|Year : 2014 | Volume
| Issue : 5 | Page : 612-619
Deep vein thrombosis of the lower limbs: A retrospective analysis of doppler ultrasound findings
Sanjay M Khaladkar, Dhaval K Thakkar, Kunal Shinde, Dolly K Thakkar, Harshawardhan Shrotri, Vilas M Kulkarni
Department of Radio-Diagnosis, Padmashree Dr. D. Y. Patil Medical College, Hospital and Research Centre, Dr. D. Y. Patil Vidyapeeth, Pimpri, Pune, Maharashtra, India
|Date of Web Publication||10-Sep-2014|
Sanjay M Khaladkar
Flat No. 5, Plot No. 8, S. No. 26/A, Tejas Bldg, Sahawas Society, Karve Nagar, Pune - 411 052, Maharashtra
Source of Support: None, Conflict of Interest: None
Background: Deep venous thrombosis (DVT) of lower limbs is one of the most common cause for the majority of deaths caused by pulmonary embolism. Many medical and surgical disorders are complicated by DVT. Most venous thrombi are clinically silent. B-mode and color Doppler imaging is needed for early diagnosis of DVT to prevent complications and sequalae of DVT. Aim and Objectives: The objectives of the following study were to evaluate the role of Doppler as an imaging modality in diagnosing DVT of lower limbs, to study the spectrum of findings on Doppler ultrasound in patients with DVT. Materials and Methods: Retrospective descriptive analysis of 78 patients of DVT diagnosed on Doppler. Results: Nearly 74% of the patients were males and 26% were females with majority belonging to fifth decade (26%). 75 (96.1%) cases showed unilateral while 3 (3.9%) cases showed bilateral lower limb involvement. In our study, predominant distribution of thrombus was found to be in above knee region with 69/78 (88.5%) patients having thrombus in the superficial femoral vein. Popliteal vein was involved in 54/78 (69.2%) patients. Complete thrombosis was observed in 54/78 (69%) cases, while partial thrombosis was observed in 24/78 (31%) cases. Subacute stage was seen in 42 cases (53.8%), acute stage in 23 cases (29.5%) while chronic stage in 13 cases (16.7%). 71 cases (91%) had multiple contiguous segmental involvement, whereas 7 cases (9%) had isolated vein involvement. Conclusion: Color Doppler is useful in diagnosing DVT in symptomatic and at risk patients and provides a non-invasive method of investigation. It is also helpful in evaluating the site, extent and stage of thrombus.
Keywords: Color flow duplex venous examination, deep venous thrombosis, duplex scanning, pulmonary embolism, venous thromboembolism
|How to cite this article:|
Khaladkar SM, Thakkar DK, Shinde K, Thakkar DK, Shrotri H, Kulkarni VM. Deep vein thrombosis of the lower limbs: A retrospective analysis of doppler ultrasound findings. Med J DY Patil Univ 2014;7:612-9
|How to cite this URL:|
Khaladkar SM, Thakkar DK, Shinde K, Thakkar DK, Shrotri H, Kulkarni VM. Deep vein thrombosis of the lower limbs: A retrospective analysis of doppler ultrasound findings. Med J DY Patil Univ [serial online] 2014 [cited 2019 Jan 16];7:612-9. Available from: http://www.mjdrdypu.org/text.asp?2014/7/5/612/140449
| Introduction|| |
Venous thromboembolism (VTE) is a significant, but relatively under diagnosed health problem. The threat of deep venous thrombosis (DVT) and pulmonary embolism (PE) is a daily concern in intensive care unit (ICU), hospitalized and bedridden patients. Early diagnosis of DVT is mandatory to prevent unnecessary deaths from PE. The incidence of DVT varies in different parts of the world for reasons that are not yet completely understood.  Though, some of the recent studies published from other Asian countries have shown that DVT is not a rarity in Asian patients as was thought earlier.  The incidence of DVT in the general population has been estimated to be 80-100/1,00,000 annually in the western societies,  4-75/1,00,000 in South-Asia.  In India, the incidence of DVT is not well highlighted and literature survey shows scanty works in this field. Most of the literature available in India is from the orthopedic departments, overall incidence of DVT in the general population is largely unknown. 
Risk of new postoperative DVT rises from 26% to 68%, respectively. In patients on bed rest in a general medical ward, the rate of DVT is 10% but in an ICU it is 29%. 
