase, and dehydrate enzymes. They vary in quantity and quality depending on the source of the parasite and the location of the cyst and metabolism of parasites such as ammonia, bilirubin, and creatinine [31].
The E. granulosus parasite spreads almost all over the world, but it is more common in rural areas with large pastoral areas, where there are large numbers of animals that are hosts of the parasite, such as cattle, sheep, and others, with the presence of definitive hosts in these areas especially dogs [32]. Echinococcosis is a health and economic problem in most parts of the world and some studies have recorded more than 50 cases per 100,000 people annually in high endemic areas, where the prevalence of the disease in China, Argentina, and East Africa was about 5–10%. The disease also kills about 1 million people a year around the world and also causes a loss of about $3 billion, including treatment and livestock expenses [15, 33].
It is also highly endemic in parts of Africa, Europe, Australia, Asia, and the Mediterranean countries [34], as well as Middle Eastern countries including Iran, Saudi Arabia, Kuwait, Jordan, Palestine, Syria, Lebanon, and Iraq [35]. The epidemiology of the disease depends on the economic and agricultural factors and the level of learning and health and social culture in the human society where the parasite is spread, and what helps to spread the disease is the mixing with pets, especially dogs, in the absence of appropriate health conditions [36].
Iraq is a highly endemic country for the disease, due to the spread of loose parasite-infected dogs [37]. Although there are many recent studies of the epidemic of this disease, it is still a major health problem and is still endemic in Iraq, where there were not enough attempts to combat it despite the availability of modern conditions and equipment for diagnosis and treatment [38].
Epidemiology of hydatosis and cystic type (CE) is still on the rise due to its global distribution and high regional prevalence, and alveolar type (AE) has been observed during the past two decades and a decrease in the rate of morbidity and mortality, especially in Asia, as a result of intensive studies of epidemiology in all countries of the world [39].
Hydatidosis is one of the oldest known diseases of the human being. This disease was described by the Egyptians in a document dating back to 1534 BC, as mentioned by the Babylonians in the Bible Talmud. It described the cyst as a bladder filled with fluid [40]. This disease arises from the formation of hydatid cysts of different sizes in different locations such as the liver and lungs in both animals and humans, and the severity of the disease depends on the number of cysts, size, and location. These cysts may lead to loss of human life in addition to economic losses in the field of livestock; the incidence of this disease is high in humans because its risk is that it is detected only by chance during radiological examinations or various surgical operations, but in animals, it is discovered during routine detection in massacres [1].
The cause of hydatidosis disease is due to two important factors. The first is that it is not possible to know the infection in the early stages since the onset of the disease because it does not show symptoms until the cyst has increased in size of the cyst, which puts pressure on the adjacent tissues [41]. The second factor is the loss of therapeutic means, and the disease is very similar to the severity of its metastasis in the metastasis stage [42]. These cysts are found in all parts of the body except hair and nails [43].
This disease is one of the endemic diseases in Iraq and it has an economic, social and health impact on the human, so conducted many studies and research to investigate methods of treatment, which surgical intervention is the most important of these methods, although the patient is exposed to many problems during surgery which may be difficult to perform at times and cannot be performed at other times [44, 45], or the patient is not surgically qualified or as a result of other serious diseases such as immune compromised patients or because of age or anesthesia or the occurrence of the cyst in places difficult for the surgeon to deal with, such as in the cysts of the heart, brain or spine, so the importance of the use of extracts of a different chemical nature treatment of aquatic cyst disease [46].
Hydatis cyst disease (HCD) is slow at the onset of infection and unseen due to slow growth and development of the cyst, which reaches a diameter of about 10–1 mm per year [33]. The appearance of clinical signs depends on the location of the affected organ, the size of the cyst, its location within the affected organ, the stages of its development, and the fertility of its components with the interaction between the related cysts between adjacent organs, especially between the hepatic vessels and bile ducts [47]. In humans, the symptoms are dependent on the affected organ, and the liver is the most exposed organ, with a rate of about 70–60%, followed by lungs 22–20%, spleen, heart, muscles, eye, and thyroid gland 6%, and the kidneys, brain, and bones 1% and don’t hardly any organ of body free from hydatid cyst except teeth, nails and hair [48].
Symptoms in the liver are: an enlarged, and it becomes sensitive when palpated with liver abscesses, in addition abdominal pain, vomiting and nausea, as well as an increase in hepatic blood pressure and in cavity of the lower vena cava also there secondary fibrosis in the ducts bile, the hydatid cyst causes significant pressure on the diaphragm when adhesion to it and leads to a breach and exit of the contents of the cyst in the chest [49]. In the lung, clinical symptoms depend on the size of the cyst and its condition whether it is healthy or torn, causing the presence of pressure of cyst inside the lobes of the lung [50] with varying severity of chest pain and coughing, hemoptysis, shortness of breath, and hemorrhage, and in the lungs, these symptoms do not appear at the first sight of the disease [51, 52, 53]. When the cyst penetrates into the pulmonary vesicles, it is a suitable environment for fungal and bacterial infections, leading to pneumonia after infection and thus destroying the lung [54].
The explosion of the hydatid cyst inside the abdominal cavity leads to a shock known as anaphylactic shock due to acute allergic reactions, and this shock leads to the severe spread of secondary cysts in the affected organ and adjacent organs, and is sometimes followed by the explosion of the cyst at any site within the body leaking its contents into the blood circulation that leads to headaches and other complications that may lead to sudden death [28].
The symptoms develop even when the cyst is small, and most cases of cerebral cyst disease were diagnosed in children [11]. This infection is serious that sometimes it leads to death; cysts in the eye are rare and cause an external tumor of the eye, dysfunction of vision, exophthalmoses, and sometimes blindness around the eyelid [17].
In the bones, cystic hydatid disease often leads to fracture because of the gradual erosion of the cortex and shows symptoms in the form of pain in the upper and lower extremities, and bone bags are abnormal in the form where the laminar layer does not form [55].
In animals, the infection is hidden, and they may be slaughtered sometimes before the onset of symptoms [56]. The severity of the symptoms varies depending on the severity of the disease and the location of the hydatid cyst. Clinical signs generally appear in the affected animal such as decrease in milk production, poor wool, and organ damage in the affected area [57, 58].
The current review included the identification of the E. granulosus worm and its intermediate and final hosts. The canine family represents the final host, while the human and farm animals represent the intermediate hosts. Several strains of E. granulosus were also observed such as G1, G2, G3, G4, G5, G6, G7, G8, G9, and G10.
The authors thank the Central Library, Library College of Science/University of Al-Qadisiyah, for providing them with the references adopted in this chapter.
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