A study on the polymorphisms of the renin angiotensin system pathway genes for their effect on blood pressure levels in males from Algeria

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1 485898JRA / Journal of the Renin-Angiotensin-Aldosterone SystemMeroufel et al Article A study on the polymorphisms of the renin angiotensin system pathway genes for their effect on blood pressure levels in males from Algeria Journal of the Renin-Angiotensin- Aldosterone System 2014, Vol. 15(1) 1 6 The Author(s) 2014 Reprints and permissions: sagepub.co.uk/journalspermissions.nav DOI: / jra.sagepub.com Djabaria Naïma Meroufel 1,2, Sounnia Médiène-Benchekor 1,3, Julie Dumont 2, Soraya Benhamamouch 3, Philippe Amouyel 2 and Thierry Brousseau 2 Abstract Introduction: Several studies have assessed the relationship between blood pressure (BP) and polymorphisms within the genes encoding angiotensinogen (AGT), angiotensin II type 1 receptor (AT1R) and angiotensin-converting enzyme (ACE). However, considering the relatively large discrepancy in frequency and impact of these variants between ethnic groups and populations, still unavailable data from Algerian population are needed. Objective: Our purpose is to evaluate the association between the AGT M235T, AT1R +1166A/C and ACE I/D polymorphisms and variations in systolic (SBP), diastolic (DBP) and pulse pressure (PP) values. Methods: The associations with BP were assessed in a representative sample of 115 male subjects free of coronary heart disease (CHD). The AGT M235T, AT1R +1166A/C and ACE I/D polymorphisms were determined by PCR-ASO and PCR- RFLP analysis, respectively. Results: We showed no associations between the AGT M235T, AT1R +1166A/C nor the ACE I/D polymorphisms with variations in BP values. However, concerning the ACE I/D polymorphism, subjects carrying the ACE I allele tended to have higher SBP (+4.1 mmhg) and PP values (+3.2 mmhg) than DD subjects (adjusted p = and p = 0.102, respectively). Conclusion: The ACE I/D polymorphism needs further investigation in a larger Algerian study, especially concerning its putative impact on SBP and PP. Keywords Angiotensin II type 1 receptor, angiotensin-converting enzyme, angiotensinogen, polymorphisms, genetic epidemiology, Algerian population Introduction Coronary heart disease (CHD) is a substantial public health problem as it is a major risk factor for many common causes of morbidity and mortality. In 2005, CHD accounted for 28.6% of all death in Algeria, and for approximately more than one-quarter of global deaths. 1 While the role of major risk factors for CHD such as hypertension, hypercholesterolemia or tobacco consumption is acknowledged, 2 evidence suggests a contribution of genetic factors. The renin angiotensin system (RAS), a two-enzyme cascade, plays an important role in the regulation of blood pressure (BP), fluid balance, electrolyte homeostasis 3 and, as a consequence, in the pathogenesis of cardiovascular disease. 4 The initial enzyme, named renin, cleaves its substrate from hepatic origin, angiotensinogen (AGT), to angiotensin I, a decapeptide. Angiotensin I undergoes a second cleavage, mainly by tissue-bound angiotensin-converting enzyme (ACE) and serine proteinase, 5 to generate angiotensin II. As a ligand of the angiotensin II type I receptor (AT1R), angiotensin II acts as a potent vasoconstrictor and 1 Laboratoire de Génétique Moléculaire et Cellulaire, Université des Sciences et de la Technologie d Oran Mohammed Boudiaf, Algeria 2 Inserm, U744, Institut Pasteur de Lille, Université Lille Nord de France, UDSL, France 3 Département de Biotechnologie, Faculté des Sciences, Université d Oran Es-Sénia, Algeria Corresponding author: Djabaria Naïma Meroufel, Laboratoire de Génétique Moléculaire et Cellulaire, Université des Sciences et de la Technologie d Oran Mohammed Boudiaf, BP 1505 ELMANAOUR, Oran, Algeria. meroufeln@yahoo.fr

