Publications by authors named "Michail Matalliotakis"

31 Publications

[Corrigendum] Role of adenosine deaminase 2 gene variants in pediatric deficiency of adenosine deaminase 2: A structural biological approach.

Mol Med Rep 2021 Jul 6;24(1). Epub 2021 May 6.

Laboratory of Genetics, Department of Biotechnology, Agricultural University of Athens, 11855 Athens, Greece.

Following the publication of the above article on modeling variants of adenosine deaminase 2 (ADA2), previously identified by Gibson [Kristen M. Gibson, Kimberly A. Morishita, Paul Dancey, Paul Moorehead, Britt Drögemöller, Xiaohua Han, Jinko Graham, Robert E. W. Hancock, Dirk Foell, Susanne Benseler, Rashid Luqmani, Rae S. M.Yeung, Susan Shenoi, Marek Bohm, Alan M. Rosenberg, Colin J. Ross, David A. Cabral and Kelly L. Brown: Identification of novel adenosine deaminase 2 gene variants and varied clinical phenotype in pediatric vasculitis. Arthritis Rheumatol 71: 1747‑1755, 2019], (reference 18 in the article), Dr. Kelly L. Brown, corresponding author of the Gibson article, drew to the authors' attention possible discrepancies identified therein. Upon examining the matters raised by Dr. K. Brown, the authors wish to publish a corrigendum for this article, and the following textual changes are required to the main text. The authors noted that it was not accurate to have referred to the p.Gly47Arg mutation as being 'novel' when this mutation was being specifically referred to, so the word 'novel' should have been omitted from the sentence in the abstract starting on line 17: 'This led to suggestions that the mutations found may affect the formation/stability of the homodimer or may influence the activity of the enzyme (15)'. However, Gibson  in their paper stated that ADA2 variant with the mutation Gly47Arg in sera from homozygous individuals was a dimer (18). Also, the word 'novel' should not have been included in the title of Fig. 3, and this should have appeared as follows: 'Figure 3. The DADA2‑associated mutation G47R in the ADA2 structure', and also, for consistency, the titles of Figs. 4 and 5 should have been written as 'Figure 4. The DADA2‑associated novel mutation R34W in the ADA2 structure' and 'Figure 5. The DADA2‑associated novel mutation A357T in the ADA2 structure'. The authors would like to add that the p.Arg34Trp variant's association with DADA2 has been previously identified in a paper by Kaljas : Human adenosine deaminases ADA1 and ADA2 bind to different subsets of immune cells. Kaijas Y, Liu C, Skaldin M, Wu C, Zhou Q, Lu Y, Aksentijevich I and Zavialow AV: Cell Mol Life Sci 74: 550‑570, 2017. In addition, the novel rare mutation identified by Gibson  as Arg9Trp associated with DADA2 lies in the signal peptide [stated by the authors as Arg8Trp because Met#1 (ATG start codon) is not included in the protein numbering] and is not obviously included in the three‑dimensional structure, and therefore the authors did not deal with it. So, the sentence in the Abstract starting on line 19 should have been written as follows: 'It was thus concluded that the Gly47Arg mutation affects the position and interaction of the dimer‑associated HN1 helical structure'. All references of Arg8Trp in the text, when referred to the Gibson article, should be changed to Arg9Trp as referred therein so as not to cause confusion. Finally, in the legend for Fig. 2, 'His358' should have been written as 'His356' (line 3), and for the purposes of clarification, where 'at the next Asn352 (2)' was written at the end of the same sentence, this text should be changed to 'at the neighboring glycosylated Asn378 [Asn352 in (2)]'. Similarly, on p. 880, the sentence at the end of the penultimate paragraph of the Results section should have been written as follows: 'This disruption could be transmitted to the neighboring His356 coordinated to the metal ion or affect the confirmed glycosylation at the neighboring glycosylated Asn378 [Asn352 in (2)]'. The authors thank Dr. K. L. Brown for drawing these matters to their attention, and emphasize that the resultant corrections and clarifications do not alter either the results or the main conclusions reported in the paper. [the original article was published in 21: 876‑882, 2020; DOI: 10.3892/mmr.2019.10862].
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http://dx.doi.org/10.3892/mmr.2021.12128DOI Listing
July 2021

Demetra Application: An integrated genotype analysis web server for clinical genomics in endometriosis.

Int J Mol Med 2021 Jun 28;47(6). Epub 2021 Apr 28.

Laboratory of Genetics, Department of Biotechnology, Agricultural University of Athens, 11855 Athens, Greece.

Demetra Application is a holistic integrated and scalable bioinformatics web‑based tool designed to assist medical experts and researchers in the process of diagnosing endometriosis. The application identifies the most prominent gene variants and single nucleotide polymorphisms (SNPs) causing endometriosis using the genomic data provided for the patient by a medical expert. The present study analyzed >28.000 endometriosis‑related publications using data mining and semantic techniques aimed towards extracting the endometriosis‑related genes and SNPs. The extracted knowledge was filtered, evaluated, annotated, classified, and stored in the Demetra Application Database (DAD). Moreover, an updated gene regulatory network with the genes implements in endometriosis was established. This was followed by the design and development of the Demetra Application, in which the generated datasets and results were included. The application was tested and presented herein with whole‑exome sequencing data from seven related patients with endometriosis. Endometriosis‑related SNPs and variants identified in genome‑wide association studies (GWAS), whole‑genome (WGS), whole‑exome (WES), or targeted sequencing information were classified, annotated and analyzed in a consolidated patient profile with clinical significance information. Probable genes associated with the patient's genomic profile were visualized using several graphs, including chromosome ideograms, statistic bars and regulatory networks through data mining studies with relative publications, in an effort to obtain a representative number of the most credible candidate genes and biological pathways associated with endometriosis. An evaluation analysis was performed on seven patients from a three‑generation family with endometriosis. All the recognized gene variants that were previously considered to be associated with endometriosis were properly identified in the output profile per patient, and by comparing the results, novel findings emerged. This novel and accessible webserver tool of endometriosis to assist medical experts in the clinical genomics and precision medicine procedure is available at http://geneticslab.aua.gr/.
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http://dx.doi.org/10.3892/ijmm.2021.4948DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8083807PMC
June 2021

Comment on "Risk of systemic lupus erythematosus in patients with endometriosis: a nationwide population‑based cohort study".

