|Year : 2014 | Volume
| Issue : 1 | Page : 43-50
|Establishing a normal reference range for thromboelastography in North Indian healthy volunteers
Arulselvi Subramanian1, Venencia Albert1, Renu Saxena2, Deepak Agrawal3, Ravindra Mohan Pandey4
1 Department of Lab Medicine, JPNATC, New Delhi, India
2 Department of Hematology, All India Institute of Medical Sciences, New Delhi, India
3 Department of Neurosurgery, All India Institute of Medical Sciences, New Delhi, India
4 Department of Biostatistics, All India Institute of Medical Sciences, New Delhi, India
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|Date of Web Publication||17-Apr-2014|
| Abstract|| |
Background: Thromboelastography (TEG) is relatively recent assay to analyze the coagulation state of a blood sample, providing a continuous visualization of physical changes occurring during blood coagulation. There is a paucity of published literature on assessment of coagulation status using TEG in Indian population. Aim: The primary aim of the following study is to establish normal reference values for TEG in North Indian healthy volunteers and secondary aim is to compare them with conventional plasma-based routine coagulation tests and the manufacturers reference range. Materials and Methods: A total of 200 healthy volunteers comprised of 100 males and 100 females of age groups between 20 and 50 years, were enrolled over a period of 1 year, i.e., 2011-2012. Thromboelastometry (TEM) was performed on TEM-A automated thromboelastometer (Framar Biomedica, Rome, Italy), using whole blood non-additive (360 µl). TEG parameters analyzed were r-time, k-time, α-angle, maximal amplitude (MA). Prothrombin time (PT), activated partial thromboplastin time (aPTT) and platelet count was performed for all volunteers. The 95% reference range was calculated as (mean-1.96 standard deviation [SD]) to (mean + 1.96 SD). Results: Our reference values for 95% of 200 volunteers were r-time: 1.8-14.2 min, k-time: 0.7-7.3 min, α-angle: 27.3-72.3° and MA: 32.1-87.9 mm. Maximum clot strength was higher in women compared with men, however statistically insignificant. Overall 14.5% (29/200) of the volunteers had at least one abnormal parameter while 74% (149/200) had deranged TEG values using the manufacturer's reference range. Statistically significant variation was seen in r-time for 84.8% (P < 0.001), for k-time, in 87.1% (P < 0.001), for α-angle in 83.7% (P < 0.001) and for MA in 84% (P < 0.001), between the manufacturer and our reference range. Conclusion: The efficacy of classical coagulation test has been well-established; on the contrary TEG is a fairly recent assay and its utility for patient management remains to be demonstrated. We observed TEG to be oversensitive in determining coagulopathy where there is no clinical presentation. The manufacturer's reference values may not be appropriate for different ethnicity. TEG may give an overall representation of hemostasis; however, it cannot replace the conventional coagulation tests. We recommend the determination of normal TEG values by each laboratory for their target population.
Keywords: Normal range, thromboelastography, volunteers
|How to cite this article:|
Subramanian A, Albert V, Saxena R, Agrawal D, Pandey RM. Establishing a normal reference range for thromboelastography in North Indian healthy volunteers. Indian J Pathol Microbiol 2014;57:43-50
|How to cite this URL:|
Subramanian A, Albert V, Saxena R, Agrawal D, Pandey RM. Establishing a normal reference range for thromboelastography in North Indian healthy volunteers. Indian J Pathol Microbiol [serial online] 2014 [cited 2021 Oct 21];57:43-50. Available from: https://www.ijpmonline.org/text.asp?2014/57/1/43/130896
| Introduction|| |
Coagulation evaluations are commonly used to assess the clinical conditions like trauma.  Trauma patients develop coagulopathy resultant of blood loss, consumption of coagulation factors and platelets and fluid transfusion. Incidence of coagulopathy in trauma patients on admission is 25-35%.  In the recent years, thromboelastography (TEG) has become a popular monitoring device for hemostasis and transfusion management in major surgery and trauma.
