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DOI:10.2214/AJR.07.2429
AJR 2007; 189:1380-1386
© American Roentgen Ray Society

Original Research

Dynamic Contrast Enhancement Patterns of Solitary Pulmonary Nodules on 3D Gradient-Recalled Echo MRI

Fuldem Yildirim Donmez1,2, Ensar Yekeler1, Violet Saeidi1, Atadan Tunaci1, Mehtap Tunaci1 and Gulden Acunas1

1 Department of Radiology, Istanbul University, Istanbul Faculty of Medicine, Istanbul, Turkey.
2 Present address: Department of Radiology, Baskent University, Faculty of Medicine, 46 Sokak No. 11/8 Yuksel Apt, 06500, Bahcelievler, Ankara, Turkey.

Received September 21, 2006; accepted after revision June 19, 2007.

 
Address correspondence to F. Yildirim Donmez (fuldemyildirim{at}yahoo.com).


Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
OBJECTIVE. The purpose of this study was to determine whether contrast enhancement features on 3D volumetric gradient-recalled echoMR images allow differentiation of benign from malignant solitary pulmonary nodules.

MATERIALS AND METHODS. Forty patients with solitary pulmonary nodules (range of greatest diameter, 7–40 mm) detected on CT underwent unenhanced MRI and contrast-enhanced MRI performed in 10 consecutive dynamic 3D volumetric gradient-recalled echo sequences every 30 seconds. Contrast enhancement patterns (homogeneous, heterogeneous, rim, peripheral, and central) of the lesions were visually evaluated, and time–intensity curves of the lesions were drawn.

RESULTS. Twenty patients had benign lesions (nine, tuberculoma; one, aspergilloma; nine, round atelectasis; one, postinflammatory nodule). The other 20 patients had malignant lesions (18, primary lung cancer; two, metastasis). At visual analysis, all 20 malignant lesions displayed peripheral enhancement with progressive heterogeneous fill-in on the late images. All nine tuberculomas and the aspergilloma had rim enhancement, and all nine round atelectasis lesions and the postinflammatory nodule had early intense homogeneous enhancement. Regarding the time–intensity curves, all malignant lesions except one lung cancer lesion had early peak enhancement with rapid washout. All benign lesions displayed early increasing enhancement with an early plateau in the second minute after contrast administration (nine tuberculomas and one aspergilloma) or a late plateau in the fourth minute (nine round atelectasis lesions and one postinflammatory nodule).

CONCLUSION. Rim contrast enhancement is highly valuable in the diagnosis of tuberculoma. Time–intensity curve types can be taken into consideration for noninvasive differentiation of lung cancer, tuberculoma, and round atelectasis.

Keywords: 3D imaging • dynamic contrast enhancement • gradient-recalled echo sequence • MRI • pulmonary nodule


Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Asolitary pulmonary nodule (SPN) is commonly encountered in daily radiologic practice, especially since the introduction of MDCT [1]. Frequent CT follow-up to determine the growth rate of SPNs is currently an acceptable approach [2, 3]. Even when low-dose CT is used for follow-up, radiation exposure of these patients is considerable, and most of them end up without a diagnosis of malignant pulmonary disease [4, 5].

Characterization of SPNs with CT is based on the morphologic features and attenuation of the nodule, which are inadequate for characterizing most uncalcified and non-fat-containing SPNs. When dynamic CT shows inconsistent results between morphologic and hemodynamic characteristics, PET/CT may be a valuable noninvasive study for evaluation of an indeterminate SPN. However, the lower sensitivity, lower specificity, and higher cost of the technique must be factored into the evaluation of any pulmonary nodule [6–8]. Because the rate of unnecessary resection of benign SPNs is as high as 30% [9–11], the aim of radiologists is not only early detection of malignant tumors but also reduction in the number of unnecessary invasive procedures such as CT-guided transthoracic biopsy, transbronchial biopsy, and surgery for benign lesions. To reduce this high percentage of resected benign SPNs, MRI has been used to characterize SPNs morphologically and kinetically.

