• Users Online: 542
  • Home
  • Print this page
  • Email this page
Home About us Editorial board Ahead of print Current issue Search Archives Submit article Instructions Subscribe Contacts Login 


 
 Table of Contents  
ORIGINAL ARTICLE
Year : 2022  |  Volume : 17  |  Issue : 1  |  Page : 14-20

Role of transrectal ultrasound and elastography in the diagnosis of prostate lesions


Department of Radiology, JNMC, DMIMS, Wardha, Maharashtra, India

Date of Submission26-Feb-2022
Date of Decision08-Mar-2022
Date of Acceptance22-Mar-2022
Date of Web Publication25-Jul-2022

Correspondence Address:
Dr. Rishabh Gupta
Department of Radiology, JNMC, DMIMS, Sawangi (Meghe), Wardha, Maharashtra
India
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jdmimsu.jdmimsu_80_22

Rights and Permissions
  Abstract 


Background: The incidence of malignancy of prostate gland has displayed a rapid rise over recent times. Transrectal ultrasound (TRUS) has brought revolution to radiologist's human prostate imaging methods. Information regarding elasticity of suspicious or abnormal lesions provided by strain elastography can enhance the detection rate of prostate malignancies as well as serve as a reliable visual guide for biopsy from these sites. In this prospective study, we aim to appraise the use of TRUS for diagnosing prostatic lesions, both benign and malignant, and compare it to the utility of strain elastography to precisely locate and guide biopsies of lesions while referring to the pathological diagnosis as the reference standard, wherever possible/needed. Materials and Methods: This was a prospective, cross-sectional study involving 82 male patients who were clinically suspected to have prostate malignancy. The patients were referred to the Department of Radiodiagnosis, AVBRH, where they underwent transrectal ultrasonography and elastography with Hitachi Aloka ultrasound (USG) Machine Arietta S70 with biplane high-frequency transrectal probe (6–10 MHz) with elastography. Results: TRUS had high sensitivity (92.45%) and specificity (78.38%) for cancer detection. Strain elastography had a sensitivity of 96.23%, specificity of 81.08%, positive predictive value (PPV) of 70.83%, and negative predictive value (NPV) of 97.83%. Based on our findings, real-time elastography had more sensitivity and higher NPV than TRUS for the identification of prostatic cancer. Hence, it can be concluded that elastography is an effective assessment tool for ruling out the possibility of malignant tumors, helping to reduce redundant biopsies. Conclusions: Transrectal ultrasonography (TRUS) is an effective tool for the assessment of prostatic lesions. TRUS has high specificity, sensitivity, NPV, and PPV when assessing lesions for prostatic cancer. Elastography has high sensitivity, high specificity, high PPV, and reliable NPV when detecting for prostatic cancer. The combination of TRUS and elastography can help more efficiently assess lesions and guide biopsies to increase the identification rate of prostatic cancer.

Keywords: Carcinoma, elastography, prostate, transrectal, ultrasound


How to cite this article:
Gupta R, Phatak SV. Role of transrectal ultrasound and elastography in the diagnosis of prostate lesions. J Datta Meghe Inst Med Sci Univ 2022;17:14-20

How to cite this URL:
Gupta R, Phatak SV. Role of transrectal ultrasound and elastography in the diagnosis of prostate lesions. J Datta Meghe Inst Med Sci Univ [serial online] 2022 [cited 2022 Aug 18];17:14-20. Available from: http://www.journaldmims.com/text.asp?2022/17/1/14/352250