Arch Gynecol Obstet 2021 Mar 23. Epub 2021 Mar 23.

Section of Molecular Pathology and Human Genetics, Department of Internal Medicine, School of Medicine, University of Crete, Heraklion, Greece.

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http://dx.doi.org/10.1007/s00404-021-06037-3DOI Listing
March 2021

Association of the DNASE1L3 rs35677470 polymorphism with systemic lupus erythematosus, rheumatoid arthritis and systemic sclerosis: Structural biological insights.

Mol Med Rep 2020 Dec 29;22(6):4492-4498. Epub 2020 Sep 29.

Laboratory of Genetics, Department of Biotechnology, Agricultural University of Athens, 11855 Athens, Greece.

Although genome‑wide association studies (GWAS) have identified hundreds of autoimmune disease‑associated loci, much of the genetics underlying these diseases remains unknown. In an attempt to identify potential causal variants, previous studies have determined that the rs35677470 missense variant of the Deoxyribonuclease I‑like 3 (DNASE1L3) gene was associated with the development of systemic lupus erythematosus (SLE), rheumatoid arthritis (RA) and systemic sclerosis (SSc). DNase1L3 is a member of the human DNase I family, representing a nuclease that cleaves double‑stranded DNA during apoptosis and serving a role in the development of autoimmune diseases. The present study aimed to determine the role of the rs35677470 variant at the DNASE1L3 gene leading to the R206C mutation in SLE, RA and SSc. The underlying mechanism potentially affecting protein structure loss of function was also assessed. DNASE1L3 evolution was investigated to define conservation elements in the protein sequence. Additionally, 3D homology modeling and in silico mutagenesis was performed to localize the polymorphism under investigation. Evolutionary analysis revealed heavily conserved sequence elements among species, indicating structural/functional importance. In silico mutagenesis and 3D protein structural analysis also demonstrated the potentially varied impact of the DNASE1L3 (rs35677470) single nucleotide polymorphism (SNP), providing an explanation for its effect on the R206C variant. Structural analysis demonstrated that the rs35677470 SNP encodes a non‑conservative amino acid variation, R206C, which disrupted the conserved electrostatic network holding secondary protein structure elements in position. Specifically, the R206 to E170 interaction forming part of a salt bridge network stabilizing two α‑helices was interrupted, thereby affecting the molecular architecture. Previous studies on the effect of this SNP in Caucasian populations demonstrated lower DNAse1L3 activity levels, which is consistent with the current results. The present study comprehensively evaluated the shared autoimmune locus of DNASE1L3 (rs35677470), which produced an inactive form of DNaseIL3. Furthermore, structural analysis explained the potential role of the produced mutation by modifying the placement of structural elements and consequently introducing disorder in protein folding, affecting biological function.
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http://dx.doi.org/10.3892/mmr.2020.11547DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7646740PMC
December 2020

Abdominal and perineal scar endometriosis: Retrospective study on 40 cases.

Eur J Obstet Gynecol Reprod Biol 2020 Sep 26;252:225-227. Epub 2020 Jun 26.

Third Department of Obstetrics and Gynecology, Aristotle University of Thessaloniki, Greece.

Objective(s): Abdominal and perineal scar endometriosis usually develop in association with a prior surgical scar. The purpose of the study was to detect and review patients' characteristics of these women over a long period.

Study Design: We retrospectively review the clinical records of 860 women with endometriosis between 1989 and 2019. Data were collected and analyzed from medical and pathological reports of 40 patients with abdominal and perineal scar endometriosis.

Results: 26 patients (3,0 %) were detected in the abdominal wall endometriosis group (AWE) (mean age 36,5 ± 3,4 years) and 14(1,6 %) cases in the perineal endometriosis (PE) group (32,5 ± 2,4 years), respectively. We observed that 92,3 % of women with AWE had undergone at least 1 cesarean section. Moreover, the majority of patients presented with abdominal pain (77, 0 %) and sensation of a mass (96,2 %). 15,4 % of cases had concurrent pelvic endometriosis and the recurrent rate of the disease was 15,4 %. All cases with perineal scar endometriosis were multiparous and delivered vaginally with episiotomy. 92,8 % of patients presented with cyclical pain and swelling. 3 cases suffered from perineal endometriosis combined with pelvic endometriosis. There was a recurrence of perineal endometriosis in 2 women (14,2 %). Surgical excision was the standard treatment of this condition and tissue biopsy confirmed the diagnosis.

Conclusions: Abdominal wall and perineal scar endometriosis are rare, multifactorial entities which are associated mainly with cesarean section and vaginal episiotomy. Clinicians should be aware of these conditions among all women of reproductive age presenting with cyclic or non-cyclic pain and swelling at the incision sites.
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http://dx.doi.org/10.1016/j.ejogrb.2020.06.054DOI Listing
September 2020

Endometriosis research in the -omics era.

Gene 2020 May 9;741:144545. Epub 2020 Mar 9.

Section of Molecular Pathology and Human Genetics, Department of Internal Medicine School of Medicine, University of Crete, Heraklion, Greece. Electronic address:

Endometriosis is a pathological condition extensively studied, but its pathogenesis is not completely understood, since its pathophysiology stems from a broad spectrum of environmental influences and genetic factors. Moreover, the nature of this condition is heterogeneous and includes different anatomical entities. Scientists actively pursue discovery of novel biomarkers in the hope of better identifying susceptible individuals in early stages of the disease. High-throughput technologies have substantially revolutionized medical research and, as a first step, the advent of genotyping arrays led to large-scale genome-wide association studies (GWAS) and enabled the assessment of global transcript levels, thus giving rise to integrative genetics. In this framework, comprehensive studies have been conducted at multiple biological levels by using the "omics" platforms, thus allowing to re-examine endometriosis at a greater degree of molecular resolution. -Omics technologies can detect and analyze hundreds of markers in the same experiment and their increasing use in the field of gynecology comes from an urgent need to find new diagnostic and therapeutic tools that improve the diagnosis of endometriosis and the efficacy of assisted reproductive techniques. Proteomics and metabolomics have been introduced recently into the every day methodology of researchers collaborating with gynecologists and, importantly, multi-omics approach is advantageous to gain insight of the total information that underlies endometriosis, compared to studies of any single -omics type. In this review, we expect to present multiple studies based on the high-throughput-omics technologies and to shed light in all considerable advantages that they may confer to a proper management of endometriosis.
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http://dx.doi.org/10.1016/j.gene.2020.144545DOI Listing
May 2020

Epidemiological aspects of the outcomes from the treatment of endometriosis: Experience from two different geographical areas.