TEG is a non-invasive diagnostic assay that can monitor and analyze the coagulation state of a blood sample, providing a continuous visualization of physical changes occurring during the blood coagulation. TEG evaluates the physical properties of the clot, via the torsion in a pin connected with a mechanical electrical transducer, suspended in cup. As the blood sample clots, the changes in rotation of the pin are converted into electrical signals that a computer uses to create graphical and numerical output. Depending on the shape of the TEG tracing, the hemostatic condition of a patient can be defined as normal, hypocoagulable (if 2 or more parameters are observed: Prolonged r-time, prolonged k-time, decreased α-angle and/or maximal amplitude [MA]) or hypercoagulable (if 2 or more of the following parameters are observed: Short r-time, short k-time, increased α-angle and/or MA). 
In comparison to the conventional tests which evaluate the coagulation pathway until the formation of the first fibrin strands, TEG takes into account the dynamic interaction of clotting factors (plasma) and platelets (cellular) elements that occurs during in vivo clotting, evaluating clot formation, its strength, platelet function and clot lysis, thus indicating an overall 'clot quality.'
According to the published literature the consequence of, dependence of TEG on manual procedures, its versatility in terms of the type of sample and different initiators that could be used resulting in difficulty to establish standards and reference values, TEG currently lacks universal recognition as a reliable routine laboratory test. 
Various studies have reported the utilization of TEG as a monitoring device for hemostasis and transfusion management in various clinical settings literature also suggests that TEG is a point of care device for rapid diagnosis and differentiation of hypercoaguable and hyperfibrinolytic conditions. Nonetheless TEG is now a part of clinical practice, wherein normal standard values are less pertinent, as the patients own baseline pre-operative results serve as the standard. Conversely such a model is not practicable in a trauma care set up. 
Hence to improve our understanding of the utility of TEG in determining the coagulation status of North Indian trauma patients and the improvement post-transfusion of blood products, it was felt necessary to establish a reference range of TEG parameters for normal healthy volunteers and to study the basic coagulation status in our target population.
| Materials and Methods|| |
The study was conducted in the Department of Laboratory Medicine, of a Level 1 Trauma Care Center, over a period of 1 year, i.e., 2011-2012. The institute ethics committee approved the study design. Healthy volunteers of age groups between 20 and 50 years, with 1:1 proportionate number of males and females were enrolled. Clinical history of all volunteers was recorded, including detailed medical condition, medication and preexisting bleeding disorders. Volunteers who have taken medications known to effect platelet function, 48 h prior to sampling and pregnant women and women on oral contraceptives were excluded from the study. Retrospectively all the blood samples which were not in proper proportions to the anticoagulant, or strongly lipemic, hyperbilirubinemic and hemolyzed, or samples collected by vein puncture taking more than 30 s and with excessive venous stasis were excluded.
Blood samples were obtained simultaneously for TEG analysis (uncitrated whole blood) and standard laboratory and coagulation tests.
Thromboelastometry (TEM) was performed on TEM-A automated thromboelastometer (Framar Biomedica, Rome, Italy), using whole blood nonadditive (360 μl). All analyses were performed with TEG disposable cups and pins as devised by the manufacturer and measurements were performed within 4 min of sampling. Normal values were determined for four TEM parameters: Reaction (r) time (time from start to initial fibrin formation); k-time (clot kinetics - measuring time taken for a certain level of clot strength is reached); α-angle (clot kinetics of clot build up and cross-linking); and MA (absolute clot strength). Anticoagulants and factor deficiencies result in prolonged r-time, k-time and α-angle; they can also be affected to a degree by platelet dysfunction or thrombocytopenia. MA is influenced by platelet count and platelet function as well as fibrinogen level.
Platelet count was done on Sysmex XE-2100 hematology analyzer (Sysmex, Kobe, Japan) on ethylenediaminetetraacetic acid-anticoagulated blood samples. Prothrombin time (PT) and activated partial thromboplastin time (aPTT) were estimated from 4.5 mL of blood in 0.5 mL of 3.2% trisodium citrate on a STA Compact automated analyzer (Diagnostica Stago, France).
The already established reference values for platelet count, PT and aPTT in our laboratory are 1-4 (lkh/cu mm), 12-16 s and 28-36 s respectively.