  Introduction Top


The incidence of malignancy of prostate gland has displayed a rapid rise over recent times.[1] Prostatic carcinoma is one of the two cancers found most commonly in men.[2] Carcinoma of prostate is a major factor affecting morbidity as well as mortality in males. Health education should be employed among population as a tool to detect the early symptoms of these conditions in men.[3] Geriatric health is an important part of community health-care system of India, as it is an important indicator of success of various health programs and policies. Among the various conditions affecting men in the geriatric age group, prostatic pathologies are a major concern as it leads to significant morbidity and mortality. Early and accurate diagnosis of prostatic conditions can immensely help improve the geriatric morbidity and mortality. Digital examination of prostate is done via the rectal route as direct examination is not possible due to its unfavorable position. This examination along with correlation from serum levels of prostate-specific antigen (PSA) provided the most reliable diagnostic tool for prostatic pathologies, in historical times. However, this method lacked accuracy and was inadequate.[4] With the invention of ultrasound and its use in medical diagnosis, a new method of prostate evaluation was born. A patient examination that indicates prostatic disease suspicion on digital rectal examination (DRE) along with elevation in serum PSA can be confirmed to be having carcinoma pathology, only on biopsy. Biopsy helps distinguish between the benign and malignant causes of prostate symptoms. Transrectal ultrasound (TRUS) has brought revolution to radiologist's human prostate imaging methods.[5] Transrectal ultrasonography (TRUS) is the radiological investigation, which is most commonly and most widely used for the evaluation of prostate gland, especially in patients who have suspicious findings on DRE and/or elevated PSA values.[6] Gray-scale ultrasound indicates areas of cancers as hypoechoic signals relative to surrounding normal prostatic tissue.[7] In gross examination, prostate cancer lesions are found to be stiff, while benign prostatic hyperplasia (BPH) maintains the original soft nature of prostate tissue.[8] A technique which has ability to display the visual map of these elastic properties of prostate gland in situ can serve as a very useful tool in locating stiff cancer areas within the otherwise soft prostate gland. This information regarding elasticity of suspicious or abnormal lesions provided by strain elastography can enhance the detection rate of prostate malignancies as well as serve as a reliable visual guide for biopsy from these sites.[9] In this prospective study, we aim to appraise the use of TRUS for diagnosing prostatic lesions, both benign and malignant, and compare it to the utility of strain elastography to precisely locate and guide biopsies of lesions when referring to the pathological diagnosis as the reference standard, wherever possible/needed.


  Materials and Methods Top


Location of study

A. V. B. Rural Hospital, Sawangi, Wardha, Maharashtra.

Sample population

Individuals suspected of/with indications of prostate abnormalities.

Study design

Prospective, cross-sectional study.

Length of the study

Two years, 2019–2021.

Sampling strategy

All individuals reported at the Department of Radio Diagnosis, AcharyaVinobhaBhave Rural Hospital, Sawangi (Meghe), Wardha under suspicion of prostate abnormalities were subjected to the study. After receiving ethical clearance and recording informed consent, the medical history of subjects was queried before a sonoelastographic examination.

Sample size

Eighty-two.

Techniques employed

TRUS and elastography of the prostate.

Equipment

Hitachi Aloka USG machine Arietta S70 with biplane high-frequency transrectal probe (6–10 MHz) with elastography.

Inclusion criteria

  1. Individuals suspected of/with symptoms of prostate abnormalities
  2. Individuals with heightened PSA levels (>4 ng/ml)
  3. Abnormalities detected during digital palpation.


Exclusion criteria

  1. Patients who are recovering from surgery
  2. Individuals with severe bleeding diatheses
  3. Individuals confirmed to have prostate cancer
  4. Individuals on coagulants
  5. Individuals who refused to offer consent or undergo a medical examination [Table 1], [Table 2], [Table 3], [Table 4].
Table 1: Transrectal ultrasound findings in correlation with histopathology

Click here to view
Table 2: Elastography grade* HPE cross tabulation

Click here to view
Table 3: The results of transrectal ultrasound, elastography, and HPE

Click here to view
Table 4: Diagnostic efficacy of TRUS and elastography for prostatic cancer detection

Click here to view



  Results Top


Age

  • Majority of our sample (48 out of 82, i.e., 58.5%) included men of age above 60 years
  • The average age of individuals with malignant tumors was 70 years
  • The average age of individuals with benign lesions was 61 years.


Histopathology results

  • 32.4% (26) of sample size were found to be having malignant lesions.
  • 67.6% (56) of sample size were found to be having benign lesions.


Benign lesion types on histology

  • Of the total 56 patients having benign prostatic disease, 34 were diagnosed with BPH, whereas 22 were diagnosed with prostatitis (on histopathology).


Malignant lesions on histopathology

  • Of the total 26 patients having malignant prostate etiology, 100%, i.e., all 26 had adenocarcinoma of prostate.


Prostate-specific antigen levels

  • The average PSA in the benign group was found to be 21.4 ng/ml.
  • The average PSA in the malignant group was far higher than the benign group, i.e., 58.6 ng/ml.


