High frequency of E148Q sequence variation in children with familial Mediterranean fever in southeast Turkey
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- Lesley Garrison
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1 Originl rticle Arch Argent Peditr 2015;113(2): / 133 High frequency of E148Q sequence vrition in children with fmilil Mediterrnen fever in southest Turkey Ünl Uluc, Assist. Prof., Aydın Ece, Prof. Dr., b Velt Şen, Assist. Prof., Slih Coşkun, Assist. Prof., c Ali Güneş, Assist. Prof., Servet Yel, Assist. Prof., İ İlhn Tn, Assist. Prof., Müsemm Krbel, Assoc. Prof., nd Chit Şhin, M. D.. Dicle University, Medicl School Deprtment of Peditrics, Diyrbkir, Turkey. b. Dicle University, Medicl School Deprtment of Peditric Rheumtology, Diyrbkir, Turkey. c. Dicle University, Medicl School Deprtment of Medicl Genetics, Diyrbkir, Turkey. Emil Address: Assist. Prof. Ünl Uluc: ulucunl@hotmil.com Conflict of interest: none. Received: Accepted: ABSTRACT Objective: The im of this study ws to investigte the spectrum of Mediterrnen fever (MEFV) gene muttions nd genotypephenotype correltion in children with fmilil Mediterrnen fever (FMF) in southest Turkey. Methods: A totl of 507 children (274 femles) with FMF nd MEFV gene muttion(s) were included. A 15-yer retrospective evlution ws conducted; prmeters nlyzed were: ge, sex, ge t symptoms onset, ge t FMF dignosis, dely between symptoms onset nd dignosis, FMF ttck symptoms, nd response to colchicine. Disese severity scores were clculted nd MEFV muttion nlysis ws performed vi rel-time PCR for the 6 most frequent muttions. Children with comorbid diseses or tested negtive for MEFV gene muttions were excluded to provide homogeneity. Results: A fmily history of FMF ws found in 60.2% (n= 305) of ptients. The most common symptoms reported for FMF ttcks were bdominl pin (98.0%), fever (93.9%) nd rthrlgi (47.3%); 75.0% of ptients (n= 380) were heterozygous, 14.2% were homozygous (n= 72) nd 10.8% were compound heterozygous (n= 55).The following MEFV gene muttion lleles were identified: E148Q (40.1%), M694V (25.9%), V726A (15.8%), R761H (7.4%), M680I (6.8%), nd P369S (4.1%). The M694V subgroup hd the lowest men ge of disese onset nd the highest men disese severity score, wheres the E148Q group hd lter men disese onset nd the lowest men disese severity score (p<0.05). Conclusion: The highest E148Q muttion frequency nd milder disese in the course of FMF in our study popultion my be due to geogrphic nd ethnic bckground dissimilrities of southest Turkey. Key words: fmilil mediterrnen fever, genotype, phenotype, muttion, southest Turkey. INTRODUCTION Fmilil Mediterrnen fever (FMF) is n utosoml recessively inherited disese chrcterized by recurrent episodes of fever ccompnied by serositis ttcks involving the peritoneum, synovi nd pleur. 1,2 FMF ptients frequently experience their first ttck in childhood. Genetic muttions of the gene leding to FMF re locted t the short rm of chromosome 16. This gene encodes protein clled pyrin which prevents excessive leukocyte migrtion to sites of inflmmtion nd tht is exclusively expressed in grnulocytes, monocytes, dendritic cells nd serosl nd synovil fibroblsts. 3-5 Pyrin prticiptes in poptosis, cell recruitment nd ctivtion of procspse-1, lso known s interleukin 1-bet (IL-1β) converting enzyme with ssocited processing nd secretion of IL-1 nd IL-8. Although the cler effect of pyrin nd the moleculr mechnism of MEFV muttions remin controversil, recent dt supports the hypothesis tht FMF is cused by loss-of-function muttions leding to incresed IL-1β ctivtion nd ccentuted immune ctivtion which results in serositis including peritonitis, pleuritic nd synovitis. 6 The most common compliction of untreted FMF is serum myloid A deposition in vrious orgns, especilly in the kidneys. FMF is treted with colchicine to prevent future ttcks nd renl myloidosis, which my led to the development of nephrotic syndrome nd eventul chronic renl insufficiency. 1-3 Although dignosis of FMF is primrily clinicl, it is possible to confirm it by performing MEFV gene muttion nlysis. 4,5 In the Middle Est more thn 85% of FMF ptients hve one of the following MEFV muttions: M694V, M694I, M680I,