Exp Ther Med 2020 Feb 5;19(2):1079-1083. Epub 2019 Dec 5.

Section of Molecular Pathology and Human Genetics, Department of Internal Medicine, School of Medicine, University of Crete, 71003 Heraklion, Greece.

The purpose of the present study was two-fold: First to review the epidemiological aspects of the experience on the surgical outcomes via laparotomy or laparoscopy, as regards endometriosis from two different academic institutions and, second, to illustrate potential differences in two different geographical areas, New Haven (US) and Greece. This retrospective study included 1,200 patients (15-80 years of age) treated via laparotomy or laparoscopy, at two different institutions, for endometriosis, between 1990 and 2017. Data were collected and analyzed from medical and pathological reports. The statistical methods used included the Student's t-test and χ test, as well as the Mann-Whitney U test. A total of 600 women from Yale University and 600 women from Greece participated in this study. Endometrioma was confirmed in 359 (29.9%) cases. Women were compatible in terms of the site of endometriomas. Left-sided cysts were observed (P<0.001) significantly more often compared with right-sided cysts in both groups. The two groups of patients had similar rates of endometriosis stages. A statistically significant positive association (P<0.001) was found for the co-existence of benign gynecological tumors (apart from endometrioma), endometriosis-associated ovarian cancer and for post-menopausal endometriosis in women with endometriosis from Greece. Moreover, similar results were observed as regards endometriosis following exposure to diethylstilbestrol (DES), non-Hodgkin's lymphoma, endometriosis-associated Lyme disease, human immuno-deficiency virus (HIV), melanoma and endometriosis in adolescents, between the two groups. To conclude, the two populations exhibited similar results as regards the surgical outcomes of endometriosis laparoscopic or open surgery. Endometriosis represents a multifactorial entity that depends on complex interactions of hormonal, genetic, immunological and environmental factors. Gynecologists should be aware that there is an association between endometriosis and cancerous diseases. It is thus suggested that the presence of comorbidities in women with endometriosis.
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http://dx.doi.org/10.3892/etm.2019.8296DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6966115PMC
February 2020

Role of adenosine deaminase 2 gene variants in pediatric deficiency of adenosine deaminase 2: A structural biological approach.

Mol Med Rep 2020 Feb 5;21(2):876-882. Epub 2019 Dec 5.

Laboratory of Genetics, Department of Biotechnology, Agricultural University of Athens, 11855 Athens, Greece.

Adenosine deaminase 2 (ADA2) belongs to the novel family of adenosine deaminase growth factors (ADGFs), which play an important role in tissue development. The deficiency of adenosine deaminase 2 (DADA2) is a recently recognized autosomal recessive autoinflammatory disease, characterized by various systemic vascular and inflammatory manifestations, which is associated with ADA2 mutations. Considering that a recent screening of an international registry of children with systemic primary vasculitis revealed novel and already known variants in ADA2, this study aimed to further investigate the functional significance of the rare variants detected, namely p.Gly47Arg, p.Gly47Ala, p.Arg8Trp, p.Leu351Gln and p.Ala357Thr, by using a structural biological approach. Three‑dimensional models of the mutants were developed and their three‑dimensional (3D) structures were subjected to detailed interaction and conformational analyses. This led to suggestions that the novel mutations found may affect the formation/stability of the homodimer or may influence the activity of the enzyme. It was thus concluded that the Arg8Trp and Gly47Arg mutations affect the position and interaction of the dimer‑associated HN1 helical structure and therefore, dimer formation and stabilization, while Leu351Gln and Ala357Thr influence the metal coordination in the active site. These findings shed further light onto the structural consequences of the mutations under investigation.
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http://dx.doi.org/10.3892/mmr.2019.10862DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6947897PMC
February 2020

Role of FN1 and GREB1 gene polymorphisms in endometriosis.

Mol Med Rep 2019 Jul 15;20(1):111-116. Epub 2019 May 15.

Section of Molecular Pathology and Human Genetics, Department of Internal Medicine, School of Medicine, University of Crete, 71003 Heraklion, Greece.

Endometriosis is a complex gynecological disorder, affecting up to 10% of women of childbearing age, characterized by the presence of functional endometrial tissue at ectopic positions generally within the peritoneum. It is a heritable condition influenced by multiple genetic, epigenetic and environmental factors, with an overall heritability estimated at approximately 50%. The aim of the present study was to evaluate the association of rs1250248 and rs11674184 single nucleotide polymorphisms (SNPs), mapping to fibronectin 1 (FN1) and growth regulation by estrogen in breast cancer 1 (GREB1) genetic loci, respectively, with the risk of endometriosis. A total of 166 women with endometriosis (stages I-IV) who were hospitalized for the condition, diagnosed by laparoscopic intervention and histologically confirmed, and 168 normal controls were recruited and genotyped. Genotyping of the rs1250248 and rs11674184 SNPs was performed with TaqMan primer/probe sets. A significant association was detected with the A allele, as well as the AA and AG genotypes of rs1250248 (FN1) in patients with endometriosis, as well as in patients with stage I and II of the disease only. The rs11674184 SNP of the GREB1 gene was not found to be associated with an increased susceptibility to endometriosis either for all patients (stages I-IV) or for subgroups of stage I and II or III and IV of the disease only. Our results demonstrated a genetic association between the rs1250248 (FN1) SNP and endometriosis at both the genotypic and allelic level. However, although rs11674184 of GREB1 constitutes one of the most consistently associated SNPs with endometriosis in European ancestry populations, it was not found to be associated with endometriosis in this study.
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http://dx.doi.org/10.3892/mmr.2019.10247DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6580018PMC
July 2019

Retrospective evaluation of pathological results among women with ovarian endometriomas versus teratomas.

Mol Clin Oncol 2019 Jun 15;10(6):592-596. Epub 2019 Apr 15.

