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reviews (AS12)

EPM304 Advanced Statistical Methods in Epidemiology

This document contains a copy of the study material located within the computer

assisted learning (CAL) session.

If you have any questions regarding this document or your course, please contact

DLsupport via DLsupport@lshtm.ac.uk.

Important note: this document does not replace the CAL material found on your

module CDROM. When studying this session, please ensure you work through the

CDROM material first. This document can then be used for revision purposes to

refer back to specific sessions.

These study materials have been prepared by the London School of Hygiene & Tropical Medicine as part of

the PG Diploma/MSc Epidemiology distance learning course. This material is not licensed either for resale

or further copying.

London School of Hygiene & Tropical Medicine September 2013 v1.0

Aim

To learn how to review and summarise information from many studies.

Objectives

By the end of this session, you should be able to:

as meta-analysis

Carry out two statistical approaches used in meta-analysis and know when to

use them

Describe how to carry out a systematic review of the medical literature

Understand the sources of bias in meta-analysis and know how to deal with

them

This session should take you between 1.5 and 2 hours to complete.

The aim of this session is to learn how to combine estimates from different studies

and systematically review the literature. Meta-analysis is a large area, and so in this

session you are given a brief introduction and overview of meta-analysis.

The contents of this session are listed opposite.

What is meta-analysis?

Why is it used?

Two main statistical approaches

Why are there differences in estimates between studies?

Issues in collecting data and various types of bias

Final thoughts and conclusions

To work through this session you should know about estimates of effect (e.g. odds

ratio, rate ratio, risk ratio) which can be obtained from a regression model or

classical methods of analysis. The statistical methods used in meta-analysis are

similar to those of the Mantel-Haenzsel method. You may wish to review the sessions

below.

Cohort Studies

AS01

SM02

It is now common for important clinical questions in medical research to be

addressed in several studies. This can be confusing for a medical practitioner. Which

studies' results should be followed? How can the information from the mass of data

published be summarised?

Meta-analysis is a quantitative tool that can be used to summarise information from

many studies.

An informal literature review can be too subjective and misleading, whereas metaanalysis can assist with an overall conclusion. This combines results from different

studies to give an overall summary estimate (and confidence interval).

Popularity of Meta-Analysis

The concept of meta-analysis is fairly easy to understand. The purpose of metaanalysis is to summarise information from different studies.

Statistical techniques are used to combine results from studies that address the

same clinical or epidemiological question.

There are two extreme views on this and some people may view meta-analysis as

making unjustified generalisations

1: An objective quantitative approach to combining evidence from separate (but

similar) studies.

2: Statistical tricks that make unjustified assumptions in producing oversimplified

generalisations out of a complex of disparate studies.

Note: Meta-analysis is common within the area of clinical trials, and is also widely

used within the general field of epidemiology.

The rationale behind a meta-analysis is to address 'problems' with the original

studies.

Any one study is often:

Interaction: Tabs: Too small:

Studies that are too small fail to give clear-cut results. Would you rely on the results

of a small study? What would you expect of the confidence interval around the

sample estimate?

Interaction: Button: clouds picture (pop up box appears):

The confidence interval for the sample estimate of a small study would be wide, as a

result it may be difficult to determine the true effect.

Interaction: Tabs: Not generalisable:

Often studies use a very select group of individuals, this makes it difficult to

generalise study results to other types of individuals.

What do you think the main purposes of a meta-analysis are? Click on one of the

boxes below.

an overall summary

Increase the sample size and simulate a very

large study that would otherwise be impossible

to do

Assess whether the effect of interest is

consistent for all studies

summary

Correct Response(pop up box appears and card appears on RHS):

Yes, meta-analysis attempts to combine information from studies addressing the

same research question to give an overall summary.

There are a number of reasons why meta-analysis is used to combine information

from relevant studies:

1. Provide a data display and objective review

2. Give a summary interpretation

3. Test an overall hypothesis

4. Estimate an average exposure effect

5. Assess whether the data are compatible with the effect of the exposure being

the same in all studies

Yes, using meta-analysis we can assess whether the data are compatible with the

effect of interest being the same in all studies.