2 134 / Arch Argent Peditr 2015;113(2): / Originl rticle V726A, nd E148Q. 2 The M694V muttion ws reported to hve reltively severe phenotype, wheres V726A nd E148Q hve been reported with milder disese course. 1-3,7 FMF is more prevlent mong certin ethnic groups such s the Turks, Arbs, Jews nd Armenins. 8 Turkey is one of the few countries in the world hving high FMF frequency with the estimted prevlence of 1:400 to 1: ,7 Gene sequence nd phenotypic chrcteristics of FMF ptients chnge ccording to geogrphic regions, which include people from certin ethnic origins both in Turkey nd in the World. 1,2,7-17 Unfortuntely, there is pucity of studies tht hve investigted the genotypic nd phenotypic vritions of FMF ptients in southest Turkey. 3 Therefore, we imed to investigte the genotypic nd phenotypic chrcteristics of children with FMF in southestern Turkey. MATERIALS AND METHODS Children dignosed s positive for MEFV gene muttions nd receiving medicl cre from Dicle University Hospitl Deprtment of Peditric Nephrology nd Rheumtology unit between 1998 nd 2013 were enrolled. FMF dignosis ws confirmed ccording to the Tel-Hshomer criteri. 4 A retrospective evlution of hospitl records ws conducted to determine ptients ge t dignosis, sex, previous symptoms, FMF fmily history, prentl consnguinity, MEFV genotype, durtion of FMF ttcks, nd response to colchicine. The dignosis of n FMF ttck ws done bsed on clinicl fetures, including fever (>38 º C), bdominl pin nd/or chest pin lsting 6-72 hours, skin rsh or rthritis nd lbortory findings including high erythrocyte sedimenttion rte nd C-rective protein. Renl biopsy ws performed in ptients with nephrotic syndrome (24 hour urinry protein >40 mg/m 2 /h, hypolbuminemi, edem nd hypercholesterolemi). Renl myloidosis ws dignosed in renl biopsy specimen bsed on existence of the morphous pink myloid deposits round the rteries, in the interstitium, or in the glomeruli with hemtoxylin & eosin stin nd demonstrting Congo red stin of the pink mteril. Complete response to colchicine ws defined s complete control of the clinicl mnifesttions nd normliztion of cute phse rectnts; incomplete response ws defined s persistence of some clinicl mnifesttions nd/ or some elevted cute phse rectnts, nd no response s no improvement in ttck frequency nd/or severity of the disese despite colchicine tretment. 19 Exclusion criteri were hving nother dignosis besides. Disese severity ws scored with criteri dpted from Prs et l. 18 by Ozen et l. 19 A score rnging from 3-5 ws considered mild disese, between 6-9 points ws moderte disese, nd greter thn 9 points ws designted s severe disese. 19 The study protocol ws pproved by the Dicle University Hospitl Ethics Committee. DNA extrction nd MEFV gene nlysis The MEFV muttion nlysis ws performed vi rel-time PCR for the 6 most frequent muttions. Genomic DNA ws extrcted from 2 ml of peripherl venous blood smples collected in tubes contining EDTA (ethylenediminetetrcetic cid). The genomic DNA ws isolted using Nucleospin Blood Kit (Qigen-GmbH, Germny) following the mnufcturer s protocol. The DNA concentrtion ws determined using Nno- Drop spectrophotometer (Thermo Scientific, USA). The 6 most common muttions locted in exon 2 (E148Q) nd exon 10 (M694I, M694V, M680I, V726A nd R761H) of the MEFV gene were determined by rel-time PCR on ABI Prism 7500 Fst (Applied Biosystems, Cliforni, USA) ccording to mnufcturer s instructions (Dr. Zeydnli FMF type 1 muttion nlysis system, Ankr, Turkey). Sttisticl nlysis Sttisticl nlyses were performed by using SPSS version 18.0 softwre (SPSS