VTE is the third most common cardiovascular illness after acute coronary syndrome and stroke. PE is the third most common cause of hospital related death and the most common preventable cause of hospital related death.  Most hospitalized patients have at least 1 or more risk factors for VTE (Wells score). 
A proximal lower-extremity DVT (defined as occurring in the popliteal vein and above) is linked to an estimated 50% risk of PE if not treated; while approximately 20-25% of calf vein thrombi propagate (in the absence of treatment) to involve the popliteal vein or above. PE occurs in between 15% and 32% of cases following DVT in a lower extremity. The majority of patients die because of a failure in diagnosis rather than inadequate therapy. In fact, the mortality rate for PE without treatment is approximately 30%. 
Many medical and surgical disorders are complicated by DVT. The common signs of DVT are pain and swelling of affected lower limbs. It may in turn cause structural damage to the valves of deep veins resulting into post phlebitic syndrome.  Exaggeration of the normal process of hemostasis may be considered as a functional cause for development of a thrombus within a vein.
The patients after a major surgery, trauma and prolonged immobilization such as in acute myocardial infarction, congestive cardiac failure, stroke and postoperative convalescence form a major group of patients at high risk for DVT. Neoplasm's, pregnancy, oral contraceptive pills and hypercoaguable states are a few other risk factors to mention.
DVT occurs along a continuum with propagation, extension and progression.  Probably because DVT do not totally obstruct the vein in early stages and also due to the presence of collateral circulation, most venous thrombi are clinically silent when they are first detectable by objective methods. Fewer than the third patients among those having symptoms in the lower extremities present with the classic syndrome of edema, calf discomfort, venous distension and pain on forced dorsiflexion of the foot (Homan's sign).
Thus to prevent the complications and sequalae by early and appropriate treatment instillation, there is a need of an objective technique to supplement and confirm the clinical diagnosis of DVT.
The diagnosis and treatment of DVT has irrevocably been altered after the introduction of Doppler ultrasound (USG) technique. The principle used is that the venous flow pattern of the vein gets distorted due to thrombotic obstruction which is readily detected by the Doppler instrument. Doppler USG can be used in pregnant women, permits multiple views in various positions of leg and it is safe, painless and inexpensive. It is also non-invasive technique and can be repeatedly used, performed rapidly in the clinic, at patient's bedside or even at home and the results are available immediately. The test is useful in high risk patients as a screening modality to ensure early diagnosis and treatment. The duplex scan can diagnose many thrombi at a stage when no major changes have occurred in the venous hemodynamic and the patient is asymptomatic or minimally symptomatic. 
| Materials and Methods|| |
A retrospective descriptive analytical study was carried out on 78 patients of DVT diagnosed on Venous Doppler in the Department of Radio-diagnosis, Padmashree Dr. D.Y. Patil Medical College, Hospital and Research Centre, Pimpri, Pune over a period of 2 years from September 2011 to September 2013. The equipments used were MicroMaxx SonoSite M-turbo portable USG machine (Probe frequency range - Linear: HFL38-13-6 MHz, Curvilinear: C60e-5-2 MHz), Siemens Acuson X300 USG machine (Probe frequency range-Linear: VF-10-5 MHz, Curvilinear: C-6-2 MHz) and Siemens Acuson Antares USG machine (Probe frequency range-Linear: VF-13-5 MHz Curvilinear: CH-6-2 MHz).
Analysis of cases of DVT was done in terms of age and sex wise distribution, symptoms and signs, predisposing conditions, anatomic distribution and stage of involvement of thrombus and pattern of involvement of veins.
The inclusion criteria are DVT diagnosed on B-mode and color Doppler study in clinically suspected cases of DVT. Pediatric and neoplastic cases were excluded.
The Doppler report described the presence or absence of deep vein thrombosis, location, extent, nature (acute, subacute or chronic) and complications, if any. Standard examination involved evaluation of common femoral vein (CFV) and superficial femoral vein first, followed by popliteal and calf veins. External iliac veins and inferior vena cava (IVC) were evaluated at last. Muscular veins in calf were examined as per the case. Proximal portion of great saphenous vein (GSV) was examined.