So why is a meta-analysis useful?

It is basically because the increased total size of the combined analysis increases the

chances of detecting a moderate but clinically and/or epidemiologically important

effect

Often the aim of a meta-analysis is more general than that of a single study.

The aim of a smaller study could be to study the effect of beta-blocker in patients of

a certain type after a heart attack.

What do you think the aim of a meta-analysis that includes this study may be?

Interaction: Button: clouds picture: (pop up box appears):

The aim of the meta-analysis could be to evaluate beta-blockers in general after a

heart attack.

Before you look at the statistical methodology, first consider the following example in

which a number of trials assessed the effect of diureticsduring pregnancy.

Interaction: Hyperlink: diuretics (pop up box appears):

Diuretic

An agent that promotes urination.

Diuretics in pregnancy for pre-eclampsia

An early meta-analysis looked at randomised controlled trials of diuretics in

pregnancy.

Note: Diuretics help to reduce blood pressure. Pre-eclampsia, a rapid increase in

blood pressure or proteinuria, is a complication in pregnancy. On the next page you

can see the results of this meta-analysis.

Interaction: Hyperlink: Pre-eclampsia (pop up box appears):

Pre-eclampsia

Blood poisoning in late pregnancy, characterised by hypertension, oedema (excess

fluid in the subcutaneous tissues) and proteinuria (excess protein in the urine).

The 9 trials shown in the table below investigated whether diuretics helped in

reducing the risk of pre-eclampsia.

First author

Weseley

Preeclampsia

/total in

treated

patients

14 / 131

Preeclampsia

/total in

control

patients

14 / 136

Odds ratio

(95% CI)

1.04 (0.48

2.28)

Flowers

21 / 385

17 / 134

Menzies

14 / 57

24 / 48

Fallis

6 / 38

18 / 40

Cuadros

12 / 1011

35 / 760

Landesman

138 / 1370

175 / 1336

Kraus

15 / 506

20 / 524

Tervila

6 / 108

2 / 103

Campbell

65 / 153

40 / 102

Total

291 / 3759

345 / 3183

0.40 (0.20

0.78)

0.33 (0.14

0.74)

0.23 (0.08

0.67)

0.25 (0.13

0.48)

0.74 (0.59

0.94)

0.77 (0.39

1.52)

2.97 (0.59

15.1)

1.15 (0.69

1.91)

0.69 (0.59

0.81)

The 2nd column shows the number of events in treated patients. The 3rd column

show the number of events in untreated (control) patients.

The table shows the odds ratio estimate for each study together with corresponding

confidence intervals. What is the odds ratio estimating the effect of?

Interaction: Button: clouds picture (pop up box appears and text appears on top

RHS):

The odds ratio estimates the effect of diuretic on reducing pre-eclampsia in

pregnancy.

Do you think it is reasonable to combine the odds ratio estimates to give a summary

estimate?

Interaction: Button: clouds picture (pop up box appears):

Most ORs are considerably less than 1, indicating a protective effect of diuretics. For

3 studies the ORs are greater than 1 - but their confidence intervals are quite wide

and overlap 1, so these studies do not provide evidence that diuretics are harmful.

Overall, there is quite wide variation in the value of the ORs, suggesting that there

may be real differences among the studies for the effect of diuretics

There are two main approaches to meta-analysis:

2. Random effects method

The latter helps to deal with heterogeneity between studies. You will now learn both

methods, when and how to apply them.

This is the simplest method for calculating a summary estimate. However, this

method makes the assumption that each study is measuring the same true effect,

e.g. odds ratio, rate ratio.

The question you should address to check if this assumption is valid is:

Q. Are the differences observed between studies only due to sampling

variation?

You can think of this as similar to stratum-specific estimates with no interaction. An

overall estimate assumes the effect is the same in each strata.

The fixed-effects method:

Assumes the true effect is the same in all studies

Gives a weight to each individual study estimate

Calculates a summary estimate by calculating a weighted average of the

individual study estimates.

So, we obtain a weighted average of the study estimates.

The tabs opposite show how this is obtained for a summary odds ratio

Note: The same formats can be used for any outcome measure.