Department of Obstetrics and Gynecology, Venizeleio and Pananio General Hospital of Heraklion, Heraklion 71409, Greece.

The coexistence of endometrioma with dermoid cyst of the ovaries is an unusual entity, although they are both common and benign gynecological tumors. The present study aimed to investigate the association between ovarian dermoid cyst (teratoma) and endometrioma. We retrospectively, included 315 women with endometrioma and 172 with ovarian teratoma. Data were collected from medical and pathological reports from two different areas between 1995 and 2018. The mean age of cases with endometrioma was similar (35.8±7.2 years) to patients with ovarian teratoma (34.2±6.8 years). Considering the types of dermoid cysts, the observed proportion of mature type was 168/172 (98%), the immature type was 4/172 (2%) and struma ovarii was14/172 (8.1%) respectively. Endometrioma was significantly more frequent in the left ovary [174/266 (65.4%)] than in the right ovary [92/266 (34.6%)], P<0.001. By contrast, ovarian teratoma were predominant in the right ovary, 98/172 (60.6%), compared to the left side, 56/172 (32.5%), P<0.001. Regarding the size of the masses, we detected an inverse distribution between the two groups. Thirteen women were detected with ovarian teratoma and endometriosis, with 6 cases being in the same ovary. Our results indicate a left lateral predispostion of endometrioma and a right of ovarian teratoma and suggest that the pathogenesis between these conditions is different. The coexistence of endometriosis with dermoid cyst of the ovary, presents a challenge to the physicians and the investigators. Further research is required to establish the relationship between endometriosis and ovarian teratoma.
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http://dx.doi.org/10.3892/mco.2019.1844DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6488942PMC
June 2019

Defining the genetic profile of endometriosis.

Exp Ther Med 2019 May 6;17(5):3267-3281. Epub 2019 Mar 6.

Section of Molecular Pathology and Human Genetics, Department of Internal Medicine, School of Medicine, University of Crete, Heraklion 71003, Greece.

Endometriosis is a pathological condition which has been extensively studied, since its pathophysiology stems from a broad spectrum of environmental influences and genetic factors. Familial studies aim at defining inheritance trends, while linkage analysis studies focus on the identification of genetic sites related to endometriosis susceptibility. Genetic association studies take into account candidate genes and single nucleotide polymorphisms, and hence target at unraveling the association between disease severity and genetic variation. The common goal of various types of studies is, through genetic mapping methods, the timely identification of therapeutic strategies for disease symptoms, including pelvic pain and infertility, as well as efficient counselling. While genome-wide association studies (GWAS) play a primary role in depicting genetic contributions to disease development, they entail a certain bias as regards the case-control nature of their design and the reproducibility of the results. Nevertheless, genetic-oriented studies and the implementation of the results through clinical tests, hold a considerable advantage in proper disease management. In this review article, we present information about gene-gene and gene-environment interactions involved in endometriosis and discuss the effectiveness of GWAS in identitying novel potential therapeutic targets in an attempt to develop novel therapeutic strategies for a better management and treatment of patients with endometriosis.
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http://dx.doi.org/10.3892/etm.2019.7346DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6447774PMC
May 2019

Clinical manifestations, evaluation and management of hyperprolactinemia in adolescent and young girls: a brief review.

Acta Biomed 2019 01 23;90(1):149-157. Epub 2019 Jan 23.

Obstetrics and Gynecology Department of Venizeleio General Hospital, Heraklion, Crete, Greece.

Hyperprolactinemia (HPrl) is considered as a rare endocrinopathy in childhood. In children and adolescent girls, there are three major categories of HPrl causes; physiological, pathological and iatrogenic. Through hypogonadotropic hypogonadism, prolactin hypersecretion and production leads to the typical functional syndrome which is observed in female children and adolescents; delayed puberty, primary or secondary amenorrhea and/or galactorrhea. Regarding prolactinomas, clinical signs manifest with mass compression of the optic chiasm and anterior pituitary gland or prolactin hypersecretion. Targeted identification of HPrl is of significant importance for proper management and follow-up. The aim of this review is to focus on the evaluation of HPrl in adolescent and young girls. In addition, we aimed to summarize the current knowledge regarding the proper management of such cases.
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http://dx.doi.org/10.23750/abm.v90i1.8142DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6502148PMC
January 2019

Keeping an Eye on Perimenopausal and Postmenopausal Endometriosis.

Diseases 2019 Mar 12;7(1). Epub 2019 Mar 12.

Section of Molecular Pathology and Human Genetics, Department of Internal Medicine, School of Medicine, University of Crete, 71003 Heraklion, Greece.

: We aimed to describe and review the epidemiological aspect of the disease pattern of a series of perimenopausal and postmenopausal women with a histology confirmation of endometriosis. : We retrospectively examined the clinical records of 184 perimenopausal and 46 postmenopausal women with endometriosis. Data were collected and analyzed from 1100 patients' charts with confirmed endometriosis and involved cases from two different geographical areas, New Haven (US) and Greece. The statistical methods included ײ and the Mann-Whitney U test. In the perimenopausal group (age 45⁻54 years), there were 184 patients (16.7%) and the postmenopausal group (55⁻80 years) had 46 (4.2%). The average age of diagnosis was (49 ± 2.3) and (61.2 ± 5.1), respectively ( < 0.01). : Advanced endometriosis was more aggressive in the perimenopausal group ( < 0.05); in the same group, we observed a higher left-sided predisposition of endometriosis in comparison with the right side ( < 0.01). Endometrioma was the most common gynecological condition among patients with perimenopausal endometriosis in relation to the postmenopausal group ( < 0.001). Additionally, we found uterine leiomyomata more prominent in the perimenopausal group ( < 0.05). In contrast, adenomyosis was found higher in postmenopausal patients ( < 0.05); further, 24 cases with dry eye we observed. : Postmenopausal endometriosis is an important underestimated condition. Although the reported situation is not common, various clinicopathological characteristics were observed in both groups. Clinicians should be aware that there is a correlation between endometriosis and endometriosis-associated ovarian cancer in perimenopausal and postmenopausal age.
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http://dx.doi.org/10.3390/diseases7010029DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6473414PMC
March 2019

Whole exome sequencing identifies hemizygous deletions in the UGT2B28 and USP17L2 genes in a three‑generation family with endometriosis.