2 2 Journal of the Renin-Angiotensin-Aldosterone System 15(1) stimulates the secretion of the antidiuretic hypertensive aldosterone. ACE also inactivates the nonapeptide bradykinin and blocks the tissue kallikrein system. Inhibition of ACE and antagonism of AT1R decrease BP in hypertensive patients 6 and prevent mortality and morbidity in patients with symptomatic or asymptomatic congestive heart failure 7 or with acute myocardial infarction (MI). 8 These findings have led to investigations between the risk for CHD and genetic variants of the RAS genes. Among the genetic mutations, the methionine to threonine substitution at position 235 (M235T) in the sequence of the AGT gene, 9 the adenine to cytosine substitution at position UTR (+1166A/C) within the AT1R gene, and the insertion/deletion (I/D) of a unique sequence of 290 bp within the ACE gene 10 have been extensively investigated in various populations with a variety of cardiovascular disorders. The allele and genotype frequencies of these three polymorphisms have been reported among Caucasians, Japanese, Emirati Arabs and several other populations but none has yet been reported for the Algerian population. The aim of the present study was to evaluate both the frequency and the impact of these polymorphisms on BP in a representative sample of men from the North Algerian population. Population study and methods The Etude Cas Témoins de l infarctus du myocarde en ORanie (ECTOR) study is a case-control study of MI in men that included a total of 259 subjects: 81 cases of MI and 178 control subjects free of CHD. The men were aged 25 to 64 years, living in Oran (Algeria), whose parents and grandparents were born in the West of the country, as previously described by Médiène-Benchekor et al. 11 In order to compare the results, the ECTOR study was designed as for the Etude Cas Témoins de l Infarctus du Myocarde (ECTIM) study, which was conducted in the French and Irish populations. 12 Hence, only male patients were included. Patients were recruited from the registers of the cardiology department of the university hospital of Oran. Controls were randomly selected from the Algerian national census list of households. Informed consent was obtained from all participants and the design of the study was approved by the local ethics committee (ANDRS). We studied the effect of the RAS gene polymorphisms on blood values only in controls to avoid putative bias in BP values expected in cases due to modifications of diet, lifestyle and/or intake of antihypertensive drugs that are commonly observed in patients who underwent an MI. Among the 178 controls, statistical analyses were carried on the 115 non-treated subjects for whom all the phenotypic and genetic data were available. Subjects who underwent antihypertensive treatment were excluded. Anthropometric measurements, clinical and biological examinations as well as prevalence of risk factors were systematically recorded. Systolic (SBPs) and diastolic blood pressures (DBPs) were measured twice, with an interval of at least five minutes, in a sitting position, after resting for at least five to 10 minutes. Pulse pressure (PP) was calculated as being the difference between SBP and DBP. Genomic DNA was extracted from peripheral blood leukocytes. Analysis of the AGT M235T, AT1R +1166A/C and ACE I/D polymorphisms For the AGT M235T polymorphism, the polymerase chain reaction (PCR) forward and reverse primers were 5 -GCTGTGACAGGATGGAAGACT-3 and 5 -AGTG GACGTAGGTGTTGAAAGC-3, respectively. The allelespecific oligonucleotide (ASO) method was used to identify the AGT M235T polymorphism. The 235T allele, encoding the methionine residue, and the 235C allele, encoding the threonine residue, were characterized by the specific probes 5 -CTGGCTCCCATCAGG-3 and 5 -CTGGCTCCCGTCAGG-3, respectively. The polymorphism was analyzed by the PCR/ASO method. The forward and reverse primers we used were 5 -CATTCCTCTGCAGCACTTCACT-3 and 5 -CGGTT CAGTCCACATAATGCAT-3, respectively. The sequence of the two probes, corresponding to either the major or minor alleles, were 5 -CAAATGAGCATTAGCTAC-3 and 5 -CAAATGAGCCTTAGCTACT-3, respectively. The AT1R A/C polymorphism was analyzed by the PCR/ASO method. The forward and reverse primers we used were 5 -CATTCCTCTGCAGCACTTCACT-3 and 5 -CGGTTCAGTCCACATAATGCAT-3, respectively. The sequence of the two probes, corresponding to either the major or minor alleles, were 5 -CAAATGAGCAT TAGCTAC-3 and 5 -CAAATGAGCCTTAGCTACT-3, respectively. For the ACE I/D polymorphism, the forward and reverse primers were 5 -CTGGAGACCACTCCCATCCT TTCT-3 and 5 GATGTGGCCATCACATTCGTCAGAT-3, respectively. The analysis included an additional PCR step to confirm the absence of the insertion in subjects carrying the ACE DD genotype. 