All the healthy volunteers enrolled in this study were categorized based on gender. A pilot study was conducted to derive the appropriate sample size, we calculated that a sample size of 100 is required to be within 5 units of the true thrombodynamic potential index (TPI) with 95% confidence interval (CI); standard deviation (SD) for TPI was estimated at 24.8, which was applied to the below given formula to calculate the sample size for the current study,
The reference normal range obtained for the study population was firstly compared with the standard coagulation assays, by checking how many of our subjects fell outside the standard coagulation parameters range; similarly it was also compared to the normal reference values given by the manufacturers. For this volunteers were categorized as normal and outliers based on the respective reference ranges.
All laboratory investigations were presented as mean and SD. The 95% reference range was calculated as (mean – 1.96 SD) to (mean + 1.96 SD). Correlation of the derived reference values with the standard coagulation assays and manufacturers range was done using Chi-square tests. Statistical significance was set at P < 0.05.
| Results|| |
Blood samples of a total of 205 volunteers were drawn for the purpose of this study; however 5 samples were retrospectively excluded based on the exclusion criteria. Therefore, we studied a total of 200 healthy volunteers recruited for the purpose of this study. Samples of 100 males with an average age of 29.05 ± 7.3 and 100 females with average age 28.29 ± 7.9 were investigated for complete blood count, coagulation parameters and TEG.
The characteristics of the study population, with a comparison of male with female are presented in [Table 1] and the distribution of the data for each TEG parameter as shown in in [Figure 1]. After confirming that the study population is following a normal distribution for all of the parameters the reference values for measured TEG variables expressed as the mean ± SD and boundary encompassing 95% (between the upper limit [mean + 1.96 SD] and lower limit [mean – 1.96 SD]) of the population were calculated are shown in [Table 2]. Central 97.5 th and 2.5 th percentile was also calculated for the TEG parameters as shown in [Table 2].
|Figure 1: Box and whisker's plot for distribution of data for all thromboelastograph parameters|
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The parameters for our population were found to be outside the derived reference range in 14.5% of the volunteers. Ten volunteers were observed to have deranged r-time, ten had deranged k-time; fourteen had deranged α-angle and deranged MA was seen in fifteen of the volunteers.
Volunteers were categorized as normal and outliers based on the normal range of platelet count, PT and aPTT. Using Chi-square test, a correlation was done between frequency of these with the categories of normal and outliers volunteers based on the derived range of TEG parameters.
Out of the 163 volunteers with a normal platelet count, TEG showed a derangement of r-time, k-time, α-angle and MA in 4.9%, 4.9%, 8% and 8.6% of the volunteers respectively, out of the 27 thrombocytopenic volunteers, derangement of r-time, k-time and MA was seen in 7.4%, 3.7% and 3.7% respectively. Only one out of the ten volunteers with thrombocytosis had an abnormal value of k-time and α-angle.
Normal PT was observed in 191 volunteers, however, based on the derived range coagulation status was derange for 4.7%, 5.2%, 6.8% and 7.3% volunteers for r-time, k-time, α-angle and MA respectively, only one of the nine volunteers with abnormal PT had r-time, α-angle and MA deranged.
Of the 19 volunteers with above normal aPTT values 5.3% had deranged r-time, k-time and MA; 15.8% had deranged α-angle.
These correlations however were not found to have any statistical significance.
[Table 3] presents the mean ± SD of r-time, k-time, α-angle and MA in volunteers with abnormal values for PLT, PT and aPTT.
According to the derived reference values 16 volunteers had one of the four parameters deranged, eight had two, four had three and one had all four TEG parameters deranged.
|Table 3: Measurement of TEG parameters in patients with deranged platelet count and coagulation parameters|
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The TEG parameters for all 200 volunteers were also analyzed using the manufacturer's reference range as shown in [Table 4].
|Table 4: The derived reference range of thromboelastogram parameters and0 the reference range of thromboelastogram parameters predefined by the manufacturers|
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When compared to men, in females we observed a slightly faster and higher initial rate of fibrin formation as illustrated by a shorter r-time and k-time time. The female group also had a higher rate of clot growth, represented by a wider α-angle. Furthermore, MA was higher in the female group. The latter suggests that maximum clot strength were higher in women. These variations were however statistically insignificant.