The advantage of using dynamic contrast-enhanced MRI in tumor characterization has been found in several studies, but in most of the studies, dynamic images were obtained with a 2D gradient-recalled echo (GRE) sequence with a long TR, which can cause susceptibility between the air space and the nodule and lead to a gap between slices [12–14]. Three-dimensional GRE volumetric interpolated breath-hold examination provides volumetric data without a gap and causes minimum susceptibility between the air space and nodules by use of acquisition with slab technique and a short TR, respectively [15–17]. In this study, SPNs were evaluated for T1- and T2-weighted signal intensity and signal-to-noise ratio (SNR). In addition, the nodules were evaluated with a 3D GRE MR angiographic sequence to evaluate qualitative and quantitative contrast enhancement features in differentiation of benign and malignant lesions.


Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Patient Population
Over a 2-year period, 40 patients (33 men, seven women; mean age, 54 years; range, 32–80 years) who had a round or oval SPN newly detected on CT were prospectively enrolled in the study. CT had been performed for a variety of clinical indications, such as heavy-smoker screening, possibility of infection, tuberculosis detected on follow-up, metastasis screening in patients with known primary cancer, and presence of a suspicious nodular lesion on a chest radiograph. The inclusion criteria were as follows: lesion size 5–40 mm, no calcification or fat in the lesion on CT, no history of immune deficiency, and no contraindication to IV injection of gadolinium or MRI examination. Patients with active infection according to laboratory findings such as leukocytosis and elevated C-reactive protein level and erythrocyte sedimentation rate and patients not able to cooperate with breath-holding were excluded.

All patients underwent MRI to characterize the signal-intensity features and contrast enhancement patterns of the lesions. Final diagnoses of the lesions were confirmed at histopathologic or microbiologic examination of the specimens, which were obtained with CT-guided transthoracic fine-needle biopsy, transbronchial needle biopsy, brush biopsy, bronchoalveolar lavage, surgery, and follow-up for 1.5–2 years (Table 1). The study protocol was approved by the institutional review board, and informed consent was obtained from the patients before MRI.


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  		TABLE 1: Methods of Diagnosis of Solitary Pulmonary Nodules

 

MRI
All patients underwent imaging on a 1.5-T MRI unit (Symphony, Siemens Medical Solutions) with gradient-switching capability of 30 mT/m. All MRI examinations were performed with a four-element phased-array torso coil. Echo-planar imaging (TR/TE, infinity/8; matrix size, 75 x 256; slice thickness, 6 mm; interslice gap, 0.6 mm) in both the axial and coronal planes was performed to localize the SPNs.

The imaging sequences were as follows: 2D T1-weighted GRE (145/4.8; flip angle, 70°; slice thickness, 6 mm; interslice gap, 0.6 mm; number of slices, 12; matrix size, 196 x 256; acquisition time, 19 seconds), T2-weighted turbo spin-echo (3,910/99; flip angle, 150°; slice thickness, 6 mm; interslice gap, 0.6 mm; number of slices, 14; matrix size, 256 x 128; acquisition time, 20 seconds), STIR turbo spin-echo (3,910/99; inversion time, 145 milliseconds; flip angle, 150°; slice thickness, 6 mm; interslice gap, 0.6 mm; number of slices, 14; matrix size, 256 x 128; acquisition time, 20 seconds), and 3D GRE fast low-angle shot (FLASH) (5.2/2.5; flip angle, 10°; slab thickness, 78–96 mm; slice thickness, 3 mm; matrix size, 196 x 256; acquisition time, 12–16 seconds). All sections were in the axial plane. The field of view varied with the size of the patient, ranging from 25 x 35 cm to 30 x 38 cm.

Two parallel (axial) saturation bands were applied above and below the imaging volume to saturate signal from inflowing blood. The patients were informed about the procedure and breath-holding before dynamic imaging. The expiratory phase was preferred for reducing the slice differences between phases. After unenhanced 3D FLASH images were obtained, 0.1 mmol/kg of gadopentetate dimeglumine (Magnevist, Bayer HealthCare) was injected at a rate of 2 mL/s through an antecubital vein and was followed by infusion of 20 mL of normal saline solution at the same rate through an automatic infusion system (Spectris, Medrad). Dynamic examinations were started at the 10th second after the initiation of injection of the IV contrast medium. A total of 10 consecutive acquisitions were made at 30-second intervals with the parameters used for the unenhanced images. All 40 dynamic MRI studies were completed successfully, and no adverse effects were detected.