13 Amplified DNA was submitted to electrophoresis in 2% agarose gels and visualized by ethidium bromide staining. The ACE alleles were visualized as fragments of 480 bp (I) and 190 bp (D). Statistical analysis SBP, DBP and PP values were compared between subgroups of genotypes by an analysis of covariance that used a general linear model. Heterozygote and homozygote subjects for the minor allele of each polymorphism were systematically gathered and compared with homozygous subjects for the major allele to gain in statistical power. The tests were adjusted according to age, body mass index

3 Meroufel et al. 3 Table 1. Clinical characteristics of the total study population (N = 115). Characteristics (BMI), diabetes, tobacco and alcohol consumption. These analyses were carried out with the SAS release V.8.2 software (SAS Statistical Institute, Cary, NC, USA), and p < 0.05 was considered as statistically significant. Results Mean±SD Age (years) a 43.8 ± 13.3 Systolic blood pressure (mmhg) a 129.1±18.8 Diastolic blood pressure (mmhg) a 84.9±32.4 Body mass index (kg/m 2 ) a 23.7± 3.4 Total cholesterol (g/l) a 1.7±0.4 LDL cholesterol (g/l) a 1.1±0.3 Triglyceride (g/l) a 1.1±0.5 HDL cholesterol (g/l) a 0.4±0.1 Smoking habit, yes (%) 50.7% Alcohol consumption, yes (%) 6.8% Diabetes (%) 7.5% HDL: high-density lipoprotein; LDL: low-density lipoprotein; a data are expressed as means ± SD. The clinical characteristics of the study population are given in Table 1. A total of 115 males with a mean age of 43.8 ± 13.3 years (range years) were included in the present study protocol. The mean SBPs and DBPs were (18.8) mmhg and 84.9 (32.4), respectively. Regarding the main risk factors for hypertension, we noticed that the mean BMI was 23.7 ± 3.4 kg/m², more than 50% of the subjects were current smokers, about 7% declared regular alcohol consumption and the prevalence of diabetes was 7.5%. The subjects presented low mean values of lipid variables compared with threshold values of vascular risk. 14 All genotype distributions were in accordance with the Hardy Weinberg equilibrium. Concerning the AGT M235T polymorphism, the frequencies of MM, MT and TT genotypes were 28.4%, 47.7%, and 23.9%, respectively. The frequency of the minor AGT 235T allele was 48%. The frequencies of the AT1R +1166AA, +1166AC and +1166CC genotypes were 68.2%, 30.3% and 1.5%, respectively, resulting in a frequency of the minor AT1R +1166C allele of 19%. Finally, the ACE II, ID and DD genotype frequencies were 6.0%, 44.7% and 49.3%, respectively. The frequency of the ACE I minor allele was 28%. We searched for putative associations between the three studied polymorphisms and SBP, DBP or PP values. As previously mentioned, subjects carrying the minor allele for each polymorphism were pooled in a unique group. Data are summarized in Table 2. For the AGT M235T and AT1R +1166A/C polymorphisms, the values of SBP, DBP and PP did not significantly differ between homozygote subjects for the major allele and subjects carrying the minor allele (p > 0.15). Concerning the ACE I/D polymorphism, subjects carrying the ACE I allele tended to have higher SBP (+4.1 mmhg) and PP values (+3.2 mmhg) than DD subjects, albeit the differences did not reach statistical significance (adjusted p = and p = 0.102, respectively). Discussion The present study has investigated the impact of polymorphisms affecting the major genes participating in the RAS on BP values in a representative sample of the Algerian population from Oran. To our knowledge, this is the first study on the impact of RAS polymorphisms in a population originating from Algeria. The frequency of the AGT 235T allele was estimated at 48%. The frequency was reported to be 78% in Asians, 77% in Blacks, but only 42% in samples from subjects of Caucasian origin. 