Hypercoagulability was seen in one male (short r-time and k-time and prolonged α-angle) and four female volunteers (one had short r-time and prolonged α-angle; two had short r-time and prolonged α-angle and MA; and only one had both prolonged α-angle and MA), also three male (two had prolonged k-time and short α-angle; one had prolonged r-time and k-time and short α-angle) and four female volunteers were hypocoagulable (one had prolonged k-time and short α-angle; one prolonged k-time and short MA; one had prolonged r-time and short α-angle and MA; one prolonged k-time and short α-angle and MA.
Hypercoagulability was seen in twelve male and thirteen female volunteers, also 49 male and 23 female volunteers were hypocoagulable by the manufacturer's reference range.
The parameters for our population were found to be outside the manufacturer's reference range in 74% of the volunteers. 52 volunteers had one of the four parameters deranged, 39 had two, 45 had three and 13 had all four TEG parameters deranged.
In total, 66 volunteers were observed to have deranged r-time and 70 had deranged k-time; 86 had deranged α-angle and deranged MA was seen in 94 of the volunteers.
On comparing the depiction of coagulation status based on the derived reference range and the reference range pre-defined by the manufacturer. A statistically significant variation was seen in r-time, as out of the 66 volunteers with r-time outside the manufacturer's reference range, 84.8% (56/66) were within the derived range (P < 0.001). Similarly for k-time, of the 70 volunteers with k-time outside the manufacturer's reference range, 87.1% (61/70) were within the derived reference values (P < 0.001). For α-angle, out of the 86 volunteers outside the manufacturer's reference range, nearly 83.7% (72/86) were within the derived reference values (P < 0.001). Out of the 94 volunteers with MA outside the manufacturer's reference range, 84% (79/94) were within the derived reference values (P < 0.001) [Table 5].
|Table 5: Comparison between the derived reference range of thromboelastogram parameters and the reference range of thromboelastogram parameters pre-defined by the manufacturers|
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| Discussion|| |
TEG was first described by Hartert in 1948 as a global test of blood coagulation,  which gives a graphical representation of the complete overview of the clotting cascade from clot formation to lysis. TEG was initially used as a research tool with only limited clinical application, however technical development and automation has renewed interest in the cell based model of hemostasis, such as TEG.
Classical coagulation tests provide only a snapshot of the coagulation status on the moment the sample was taken, as these tests are based on isolated static end points,  the influence of hypothermia is not measured as these are performed in plasma at a normal and standardized temperature of 37°C.  In addition the correlation of laboratory-based coagulation tests with clinical bleeding is currently imprecise and requires a more rapid evaluation of hemostasis and fibrinolysis.  Point-of-care coagulation monitoring device, such as TEG may overcome several limitations of routine coagulation tests.
TEG offers information on portions of the clotting process that the conventional tests cannot, such as fibrinolysis and hypercoagulability and has the potential to direct the transfusion.  TEG results are available within a short time frame making them relevant to clinical decision-making.
TEG has been advocated as a useful guide to blood transfusion practice in cardiac surgery  liver transplantation,  identification of patients with overt disseminated intravascular coagulation,  hypercoagulability and prediction thromboembolic events in surgical patients. 
TEG has a place in trauma providing a bedside, point of care test in a dynamic rapidly evolving situation. 
Clinical studies including more than 5000 surgical and/or trauma patients have reported on the benefit of using viscoelastic hemostatic assays (VHA) such as TEG when compared to plasma-based routine coagulation tests, like PT and aPTT to identify coagulopathy and guide transfusion therapy. However, at present no VHA guided transfusion therapy has been prospectively and independently validated in trauma patients, which is highly warranted. 
The current study was undertaken in a level 1 trauma care center, to evaluate the potential clinical application of TEG. We studied the coagulation status of the 200 healthy volunteers with routine coagulation tests and TEG and derived a normal reference values for TEG parameters.
The number of healthy volunteers needed to establish reference normal values is debatable. The National Committee for Clinical Laboratory Standards document (C28-A2) recommends a minimum sample of 120 reference values for each reference population or subclass. This is the smallest number of samples that allows the determination of a 90% CI around the reference limits (e.g., the 2.5 th and 97.5 th percentile). Greater confidence or improved precision in an estimated 95% reference interval can be accomplished from a larger sample of reference individuals.  We decided to include 200 volunteers.