Image Interpretation
All data were subjected to qualitative and quantitative evaluation at a workstation (Leonardo, Siemens Medical Solutions). Three blinded radiologists with 8, 6, and 5 years of experience conducted the image analysis by consensus. The volumetric and region of interest (ROI) measurements were performed by the radiologist with 8 years of experience in thoracic radiology. The sizes of the lesions were determined by largest diameter. The lesions were evaluated on the basis of three criteria: signal intensity characteristics, SNR, and dynamic contrast enhancement features. The readers subjectively assessed the signal characteristics of the lesions as hypointense, isointense, and hyperintense in comparison with thoracic wall muscle on T1-weighted GRE, T2-weighted turbo spin-echo, and STIR images. For objective evaluation, an ROI (mean, 0.69 cm2; range, 0.09–1.10 cm2) was drawn over the lesion. The ROI was made as large as possible to involve a minimum of 50% of the lesion and to avoid hemodynamic inhomogeneity. On the same slice, another ROI of the same size was placed in three different areas on the background noise in the phase-encoding direction, and three measurements were averaged to calculate the SNR as the signal intensity of the lesion divided by the SD of the background noise.

Contrast enhancement features (homogeneous, heterogeneous, rim, peripheral, and central) of the lesions on dynamic contrast-enhanced 3D FLASH images were visually assessed, as was curve type. Contrast enhancement was noted as rim enhancement when a thin layer of contrast enhancement was limited to the outer margin of the lesion and as peripheral enhancement when thick contrast enhancement surrounded the lesion, which showed progressive central filling. For obtaining the curve, the ROI was positioned in the peripheral nonnecrotic area of the lesion where there was the most prominent enhancement. In the case of rim enhancement alone, the ROI was placed only on the rim. Time–signal intensity curves were obtained with the Mean Curve program (Siemens Medical Solutions).

Statistical Analysis
All statistical analyses were performed with SPSS statistical software (SPSS). Signal-intensity features of the malignant and benign lesions were tested for significance with the Mann-Whitney U test. Categoric variables were compared by use of the chi-square test. A value of p < 0.05 was considered statistically significant. For data sets with more than two variables, as in comparison of SNRs of malignant lesions, tuberculomas, and round atelectasis, nonparametric analysis of variance (Kruskal-Wallis) was performed. Bonferroni adjustment was applied for p values in those cases.


Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Twenty malignant lesions (18 lung cancer and two metastasis) and 20 benign lesions (nine tuberculoma, one aspergilloma, nine round atelectasis, and one postinflammatory nodule) were diagnosed. The histologic types of the 18 cases of lung cancer were adenocarcinoma (n = 9), squamous cell carcinoma (n = 5), small cell carcinoma (n = 3), and carcinoid (n = 1) (Table 2). The size range of all 40 lesions was 7–40 mm (7–32 mm for benign lesions, 10–40 mm for malignant lesions). The mean size of all of the lesions was 25.7 mm (benign lesions, 21.7 mm; malignant lesions, 29 mm). The number and mean largest diameter of the lesions according to histopathologic results are tabulated in Table 2. All of the lesions were round or oval. Two of the tuberculomas had small cavitations, and two adenocarcinomas had central necrosis.


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  		TABLE 2: Histopathologic Findings in Solitary Pulmonary Nodules (n = 40)

 

In subjective evaluation of the signal intensity characteristics, the lesions were grouped as malignant and benign on the basis of morphologic appearance. The T1- and T2-weighted signal intensity features of all lesions are tabulated in Table 3. Signal intensity features of the malignant and benign lesions were not different in the T1-weighted GRE (p = 0.056) and T2-weighted (p = 1) sequences.


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  		TABLE 3: Signal Intensity Features of Lesions Compared with Thoracic Wall Muscle (n = 40)

 

Round atelectasis lesions had the highest SNRs, and tuberculomas had the lowest SNRs on both T1-weighted GRE and T2-weighted sequences. Round atelectasis had a significantly higher SNR than did either malignant lesions or tuberculomas on T2-weighted images (p < 0.05) or tuberculomas on T1-weighted GRE images (p = 0.003). When malignant lesions and tuberculomas were compared, the former had a significantly higher SNR on T1-weighted GRE (p <0.05) but not on T2-weighted images.