Interaction: Tabs: Step 1:

The weight for each study is the inverse of the variance of the study, this gives more

weight to studies that are more precise. Choosing the weights in this way minimises

the variability of the summary log odds ratio.

wi

=

1

vi

Interaction: Tabs: Step 2:

Using the weights and the estimated log odds ratios in each study

i , the summary

W ii

i-1

F =

W i

i-1

Where F (for 'fixed') denotes the assumption that the effect of diuretic is the same in

each study.

Interaction: Tabs: Step 3:

To calculate confidence intervals and do hypothesis tests on the summary estimate

you need the variance of the summary estimate. This is calculated as

1

u

W i

i-1

Most statistical packages will perform a fixed-effects meta-analysis. Below you can

see the results for the studies that assessed the effect of pre-eclampsia during

pregnancy.

Fixed effects meta-analysis

(exponential form)

Metho

d

Fixed

Pooled

Estima

te

0.672

95% confidence

interval

Lower

Upper

0.564

0.800

Asymptotic

z value

4.455

Pvalue

< 0.001

No. of

studies

9

confidence interval of 20% to 44%. This is a statistically significant reduction (P <

0.001).

The standard way of presenting results of a meta-analysis graphically is shown

opposite. This is known as a 'forest plot'. Click 'show' to see a forest plot for the preeclampsia meta-analysis.

Interaction: Button: Show (graph pops up in new window):

Interaction: Tabs: 1:

For each study, the box area is proportional to the weight for the study, this is to

stop attention being drawn to extreme estimates. What do you notice about the

confidence interval for the studies with larger boxes?

Interaction: Button: clouds picture (pop up box appears):

The confidence interval for studies with a larger box are narrower, i.e. more precise.

Interaction: Tabs: 2:

The diamond and broken vertical line represent the overall summary estimate. The

confidence interval is given by the width of the diamond.

Interaction: Tabs: 3:

The unbroken vertical line is the null value, i.e. odds ratio of 1 = no effect.

Interaction: Tabs: 4:

Notice that the x-axis for the odds ratio is on a log scale. This is to obtain symmetry

in the plot.

Look again at the forest plot.

Notice that the large trial (Landesman) dominates. Notice also that this trial has the

smallest confidence interval. The combined estimate of the odds ratio is closest to

this trial.

Do you think you can assume homogeneity across these trials, i.e. are the results

compatible with the true effect being the same in all studies?

Interaction: Button: clouds picture (pop up box appears):

Look at the degree of overlap in the CIs of the studies with the combined estimate

(indicated by the dotted line). One study (Cuadros) shows no overlap, and two

others (Fallis and Campbell) show only borderline overlap with the combined

estimate. Also, the variation in ORs among studies is quite wide. These findings

suggest that there may be real differences among the studies for the effect of

diuretics

The fixed-effects method is based on the assumption that the true effect does not

differ between studies.

This assumption should be checked, and if there is a difference then a random

effects method should be used to obtain a summary estimate. You will find out more

about this on the next page.

Interaction: Button: Show (pop up box appears):

The test for heterogeneity is based on the distance between the individual study

estimates and the summary estimate from the fixed-effects method.

Q=

W i(i - F)

i-1

This is large if the average distance between the individual study effects and the

summary effect is large.

This statistic is referred to the distribution,

if statistically significant then there is evidence against the null hypothesis of a

common effect for all studies.

if not statistically significant, there is no evidence for a heterogenous effect across

trials. ie we would conclude that there is a common effect (homogeneity) across

trials.

You do not have to do this calculation by hand statistics packages that perform

meta-analysis will include a test for heterogeneity

If the effects shown in each study differ, then a random effects method should be

used to obtain a summary estimate.

The interpretation of the summary estimate is that it is a mean effect about which it

is assumed that the true study effects vary

In

the true effects are allowed to differ, i.e. it allows for interaction

the true effects vary randomly about the population average

the between-study variance is estimated

the variance is used to modify the study weights

The formula for the random-effects summary estimate is similar to that for the fixedeffects summary estimate. The difference is the weighting. The weights include a

between study variance.