Our overall normal ranges for 95% of 200 volunteers were r-time: 1.8-14.2 min, k-time: 0.7-7.3 min, α-angle: 27.3-72.3° and MA: 32.1-87.9 mm. Normal values for 95% of 100 male volunteers were r-time: 2.2-14.8 min, k-time: 1.3-7.6 min, α-angle: 26.2-66.7° and MA: 26.2-84.7 mm. Reference range values for 95% of 100 female volunteers were r-time: 2.1-14.2 min, k-time: 0.4-6.9 min, α-angle: 30.3-76.1° and MA: 35.8-90.0 mm. The hypercoaguable coagulation status of the female volunteers influenced the overall reference values, evident by the wider overall range, in contrast to the gender specific ranges of the TEG parameters. Therefore, we suggest that normal values of TEG should be defined for men and women separately.
Similar methodology used by Scarpelini et al. calculated reference ranges for 95% for 118 healthy volunteers that were r-time: 3.8-9.8 min, k-time: 0.7-3.4 min, α-angle: 47.8-77.7°, MA: 49.7-72.7 mm.  Chan et al. in their study used adult controls derived from a population of 25 volunteers, who had a median age of 31.24 year and an interquartile range of 14.17 year to compare for reference values for kaolin-activated TEG between pediatric and adult population  [Table 6].
The laboratory at Texas Children's Hospital, Houston, established the ranges for children and adults, mean ± SD of adults, 39.1 ± 10.4 y (n = 21) for r-time (min) k-time (min) α-angle (°) MA (mm) are as follows 8.0 ± 2.0, 1.8 ± 0.4, 64.7 ± 5.3, 63.5 ± 4.2, respectively.  Similarly TEG was performed on 50 healthy adult volunteers to allow comparisons between pediatric and adult values, mean ± SD. values for r-time (min) k-time (min) α-angle (°) MA (mm) were found to be 16.1 ± 3.3, 9.2 ± 2.4, 30.1 ± 6.7, 51.6 ± 5.8, respectively  however these studies did not define a normal reference value for TEG parameters in adult controls.
Two variables of TEG, MA and k-time, have been suggested to be linearly related with log10 [platelet (/mL),  we observed one (3.7%) volunteer to have an elevated MA and k-time, out of the 27 thrombocytopenic volunteers and one female volunteer had elevated k-time, from the ten thrombocytic volunteers.
Out of the volunteer with elevated PT (9) and aPTT (19), we observed one female to have low r-time and high α-angle.
In our study population we demonstrated gender differences in coagulation, when compared to men, higher clot strength as well as the viscoelastic property of the formed clot was observed in the female volunteers; also a slightly faster and higher initial rate of fibrin formation was observed in women compared to men.
Gorton et al. in their study have reported significant gender-related differences in TEG variables, with a significant (P 0.0001) trend of increasing coagulability from men through non-pregnant to pregnant women, which may be due to endogenous hormones, the median and interquartile range (min-max) of r-time (min) k-time (min) α-angle (°) MA (mm) was reported as 23.5 (25.5, 38.5), 18.5 (14.7, 23.0), 22.5 (19.0, 28.7), 51.0 (46.2, 57.5) for healthy males and 22.5 (18.2, 31.2), 11.5 (10.0, 14.0), 36.0 (30.0, 41.0), 59.5 (53.7, 64.0) for non-pregnant females, respectively. 
In a study by Scarpelini et al. determined the normal TEG values for healthy volunteers, using hemoscope 5000 device, they found that even healthy and non-traumatized women are more hypercoagulable than men based on their TEG profile. 
Roeloffzen et al. studied 120 healthy adults with a combination of 60 males and 60 females and with a mean age 50 ± 17 years and observed significant differences in coagulability between male and female subjects. Except for r-time measured (P = 0.06), all other TEG variables in the female group were statistically significant in hypercoagulability, when compared with the male group, whereas differences in classical coagulation between both sexes were statistically insignificant. In women, a significantly faster and higher initial rate of fibrin formation as illustrated by a shorter r-time and k-time time; also a significantly higher rate of clot growth, represented by a wider α-angle was reported. 