Prostate size/volume

  • The average prostate size of our sample was calculated to be at 37.8 cm3
  • 21 out of total 82 had high-grade prostatomegaly (>40 cc), and all of these 21 were found to have BPH.


Symptoms

  • The most common symptom of prostatic pathology is lower urinary tract symptom (urinary urgency, hesitation, and high frequency of micturition). Among these, majority of the patients were found to be having benign lesions
  • Majority of the patients with hematuria (total 20) complaints were those having malignant lesions (17 out of 40 were malignancy affected).


TRUS observations

  • Focal hypoechoic lesions were found in 37 out of 82 patients. Of these 37 patients, only 13 were found to be malignant on histopathology
  • We assigned benign nature to remaining 45 patients. Of these 45 patients, 2 were found to be malignant on histopathology
  • TRUS correctly diagnosed 13 malignant lesions and missed 2 malignant lesions
  • TRUS correctly diagnosed 43 benign lesions.


Elastography observations

  • Upon correlation with gray scale/TRUS, we assigned 36 patients to be malignant on elastography. This consisted of 17 patients from Grade V, 16 patients from Grade IV, and two patients from Grade III
  • Of the 36 patients that were assigned malignant on elastography, 26 turned out be malignant on histopathology
  • Elastography wrongly diagnosed ten patients as malignant prostate etiology.


Performance of TRUS and elastography

The area under ROC curve for TRUS was 87.57%.

  • Area >50% implied prominent significance of TRUS gray scale for prostate cancer detection
  • The area under ROC curve for elastography was 89.56%.
  • Area >50% implied prominent significance of elastography for prostate cancer detection.
  • This area was higher than the area under ROC curve for TRUS
  • This implied that elastography was a modality that performs better than TRUS for prostate cancer detection [Graph 1], [Graph 2], [Graph 3], [Graph 4], [Graph 5], [Graph 6] and [Figure 1], [Figure 2], [Figure 3], [Figure 4]..

Figure 1: Case 1: On transrectal B-mode ultrasonography, the prostate was enlarged in size and shows uniform echogenicity with no demonstrable lesions. Hyperechoic Foley's tube was seen within the urethra. On elastography, the prostate gland shows symmetric heterogeneous strain (mosaic and symmetrical pattern of blue and green). Elastography Grade II

Click here to view
Figure 2: Case 2: On elastography, the prostate gland shows an asymmetric stiff lesion in the right gland, which was not related to any corresponding hypoechoic area on transrectal gray scale ultrasonography. Elastography Grade III

Click here to view
Figure 3: Case 3: On transrectal ultrasonography, the prostate was enlarged in size and shows heterogeneous echogenicity with a hypoechoic lesion in right peripheral zone. On elastography, the hypoechoic lesion and surrounding area showed increased stiffness (the entire lesion and surrounding area appeared blue). Elastography Grade V

Click here to view
Figure 4: Case 4- On transrectal B-mode ultrasonography, the prostate was enlarged in size and shows heterogeneous echogenicity with hypoechoic lesion in central zone on the right. On elastography, the hypoechoic lesions show stiffness in the center of the lesion and strain at the periphery (periphery of the lesion in green and the central part in blue). Elastography Grade IV

Click here to view


Cases

Case 1

Case 1 was a 57-year-old male patient with lower urinary tract symptoms such as increased frequency of micturition and nocturia.

Case 2

Case 2 was a 75-year-old male patient with complaints of hematuria.

Histopathology: Acute prostatitis.

Case 3

Case 3 was a 72-year-old male patient with lower urinary tract symptoms.

Histopathology: Prostatic adenocarcinoma. Gleason's score: 6.

Case 4

Case 4 was a 74-year-old male patient with lower urinary tract symptoms and hematuria.

Histopathology: Prostatic adenocarcinoma. Gleason's score: 7.


  Discussion Top


Age

The participants of this study were aged between 53 and 88 years with approximately 58.5% (n = 48) subjects being above 60 years of age. The observed higher incidence of prostatic pathology in older age coincides with observations by Jemal et al.[10] The average age of individuals with malignant tumors was 70 years, while the same for those with benign tumors was 61 years. This observation is in line with the study conducted by Al-Fartosy and Ati,[11] where they reported the average age of prostatic malignancy (68 years) to be higher than the average age of BPH (65 years).