Visual analysis of the contrast enhancement patterns showed that all of the histopathologically malignant lesions (n = 20) displayed peripheral enhancement with progressive heterogeneous fill-in on the late images (Figs. 1A, 1B, 1C, 1D, 1E, 1F). Only one adenocarcinoma had diffusely homogeneous enhancement (Fig. 2A). All of the histopathologically benign lesions had either rim enhancement (nine tuberculomas, one aspergilloma) (Fig. 3A) or early intense homogeneous enhancement (nine round atelectasis lesions, one postinflammatory nodule) (Fig. 4A).


Figure 1
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  		Fig. 1A —48-year-old man with adenocarcinoma of left lung. Dynamic contrast-enhanced 3D fast low-angle shot images (TR/TE, 5.2/2.5; flip angle, 10°; slab thickness, 78–96 mm; slice thickness, 3 mm; matrix size, 196 x 256) show peripheral enhancement with progressive heterogeneous fill-in of left apical lung cancer.

 

Figure 2
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  		Fig. 1B —48-year-old man with adenocarcinoma of left lung. Dynamic contrast-enhanced 3D fast low-angle shot images (TR/TE, 5.2/2.5; flip angle, 10°; slab thickness, 78–96 mm; slice thickness, 3 mm; matrix size, 196 x 256) show peripheral enhancement with progressive heterogeneous fill-in of left apical lung cancer.

 

Figure 3
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  		Fig. 1C —48-year-old man with adenocarcinoma of left lung. Dynamic contrast-enhanced 3D fast low-angle shot images (TR/TE, 5.2/2.5; flip angle, 10°; slab thickness, 78–96 mm; slice thickness, 3 mm; matrix size, 196 x 256) show peripheral enhancement with progressive heterogeneous fill-in of left apical lung cancer.

 

Figure 4
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  		Fig. 1D —48-year-old man with adenocarcinoma of left lung. Dynamic contrast-enhanced 3D fast low-angle shot images (TR/TE, 5.2/2.5; flip angle, 10°; slab thickness, 78–96 mm; slice thickness, 3 mm; matrix size, 196 x 256) show peripheral enhancement with progressive heterogeneous fill-in of left apical lung cancer.

 

Figure 5
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  		Fig. 1E —48-year-old man with adenocarcinoma of left lung. Dynamic contrast-enhanced 3D fast low-angle shot images (TR/TE, 5.2/2.5; flip angle, 10°; slab thickness, 78–96 mm; slice thickness, 3 mm; matrix size, 196 x 256) show peripheral enhancement with progressive heterogeneous fill-in of left apical lung cancer.

 

Figure 6
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  		Fig. 1F —48-year-old man with adenocarcinoma of left lung. Dynamic contrast-enhanced 3D fast low-angle shot images (TR/TE, 5.2/2.5; flip angle, 10°; slab thickness, 78–96 mm; slice thickness, 3 mm; matrix size, 196 x 256) show peripheral enhancement with progressive heterogeneous fill-in of left apical lung cancer.

 

Figure 8
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  		Fig. 2A —45-year-old man with adenocarcinoma of right lung. Dynamic contrast-enhanced 3D fast low-angle shot late-phase image (TR/TE, 5.2/2.5; flip angle, 10°; slab thickness, 78–96 mm; slice thickness, 3 mm; matrix size, 196 x 256) shows diffusely enhancing mass (arrows) on posterobasal segment of right lung.

 

Figure 10
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  		Fig. 3A —52-year-old woman with tuberculosis. Dynamic contrast-enhanced 3D fast low-angle shot image (TR/TE, 5.2/2.5; flip angle, 10°; slab thickness, 78–96 mm; slice thickness, 3 mm; matrix size, 196 x 256) shows rim enhancement of left apical tuberculoma (arrows).

 

Figure 12
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  		Fig. 4A —56-year-old man with round atelectasis. Dynamic contrast-enhanced 3D fast low-angle shot image (TR/TE, 5.2/2.5; flip angle, 10°; slab thickness, 78–96 mm; slice thickness, 3 mm; matrix size, 196 x 256) shows intense homogeneous enhancement of round atelectasis lesion (arrow).

