Home About us Current issue Back issues Submission Instructions Advertise Contact Login   

Search Article 
  
Advanced search 
 
Saudi Journal of Kidney Diseases and Transplantation
Users online: 4748 Home Bookmark this page Print this page Email this page Small font sizeDefault font size Increase font size 
 

ORIGINAL ARTICLE Table of Contents   
Year : 2007  |  Volume : 18  |  Issue : 4  |  Page : 556-564
Prevalence and Clinical Findings of Biopsy-Proven Glomerulonephritidis in Iran


1 Division of Nephrology, Isfahan University of Medical Sciences and Health Services, Isfahan, Iran
2 Division of Nephrology, Iran University of Medical Sciences and Health Services, Tehran, Iran
3 Division of Nephrology, Department of Internal Medicine, Saint Louis University Health Sciences Center, Saint Louis, Missouri, USA

Click here for correspondence address and email
 

   Abstract 

Epidemiological data of renal diseases is population-based and have great geographic variability. Due to the lack of a national renal data registry system, there is no information on the prevalence rate, and clinical and laboratory features of various glomerulo­nephritidis (GNs) in Iran. In a retrospective cross sectional study, we analyzed 462 adult renal biopsies in Tehran, Iran. We determined the prevalence rate and the frequency of different clinical and laboratory findings in patients with different GNs. We also compared our results with the reports from other countries. There were 267 (57.8%) males and 195 (42.2%) females. The mean (± SD) age was 33.6 ± 15.7 (range, 13-75) years. A total of 55 biopsies, which had revealed pathologies other than GNs, were excluded. Among the remaining 407 biopsies, membranous glomerulopathy (MGN) was the most common GN (23.6%), followed by IgAN (13.5%), membranoproliferative GN (MPGN) (11.5%), systemic lupus nephritis (SLE-GN) (10.6%), focal and segmental glomerulosclerosis (FSGS) (10.3%), and minimal change disease (MCD) (9.8%). Our study shows that MGN is the most common form of GN, followed by IgAN, MPGN, SLE­GN, FSGS and MCD in adult patients in Iran. A multi-center study with a larger sample size is needed for more comprehensive data in Iranian population.

Keywords: Glomerulonephritidis, Epidemiology; Renal biopsy, Glomerulopathy, Iran

How to cite this article:
Naini AE, Harandi AA, Ossareh S, Ghods A, Bastani B. Prevalence and Clinical Findings of Biopsy-Proven Glomerulonephritidis in Iran. Saudi J Kidney Dis Transpl 2007;18:556-64

How to cite this URL:
Naini AE, Harandi AA, Ossareh S, Ghods A, Bastani B. Prevalence and Clinical Findings of Biopsy-Proven Glomerulonephritidis in Iran. Saudi J Kidney Dis Transpl [serial online] 2007 [cited 2019 Dec 6];18:556-64. Available from: http://www.sjkdt.org/text.asp?2007/18/4/556/36512

   Introduction Top


Glomerulonephritidis (GNs) remain the third most common cause of end-stage renal failure. [1] Epidemiological data of renal diseases is population-based and has great variability according to the geographic area, socioeconomic condition, race, indication for biopsy, and differences in genetic susceptibility and envi­ronmental exposure.[2],[3],[4],[5] Due to the lack of a nationwide renal data registry system, there is no information on the frequency of different GNs in Iran. Furthermore, the great varia­bility of clinical manifestations confounds the determination of a definitive diagnosis based on the clinical features alone, [6] and thus, kidney biopsy remains the gold standard test for the diagnosis of GNs. However, this procedure is invasive, has some associated morbidity, and in some circumstances may be contraindi­cated. Due to the great variety of glomerular diseases the approach to these patients heavily relies on the clinical, laboratory and pathologic findings.[6] In this study we ana­lyzed the clinical and laboratory findings of 407 adult patients whose native kidney biop­sies had revealed different forms of GNs, over a 3-year period in Tehran, Iran. We also com­pare our results with the reports from other countries.