15 The frequency of the AT1R +1166C allele was 19% in the present Algerian sample. It was shown to be higher in Caucasians (27%), 16 but lower in African Americans (8%) 17 and in Japanese (3%). 18 Concerning the ACE gene, the most frequent allele in the present population was the ACE D allele (72%). It was similar to that observed in Omanis (71%) or Somalis (73%), and higher than in Sudanese (64%), Emirati Arab (61%), 19 Egyptian (67%), Jordanian (66%) or Syrian populations (60%). 20 The D allele frequency was also lower in Blacks (60%), 15 in Caucasians (56%), 15 in Tunisians (42%), 21 and even more in Asians (39%). 15 No effect of AGT polymorphisms on SBP, DBP, or PP can be shown in the present study. Bautista et al. found that the AGT M235T polymorphism was not significantly associated with hypertension and BP values in a Hispanic population. 22 Similar results were obtained in the Surinamese in The Netherlands: Study on Ethnicity and Health (SUNSET) study 23 and in meta-analyses realized in Japanese populations. 24 On the other hand, the AGT M235T SNP was associated with hypertension in many countries with subjects of Caucasian, 25 Taiwanese, 26 Turkish 27 and Dutch 28 origins. In a meta-analysis of 22 publications, hypertension was significantly associated with the AGT 235T allele, compared with subjects carrying the MM genotype, those with homozygotes for the TT genotype had a 21% excess risk (odds ratio (OR) (95% confidence limits (CL)) = 1.21 (1.11; 1.32)). 29 In the present study, SBP and DBP values were not significantly different among the AT1R +1166A/C genotypes. The same results have been shown in Colombian, 22 Japanese 30 and German population samples. 31 Within 548 German participants in the Multinational MONItoring of trends and determinants in CArdiovascular disease (MONICA) study, the prevalence of +1166CC homozygous was only 5%, and BP levels as well as the prevalence of hypertension were not related to the AT1R +1166A/C polymorphism. 31 In contrast, the AT1R +1166C allele was

4 4 Journal of the Renin-Angiotensin-Aldosterone System 15(1) Table 2. Comparison of systolic blood pressure (SBP) and diastolic blood pressure (DBP) between subgroups of AGT M235T, AT1R +1166A/C and ACE I/D genotypes in 115 control subjects. Data are means (SD), mmhg. Genotypes N SBP DBP PP AGT M235T MM (13.6) 84.8 (11.4) 44.1 (7.9) MT (15.2) 81.4 (10.4) 47.4 (11.7) TT (17.0) 81.8 (10.3) 44.4 (12.7) Crude p Adjusted p a MM (13.6) 84.8 (11.4) 44.1 (7.9) MT+TT (15.8) 81.5 (10.3) 41.3 (12.1) Crude p Adjusted p a AT1R +1166A/C AA (14.8) 81.5 (10.1) 46.0 (11.2) AC+CC (16.4) 84.5 (11.3) 45.2 (11.5) Crude p Adjusted p a ACE I/D DD (13.8) 81.8 (10.6) 44.0 (10.3) ID (15.9) 83.0 (11.2) 47.8 (11.8) II (17.8) 81.7 (8.5) 44.8 (13.0) Non-adjusted p Adjusted p DD (13.8) 81.8 (10.6) 44.0 (10.3) ID+II (16.2) 82.7 (10.7) 47.2 (12.0) Crude p Adjusted p a PP: pulse pressure; a tests adjusted for age, body mass index, diabetes, current smoking and alcohol consumption. associated with increased DBP values in Caucasian individuals. 23,32 In three independent studies, the AT1R +1166C allele was also associated with high SBP values in normotensive subjects. 23,33,34 Moreover, the frequencies of the +1166C allele and the +1166CC genotype in 108 Caucasian hypertensive patients with a family history of hypertension were significantly higher than in 84 normotensive controls. 31 In +1166CC homozygotes compared with A allele carriers and the other subjects combined, the OR for hypertension was 7.3 (1.9; 31.9). 31 According to our results, a slight tendency of higher SBP and PP was suggested in subjects carrying the ACE I allele. The tests failed to reach statistical significance, probably because of the lack of power of the present study. Nevertheless, this latter association needs to be checked in a larger Algerian independent study. Many studies have investigated the association between ACE I/D polymorphism and hypertension and their findings diverged. The ACE I/D polymorphism was not associated with hypertension and/or high BP in Emirati Arabs, 35 Spanish, 36 Dutch 23,28 and Cuban 37 populations. In a metaanalysis, in which 23 case-control studies were combined, hypertension or having a family history of hypertension was not significantly associated with the ACE D allele. In 12,230 subjects (74 groups) and in the subgroup analyses, the BP levels showed only small and non-significant variations according to the genotype. 