Symptoms

According to the findings, the most commonly manifested symptom of prostatic disease was lower urinary tract infection, urinary urgency, hesitation, and frequent micturition. 75.6% of subjects (n = 62) had lower urinary tract-related symptoms. Benign tumors were discovered in 53 subjects, whereas nine patients were diagnosed with malignant tumors. The second more commonly presented condition was hematuria, which was observed in 20 subjects (20.7%). Of these, 3 were benign, whereas the rest 17 were malignant tumors. Of the sample populace, 156 (67.6%) of prostatic abnormalities found were benign, whereas 26 (32.4%) were malignant. All of the latter were adenocarcinomas.

Prostate-specific antigen level

Only individuals with PSA levels above 4 ng/mL were included in the sample. This was because Thompson et al.[12] and Schröder et al.[13] opined that that individuals with BPH and prostatitis had elevated PSA levels (>4 ng/mL). The findings indicated that the average PSA level of subjects with malignant lesions was 58.6 ng/mL, while individuals with benign conditions had an average PSA level of 21.4 ng/mL. This is in line with the conclusions from the study of Al-Fartosy and A ti. 107 where they reported average PSA of prostatic malignancy (73.2 ng/mL) to be higher than that of benign prostatic diseases (7 ng/mL). Few other studies that concluded that patients with prostatic malignancy had higher PSA than those with BPH were those of Stamey et al.[14] and Malati et al.[15]

Prostate volume

The subjects' prostates ranged in volume between 8 and 89 cm3, with the average being 37.8 cm3. 22 (26.2%) subjects presented with high-grade prostatomegaly (prostate size >40 cc), with all 22 subjects having BPH. The volume of the prostate of these specific subjects ranged between 42 and 89 cm3. As reported by Qu et al.,[16] prostates of higher volume were highly indicative of BPH. The older patients with BPH had a higher prostatic volume and higher PSA levels than BPH patients of younger age. This observation was in line with the conclusions from the studies of Mochtar et al.[17] and Roehrborn et al.[18]

TRUS gray scale

Focal hypoechoic lesions were found in 37 out of 82 patients. Of these 37 patients, only 13 were found to be malignant on histopathology. This is in line with the previous findings, such as Applewhite et al.'s[19] report on the varying appearances of prostate carcinomas on ultrasonograms. Unfortunately, TRUS alone is an inefficacious tool for assessing the presence of prostatic tumors. This is because some prostatic tumors can appear as hypoechoic areas which, when being distinct from normal parenchyma, are often noncancerous. In addition, malignant tumors can be isoechoic in its early stage; tumors can also be hyperechoic. Such variability makes TRUS somewhat ineffective.

In accordance with our findings, TRUS had a positive predictive value (PPV) of 67.12% and negative predictive value (NPV) of 95.6%. Among the 37 hypoechoic abnormalities discovered using TRUS, 13 were adenocarcinomas and 24 were benign. This is in line with the study conducted by Sharma et al.,[20] which states that majority of focal hypoechoic lesions in prostate gland are malignant in nature. Our calculations indicated that TRUS missed 4 malignant lesions and correctly diagnosed 49 malignant lesions. TRUS also correctly diagnosed 87 benign lesions and missed 24 benign lesions. Thus, TRUS had high sensitivity (92.45%) and specificity (78.38%) for cancer detection. In comparison, Terris et al.[21] reported lower sensitivity (53.3%) and specificity (75%) for TRUS.

Strain elastography

The elastographic approach we adopted was previously employed by Kamoi et al.[22] Of the total 46 subjects which were allotted benign nature on elastography, all indicated benign histopathology. This result is similar to the findings of Aigner et al.[23] Aigner et al.'s study reported that only 3 of 43 subjects had malignant tumors according to their normal elastographic data. In comparison, all our cases that underwent normal elastography were benign tumors. Thirty-six subjects were suspected to have prostatic cancer in accordance with the real-time elastography results. However, only 26 subjects had prostatic cancer. Ten cases that underwent real-time elastography were revealed to be false positives. Histopathological analysis revealed all ten to be either BPH or prostatitis (benign pathology).