   Materials and Methods Top


In a retrospective cross sectional study, we analyzed 462 renal biopsies performed in Tehran, Iran. The biopsies had been per­formed in an adult referral university medical center. The indications for renal biopsy were: idiopathic nephrotic syndrome; rapidly prog­ressive renal failure; evaluation and follow­up for collagen diseases, predominantly SLE with proteinuria; abnormal urine sediment or reduced renal function; glomerular protei­nuria of unknown etiology accompanied by abnormal urine sediment or persistent pro­teinuria of >1 gm/day; persistent or recurrent glomerular hematuria with proteinuria more than 500 mg/day or acute renal failure (ARF) of unknown etiology with normal kidney size and no obstruction. [7]

We determined the frequency of different clinical and laboratory findings in these pa­tients. Renal biopsies were processed for light and immunofluorescence microscopy in all specimens. In all cases, sections were stained with Hematoxylin and Eosin (H and E), Masson's trichrome, periodic acid-Schiff (PAS), and Silver Jone's stain.

Clinical information was obtained from the biopsy requisition forms, and by reviewing the patients' medical records. All data rela­ted to the final diagnosis, age, sex, clinical presentation, serum levels of cholesterol, triglyceride, creatinine and complements (C3, C4 and CH50), and the presence of micros­copic hematuria, hypertension (systemic blood pressure >140/90 mm Hg), and proteinuria were recorded.

The clinical presentations were classified as the nephrotic syndrome (>3.5 grams protei­nuria), nephritic syndrome (active urinary se­diment with/without azotemia), ARF, chronic renal failure (CRF, azotemia of >3 months duration), asymptomatic urinary abnormality (AUA), and rapidly progressive GN (RPGN, doubling of serum creatinine over a 3 months period). [8] Hypertriglyceridemia and hypercho­lesterolemia were considered if the plasma concentrations were > 200 mg/dl.


   Statistical analysis Top


Analysis was performed using the statistical package of social science (SPSS)­version 10. Mean ± SD values of laboratory data were compared using ANOVA, between different clinicopathological diagnoses. P <0.05 was considered statistically significant.


   Results Top


We reviewed 462 adult renal biopsies, 407 (88%) of which had shown some form of GN. There were 267 (57.8%) males and 195 (42.2%) females; mean (± SD) age was 33.6 ± 15.7 (range, 13-75) years. The frequency of various GNs is presented in [Table - 1].

Membranous glomerulopathy (MGN) was the most common GN (23.6%), followed by IgAN (13.5%), membranoproliferative GN (MPGN) (11.5%), systemic lupus nephritis (SLE-GN) (10.6%), focal and segmental glo­merulosclerosis (FSGS) (10.3%), and mini­mal change disease (MCD) (9.8%) [Table - 1]. These 6 entities comprised the majority (79.4%) of all GNs. The mean age of patients at presentation, male:female ratio (M:F), the average 24-hours urine protein excretion, serum cholesterol, triglyceride and creatinine concentrations are shown in [Table - 2].

The frequency (%) of presenting syndromes i.e., nephrotic syndrome, nephritic syndrome, ARF, CRF, asymptomatic urinary abnormal­lity, and RPGN in the six common GNs is presented in [Table - 3].

Proteinuria was present in almost all the study patients. The frequency (%) of hyper­tension, microscopic hematuria, hypertrigly­ceridemia, hypercholesterolemia, and serum creatinine >1.4 mg/dl, at the time of presen­tation, is shown in [Table - 4]. There was no significant difference in triglyceride concen­trations (p=0.27) among different GNs; how­ever, the difference was significant in regard to serum cholesterol, and creatinine concen­trations (p < 0.005).


   Discussion Top


In our series, MGN was the most common form of GN (23.6%), followed by IgAN, MPGN, SLE-GN, FSGS and MCD. These six entities comprised 79.4% of all GNs in our biopsy series. MGN is the most common cause (25%) of idiopathic nephrotic syndrome in adults, world wide.[1],[6] The male : female ratio has been reported as 2:1, with the peak incidence being in the fourth and fifth decades of life. Clinical manifestations of MGN show significant geographic variation. Patients from Australia and Japan have a lower frequency of the nephrotic syndrome, as compared to patients from Europe or North America.[6] Microscopic hematuria and hyper­tension (HTN) have been reported in 30­-50% of the patients at presentation.[1],[6],[9] In our series, the mean age of patients with MGN was 43 years, M:F ratio was 1.5:1, there was a high prevalence of the nephrotic syndrome (84.5%) and hyperlipidemia (hyper­triglyceridemia 64.6% and hypercholestero­lemia 88.5%) at presentation. The high pre­valence of the nephrotic syndrome and azo­temia in our series may be due to increased severity of the disease among patients seen in our hospital which is a referral center for renal disease in Tehran, Iran. The other clini­cal manifestations were HTN (38.5%), mic­roscopic hematuria (13.5%), and serum crea­tinine >1.4 mg/dl (15.6%). The serum com­plement levels were reduced in only 5% of the patients.