10 Conversely, Henskens et al. confirmed an association of the ACE D allele with SBP and DBP in a healthy normotensive population. 33 Moreover, significant associations were reported between ACE I/D and hypertension in African, 38 Bangladeshi 39 and Turkish 27 populations. Among Hispanics, subjects with the ACE DD genotype were 1.56 (1.05; 2.33) times more likely to be hypertensive than carriers of the ACE I allele. Also, adjusted SBPs and DBPs were 4.58 (0.39; 9.56) and 3.32 (0.78; 5.86) mmhg higher in ACE DD homozygous individuals than in carriers of the ACE I allele, respectively. 23 Overall, the discrepancies between the different reports and our present study are likely a consequence of not only different sample size, but most important, of different criteria as well, specifically clinical presentation, age, ethnic background, geographical area and concomitant environmental risk factors. Nevertheless, because of the small size of the sample, the statistical power of the present study was relatively low, being 64%, 52% and 70% for the AGT M235T, AT1R +1166A/C and ACE I/D polymorphisms, respectively.

5 Meroufel et al. 5 Conclusion The small size of our study requires a replication of the results in a larger sample of the population. Nevertheless, the present study does not exclude the effect of RAS gene polymorphisms on BP values, at least for the ACE I/D polymorphism. Heterozygous and homozygous subjects with the I allele showed a tendency of increased in SBP and PP compared to the frequent DD subjects. For this reason, the study could be considered as a pilot study. Conflict of interest None declared. Funding This study was supported by the Ministère de l Enseignement Supérieur et de la Recherche Scientifique (MESRS, Algeria), the Agence National de Développement de la Recherche en Santé (ANDRS, Algeria) and the Institut National de la Santé et de la Recherche Médicale (INSERM, France). DNM was supported by the Ministère de l Enseignement Supérieur et de la Recherche Scientifique (Algeria) and the Centre National des Œuvres Universitaires et Scolaires (CNOUS, France). JD was supported by the Conseil Régional Nord Pas-de-Calais (France) and the Institut National de la Santé et de la Recherche Médicale (Inserm, France). References 1. Projet INCO-MED-TAHINA (Transition Health Impact In North Africa). Synthèse enquête mortalité, tahina/home/doc/synthese-mortalite-finalpdf1.pdf (2005, accessed 10 July 2012). 2. Seeman T, Mendes de Leon C, Berkman L, et al. Risk factors for coronary heart disease among older men and women: A prospective study of community-dwelling elderly. Am J Epidemiol 1993; 138: Sealey JF, James GD and Laragh JH. The renin-angiotensinaldosterone system for normal regulation of blood pressure and sodium and potasium homeostasis. In: Laragh JH and Brenner BM (eds) Hypertension: Pathophysiology, diagnosis and management, vol 2. New York, NY, USA: Raven Press, 1995, pp Dzau VJ. Tissue renin-angiotensin system in myocardial hypertrophy and failure. Arch Intern Med 1993; 153: Urata H, Nishimura H and Ganten N. Chymase-dependent angiotensin II forming system in humans. Am J hypertens 1996; 9: Azizi M, Guyene TT, Chatellier G, et al. Additive effects of losartan and enalapril on blood pressure and plasma active renin. Hypertension 1997; 29: Pfeffer MA, Braunwald E, Moyé LA, et al. Effect of captopril on mortality and morbidity in patients with left ventricular dysfunction after myocardial infarction. N Engl J Med 1992; 327: Lewis EJ, Hunsicker LG, Bain RP, et al. The effect of angiotensin-converting enzyme inhibition on diabetic nephropathy. N Engl J Med 1993; 330: Staessen JA, Kuznetsova T, Wang JG, et al. M235T angiotensinogen gene polymorphism and cardiovascular renal risk. J Hypertens 1999; 17: Staessen JA, Wang JG, Ginocchio G, et al. The deletion/insertion polymorphism of the converting enzyme and cardiovascular-renal risk. J Hypertens 1997; 15: Médiène-Benchekor S, Brousseau T, Richard F, et al. Blood lipid concentrations and risk of myocardial infarction. 