Mol Med Rep 2019 Mar 3;19(3):1716-1720. Epub 2019 Jan 3.

Section of Molecular Pathology and Human Genetics, Department of Internal Medicine, University of Crete, Heraklion 710 03, Crete, Greece.

Endometriosis is an enigmatic condition with an unknown etiology and a poorly understood pathogenesis. It is considered to appear from the interplay of many genetic and environmental factors, affecting up to 10% of women and represents a major cause of pain and infertility. The familial association of endometriosis, as demonstrated through monozygotic twin and family studies suggests a genetic contribution to the disease, with further case‑control and genome‑wide association studies (GWAS) detecting various endometriosis risk factors. In a recent study, we described a unique, three‑generation family of Cretan origin (Greece) with 7 females with surgically confirmed endometriosis (grandmother, 3 daughters and 3 granddaughters). All the affected members of this family displayed a variety of clinical manifestations and complications. In the present study, to further analyze the genetic variants conferring the risk of developing endometriosis, whole exome sequencing (WES) was performed, using the AmpliSeq technology on the Ion Proton platform. An initial analysis of 64 variants that were detected across the 14 genes previously confirmed to be associated with endometriosis, did not identify any deleterious exonic variants in these genes. However, further analysis revealed 2 hemizygous deletions in the grandmother that segregate in several of her affected offspring. The first deletion was found in the UGT2B28 locus, spanning 7 informative sequence variants across at least 14 kb. The second deletion, located in USP17L2, spans 3 informative variants across at least 2 kb. On the whole, the findings of the presents study implicate 2 additional genes in the pathogenesis of endometriosis, apart from those already identified by GWAS.
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http://dx.doi.org/10.3892/mmr.2019.9818DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6390005PMC
March 2019

Co-existence of endometriosis with 13 non-gynecological co-morbidities: Mutation analysis by whole exome sequencing.

Mol Med Rep 2018 Dec 1;18(6):5053-5057. Epub 2018 Oct 1.

Section of Molecular Pathology and Human Genetics, Department of Internal Medicine, School of Medicine, University of Crete, Heraklion 71003, Greece.

Endometriosis is an enigmatic condition with an unknown etiology and poorly understood pathogenesis and women with endometriosis represent a high-risk population group for a large category of chronic conditions. The study focused on a 67-year-old woman who presented with a 40-year history of familial endometriosis associated with various non-gynecological co-morbidities, thus representing a unique case from a cohort of 1,000 patients with endometriosis. Her family history included infertile members suffering from endometriosis. Thirteen non-gynecological co-morbidities were documented throughout the years, including five autoimmune diseases (i.e., systemic lupus erythematosus, ankylosing spondylitis, multiple sclerosis, bronchial asthma and Crohn's disease), urinary bladder diverticulum, osteoporosis, multinodular goiter, cardiovascular diseases, gastroesophageal reflux disease, malignant tumor of urinary bladder, Barrett's esophagus and bilateral cataract. In order to understand the potential role of gene mutations in the development of all those co-morbidities, whole exome sequencing was performed and the presence of various disease-associated, potentially causal missense variants, were observed. These findings are in accordance with the previously suggested common underlying etiologic pathway for some, but not all, autoimmune disorders. This unusual case provides novel insights demonstrating that endometriosis can coexist with various chronic autoimmune diseases and other conditions, including non-gynecological malignancies, which possibly share a common genetic cause, a fact that should be taken into consideration seriously by clinicians.
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http://dx.doi.org/10.3892/mmr.2018.9521DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6236265PMC
December 2018

Endometriosis and fertilisation.

Exp Ther Med 2018 Aug 13;16(2):1043-1051. Epub 2018 Jun 13.

Section of Molecular Pathology and Human Genetics, Department of Internal Medicine, School of Medicine, University of Crete, Heraklion 71003, Crete, Greece.

The aim of the present review was to discuss a matter of concern in the clinical field of obstetrics/gynecology, namely the potency of fertilization (IVF) in the management of endometriosis-associated infertility. Endometriosis is a medical condition affecting one tenth of women in their fertile years, and accounts for up to 50% of infertile women. Thus, such high prevalence has established the necessity for investigating the effectiveness of available techniques in eradicating the disease and constraining infertility as well as the accompanying pain symptoms of endometriosis. The underlying mechanisms connecting endometriosis with low fecundity have been extensively studied, both in terms of genetic alterations and epigenetic events that contribute to the manifestation of an infertility phenotype in women with the disease. Several studies have dealt with the impact of IVF in pregnancy rates (PRs) on patients with endometriosis, particularly regarding women who wish to conceive. Results retrieved from studies and meta-analyses depict a diverse pattern of IVF success, underlining the involvement of individual parameters in the configuration of the final outcome. The ultimate decision on undergoing IVF treatment should be based on objective criteria and clinicians' experience, customized according to patients' individual needs.
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http://dx.doi.org/10.3892/etm.2018.6307DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6090275PMC
August 2018

Association between ovarian cancer and advanced endometriosis.

Oncol Lett 2018 May 16;15(5):7689-7692. Epub 2018 Mar 16.

Department of Obstetrics and Gynecology, Venizeleio General Hospital, 71409 Heraklion, Crete, Greece.

We retrospectively analyzed clinicopathological data in two different countries over the past years on the association between ovarian endometriosis and ovarian carcinoma. Medical and pathological reports were evaluated from 1,000 patients with endometriosis from two different geographical areas. The prevalence and women characteristics of cases were analyzed. Endometriosis-associated ovarian cancer was present in 20 (2%) cases, among the study subjects. The observed prevalence was 12 (60%) for endometrioid carcinoma, 4 (20%) for clear cell ovarian carcinoma, 2 (10%) for serous and 2 (10%) for mucinous adenocarcinoma. A higher proportion of endometrioid carcinoma cases were noted in comparison with other types (P<0.001). We found only 3/20 (15%) postmenopausal cases. In all cases, we reported advanced stage of endometriosis (stage III or IV). Left-sided endometrioid carcinoma were notably more common than right-sided ones (P<0.001). In the majority of cases, malignant transformation of endometriosis was observed in endometrioid carcinoma or clear cell carcinoma of the ovary. Further research is required to establish the relationship between endometriosis and ovarian cancer.
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http://dx.doi.org/10.3892/ol.2018.8287DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5920362PMC
May 2018

A focus on the distinctions and current evidence of endometriosis in adolescents.