Inc., Chicgo, IL, USA). Student s t-test ws utilized to mke comprisons between two independent groups of normlly distributed numericl dt. Comprisons of dt tht not normlly distributed were done by the Mnn-Whitney U-test or the Kruskl-Wllis test. Ctegoricl vribles were evluted by Chi-squred test. A p-vlue less thn 0.05 ws ccepted s sttisticlly significnt. RESULTS Demogrphics The demogrphic nd clinicl chrcteristics of FMF subjects re outlined in Tble 1. The study enrolled 507 children of 339 unrelted fmilies; 54% were femle nd the men ge ws 8.6±3.7 yers. There ws men dely in dignosis of FMF for 2.3±2.2 yers (Tble 1). There were no
3 High frequency of E148Q sequence vrition in children with fmilil Mediterrnen fever in southest Turkey / 135 differences in men ge, ge of symptoms onset, ge t dignosis, dely between symptoms onset nd dignosis, nd disese severity scoring between femle nd mle ptients (p>0.05, dt not shown). Clinicl fetures A fmily history of FMF ws documented in 60.2% of ptients. Of positive FMF fmily history, 49.8% only hd one ffected fmily member (n= 152), 16.6% hd two ffected fmily members (n= 84), nd 13.6% hd three or more fmily members with FMF (n= 69). Consnguineous mrriges were found in 41.4% of prents (n= 201) (Tble 1). Most common FMF ttck symptoms were bdominl pin (98.0%), fever (93.9%), nd rthrlgi (47.3%). The men disese severity score ws 6.1 (rnge 3-12) in 389 ptients. The symptoms nd disese severity score, ttck durtion nd ttck pttern of 452 FMF children re given t Tble 2. Moderte disese is the most frequent chrcteristics of ptients. Severe disese, ttck durtion more thn 72 hours nd more thn 4 ttcks per month were the lest frequent fetures of the FMF ptients (Tble 2). Regulr colchicine use ws found in 73.9% of ptients, intermittent colchicine use in 22.4% of ptients, nd non-complince ws demonstrted in 3.6% of ptients. Complete response to tretment with resolution of symptoms ws Tble 1. Demogrphic nd some clinicl chrcteristics of the ptients (N 389) n (%) or Men ± SD (rnge) Age, yers 8.6 ± 3.7 (1-17.5) Femle / Mle 274/233 Prentl consnguinity 210 (41.4) Fmily history of FMF 305 (60.2) Age t onset, yers 5.9 ± 3.4 (1-16.3) Age t dignosis, yers 8.3 ± 3.4 (1-16.6) Dely in dignosis, yers 2.3 ± 2.2 (0-12) Follow up period, yers 7.4 ± 3.5 (0.5-12) Disese severity score 6.1 ± 1.9 (3-12) Abdominl pin 497 (98.0) Fever 476 (93.9 ) Arthrlgi 240 (47.3) Mylgi 120 (23.7) Arthritis 80 (15.8) Chest pin 66 (13.8) Erysipels-like erythem 59 (11.6) SD: Stndrd devition. chieved in 68.3%, decresed disese severity in 25.7%, nd no response in 6.0% of ptients. Renl myloidosis developed in 1.4% (n= 7). Five of the ptients with renl myloidosis were homozygous for the M694V muttion nd two of them were compound heterozygous with M694V/V726A nd M694V/M680I muttions. Two of these ptients with myloidosis were phenotype II FMF ptients. Ptient genotypes The most frequently identified independent MEFV muttion ws E148Q in 40.1% of ptients followed by M694V in 25.9% nd V726A in 15.8% (Tble 3). The most common heterozygous genotype ws E148Q/Null in 36.3% of ptients, 12.0% of ptients demonstrted the V726A/Null genotype, nd nother 12.0% hd the M694V/ Null genotype. The most widespred doublemutnt genotypes detected were M694V/ M694V t 7.7% nd E148Q/E148Q t 3.7% (Tble 3). Tble 2. Disese severity score, ttck durtion nd ttck pttern of 452 FMF children N (%) Disese severity Mild 187 (41.4) Moderte 242 (53.5) Severe 23 (5.1) Attck durtion (hours) <12 88 (19.5) (15.0) (31.0) (26.5) >72 36 (8.0) Attck frequency (per month) Rndom 88 (19.5) <1 ttck 98 (20.8) 1-2 ttck 159 (35.2) 3-4 ttck 64 (14.2) >4 ttck 47 (10.3) Tble 3. The distribution of MEFV gene muttions in the study group Muttion Number (%) of independent lleles* (n=634) E148Q 254 (40.1) M694V 164 (25.9) V726A 100 (15.8) R761H 47 (7.4) M680I 43 (6.8) P369S 26 (4.1) *Totlly 380 lleles were null.