IgAN is now regarded as the most common form of GN in the world.[6],[10],[11] Its prevalence rate varies in different geographic regions, [8] it is most prevalent in Asia (30-40%) and rela­tively less prevalent in Europe (20%) and North America (10%).[10],[11] Its incidence varies from two per 10,000 people in France and Germany to between 2.0 and 4.8% of the population in Singapore.[6],[11] The M:F ratio has been reported to be 2:1. [6] Around 30-40% of these patients present with microscopic hematuria. HTN has been reported in only 8% of the patients at the time of presen­tation. [11] IgAN was the second most common GN, after MGN, in our series. The lower prevalence rate of IgAN in our series may be due to our higher threshold for renal biopsy, i.e., exclusion of patients with isolated hema­turia and/or proteinuria of <1gm/day, and lack of a nationwide screening program of school children for detection of early cases, as pe­formed routinely in some countries. The mean age at presentation was 32.8 years, M:F ratio was 3.2 : 1; 45.5% had nephrotic and 33% had a nephritic picture at presentation. Moreover, around half of our patients had HTN, 40% had microscopic hematuria, 54.5% had hypercholesterolemia, and 34.5% had serum creatinine > 1.4 mg/dl, at the time of renal biopsy.

FSGS comprises 2 to 41% of the primary GNs in the world. [2] In the past 20 years, the prevalence of primary FSGS has risen from <10% to 25% of all adult primary GNs. [6]

FSGS comprises 6-15% of GNs in Europe and 2-11% of GNs in Asia. [2] FSGS is slightly more common in males (M:F ratio, 1.4:1), with microscopic hematuria occurring in over one half of the patients, and HTN in one third of the patients at presentation. [6]

In a report by Cattran, half of the adult pa­tients had the nephrotic syndrome, a third had microscopic hematuria, and 35% had HTN at presentation. [1] In our series, mean age at pre­sentation was 30.4 years, males were almost twice the females, mean protein excretion rate was 5.8 gm/24 hours with 57% of patients presenting with the nephrotic syndrome, 60% had HTN, 19% had microscopic hematuria, 69% hypercholesterolemia, 55% had hyper­triglyceridemia and 55% had serum creatinine >1.4 mg/dl at the time of presentation.

MCD is responsible for 10-15% of the pri­mary the nephrotic syndromes in adults. [6] It has a variable geographic distribution, being more common in Asia than North America or Europe, [12] and is equally distributed between the two sexes. [6] In our series, MCD comprised 9.8% of the biopsies. It was slightly more prevalent among males (M:F, 1.3:1), with an average age at presentation of 35 years, mean protein excretion rate of 7.8 gm/24 hours. In our patients, 95% presented with the nephrotic syndrome, 25% had HTN, 12.5% micros­copic hematuria, 87.5% hypercholestero­lemia, and 17.5% had serum creatinine >1.4 mg/dl at the time of presentation.

Recent studies have focused on the signi­ficance of epidemiologic and clinical features of SLE-GN, and report a F:M ratio of 8­13:1. [13] The serum complements are usually decreased in the active phase, and often decline before clinical flare up. [13] In our series, SLE-GN accounted for 10.6% of all GNs; the patients were the youngest (mean age, 24.4 years) among all GNs, there were 10 times more females than males, 65% pre­sented with the nephrotic syndrome, and only 21% presented with a nephritic picture. At the time of biopsy, 53.5% of our patients had HTN, 35% had microscopic hematuria, around two thirds had hyperlipidemia, 51% had serum creatinine >1.4 mg/dl, and around 80% had reduced serum complement levels.

MPGN accounts for a wide range (2% to 49%; average, 12.5%) of GNs world wide; 50% of the patients present with the nephrotic syndrome, and 30% present with mild and asymptomatic proteinuria. [6] In our series, MPGN accounted for 11.5% of all GNs; average age was 28.6 years, there were slightly more males (M:F ratio, 1.2:1), and almost all patients presented with proteinuria (average of 5.5 gm/day). At presentation, 66% of our patients had the nephrotic syn­drome, 13% had a nephritic picture, 60% were hypertensive, 34% had microscopic hematuria, 72.5% were hypercholesterolemic, 57.5% had elevated serum creatinine >1.4 mg/dL, and around one half of our patients were hypocomplementemic. In Iran, the pre­valence rate of hepatitis B has been reported to be between 1.1% and 9% in different pro­vinces, [14],[15] and there has been ten-time higher incidence of hepatitis C among MPGN patients than in normal population. [16] Unfor­tunately, we do not have any information on the status of hepatitis B or C of the MGN or MPGN patients in the present study.