 
When the time–signal intensity curve types of the lesions were assessed, all but one of the 18 lung cancer lesions and the two metastatic lesions had a type A pattern (early increasing enhancement with rapid washout) (Fig. 1G). One lung cancer lesion had a type D pattern (gradually increasing enhancement) (Fig. 2B). Nine tuberculomas and one aspergilloma had a type B pattern (early increasing enhancement with early plateau in second minute [range, 1.8–2.1 minutes]) (Fig. 3B). All of the nine atelectasis lesions and one postinflammatory nodule had a type C pattern (early increasing enhancement with late plateau in fourth minute [range, 3.9–4.2 minutes]) (Fig. 4B). The types of the curves are tabulated in Table 4.


Figure 7
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  		Fig. 1G —48-year-old man with adenocarcinoma of left lung. Time–signal intensity curve obtained from periphery of lesion in A shows type A pattern (early increasing enhancement with rapid washout).

 

Figure 9
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  		Fig. 2B —45-year-old man with adenocarcinoma of right lung. Time–signal intensity curve obtained from lesion in A shows type D pattern (gradually increasing enhancement).

 

Figure 11
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  		Fig. 3B —52-year-old woman with tuberculosis. Time–signal intensity curve obtained from rim of tuberculoma in A depicts type B pattern (early increasing enhancement with early plateau at second minute).

 

Figure 13
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  		Fig. 4B —56-year-old man with round atelectasis. Time–signal intensity curve obtained from lesion in A shows type C pattern (early increasing enhancement with late plateau at fourth minute).

 

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  		TABLE 4: Time–Intensity Curves of Lesions Obtained on Dynamic 3D Fast Low-Angle Shot Images (n = 40)

 


Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
In the past, MRI of the lung was not effective because of low proton density and strong susceptibility artifacts at air–tissue interfaces, low signal intensity, inevitable artifacts caused by breathing and cardiac pulsation, and poor image resolution. Breath-hold 2D GRE sequences were used in initial experience, but they did not avoid ghosting artifacts from pulsating vessels. These images, therefore, were not routinely used [18, 19]. Since the introduction of 3D MRI techniques, fewer artifacts occur on pulmonary MR images than on 2D GRE images [15]. Volumetric interpolated breath-hold examination, a 3D GRE technique, meets the needs of minimizing partial volume effects, maximizing image contrast enhancement, and improving evaluation of the tissue [20]. High spatial resolution, thin slices, and short acquisition times make 3D GRE sequences a promising technique for dynamic imaging of the lung [18].

Several studies of dynamic MRI of the lung for differentiation of malignant from benign nodules have been described. Ohno et al. [12] stated that mean relative enhancement ratio and mean slope of enhancement were valuable in differentiation. Tozaki et al. [17] concluded that internal enhancement and visual washout were signs of malignancy with a positive predictive value of 91%. In this study, we described four distinctive curve types objectively obtained with software rather than a visual evaluation that enable differentiation of benign and malignant nodules. We also described subgroups of benign lesions, such as tuberculoma and round atelectasis. The type A curve, showing early washout, was found 95% sensitive for malignant nodules. Type B and C curves had specificity and sensitivity ratios of 100% for all remaining lesions, showing that the dynamic MRI characteristics of lesions are valuable criteria. In another study [12], overlapping of active infection and malignancy in analysis of maximum relative enhancement ratio and slope of enhancement explained both increased blood flow and perfusion and capillary permeability. We did not include patients with laboratory findings of active infection, which may be why the washout pattern was unique for malignant nodules. The different plateau times for tuberculoma (second minute) and round atelectasis (fourth minute) can be explained by increased blood flow to the inflamed rim of the tuberculomas, which led to an earlier equilibrium phase.

In addition to identification of curve types, visual analysis of the enhancement patterns was helpful for differentiating benign and malignant nodules. In this study, increased vascularity of the malignant nodules manifesting as early peripheral enhancement with progressive diffuse heterogeneous fill-in on late dynamic MR images was highly suggestive of lung carcinoma.