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Absence of an association with the risk of coronary artery disease and myocardial infarction and of a synergistic effect with angiotensinconverting enzyme gene polymorphism on the risk of these diseases. Eur Heart J 1998; 19: Hindorff LA, Heckbert SR, Tracy R, et al. Angiotensin II type 1 receptor polymorphisms in the cardiovascular health study: Relation to blood pressure, ethnicity, and cardiovascular events. Am J Hypertens 2002; 15: Aoki S, Mukae S, Itoh S, et al. Genetic background in patients with acute myocardial infarction. Jpn Heart J 2001; 42: Bayoumi RA, Simsek M, Yahya TM, et al. Insertion-deletion polymorphism in the angiotensin-converting enzyme (ACE) gene among Sudanese, Somalis, Emiratis, and Omanis. Hum Biol 2006; 78: Salem AH and Batzer MA. High frequency of the D allele of the angiotensin-converting enzyme gene in Arabic populations. BMC Res Notes 2009; 2: Mahjoub S, Mehri S, Bousaada R, et al. 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6 6 Journal of the Renin-Angiotensin-Aldosterone System 15(1) 25. Krizanová O, Obdrzálková D, Poláková H, et al. Molecular variants of the renin-angiotensin system components in the Slovak population. Physiol Res 1997; 46: Kunz R, Kreutz R, Beige J, et al. Association between the angiotensinogen 235T-variant and essential hypertension in whites: A systematic review and methodological appraisal. Hypertension 1997; 30: Agachan B, Isbir T, Yilmaz H, et al. Angiotensin converting enzyme I/D, angiotensinogen T174M-M235T and angiotensin II type 1 receptor A1166C gene polymorphisms in Turkish hypertensive patients. Exp Mol Med 2003; 35: van den Born BJ, van Montfrans GA, Uitterlinden AG, et al. The M235T polymorphism in the angiotensinogen gene is associated with the risk of malignant hypertension in white patients. J Hypertens 2007; 25: Mondry A, Loh M and Liu P. Polymorphisms of the insertion/ deletion ACE and M235T AGT genes and hypertension: Surprising new findings and meta-analysis of data. BMC Nephrol 2005; 6: Zhang X, Erdmann J, Regitz-Zagrosek V, et al. Evaluation of three polymorphisms in the promoter region of the angiotensin II type 1 receptor gene. J Hypertens 2000; 18: Wang WY, Zee RY, Morris BJ, et al. Association of angiotensin II type 1 receptor gene polymorphism with essential hypertension. Clin Genet 1997; 51: Barbeau P, Kulharya A, Harshfield G, et al. Association between angiotensin II type I receptor polymorphism and resting hemodynamics in black and white youth. Ethn Dis 2002; 12: S Henskens LH, Spiering W, Stoffers HE, et al. Effects of ACE I/D and AT1R-A1166C polymorphisms on blood pressure in a healthy normotensive primary care population: First results of the Hippocates study. J Hypertens 2003; 21: Reich H, Duncan JA, Weinstein J, et al. Interactions between gender and the angiotensin type 1 receptor gene polymorphism. Kidney Int 2003; 63: Frossard PM, Hill SH, Elshahat YI, et al. Associations of angiotensinogen gene mutations with hypertension and myocardial infarction in a gulf population. Clin Genet 1998; 54: Poch E, de La Sierra A, González-Núñez D, et al. Genetic polymorphisms of the renin-angiotensin system and essential hypertension [in Spanish]. Med Clin (Barc) 2007; 118: Nápoles OC, Castellanos MS, Leal L, et al. A polymorphism study in a Cuban hypertensive population. Clin Chim Acta 2007; 378: Sagnella GA, Rothwell MJ, Onipinla AK, et al. A population study of ethnic variations in the angiotensin-converting enzyme I/D polymorphism: Relationships with gender, hypertension and impaired glucose metabolism. J Hypertens 1999; 17: Morshed M, Khan H and Akhteruzzaman H. Association between angiotensin I-converting enzyme gene polymorphism and hypertension in selected individuals of the Bangladeshi population. J Biochem Mol Biol 2002; 33:

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