The frequency of different GNs in other geographic regions of the world is presented in table 5. [17],[18],[19],[20],[21],[22],[23],[24],[25],[26],[27],[28],[29],[30],[31],[32],[33] Unfortunately, many reports lack detailed information about clinical and laboratory indices. IgAN was the most common GN reported in Australia, France, Japan, Italy, Hong Kong, and Saudi Arabia. FSGS was the most common GN in Brazil, Zaire, USA, Saudi Arabia, and Kuwait. MPGN was the most common GN reported in Moscow and China. MGN, which is the most common GN in our series, has been reported as the most common GN in United Arab Emirates, and Macedonia, and is among the top in the USA.

Recent data point to genetic, biologic, and socioeconomic factors that may be contribu­ting to these findings. [34] The contribution of clinical epidemiology to evidence-based nephrology is not limited to randomized controlled trials. [35] Epidemiological studies on the prevalence rate, and clinical and labo­ratory findings can lead to a higher index of suspicion to a particular diagnosis that may lead to timely appropriate therapeutic intervention. Whether empiric epidemiologic data can be used in treating individual patients, and how, remains controversial. Moreover, like other fields in medical research, epidemiology has some metho­dological limitations that must be taken into account. [35]

Our study has several shortcomings. We did not elaborate on the remaining variants of GNs, sub-types of MPGN (I or II), and asso­ciated conditions such as malignancy or drug consumption. Further studies with larger sam­ple size, and survival analysis of patients are needed for better understanding of the epi­demiologic features of GNs in the Iranian population.