Best Pract Res Clin Obstet Gynaecol 2018 Aug 19;51:138-150. Epub 2018 Feb 19.

Department of Pediatrics, NYU School of Medicine, New York, USA.

Endometriosis (EM) occurring in adolescents presents distinct clinical and histologic characteristics compared to the disease in women. Because the symptoms of EM are nonspecific, often overlapping with those experienced in a range of gynecological and gastrointestinal conditions, the process of reaching a diagnosis of EM is often delayed. The diagnosis of EM is suspected depending on the history and the symptoms and signs, is corroborated by physical examination and imaging techniques, and is finally proved by histological examination of specimens collected during laparoscopy. Currently, there is insufficient evidence to make strong recommendations for management in adolescents who may have EM. This short report reviews some peculiarities of EM in adolescents and provides an update of recent knowledge of the diagnosis and treatment of EM. We hope that the present contribution may help to bring more attention to the clinical diagnosis of EM and consequently aid in decreasing diagnostic delay.
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http://dx.doi.org/10.1016/j.bpobgyn.2018.01.023DOI Listing
August 2018

Co-existence of benign gynecological tumors with endometriosis in a group of 1,000 women.

Oncol Lett 2018 Feb 20;15(2):1529-1532. Epub 2017 Nov 20.

Department of Obstetrics and Gynecology, Venizeleio General Hospital, 71409 Heraklion, Crete, Greece.

The purpose of this study was two-fold, first to investigate the association between endometriosis and the risk of benign gynecologic tumors and, secondly, to evaluate the distribution of endometrioma and ovarian cysts in women with endometriosis. The medical and pathological reports of 1,000 women with endometriosis were retrospectively reviewed. The incidence of ovarian cysts, uterine leiomyomas and adenomyosis, as well as the side of ovarian cysts were further compared. A total of 295 cases of endometriomas, 172 cases of adenomyosis, 173 cases of ovarian cysts and 89 cases of uterine leiomyomas were confirmed histologically in patients with endometriosis. Serous cysts represented the most frequent diagnosis (n=81, 8.1%) in women with ovarian cysts, followed by dermoid cysts (n=15, 1.2%). In women with unilateral endometriomas, the observed proportion of left-sided cysts was found in 65.6% (164 of 250), significantly higher compared with right-sided cysts (86 out of 250, 34.4%) (P<0.001). Moreover, patients with other ovarian cysts were recognized as left-sided in 60% (96 out of 160) of cases, significantly higher compared with right-sided cysts (64 out of 160, 40%) (P<0.01). On the whole, the current study indicates that endometriosis may be associated with an increased risk of benign gynecological tumors, such as ovarian cysts, adenomyosis and leiomyomas. The results of this study confirm a left lateral predisposition of endometriomas and ovarian cysts.
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http://dx.doi.org/10.3892/ol.2017.7449DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5774344PMC
February 2018

Corrigendum to "The Severity of Retinopathy in the Extremely Premature Infants".

Int Sch Res Notices 2017 22;2017:4713420. Epub 2017 Nov 22.

Department of Obstetrics and Gynecology, Venizeleio General Hospital of Heraklion, Crete, Greece.

[This corrects the article DOI: 10.1155/2017/4781279.].
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http://dx.doi.org/10.1155/2017/4713420DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5735628PMC
November 2017

Association of non-Hodgkin's lymphoma with advanced endometriosis.

J BUON 2017 Nov-Dec;22(6):1603-1604

Department of Obstetrics & Gynecology, Venizeleio General Hospital of Heraklion, Crete, Greece.

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July 2019

The role of IL‑16 gene polymorphisms in endometriosis.

Int J Mol Med 2018 Mar 9;41(3):1469-1476. Epub 2018 Jan 9.

Section of Molecular Pathology and Human Genetics, Department of Internal Medicine, School of Medicine, University of Crete, 71003 Heraklion, Crete, Greece.

Endometriosis is one of the most common gynecological diseases affecting up to 10% of the female population of childbearing age and a major cause of pain and infertility. It is influenced by multiple genetic, epigenetic and environmental factors. Interleukin‑16 (IL‑16) is a proinflammatory cytokine playing a pivotal role in many inflammatory and autoimmune diseases as well as in the pathogenesis of endometriosis. The aim of the present study was to evaluate the association of two IL‑16 gene single nucleotide polymorphisms (SNPs), rs4072111 and rs11556218, with the risk of endometriosis in women from Greece as well as to gain insight about the structural consequences of these two exonic SNPs regarding development of the disease. A total of 159 women with endometriosis (stages I‑IV) hospitalized for endometriosis, diagnosed by laparoscopic intervention and histologically confirmed, and 146 normal controls were recruited and genotyped. Subjects were genotyped using a polymerase chain reaction restriction fragment length polymorphism (PCR‑RFLP) strategy. A significant association was detected regarding the GG and GT genotype as well as 'G' allele of rs11556218 in patients with endometriosis. The rs4072111 SNP of the IL‑16 gene was not found to be associated with an increased susceptibility to endometriosis either for all patients (stages I‑IV) or for stage III and IV of the disease only. Our results demonstrated that rs11556218 is associated with endometriosis in Greek women, probably by resulting in the aberrant expression of IL‑16, as suggested by the bioinformatics analysis conducted on the SNP‑derived protein sequences, which indicated a possible association between mutation and functional modification of Pro‑IL‑16.
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http://dx.doi.org/10.3892/ijmm.2018.3368DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5819913PMC
March 2018

The Severity of Retinopathy in the Extremely Premature Infants.

Int Sch Res Notices 2017 18;2017:4781279. Epub 2017 Oct 18.

Neonatology Department, Venizeleio General Hospital of Heraklion, Crete, Greece.

Objective: We aimed to investigate the incidence and the severity of retinopathy of extremely premature infants and to evaluate the risk factors and outcome of the cases.