4 136 / Arch Argent Peditr 2015;113(2): / Originl rticle A totl of 75.0% of ptients (n= 380) were heterozygous, 14.2% of ptients (n= 72) were homozygous, nd 55 (10.8%) were compound heterozygous (Tbles 4, 5). No significnt differences were found between men ge (p= 0.66) nd ge t dignosis (p= 0.72) between homozygous, compound heterozygous nd heterozygote ptient groups (dt not shown). However, homozygous ptients did hve significntly lower men ge t symptom onset when compred with the heterozygote group t 4.2±2.7 yers versus 6.3±3.5 yers, respectively (p= 0.005). There were significnt differences in men disese severity scores between homozygous (6.9±2.0 points) when compred to compound heterozygous Tble 4. MEFV genotypes in peditric ptients with fmilil Mediterrnen fever MEFV genotype (n=507) One llele Number (%) Two lleles Number (%) E148Q / (36.3) M694V / M694V 39 (7.7) V726A / - 72 (14.2) E148Q / E148Q 19 (3.7) M694V / - 61 (12.0) E148Q / P369S 14 (2.8) R761H / - 34 (6.7) M694V / V726A 12 (2.4) M680I / - 17 (3.3) M680I / M680I 8 (1.6) P369S / - 12 (2.4) E148Q / M694V 7 (1.4) E148Q / V726A 6 (1.2) M680I / V726A 4 (0.8) M694V / M680I 4 (0.8) R761H / R761H 4 (0.8) Others / Others 10 (2.0) Tble 5. Clinicl fetures of homozygous or heterozygous specific muttions Specific muttions Differences (p) E148Q M694V Others (n= 228) (n= 119) (n= 160) Age, yers* 8.9 ± ± ± 3.7 Age t onset, yers* 6.8 ± ± ± , b 0.012, c 0.037, d Age t dignosis, yers* 8.9 ± ± ± 3.1 Dely in dignosis, yers* 2.1 ± ± ± 2.3 Disese severity score* 5.62 ± ± ± , b 0.001, c, d Fever (%) Abdominl pin (%) Arthrlgi (%) Mylgi (%) Arthritis (%) Chest pin (%) Erysipels-like erythem (%) Colchicine response Complete response 165 (72.4) 73 (61.3) 108 (67.5) Incomplete response 59 (25.9) 37 (31.1) 45 (28.1) No response 4 (1.7) 9 (7.6) 7 (4.4) * Men ± Stndrd devition. Differences:. mong three muttions groups, b. E148Q vs. M694V, c. E148Q vs. Others, d. M694V vs. Others. : Not significnt (p>0.05).
5 High frequency of E148Q sequence vrition in children with fmilil Mediterrnen fever in southest Turkey / 137 nd heterozygous (5.9±1.9 nd 5.7±1.7 points, respectively) (p= 0.007). Ptients were further divided into subgroups if they hd one or two E148Q, M694V, or other mutted lleles. There were no significnt differences in the clinicl findings between ll three subgroups (p>0.05; Tble 5). Although, response to colchicine ws found to be best in E148Q subgroup nd the worst in M694V subgroup, the difference between subgroups did not rech to sttisticlly significnt level (p= 0.062) (Tble 5). However, significnt differences were identified in men ge of symptoms onset nd disese severity scores between the three subgroups (p= nd p= 0.001, respectively).the M694V subgroup hd the lowest ge of disese onset nd the highest disese severity scores, while the E148Q subgroup demonstrted n older men ge of disese onset with the lowest severity scores (Tble 5). DISCUSSION Fmilil Mediterrnen fever is hereditry disese tht is more prevlent in ethnics groups ner the Mediterrnen Se. 2 Prticulr muttions re more frequently observed in certin ethnic groups or geogrphic regions. For exmple, the M694V muttion hs been more frequently identified in Turks nd North Africn Jews, while the V726A muttion hs been found to be more prevlent in Ashkenzi Jews, Armenins, nd Arbs. 1-2, 5, 7 Although, heterozygous ptients tend to show reltively mild disese, heterozygous cnnot be distinguished from homozygous FMF ptients by disese severity. 1 Significnt interregionl vritions hve been observed in studies investigting MEFV gene muttion frequencies throughout Turkey (Tble 6). 3,5,9-16,20,21 The most common muttion chrcterized in Turks is the M694V muttion with the frequency of 30-50%. The E148Q muttion occurs t frequency rnging from % ccording to some previous studies. 7, 15,16, Although, there were disgreement regrding whether the E148Q muttion even exhibit disese, it hs been reported s disese cusing muttion in FMF. 20 Two recent studies from estern nd southest Turkey reported tht the E148Q muttion occurs t frequencies of 34.1% nd 30.7% in these popultions, respectively, which is pproximte to the frequency tht we identified t 40.1%. 3,13 A study from western Turkey, reported tht the M694V muttion occurs most frequently t 48.6% nd is followed by the E148Q, M680I nd V726A muttions. 9 A comprehensive study with dult nd peditric FMF ptients from the entire country of Turkey lso reported tht the M694V muttion ws the most frequent t 51.4%, which ws followed by M680I nd V726A. 5 Our study reveled higher E148Q muttion frequency (40.1%) thn our previous study (30.7%); however, the M694V frequency tht we observed in present study is similr to our previous study (25.9% versus 26.0%, respectively). 3 The differences between our first nd second studies my be resulted from inclusion of more ptients in the ltter study. Although some previous studies 22,23 hve proposed E148Q sequence vrition s polymorphism rther thn disese cusing Tble 6. The most common MEFV muttions reported in different studies from the vrious regions of Turkey nd some ethnic origins of other ntionlities Reference Geogrphic regions Number of Muttions (%) of Turkey ptients M694V V726A M680I E148Q R761H P369S Tunc et l. 5 All over the Turkey NR NR NR Ylcinky et l. 11 Middle NR NR NR Yesild et l. 12 Middle Demirky et l. 15 Middle NR Özdemir et l. 13 Middle- est Yiğit et l. 14 North NR NR Öztürk et l. 20 West Ece et l. 3 Southest Present study Southest NR: not reported.