 
   References Top

1.Cattran DC. Outcomes research in glomerulo­nephritidies. Semin Nephrol 2003; 23:340-54.  Back to cited text no. 1    
2.Kitiyakara C, Kopp JB, Eggers P. Trends in the epidemiology of focal segmental glomerulosclerosis. Semin Nephrol 2003; 23:172-82.  Back to cited text no. 2    
3.Choi IJ, Jeong HJ, Han DS, et al. An analysis of 4,514 cases of renal biopsy in Korea. Yonsei Med J 2001;42:247-54.  Back to cited text no. 3    
4.Yahya TM, Pingle A, Boobes Y, Pingle S. Analysis of 490 kidney biopsies: Data from the United Arab Emirates renal diseases Registry. J Nephrol 1998;11: 148-50.  Back to cited text no. 4    
5.Briganti EM, Dowling J, Finlay M, et al. The incidence of biopsy-proven glome­rulonephritidies in Australia. Nephrol Dial Transplant 2001;16:1364-7.  Back to cited text no. 5    
6.Falk RJ, Jennette JC, Nachman PH. Primary Glomerular Disease. In: Brenner BM. Brenner and Rector's The Kidney. Philadelphia: WB Saunders Company; 2004. p. 1293-380.  Back to cited text no. 6    
7.Massry SG, Glassock RJ, eds. Massry and Glassock's Textbook of Nephrology. 4 th ed. Lippincott Williams and Wilkins: Philadelphia; 2001. p. 1743.  Back to cited text no. 7    
8.Denker BM, Brenner BM. Azotemia and urinary abnormalities. In: Kasper DL, Braunwald E, Fauci A, Hauser S, Longo D, Jameson JL, eds. Harrison's Principles of Internal Medicine: 16th edition: NewYork: McGraw-Hill Book Co; 2005. p. 247.  Back to cited text no. 8    
9.Forland M, Spargo BH. Clinico-pathological correlations in idiopathic nephrotic syndrome with membranous nephropathy. Nephron 1969;6:498-525.  Back to cited text no. 9    
10.D'amico G. the commonest glomerulo­nephritidies in the world: IgA nephropathy. Q J Med 1987;64:709-27.  Back to cited text no. 10    
11.Clarkson AR, Woodroffe AJ, Faull RJ. Immunoglobulin A Nephropathy and Henoch-Schonlein purpura. In: Schrier RW. Ed. Disease of the kidney and urinary tract. Philadelphia: Lippincot; 2001. p. 1691-716.  Back to cited text no. 11    
12.Sharples PM, Poulton J, White RH. Steroid responsive nephrotic syndrome is more common in Asians. Arch Dis Child 1985; 60:1014-7.  Back to cited text no. 12    
13.Appel GB, Radhakrishnan J, D'Agati VD. Secondary Glomerular Disease. In: Brenner BM. Brenner and Rector's The Kidney. Philadelphia: WB Saunders Company; 2004. p. 1381-481.  Back to cited text no. 13    
14.Zali MR, Mohammad K, Farhadi A, Masjedi MR, Zargar A, Nowroozi A. Epidemiology of hepatitis B in the Islamic Republic of Iran. East Mediterr Health J 1996;2:290-8.  Back to cited text no. 14    
15.Merat S, Malekzadeh R, Rezvan H, Khatibian M. Hepatitis B in Iran. Arch Iran Med 2000;3:192-201.  Back to cited text no. 15    
16.Broumand B, Ghaleh-Baghi B, Abbasi M, Bonabi NB. The association between hepatitis C and membranoprolifrative glomerulonephritis. Nephrology 1997;3: S365.  Back to cited text no. 16    
17.Mitwalli AH, Al Wakeel JS, Al Mohaya SS, Malik HG. Pattern of glomerular disease in Saudi Arabia. Am J Kidney Dis 1996;27: 797-802.  Back to cited text no. 17    
18.Al-Homrany MA. Pattern of renal diseases among adults in Saudi Arabia: A clinico­pathologic study. Ethn Dis 1999; 9:463-7.  Back to cited text no. 18    
19.Korbet SM, Genchi RM, Borok RZ, Shwartz MM. The racial prevalence of glomerular lesions in nephritic adults. Am J Kidney Dis 1996;27:647-51.  Back to cited text no. 19    
20.Chen H, Tang Z, Zeng C, et al. Pathological demography of native patients in a nephrology center in China. Chin Med J (Engl) 2003;116:1377-81.  Back to cited text no. 20    
21.Heaf J, Lokkegaard H, Larsen S. The epidemiology and prognosis of glome­rulonephritidies in Denmark 1985-1997. Nephrol Dial Transplant 1999;14:1889-97.  Back to cited text no. 21    
22.Khoo JJ. Renal biopsies in Johor: A 7-years study. Malays J Pathol 2001;23: 101-4.  Back to cited text no. 22    
23.Hurtado A, Escudero E, Stromquist CS, et al. Distinct pattern of glomerular disease in Lima, Peru. Clin Nephrol 2000;53:325-32.  Back to cited text no. 23    
24.Polenakovic MH, Grcevska L, Dzikova S. The incidence of biopsy-proven primary glomerulonephritidies in the Republic of Macedonia-long-term follow-up. Nephrol Dial Transplant 2003; 18:26-7.  Back to cited text no. 24    
25.El-Reshaid W, El-Reshaid K, Kapoor MM, Madda JP. Glomerulopathy in Kuwait: The spectrum over the past 7 years. Ren Fail 2003;25:619-30.  Back to cited text no. 25    
26.Chan KW, Chan TM, Ceng IK. Clinical and pathological characteristics of patients with glomerular diseases at a university teaching hospital: 5-years prospective review. Hong Kong Med J 1999;5:240-4.  Back to cited text no. 26    
27.Dzhanaliev BR, Varshavskii VA, Laurinavichus AA. Primary glomerulo­pathies: Incidence, dynamics and clinical manifestations of morphological variants. Arkh Patol 2002;64:32-5.  Back to cited text no. 27    
28.Serov VV, Varshavsky VA, Schill H, Nizze H. Incidence of glomerular diseases in kidney biopsy materials using WHO classification. Zentralbl Allg Pathol 1986;132:471-5.  Back to cited text no. 28    
29.Pakasa M, Mangani N, Dikassa L. Focal and segmental glomerulosclerosis in nephrotic syndrome: A new profile of adult nephrotic syndrome in Zaire. Mod Pathol 1993;6:125-8.  Back to cited text no. 29    
30.Bahiense-Oliveira M, Saldanha LB, Mota EL, Penna DO, Barros RT, Romao-Junior JE. Primary glomerular diseases in Brazil (1979-1999): Is the frequency of focal and segmental glomerulosclerosis increasing? Clin Nephrol 2004;61:90-7.  Back to cited text no. 30    
31.Mazzarolo Cruz HM, Cruz J, Silva AL Jr, Saldanha LB, de Oliveira Penna D. Prevalence of adult primary glomerular diseases: Retrospective analysis of 206 kidney biopsies (1990-1993). Rev Hosp Clin Fac Med Sao Paulo 1996;51:3-6.  Back to cited text no. 31    
32.Simon P, Ramee AP, Autuly V, Laruelle E, Charasse C, Cam G, et al. Epide­miology of primary glomerular diseases in a French region. Variations according to period and age. Kidney Int 1994;4: 1192-8.  Back to cited text no. 32    
33.Antonovych TT, Sabins SG, Broumand BB. A study of membranoproliferative glomerulonephritis in Iran. Ann Saudi Med 1999;19:505-10.  Back to cited text no. 33    
34.Halevy D, Radhakvishnan J, Appel GB. Racial and socioeconomic factors in glomerular disease. Semin Nephrol 2001;21:403-10.  Back to cited text no. 34    
35.Frimat L. Contribution of clinical epide­miology to evidence-based nephrology. Nephrologie 2001;22:199-203.  Back to cited text no. 35    