To ensure adequate distention of the venous system, patients were examined in a sitting position or in reverse Trendelenburg's position at about 15 or 20°.  Characteristics of venous flow and the effects of compression were examined in all venous segments. Relevant Doppler information was obtained from color flow signal during color Doppler study of venous segment imaged at any 1 time. 
CFV, sapheno-femoral junction, superficial and deep femoral veins, popliteal vein, anterior and posterior tibial veins, peroneal veins and muscular veins were evaluated in longitudinal and transverse plane initially on B-mode and then on color Doppler study. Linear array transducers (13-5 MHz frequency range depending on the machine) were used for femoral and popliteal venous segments and for calf veins. Convex transducers (6-2 MHz frequency range depending on the machine) were used for evaluation of iliac veins and IVC. Presence, characteristics and extent of thrombus was looked for. Compression technique, Valsalva maneuver and augmentation were used to evaluate complete/partial thrombosis, proximal obstruction and patency of distal veins respectively. Recanalization and collaterals were looked for. Isolated/multiple contiguous or non-contiguous segment involvement of DVT was looked for. The examination of the calf veins included an attempt at visualization of the gastrocnemius and soleal veins.
When Doppler signals were abnormal or when there were other findings suggestive of obstruction at the level of groin, the iliac veins were examined. 
The following criteria were followed in this study for DVT diagnosis: 
- Visualization of thrombus.
- Vein compressibility.
- Vein size.
- Respiratory changes.
The veins were evaluated for: 
- Absent or reduced compressibility of the vein.
- Thrombus in the vein, static echoes in complete color fill in full expansion of vein.
- Static valve leaflets.
- Absent flow on spectral color Doppler.
- Impaired or absent augmentation of flow.
- Loss of spontaneous and respiratory variation.
- Increased flow in controlled canal.
| Results|| |
A total of 78 patients were identified to have DVT. The age of patients ranged from 21 to 83 years with a mean age of 47 years. The incidence was highest in the fifth decade [Table 1]. Out of the 78 patients showing evidence for DVT, male predominance was found that constituted 74.4% of the cases [Table 2]. Edema (61%), pain and edema (17%), previous history of DVT (11%), pain (8%) were the presenting symptoms while 3% patients presented with PE [Table 3]. It was found that prolonged hospitalization/immobilization were the most common predisposing factor, followed by postoperative cause and trauma. However no predisposing condition was found in the majority of the patients [Table 4]. Bilateral lower limb DVT was observed in 3 cases (4%), unilateral lower limb involvement was seen in 75 (96%) cases, thus showing predominant unilateral lower limb involvement. Total number of extremities involved were 81.
Left lower limb involvement was seen in 67 (82.7%) cases, right lower limb involvement was seen in 14 (17.3%) cases. The left lower limb predominance was noted in our study. Predominant distribution of thrombus in our study was found to be in the above knee region with approximately (88.5%) of the patients having thrombus in the superficial femoral vein. Popliteal vein [Figure 1] and [Figure 2] was involved in 69.2% of the patients [Table 5].
|Figure 1: Transverse color mode image showing absent color flow in popliteal vein with echogenic lumen suggestive of subacute thrombus. The vein size has also increased substantially as compared to the popliteal artery. Color fl ow is seen in popliteal artery (blue)|
Click here to view
|Figure 2: Transverse B-mode image showing subacute thrombus in the popliteal vein. The popliteal vein is also seen to increase in size substantially than the corresponding popliteal artery|
Click here to view
The predominant stage of DVT was that of subacute thrombus (53.8%) [Figure 3], followed by acute stage (29.5%) [Figure 4] and [Figure 5] and chronic stage (16.7%) [Table 6]. Complete thrombosis was observed in 54/78 (69%), while partial thrombosis was observed in 24/78 (31%). Thus predominant type of occlusion was that of the complete type [Figure 6] and [Figure 7] followed by partial type [Figure 8] and [Figure 9].