6 138 / Arch Argent Peditr 2015;113(2): / Originl rticle muttion, more recent study 24 hve reported 85% of their ptients who were homozygous for E148Q hd typicl FMF ttcks. During ttcks, cute phse rectnts hve been found rised nd fter ttcks they returned to norml limits nd these ptients hd good response to colchicine tretment. In other two studies 25,26 FMF ssocited myloidosis hve been reported in ptients who were heterozygous for E148Q nd in ptient homozygous for both E148Q nd V726A (E148Q V726A / E148Q V726A). Despite clinicl heterogeneity, high frequency of symptoms in these previous studies re in ccordnce with our results. Our results indicted tht the M694V group demonstrtes higher disese severity scores, while ptients with the E148Q muttion hve lter disese onset with milder disese course (Tble 1). Previous studies lso reported more severe disese phenotypes with the M694V muttion. 3,20 In our study, ptients with homozygous muttions showed greter disese severity nd erlier disese onset when compred with heterozygous, which is in ccordnce with previous reports. 1-3,5 Ptients tht re homozygous for the M694V muttion hve highly ggressive disese course nd develop renl myloidosis. 1-3 The ptients tht we dignosed with renl myloidosis were either homozygous or compound heterozygous for the M694V muttion. In Turkey, FMF presents heterogeneous genotype nd disese course. Therefore, in our study, we found low rte of homozygous muttions (pproximtely 14%) nd heterogeneous clinicl findings despite high rte of prentl consnguinity. In some previous studies from Turkey, in spite of high consnguineous mrriges rtes from ll over the country, low homozygosity rtios (9-12%) hve been reported in FMF ptients similr to our results. 12,13 Other studies reveled tht the E148Q muttion hs been ssocited with milder FMF disese. 3,20 Reltively mild FMF disese together with low disese severity scores were demonstrted in the mjority of our ptients, which my be due to the high frequency of E148Q muttions. 1,3,20 No significnt difference in dignosis ge mong different genotype subgroups of our study, my be relted to ineffective use of helth services in some of our ptients with low socio-economic sttus. A previous study bout symptoms ssocited with FMF ttcks found tht 80-94% of ptients demonstrted fever, 55-91% hd bdominl pin, 21-84% complined of chest pin, nd 27-70% hd rthritis. 2 In our study, we identified reltively lower rtes of chest pin (13.8%), nd rthritis (15.8%). Considering the high frequency of fmilil FMF history in our study, erly dignosis due to lertness of fmily might hve led to esily dignosing FMF without some vribles such s chest pin nd rthritis in these ptients. It is known tht, FMF my mnifest only with fever in younger children nd therefore dignosis is most likely delyed in smll children. 27 In our study, regulr nd intermittent colchicine use ws identified in 73.9% nd 22.4% of ptients, respectively. Complete response to tretment ws observed in 68.3% of ptients. It hs been reported tht response to colchicine my result in complete disppernce of ttcks in 60-70% of ptients, nd 5% of ptients re completely resistnt to colchicine. 28 It is possible tht in our study intermittent colchicine use might be responsible for prtil or no response to tretment. Ptient with AA-type myloidosis nd positive fmily history of FMF but without FMF clinicl fetures re described s phenotype II. 5 There were two ptients with phenotype II in our study, both of them with homozygous muttions. This suggests tht phenotype II is very rre in our FMF ptients. Highly consnguineous mrriges re most common in the estern nd southestern regions of Turkey. 