Top
Correspondence Address:
Afsoon Emami Naini
Department of Nephrology, Noor Hospital, Isfahan University of Medical Sciences, Isfahan
Iran
Login to access the Email id


PMID: 17951943

Rights and Permissions



 
 
    Tables

  [Table - 1], [Table - 2], [Table - 3], [Table - 4], [Table - 5]

This article has been cited by
1 Histopathologic patterns of adult renal disease in Kermanshah, Iran: A 6-year review of two referral centers
Mardanpour, K. and Rahbar, M.
Caspian Journal of Internal Medicine. 2013; 4(3): 717-721
[Pubmed]
2 Glomerular diseases in the Military Hospital of Morocco: Review of a single centre renal biopsy database on adults
Aatif, T. and Benyahia, M. and Maoujoud, O. and Montasser, D.I. and Oualim, Z.
Indian Journal of Nephrology. 2012; 22(4): 257-263
[Pubmed]
3 Distribution of renal histopathology in Guilan a single-center report
Monfared, A. and Khosravi, M. and Lebadi, M. and Zamir, S.A.M.R. and Hoda, S. and Habibzadeh, S.M. and Besharati, S.
Iranian Journal of Kidney Diseases. 2012; 6(3): 173-177
[Pubmed]
4 Renal biopsy findings in Iran: Case series report from a referral kidney center
Ossareh, S. and Asgari, M. and Abdi, E. and Nejad-Gashti, H. and Ataipour, Y. and Aris, S. and Proushani, F. and Ghorbani, G. and Hayati, F. and Ghods, A.J.
International Urology and Nephrology. 2010; 42(4): 1031-1040
[Pubmed]
5 Challenges in clinical-pathologic correlations: Acute tubular necrosis in a patient with collapsing focal and segmental glomerulosclerosis mimicking rapidly progressive glomerulonephritis
Rodamilans, M.F. and Barros, L.L. and Carneiro, M.M. and Dos Santos, W.L.C. and Rocha, P.N.
Renal Failure. 2010; 32(8): 1005-1008
[Pubmed]
6 The incidence of biopsy-proven glomerulonephritis in Cairo University, Egypt: A 5-year study
Ibrahim, S. and Fayed, A.
NDT Plus. 2009; 2(5): 431-432
[Pubmed]
7 Pattern of glomerulonephritis in Iran: A preliminary study and brief review
Mohammadhoseiniakbari, H. and Rezaei, N. and Rezaei, A. and Roshan, S.K. and Honarbakhsh, Y.
Medical Science Monitor. 2009; 15(9): PH109-PH114
[Pubmed]



 

Top
 
 
    Similar in PUBMED
    Search Pubmed for
    Search in Google Scholar for
  Related articles
    Email Alert *
    Add to My List *
* Registration required (free)  
 


 
    Abstract
    Introduction
    Materials and Me...
    Statistical analysis
    Results
    Discussion
    References
    Article Tables
 

 Article Access Statistics
    Viewed3069    
    Printed79    
    Emailed0    
    PDF Downloaded550    
    Comments [Add]    
    Cited by others 7    

Recommend this journal