Correlation of the normal and outlier volunteer groups based on TEG normal values and conventional parameters, depicted variations as 4% of the male volunteers with normal PT and aPTT had deranged r-time, 5% had deranged k-time, 6% had deranged α-angle and 4% had deranged MA. Similar variations were also seen in female volunteers, suggesting a weak correlation of the assessment of coagulation status between TEG and routine plasma based coagulation tests [Table 7].
|Table 7: Correlation of the derived reference range of thromboelastogram parameters with the standard coagulation parameters in healthy volunteers|
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Correspondingly numerous studies have attempted to correlate TEG with standard coagulation tests and concluded that the association is weak. An important reason for this difference may reside in the fact that conventional tests are performed in plasma without platelets and tissue bearing cells (the cellular component) while TEG is done in whole blood. 
Overall 74% (149/200) of the volunteers had at least one abnormal parameter using the manufacturer's reference range which decreased to 14.5% (29/200) using the reference values derived in the study, which however, is still a high value of outliers in a study population comprising of healthy volunteers, suggesting that TEG may be oversensitive in identification of coagulation abnormalities.
Published evidence supporting the manufacturer's normal values for TEG is limited, as the available literature of normal TEG values is either in surgical patients, rather than healthy volunteers, or from a small sample size of volunteers. 
We observed that 33%, 35%, 43% and 47% of the volunteers were out of the manufacture's reference range for r-time, k-time, α-angle and MA respectively. We also found statistically significant variation between our normal reference and manufactures range in identifying the volunteers who were coagulopathic [Table 5].
Similar results were reported by Scarpelini et al., they found that 16.9%, 5.9%, 12.7% and 12.7% of the volunteers were out of the manufacture's reference range for r-time, k-time, α-angle and MA respectively,  which was lower than our results. They also reported that 18.6% of the volunteers had at least one abnormal parameter while 10 (8.5%) would have been considered coagulopathic had the manufacturer's values been used, resulting in a test specificity of 81%. 
These findings indicate that normal TEG values proposed by the manufacturer using citrated blood and kaolin activation may not be appropriate for different populations, as it might result in the incorrect determination of coagulopathy in individuals without any clinical manifestations of coagulation abnormalities.
Limitations of the present study are that (1) the volunteers included were not scrutinized for a H/O smoking and alcohol abuse, as both clinical and basic research have linked smoking to abnormalities of coagulation and fibrinolysis. (2) TEG investigations were not done in duplicates, as is the case for classical coagulation assays. (3) In clinical practice, where TEG is used as a rapid point of care test of hemostasis, coagulation activators are often added to the blood samples. As we used only whole blood samples without activators, the study observations may not be applicable to other methods of TEG measurement.
| Conclusions|| |
Despite their limitations, it's crucial to state that the classical coagulation test are well standardized, are subjected to meticulous quality control procedures making them reproducible and reliable. Their efficacy has been well-established; on the contrary cell based hemostasis diagnostic assay are fairly recent and its utility for patient management remains to be demonstrated in prospective randomized clinical trials. Although TEG is a good test to monitor bed side coagulation status, it does require standard coagulation test to identify coagulation abnormalities. TEG may give an overall representation of hemostasis; however it cannot replace the conventional coagulation tests.
Our overall reference values for 95% of 200 volunteers were r-time: 1.8-14.2 min, k-time: 0.7-7.3 min, α-angle: 27.3-72.3° and MA: 32.1-87.9 mm.
However, we observed TEG to be oversensitive and the results of our study also indicate that many healthy individuals in our population would be incorrectly identified as coagulopathic by the manufacturer's reference values. Hence we recommend that studies with adequate sample size of healthy volunteers should be conducted in all laboratories, to determine the normal TEG values for their target population.
| Acknowledgments|| |
The authors would like to acknowledge Dr. Vedanand Arya, Dr. Sulekha Karjee for encouraging participation of healthy volunteers in the study, Mr. Krishan for running the TEG samples and Mr. Ashish Datt Upadhyay for helping in statistical analysis.
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Departments of Lab Medicine, JPNATC, All India Institute of Medical Sciences, New Delhi - 110 022
Source of Support: Done as an Institute of All India Institute of Medical
Sciences Project., Conflict of Interest: None
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7]
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