|Figure 3: Transverse B-mode image showing the non-compressible thrombosed popliteal vein|
Click here to view
|Figure 4: Transverse axis image of the femoral vessels showing a substantially large femoral vein as compared to femoral artery with anechoic lumen|
Click here to view
|Figure 5: On long axis color flow image, blood flow is seen around the thrombus on both sides suggestive of a free floating edge of thrombus|
Click here to view
|Figure 6: Transverse B-mode image showing echogenic (subacute) thrombus in the common femoral vein extending into great saphenous vein|
Click here to view
|Figure 7: Transverse color mode image showing complete absent color flow in common femoral vein and great saphenous vein due to thrombosis. Flow is evident in common femoral artery|
Click here to view
|Figure 8: Transverse color mode image showing partial peripheral flow with partial anechoic lumen in popliteal vein suggestive of partially occluding acute thrombus|
Click here to view
|Figure 9: Longitudinal image showing partially occluding anechoic thrombus in the popliteal vein|
Click here to view
The pattern of involvement was predominantly of multiple contiguous type which constituted around 91% with 9% of the patients having isolated venous involvement. It was divided into three groups [Table 7]:
- Isolated - thrombus confined to one venous segment.
- Multiple contiguous - thrombus extending across two contiguous anatomical venous segments.
- Multiple non-contiguous - thrombus in multiple different non-contiguous anatomical venous segments.
| Discussion|| |
The varied signs and symptoms that are associated with DVT make the diagnosis of DVT difficult and challenging. Furthermore, the thrombi may be asymptomatic making it exceedingly difficult to diagnose on clinical presentation. For proper management of the patients with DVT, the nature, location and the extent of the thrombus is necessary to know.
The study included assessment of spectrum of findings of DVT by using B-mode and color Doppler USG. All the major deep veins and superficial veins of the lower limb were examined in all patients along with the external iliac, common iliac and IVC in indicated cases. Retrospective descriptive analysis of 78 patients of DVT diagnosed on Doppler was done.
Duplex USG has a sensitivity and specificity of about 95% and 98%, respectively, for detecting DVT in symptomatic patients. In cases of isolated calf vein thrombosis, serial Doppler study (once weekly for 2 weeks) is suggested for propagation of thrombus into the proximal veins (popliteal vein or above). 
The age group of patients with DVT ranged from 21 to 90 years in our study. The majority of the patients belonged to the fifth decade (26%). In the study conducted by Hill et al.  they had found that mean age of patients shown to have DVT was in sixth decade.
In our study, 74% of the patients were males and 26% were females. Thus males dominated the study group. This correlates well with the study conducted by Hill et al.  which had higher incidence of DVT among males.
The majority of the patients in our study had edema as the most common presenting symptom which constituted 61% of all the patients, followed by pain and edema (17%), previous history of DVT (11%), pain (8%) and PE (3%). This correlates well with the study conducted by Glover and Bendick  and Eze et al.  in which 25 patients with unilateral leg swelling were found to have DVT. In their study, only 5% of patients were found to have DVT in absence of leg swelling. This is well explained by the normal venous physiology that when major venous channels get occluded, there is resultant increase in venous pressure and volume which manifests into edema. This also correlates with the study conducted by Langsfeld et al.  who found edema as the most common sign in patients diagnosed with DVT.
The two patients (3%) that presented with PE were retrospectively diagnosed to have DVT. Duplex USG should be done between 7 th and 14 th day in bedridden and ICU patients and following surgery for early diagnosis of DVT. Follow up Doppler should be done for detecting propagation of thrombus in cases of calf vein thrombosis. 
Out of the 78 cases showing evidence for thrombosis, the most common predisposing condition was prolonged hospitalization in 25 cases (32.1%), followed by 8 (10.2%) postoperative cases, 5 (6.41%) patients had history of trauma and 3 (3.8%) females were long term oral contraceptive users. 37 patients (47.4%) however had no known predisposing condition. Heit et al.  had concluded in their study that hospital or nursing home confinement, surgery, trauma, malignant neoplasm, chemotherapy are independent and important risk factors for VTE.
75 (96.1%) cases showed unilateral lower limb involvement, whereas 3 (3.9%) cases showed bilateral lower limb involvement. No case with unilateral symptom had bilateral involvement. Also no case with bilateral symptoms had unilateral involvement in our study. This correlated well with the study conducted by Sheiman and McArdle  in 1995 who in their study indicated a low incidence of thrombosis in contralateral extremity.
Out of the 81 limbs showing evidence for thrombosis amongst the 78 patients (3 cases of bilateral limb involvement), the commonest involvement was found to be of the left lower limb. 67 cases (82.7%) showed left lower limb involvement as compared to 14 cases (17.3%) showing right lower limb involvement. This correlated well with the venographic study conducted by Stamatakis et al.  who found out that major thrombi occurred more frequently in left lower limb.