Materials And Methods: Out of 200 premature births, we retrospectively reviewed 9 cases that developed ROP. We excluded cases where ROP developed in newborns > 30 weeks of gestational age and cases where medical notes were unavailable or incomplete. Topical drops of cyclopentolate 1% and phenylephrine 5% were instilled and fundoscopy was performed using a direct ophthalmoscope.

Results: The incidence of ROP was 4.5% in the 9-year period. The infants were divided into two groups. Group 1 included premature infants ≤27 weeks of age and Group 2 included those >27 weeks but ≤ 30 weeks of age. We found that the infants of Group 1 showed advanced stages of ROP in comparison to Group 2. Out of 18 eyes, 11 eyes had stage 3 ROP and they were all found in Group 1 (100% of cases).

Conclusion: The severity of ROP was associated with earlier gestational age, lower birth weight, and oxygen supplementation. Constant cooperation between physicians and nursing staff is necessary to avoid undetected cases and further prevent ROP related blindness.
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http://dx.doi.org/10.1155/2017/4781279DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5664283PMC
October 2017

Importance of Leadership Style towards Quality of Care Measures in Healthcare Settings: A Systematic Review.

Healthcare (Basel) 2017 Oct 14;5(4). Epub 2017 Oct 14.

Florence Nightingale Faculty of Nursing and Midwifery, King's College, London SE18WA, UK.

Effective leadership of healthcare professionals is critical for strengthening quality and integration of care. This study aimed to assess whether there exist an association between different leadership styles and healthcare quality measures. The search was performed in the Medline (National Library of Medicine, PubMed interface) and EMBASE databases for the time period 2004-2015. The research question that guided this review was posed as: "Is there any relationship between leadership style in healthcare settings and quality of care?" Eighteen articles were found relevant to our research question. Leadership styles were found to be strongly correlated with quality care and associated measures. Leadership was considered a core element for a well-coordinated and integrated provision of care, both from the patients and healthcare professionals.
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http://dx.doi.org/10.3390/healthcare5040073DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5746707PMC
October 2017

The role of gene polymorphisms in endometriosis.

Mol Med Rep 2017 Nov 29;16(5):5881-5886. Epub 2017 Aug 29.

Section of Molecular Pathology and Human Genetics, Department of Internal Medicine, School of Medicine, University of Crete, Heraklion 710 03, Greece.

Endometriosis is a benign gynecologic disorder, affecting up to 10% of women, characterized by the presence of functional endometrial tissue at ectopic positions generally within the peritoneum. It is a heritable condition influenced by multiple genetic and environmental factors, with an overall heritability estimated at approximately 50%. In this study, we investigated whether single nucleotide polymorphisms (SNPs) rs7521902, rs10859871 and rs11031006, mapping to WNT4, VEZT and FSHB genetic loci, respectively, are associated with risk for endometriosis in a Greek population. This study included 166 women with histologically confirmed endometriosis diagnosed through surgery and 150 normal controls. Genotyping of the rs7521902, rs10859871 and rs11031006 SNPs was performed with Taqman primer/probe sets. A significant association was detected with the AC genotype of rs7521902 (WNT4) in patients with stage III and IV disease only. Evidence for association with endometriosis was also found for the AC genotype of the rs10859871 of VEZT. Notably, a significant difference in the distribution of the AG genotype and the minor allele A of FSHB rs11031006 SNP was found between the endometriosis patients and controls. We found a genetic association between rs11031006 (FSHB) SNP and endometriosis. WNT4 and VEZT genes constitute the most consistently associated genes with endometriosis. In the present study, an association of rs7521902 (WNT4) and rs10859871 (VEZT) was confirmed in women with endometriosis at the genotypic but not the allelic level.
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http://dx.doi.org/10.3892/mmr.2017.7398DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5865763PMC
November 2017

Genetic association study in a three-generation family with seven members with endometriosis.

Mol Med Rep 2017 Nov 23;16(5):6077-6080. Epub 2017 Aug 23.

Section of Molecular Pathology and Human Genetics, Department of Internal Medicine, School of Medicine University of Crete, Heraklion 71003, Greece.

The aim of this study was to investigate whether five single nucleotide polymorphisms (SNPs), associated with endometriosis, may confer new insight towards a genotype‑phenotype association with endometriosis. We studied a three-generation family with seven women who had endometriosis. Blood specimens were obtained from all the affected female family members. The entire family was genotyped for five SNPs mapped to WNT4, VEZT, FSHB and IL-16 genetic loci. We further evaluated the members of the family with endometriosis and described all obstetric and gynecological complications caused by the disease in these seven women. The five SNPs analyzed did not reveal any genotype-phenotype correlation with the disease. The members of the family with endometriosis showed a variety of clinical manifestations and complications. None of the five genetic markers examined correlated genotype with phenotype in the case of the Greek three-generation family examined. Therefore, we conclude that more gene polymorphisms must be investigated in the members of this family to gain insight regarding a genotype‑phenotype correlation in endometriosis and the potential development of a personalized care for the patients based on these data.
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http://dx.doi.org/10.3892/mmr.2017.7337DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5865811PMC
November 2017

Extra pelvic endometriosis: Retrospective analysis on 200 cases in two different countries.

Eur J Obstet Gynecol Reprod Biol 2017 Oct 18;217:34-37. Epub 2017 Aug 18.

Department of Obstetrics & Gynecology and Reproductive Sciences Yale University School of Medicine, USA. Electronic address:

Objective(s): The purpose of the study was to review patients' characteristics and the location of extrapelvic endometriosis.

Study Design: Out of 1000 women with endometriosis during a 20year period, we found 200 cases with extra pelvic endometriosis. Medical reports were evaluated and the diagnosis was confirmed on the pathological specimen. This study involved cases from two different geographical areas, New Haven and Crete. The age, parity, symptoms, previous surgeries, diagnostic modalities, histopathological evaluation and location of endometriotic implants found in other areas were recorded and analyzed from the patient's charts.

Main Outcome Measure(s): Statistical methods included x and Mann-Whitney U test s measuring incidence of right-VS left sided endometriosis.