In accordance with our findings, the PPV of elastography was 70.83%, which is comparable to Aigner et al.'s[23] findings. Majority of elastography Grade IV and V lesions turned out to be malignant on histopathology. The findings of this study indicate that elastography has high sensitivity and NPV, much like in Aigner et al.'s study.[23]

Comparison

Based on our findings, real-time elastography has more sensitivity and higher NPV than TRUS for the identification of prostatic cancer. Hence, it can be concluded that elastography is an effective assessment tool for ruling out the possibility of malignant tumors, helping to reduce redundant biopsies. This is in line with the conclusion made from the study of Tsutsumi et al.[24] that elastography when performed in addition to gray scale transrectal ultrasonography improves prostate cancer detection rate. The area under the regional-operational curve (ROC) is higher for elastography (89%) as compared to TRUS (87%), both being significant (i.e., >50%). This indicates that both TRUS and elastography have a significant and useful role for prostate pathology (cancer) evaluation; however, elastography performs better than TRUS.


  Conclusion Top


  1. Transrectal ultrasonography (TRUS) is an effective tool for the assessment of prostatic lesions
  2. TRUS is useful for calculating prostate size and grading prostatomegaly in cases of BPH
  3. On TRUS, hypoechoic abnormalities with higher vascularity are strong indicators of malignant tumors
  4. TRUS has high specificity, sensitivity, NPV, and PPV when assessing lesions for prostatic cancer
  5. Elastography has high sensitivity, high specificity, high PPV, and reliable NPV when detecting for prostatic cancer
  6. Elastography has reliable ability to display the homogenous tissue nature in cases of BPH and differentiate it from malignancy
  7. The specificity of elastography for malignancy can be increased when considering only Grade IV and V lesions
  8. Elastography is an effective technique for ruling out malignancies in comparison to TRUS. This implies that unnecessary biopsies may be avoided if elastography is employed
  9. The combination of TRUS and elastography can help more efficiently assess lesions and guide biopsies to increase the identification rate of prostatic cancer.


Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Jain S, Saxena S, Kumar A. Epidemiology of prostate cancer in India. Meta Gene 2014;2:596-605.  Back to cited text no. 1
    
2.
Nelen V. Epidemiology of prostate cancer. Recent Results Cancer Res 2007;175:1-8.  Back to cited text no. 2
    
3.
Dawam D, Rafindadi AH, Kalayi GD. Benign prostatic hyperplasia and prostate carcinoma in native Africans. BJU Int 2000;85:1074-7.  Back to cited text no. 3
    
4.
Halpern JA, Oromendia C, Shoag JE, Mittal S, Cosiano MF, Ballman KV, et al. Use of digital rectal examination as an adjunct to prostate specific antigen in the detection of clinically significant prostate cancer. J Urol 2018;199:947-53.  Back to cited text no. 4
    
5.
Melchior SW, Brawer MK. Role of transrectal ultrasound and prostate biopsy. J Clin Ultrasound 1996;24:463-71.  Back to cited text no. 5
    
6.
Cupp MR, Oesterling JE. Prostate-specific antigen, digital rectal examination, and transrectal ultrasonography: Their roles in diagnosing early prostate cancer. Mayo Clin Proc 1993;68:297-306.  Back to cited text no. 6
    
7.
Shinohara K, Wheeler TM, Scardino PT. The appearance of prostate cancer on transrectal ultrasonography: Correlation of imaging and pathological examinations. J Urol 1989;142:76-82.  Back to cited text no. 7
    
8.
Dudea SM, Giurgiu CR, Dumitriu D, Chiorean A, Ciurea A, Botar-Jid C, et al. Value of ultrasound elastography in the diagnosis and management of prostate carcinoma. Med Ultrason 2011;13:45-53.  Back to cited text no. 8
    
9.
Correas JM, Tissier AM, Khairoune A, Khoury G, Eiss D, Hélénon O. Ultrasound elastography of the prostate: State of the art. Diagn Interv Imaging 2013;94:551-60.  Back to cited text no. 9
    
10.
Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, et al. Cancer statistics, 2008. CA Cancer J Clin 2008;58:71-96.  Back to cited text no. 10
    