Differentiation of tuberculoma from lung cancer on the basis of T1- and T2-weighted signal intensity was studied by Chung et al. [21]. They found that nine of 11 tuberculomas but only two of 17 lung cancer lesions were hypointense on T2-weighted images. Conversely, in our patient group, all nine tuberculomas were hyperintense on T2-weighted images. Seven of these lesions were found to have caseation necrosis at histopathologic examination. The discrepancy between the two studies may be due to the different stages of tuberculoma. If it is a relatively newly formed lesion, tuberculoma may contain a liquefied component rather than fibrosis, and the liquid appears as high signal intensity on T2-weighted images. On dynamic contrast-enhanced images, we found that tuberculomas had thin rimlike enhancement. This finding corresponded to the fibrous capsule and epithelioid granulomas in a study by Sakai et al. [22], whereas on pathologic examination the central portions that did not become enhanced were composed of caseous necrosis.

Round atelectasis is said to be strongly associated with asbestos exposure and may be associated with pleural scarring from tuberculosis and other causes. In a study including 20 patients followed 1 month–4 years, it was concluded that pleural effusion in the absence of exposure to asbestos can cause round atelectasis. The pathogenesis of round atelectasis involves initial injury to the pleura, pleural effusion or an inflammatory reaction, and subsequent fibrosis. The fibrous tissue matures and contracts, collapsing the underlying lung [23, 24]. Morphologic CT findings are mostly diagnostic, but in some cases they can be indeterminate. Therefore, other criteria are being investigated with different imaging techniques. Hakomaki et al. [25] found that on contrast-enhanced CT, round atelectasis had higher attenuation values and more homogeneous enhancement than malignant lung tumors. McAdams et al. [26] suggested that round atelectasis is not metabolically active on 18F-FDG PET; thus FDG PET can play a role in differentiating round atelectasis from malignant lesions when there are few or atypical features of round atelectasis on chest radiographs and CT. Few articles have been written on the MRI appearance of round atelectasis.


Figure 14
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  		Fig. 5 —Algorithm for evaluation of solitary pulmonary nodules.

 
Yamaguchi et al. [27] found that round atelectasis became homogeneously enhanced after administration of gadolinium to eight patients, two of whom underwent dynamic imaging. One of the lesions had early enhancement in the medial caudal portions, and the other had inhomogeneous enhancement, but both had homogeneous enhancement in the late phase. In our study, regardless of the cause of the lesions, all cases of round atelectasis had an intense homogeneous enhancement pattern. Besides the significant enhancement pattern of the lesions, round atelectasis was found separate from malignant lesions and tuberculomas on the basis of having the highest SNRs on both T1-and T2-weighted images. This finding may be a clue to differentiating round atelectasis from other lesions on unenhanced images. However, round atelectasis is most commonly diagnosed on the basis of its typical morphologic features on CT. Therefore, data on signal characteristics in large series were not available in the literature for comparison with our findings.

In the approach to SPNs in our routine practice, we compare the lesion to the findings on previous chest radiographs or CT scans. We leave the lesion alone if there is no change in size over a 2-year period. If the lesion increases in size or changes in shape, we perform a biopsy. For a lesion newly detected on a chest radiograph, we perform CT, evaluate the morphologic criteria as benign or malignant, and in the case of suspicion of malignancy, we perform a biopsy. In this study, however, we found MRI useful in evaluation of patients who had newly detected SPNs on chest radiographs or CT scans before any invasive procedure was performed, so MRI has been included in our algorithm (Fig. 5). For instance, if the result of visual and time–intensity curve analysis of contrast enhancement had been used as the sole criterion, invasive procedures would have been avoided in the cases of 18 patients in this study who had benign nodules.

There were several limitations to our study. First was the relatively small number of patient groups. The statistical analysis would have been more accurate in the subgroups if the number of patients had been larger. Second, because the contrast enhancement patterns were determined by consensus, it was not possible to assess interobserver differences.

In conclusion, the signal intensity features and SNRs of SPNs depicted on T1- and T2-weighted MR images are not sufficient for definite differentiation of malignant and benign lesions. Rim contrast enhancement is significant for tuberculoma, rapid washout for lung cancer, and intense homogeneous enhancement for round atelectasis. Time–signal intensity curves are highly valuable in differentiation of malignant lesions, tuberculoma, and round atelectasis.


References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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