Results: 200 patients with extrapelvic endometriosis and 800 patients with pelvic endometriosis were included in the study. The gastrointestinal tract represents the most common location of extrapelvic endometriosis with 104/200(52%) cases (p<0, 01), followed by the urinary system with70/200(35%) cases. We observed the Left-sided ureter being involved in 49/200(24, 5%) cases, significantly higher compare with the right-sided ureter 21/100(10, 5%) (p <0, 01). All women had similar characteristics involving age, weight, main complaints, age of menarche, endometriosis stages, gravid and family history of endometriosis.

Conclusion(s): The gastrointestinal tract and the urinary system are the most common sites of the extrapelvic endometriosis, which was obvious in both countries. Moreover, we observed that there are no significant differences in demographic variants, menstrual and reproductive characteristics in women with extrapelvic and pelvic endometriosis.
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http://dx.doi.org/10.1016/j.ejogrb.2017.08.019DOI Listing
October 2017

Approaches to teach evidence-based practice among health professionals: an overview of the existing evidence.

Adv Med Educ Pract 2017 7;8:455-464. Epub 2017 Jul 7.

Department of Family and Child Health, Florence Nightingale Faculty of Nursing and Midwifery, London, UK.

Health care professionals' adoption of evidence-based practice (EBP) remains limited, although most health care professionals are familiar with EBP and believe in its value. This systematic review aimed to bring together the best methods used to teach EBP to health professionals. The authors conducted a systematic search for the period 2005-2015 (an update of the search took place in October 2016) using PubMed interface (Medline). MeSH terms as well as free-text keywords were used. Studies were analyzed and evaluated by title and abstract. Those studies which fulfilled the inclusion criteria were assessed by full text. References of articles were also taken into consideration for identifying relevant studies not found through algorithm search. Twenty articles were found to be relevant. The majority of the studies were conducted among nurses (n=7) and physicians (n=6), and only a few among professionals from mixed disciplines (n=5). Two studies were conducted among chiropractors (n=1) and faculty members from a naturopathic and classical Chinese medicine institution (n=1). Researchers used a variety of different approaches, which varied with respect to duration and organization. We divided interventions into two categories. Single interventions included either a workshop, or a journal club, or a conference, or a lecture, or online learning tools, whereas multiple interventions included a combination of these approaches. An increase in EBP competencies and attitudes was reported in nine studies. Teaching methods for optimizing EBP among health professionals could become a robust standardized procedure of the medical educational curricula and lifelong learning of health care professionals.
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http://dx.doi.org/10.2147/AMEP.S134475DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5508813PMC
July 2017

Endometriosis in Adolescent and Young Girls: Report on a Series of 55 Cases.

J Pediatr Adolesc Gynecol 2017 Oct 27;30(5):568-570. Epub 2017 May 27.

Department of Obstetrics and Gynecology and Reproductive Sciences Yale University School of Medicine, New Haven, Connecticut.

Study Objective: The aim of this retrospective study was to evaluate endometriosis in adolescent and young girls and further to review the menstrual, reproductive characteristics, and risk factors.

Design And Setting: We reviewed the medical records of adolescent and young girls with endometriosis from 2 different countries. Data were collected and analyzed from charts of 900 patients with endometriosis.

Participants And Interventions: Fifty-five female adolescents aged between 13 and 21 years (mean age 18.3 years) participated in our series. This study was conducted in the Obstetric and Gynecology Department of Venizeleio General Hospital of Crete and involved all patients diagnosed with endometriosis between 1996 and 2016.

Main Outcome Measures: Statistical methods included χ and Mann-Whitney U test.

Results: Of 900 patients with endometriosis we found 55 female adolescents (6.1%). The mean age was 18.3 ± 2.3 years, significantly younger compared with the advanced endometriosis patients (32.7 ± 7.2; P < .001). Regarding the menstrual reproductive and others characteristics, we observed several differences in adolescent young girls compared with the advanced age endometriosis group. The factors associated with an increased risk for young women include age at menarche, dysmenorrhea, history of asthma, and a positive family history of endometriosis. Additionally, we report on 16 of 55 (32%) adolescent women with endometriosis and congenital malformations (P < .01) and 5 patients who were diagnosed with dry eye syndrome.

Conclusion: There is an association between endometriosis in adolescent and young women and risk factors including early menarche, early onset of dysmenorrhea, history of asthma, previous surgical procedures, obstructive genital anomalies, and family history of endometriosis.
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http://dx.doi.org/10.1016/j.jpag.2017.05.007DOI Listing
October 2017

Educational strategies for teaching evidence-based practice to undergraduate health students: systematic review.

J Educ Eval Health Prof 2016 22;13:34. Epub 2016 Sep 22.

Department of Child and Family Health, Florence Nightingale Faculty of Nursing and Midwifery, London, UK.

Purpose: The aim of this systematic review was to find best teaching strategies for teaching evidence-based practice (EBP) to undergraduate health students that have been adopted over the last years in healthcare institutions worldwide.

Methods: The authors carried out a systematic, comprehensive bibliographic search using Medline database for the years 2005 to March 2015 (updated in March 2016). Search terms used were chosen from the USNLM Institutes of Health list of MeSH (Medical Subject Headings) and free text key terms were used as well. Selected articles were measured based on the inclusion criteria of this study and initially compared in terms of titles or abstracts. Finally, articles relevant to the subject of this review were retrieved in full text. Critical appraisal was done to determine the effects of strategy of teaching evidence-based medicine (EBM).

Results: Twenty articles were included in the review. The majority of the studies sampled medical students (n=13) and only few conducted among nursing (n=2), pharmacy (n=2), physiotherapy/therapy (n=1), dentistry (n=1), or mixed disciplines (n=1) students. Studies evaluated a variety of educational interventions of varying duration, frequency and format (lectures, tutorials, workshops, conferences, journal clubs, and online sessions), or combination of these to teach EBP. We categorized interventions into single interventions covering a workshop, conference, lecture, journal club, or e-learning and multifaceted interventions where a combination of strategies had been assessed. Seven studies reported an overall increase to all EBP domains indicating a higher EBP competence and two studies focused on the searching databases skill.

Conclusion: Followings were deduced from above analysis: multifaceted approach may be best suited when teaching EBM to health students; the use of technology to promote EBP through mobile devices, simulation, and the web is on the rise; and the duration of the interventions varying form some hours to even months was not related to the students' EBP competence.
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http://dx.doi.org/10.3352/jeehp.2016.13.34DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5066070PMC
April 2017