11.
Al-Fartosy AJ, Ati MH. A predictive clinical markers to make prostate cancer and benign prostate hyperplasia easy diagnosis. Biochem Cell Arch 2021;21:2939-47.  Back to cited text no. 11
    
12.
Thompson IM, Pauler DK, Goodman PJ, Tangen CM, Lucia MS, Parnes HL, et al. Prevalence of prostate cancer among men with a prostate-specific antigen level<or=4.0 ng per milliliter. N Engl J Med 2004;350:2239-46.  Back to cited text no. 12
    
13.
Schröder FH, Carter HB, Wolters T, van den Bergh RC, Gosselaar C, Bangma CH, et al. Early detection of prostate cancer in 2007. Part 1: PSA and PSA kinetics. Eur Urol 2008;53:468-77.  Back to cited text no. 13
    
14.
Stamey TA, Yang N, Hay AR, McNeal JE, Freiha FS, Redwine E. Prostate-specific antigen as a serum marker for adenocarcinoma of the prostate. N Engl J Med 1987;317:909-16.  Back to cited text no. 14
    
15.
Malati T, Kumari GR, Murthy PV, Reddy CR, Prakash BS. Prostate specific antigen in patients of benign prostate hypertrophy and carcinoma prostate. Indian J Clin Biochem 2006;21:34-40.  Back to cited text no. 15
    
16.
Qu X, Huang Z, Meng X, Zhang X, Dong L, Zhao X. Prostate volume correlates with diabetes in elderly benign prostatic hyperplasia patients. Int Urol Nephrol 2014;46:499-504.  Back to cited text no. 16
    
17.
Mochtar CA, Kiemeney LA, van Riemsdijk MM, Barnett GS, Laguna MP, Debruyne FM, et al. Prostate-specific antigen as an estimator of prostate volume in the management of patients with symptomatic benign prostatic hyperplasia. Eur Urol 2003;44:695-700.  Back to cited text no. 17
    
18.
Roehrborn CG, Boyle P, Gould AL, Waldstreicher J. Serum prostate-specific antigen as a predictor of prostate volume in men with benign prostatic hyperplasia. Urology 1999;53:581-9.  Back to cited text no. 18
    
19.
Applewhite JC, Matlaga BR, McCullough DL, Hall MC. Transrectal ultrasound and biopsy in the early diagnosis of prostate cancer. Cancer Control 2001;8:141-50.  Back to cited text no. 19
    
20.
Sharma M, Nerli RB, Nutalapati SH, Ghagane SC. Hypoehoic lesions on transrectal ultrasound and its correlation to Gleason grade in the diagnosis of clinically significant prostate cancer: A prospective study. South Asian J Cancer 2021;10:155-60.  Back to cited text no. 20
    
21.
Terris MK, Freiha FS, McNeal JE, Stamey TA. Efficacy of transrectal ultrasound for identification of clinically undetected prostate cancer. J Urol 1991;146:78-83.  Back to cited text no. 21
    
22.
Kamoi K, Okihara K, Ochiai A, Ukimura O, Mizutani Y, Kawauchi A, et al. The utility of transrectal real-time elastography in the diagnosis of prostate cancer. Ultrasound Med Biol 2008;34:1025-32.  Back to cited text no. 22
    
23.
Aigner F, Pallwein L, Junker D, Schäfer G, Mikuz G, Pedross F, et al. Value of real-time elastography targeted biopsy for prostate cancer detection in men with prostate specific antigen 1.25 ng/ml or greater and 4.00 ng/ml or less. J Urol 2010;184:913-7.  Back to cited text no. 23
    
24.
Tsutsumi M, Miyagawa T, Matsumura T, Kawazoe N, Ishikawa S, Shimokama T, et al. The impact of real-time tissue elasticity imaging (elastography) on the detection of prostate cancer: Clinicopathological analysis. Int J Clin Oncol 2007;12:250-5.  Back to cited text no. 24
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4]
 
 
    Tables

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



 

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

 
  In this article
Abstract
Introduction
Materials and Me...
Results
Discussion
Conclusion
References
Article Figures
Article Tables

 Article Access Statistics
    Viewed306    
    Printed18    
    Emailed0    
    PDF Downloaded42    
    Comments [Add]    

Recommend this journal


[TAG2]
[TAG3]
[TAG4]