12,29 The men rte of consnguineous mrriges is 20.9% in overll Turkey, while this rte is 4.8% in western nd 40.4% in estern prts of the country. 29 Therefore, our study smple lso showed high prentl consnguinity (41.4%). An elevted degree of prentl consnguinity my hve contributed to the high rtes of FMF fmily history, s utosoml recessive disorders tend to occur more frequently in consnguineous mrriges. Becuse Turkey historiclly locted long immigrtion routes, it is nerly impossible to determine the exct ncestry of specific ethnic groups. Yet, inhbitnts of southestern Turkey re predominntly Kurdish nd Arbic in origin. Differences in MEFV muttion gene pools between southestern nd other regions of Turkey my be due to southestern Turkey s unique ethnic composition, nd likely explins why there is reltively high frequency of the E148Q muttion in this region. Our study nd some previous reports suggest tht E148Q muttion is relted to FMF, 19,30 since the frequency of E148Q
7 High frequency of E148Q sequence vrition in children with fmilil Mediterrnen fever in southest Turkey / 139 is 6.5% in helthy Turkish popultion. 30 In conclusion, the E148Q muttion is the most frequent MEFV muttion in southestern Turkey nd is ssocited with milder disese phenotypes nd lter disese onset. This is in contrst to other regions of Turkey nd the most res of the world. This difference my be relted to ethnic nd geogrphic differences of this loction. REFERENCES 1. Mrek-Ygel D, Berkun Y, Pdeh S, Abu A, et l. Clinicl disese mong ptients heterozygous for fmilil Mediterrnen fever. Arthritis Rheum 2009;60(6): Ben-Chetrit E, Touitou I. Fmilil mediterrnen Fever in the world. Arthritis Rheum 2009;61(10): Ece A, Çkmk E, Uluc Ü, Kelekçi S, et l. The MEFV muttions nd their clinicl correltions in children with fmilil Mediterrnen fever in southest Turkey. Rheumtol Int 2014;34(2): Livneh A, Lngevitz P, Zemer D, Zks N, et l. Criteri for the dignosis of fmilil Mediterrnen fever. 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E148Q is disese-cusing MEFV muttion: phenotypic evlution in ptients with fmilil Mediterrnen fever. Ann Rheum Dis 2005;64(5): Ozturk C, Hlicioglu O, Coker I, Gulez N, et l. Assocition of clinicl nd geneticl fetures in FMF with focus on MEFV strip ssy sensitivity in 452 children from western Antoli, Turkey. Clin Rheumtol 2012;31(3): Ben-Chetrit E, Lerer I, Mlmud E, Domingo C, et l. The E148Q muttion in the MEFV gene: is it disese-cusing muttion or sequence vrint? Hum Mutt 2000;15(4): Mimouni A, Mgl N, Stoffmn N, Shoht T, et l. Fmilil Mediterrnen fever: effects of genotype nd ethnicity on inflmmtory ttcks nd myloidosis. Peditrics 2000;105(5):E Toploglu R, Ozltin F, Yilmz E, Ozen S, et l. E148Q is disese-cusing MEFV muttion: phenotypic evlution in ptients with fmilil Mediterrnen fever. Ann Rheum Dis 2005;64(5): Akr N, Akr E, Ylçinky F. E148Q of the MEFV gene cuses myloidosis in fmilil Mediterrnen fever ptients. Peditrics 2001;108(1): Livneh A, Lngevitz P, Shinr Y, Zks N, et l. MEFV muttion nlysis in ptients suffering from myloidosis of fmilil Mediterrnen fever. Amyloid 1999;6(1): Ylcinky F, Ozckr ZB, Tnyildiz M, Elhn AH. Fmilil Mediterrnen fever in smll children in Turkey. Clin Exp Rheumtol 2011;29(4 Suppl 67):S Ben-Chetrit E, Amr S. About colchicine complince, resistnce nd virulence. Clin Exp Rheumtol 2009;27(2 Suppl 53):S Erdem Y, Tekşen F. Genetic screening services provided in Turkey. J Genet Couns 2013;22(6): Toploglu R, Yildiz C, Tskirn E, Korkmz E, et l. PW The sequence nlysis in E148Q homozygous ptients. Peditr Rheumtol Online J 2013;11(Suppl 1):A57.
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