In our study, thrombosis was localized to the superficial femoral vein in 69 limbs (85.2%), CFV in 57 limbs (70.3%), popliteal vein in 54 limbs (66.66%), posterior tibial vein in 49 limbs (60.5%), anterior tibial vein in 25 limbs (30.8%), peroneal vein in 4 limbs (4.9%), external iliac vein in 18 limbs (22.22%), common iliac vein in 11 limbs (13.6%) and the superficial venous system was involved simultaneously in 7 limbs (8.6%). All the superficial venous systems involved showed direct contiguous extension either through the femoral into GSV or through the popliteal into short saphenous vein. Out of the 5 cases (6.4%) of isolated DVT, the posterior tibial vein was involved in 3 limbs, anterior tibial and superficial femoral in 1 limb each.
Thus the present study localized thrombus predominantly in the thigh or popliteal region (85.2%) as compared to the isolated calf DVT in 4 limbs (4.9%). This correlated well with the study conducted by Markel et al.  who concluded that proximal limb involvement was more common pattern of involvement as compared to the isolated calf DVT.
The predominant stage of DVT in the cases showing evidence for thrombosis was that of the subacute stage seen in 42 cases (53.8%) as compared to the acute stage of involvement seen in 23 cases (29.5%) and chronic stage seen in 13 cases (16.7%) in our study. These findings corroborate well with study conducted by Hill et al.  who found that the positivity rate for acute DVT was 17.4%.
In our study, out of the 78 cases involved, 71 cases (91%) had multiple contiguous segmental involvement of the veins. Whereas 7 cases (9%) had isolated vein involvement. Multiple non-contiguous segmental involvement was not found in our study. The study conducted by Hill et al.  in 1997 showed 34% cases had isolated thrombi confined to one venous segment, 52% thrombi were multiple contiguous type and 8% multiple non-contiguous type.
| Conclusion|| |
DVT of lower limbs is one of the most common cause for majority of deaths due to PE which can be detected reliably, non-invasively and rapidly by the use of Duplex Doppler USG. It has become the first line in investigation of DVT. Gray scale findings together with color Doppler helps in qualitative evaluation of the venous system of lower limbs. Duplex Doppler USG can help in early detection of DVT in clinically suspected cases and help in prompt treatment of the patients as early and prompt treatment is crucial in the course of DVT. It is also helpful in evaluating the site, extent and stage of thrombus. Thus weighing the limitations and the advantages offered by the Duplex Doppler USG, it is a good, reliable, inexpensive and rapid method of investigation at present for the investigation of DVT of lower limbs.
| References|| |
|1.||Angral R, Islam MS, Kundan S. Incidence of deep vein thrombosis and justification of chemoprophylaxis in Indian patients: A prospective study. Bangladesh Med Res Counc Bull 2012;38:67-71. |
|2.||Nathan S, Aleem MA, Thiagarajan P, Das De S. The incidence of proximal deep vein thrombosis following total knee arthroplasty in an Asian population: A Doppler ultrasound study. J Orthop Surg (Hong Kong) 2003;11:184-9. |
|3.||Hansson PO, Welin L, Tibblin G, Eriksson H. Deep vein thrombosis and pulmonary embolism in the general population. ′The Study of Men Born in 1913′. Arch Intern Med 1997;157:1665-70. |
|4.||Agarwala S, Bhagwat AS, Modhe J. Deep vein thrombosis in Indian patients undergoing major lower limb surgery. Indian J Surg 2003;65:159-62. |
|5.||Chinglensana L, Rudrappa S, Anupama K, Gojendra T, Singh KK, Chandra ST. Clinical profile and management of deep vein thrombosis of lower limb. J Med Soc 2013;27:10-4. |
|6.||Ageno W, Agnelli G, Imberti D, Moia M, Palareti G, Pistelli R, et al. Risk factors for venous thromboembolism in the elderly: Results of the master registry. Blood Coagul Fibrinolysis 2008;19:663-7. |
|7.||Ozaki A, Bartholomew JR. Pulmonary Embolism. Cleveland Clinic. Cleveland: Clinic; 2012. Available from: http://www.clevelandclinicmeded.com/. Published: December 2012. |
|8.||Wells PS, Anderson DR, Ginsberg J. Assessment of deep vein thrombosis or pulmonary embolism by the combined use of clinical model and noninvasive diagnostic tests. Semin Thromb Hemost 2000;26:643-56. |
|9.||Fraser JD, Anderson DR. Deep venous thrombosis: Recent advances and optimal investigation with US. Radiology 1999;211:9-24. |
|10.||Hill SL, Holtzman GI, Martin D, Evans P, Toler W, Goad K. Selective use of the duplex scan in diagnosis of deep venous thrombosis. Am J Surg 1995;170:201-5. |
|11.||Comerota AJ, Katz ML, Greenwald LL, Leefmans E, Czeredarczuk M, White JV. Venous duplex imaging: Should it replace hemodynamic tests for deep venous thrombosis? J Vasc Surg 1990;11:53-9. |
|12.||Lunt MJ. Review of duplex and colour Doppler imaging of lower-limb arteries and veins. J Tissue Viability 1999;9:45-55. |
|13.||Zwiebel WJ. Introduction to Vascular Ultrasonography: Technique for Extremity Venous Ultrasound Examination. 5 th ed. Philadelphia, Pennsylvania 19106: Elsevier Saunders; 2005. |
|14.||Goran AM. Deep vein thrombosis of the lower limbs in Duhok: A descriptive study using Doppler ultrasound. Duhok Med J 2009;3:64-72. |
|15.||Hill SL, Holtzman GI, Martin D, Evans P, Toler W, Goad K. The origin of lower extremity deep vein thrombi in acute venous thrombosis. Am J Surg 1997;173:485-90. |
|16.||Glover JL, Bendick PJ. Appropriate indications for venous duplex ultrasonographic examinations. Surgery 1996;120:725-30. |
|17.||Eze AR, Comerota AJ, Kerr RP, Harada RN, Domeracki F. Is venous duplex imaging an appropriate initial screening test for patients with suspected pulmonary embolism? Ann Vasc Surg 1996;10:220-3. |
|18.||Langsfeld M, Hershey FB, Thorpe L, Auer AI, Binnington HB, Hurley JJ, et al. Duplex B-mode imaging for the diagnosis of deep venous thrombosis. Arch Surg 1987;122:587-91. |
|19.||Heit JA, Silverstein MD, Mohr DN, Petterson TM, O′Fallon WM, Melton LJ 3 rd . Risk factors for deep vein thrombosis and pulmonary embolism: A population-based case-control study. Arch Intern Med 2000;160:809-15. |
|20.||Sheiman RG, McArdle CR. Bilateral lower extremity US in the patient with unilateral symptoms of deep venous thrombosis: Assessment of need. Radiology 1995;194:171-3. |
|21.||Stamatakis JD, Kakkar VV, Lawrence D, Bentley PG. The origin of thrombi in the deep veins of the lower limb: A venographic study. Br J Surg 1978;65:449-51. |
|22.||Markel A, Manzo RA, Bergelin RO, Strandness DE Jr. Pattern and distribution of thrombi in acute venous thrombosis. Arch Surg 1992;127:305-9. |
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7]
|This article has been cited by|
||Clinical implications of the anatomical variation of deep venous thrombosis
| ||Ayman El-Menyar,Mohammad Asim,Gaby Jabbour,Hassan Al-Thani |
| ||Phlebology: The Journal of Venous Disease. 2018; 33(2): 97 |
|[Pubmed] | [DOI]|
||Prevalence of lower limb deep venous thrombosis among adult HIV positive patients attending an outpatient clinic at Mulago Hospital
| ||Sosthene Tsongo Vululi,Samuel Bugeza,Muyinda Zeridah,Henry Ddungu,Akello Betty Openy,Mubiru Frank,Rosalind Parkes-Ratanshi |
| ||AIDS Research and Therapy. 2018; 15(1) |
|[Pubmed] | [DOI]|
||Recurrent Deep Vein Thrombosis After the First Venous Thromboembolism Event: A Single-Institution Experience
| ||Mohammad Asim,Hassan Al-Thani,Ayman El-Menyar |
| ||Medical Science Monitor. 2017; 23: 2391 |
|[Pubmed] | [DOI]|