This is complex and is not discussed here, you only need to know that this variance

is taken into account and that is how the random effects method differs from the

fixed effects method.

W *ii

i-1

R =

W *i

i-1

Most statistical packages will perform a random-effects meta-analysis. Below you can

see the results for the trials that assessed the effect of diuretics during pregnancy.

Random effects meta-analysis

Metho

d

Pooled

estima

te

95% confidence

interval

Lower

Upper

Asymptotic

z value

Pvalue

No. of

studies

Random

0.596

0.400

0.889

2.537

0.011

studies, on average their effect is to reduce the

odds of pre-eclampsia by around 40%

The true effect of diuretics is to reduce preeclampsia by 40%

reduces pre-eclampsia

Interaction: Hotspot: While the effect of diuretics varies between studies, on

average their effect is to reduce the odds of pre-eclampsia by around 40%:

Correct Response (pop up box appears):

Yes, we estimate that on average diuretics reduce the odds of pre-eclampsia by

around 40% (the estimate of the OR is 0.6). We estimate this overall OR using a

random-effects meta-analysis, because we have evidence that the true effect of

diuretics on pre-eclampsia varied among the studies

Interaction: Hotspot: The true effect of diuretics is to reduce pre-eclampsia by

40%:

Incorrect Response (pop up box appears):

No, you cannot say what the true effect is. The summary estimate can only estimate

the true effect. You can be 95% confident that the true effect will lie within the

confidence intervals. ORR = 0.60 (0.40 to 0.89).

Interaction: Hotspot: There is evidence that the effect of diuretics reduces preeclampsia:

Correct Response (pop up box appears):

Yes, that's correct, the sample estimate shows evidence that the effect of diuretics

reduces pre-eclampsia. ORR = 0.60 (0.40 to 0.89), P = 0.01.

Use the 'swap' button below to swap between the fixed-effects and random-effects

results.

How does the estimate from the random-effects method compare to that from the

fixed-effects method?

Interaction: Button: clouds picture (pop up box appears and text appears on top

RHS)

The random-effects summary estimate is somewhat smaller than the fixed-effects

estimate, but the confidence interval is much wider. This means that it overlaps

more with the individual trial estimates.

Fixed-effects summary estimate

ORF = 0.67 (0.56 to 0.80)

Random-effects summary estimate

ORR = 0.60 (0.40 to 0.89)

Interaction: Button: Swap (table at bottom LHS changes to the following):

Fixed effects meta-analysis (exponential form)

Metho

d

Fixed

Pooled

estima

te

0.672

95% confidence

interval

Lower

Upper

0.564

0.800

Asymptotic

z value

4.455

Pvalue

< 0.001

No. of

studies

9

The results below now include the test for heterogeneity. What can you conclude

from this test?

Interaction: Button: clouds picture (pop up box appears):

There is strong evidence (P = 0.001) that the effect of diuretics differs between

studies. The random effects method should be used for this meta-analysis.

Metho

d

Pooled

estima

te

95% confidence

interval

Lower

Upper

Asymptotic

z value

No.of

studies

Pvalue

Random

0.596

0.400

0.889

2.537

0.011

9

Test for heterogeneity: Q = 27.265 on 8 degrees of freedom (P

= 0.001)

It is instructive to compare the weights used in the fixed- and random-effects metaanalyses. Consider the table below. What is different about the random effect

weights, and how do you think this affects the summary estimate?

Interaction: Button: clouds picture (pop up box appears and text appears on top

RHS):

The weights are much more similar for the random-effects estimate than the fixedeffect estimate, because of the inclusion of the estimated between-study variance.

This means that smaller studies will be given greater weight in random-effects metaanalysis.

The wider confidence intervals for the random-effects estimate reflect the greater

uncertainty because it is assumed that, in addition to sampling variation, the true

effect varies between studies.

Random-effects meta-analysis will, in general, be more conservative than fixedeffects meta-analysis: confidence intervals will be wider and P-values will be larger.

Therefore, if you are unsure which to use then the random effects method is safer.

Study

Weseley

6.27

Random

weights

2.57

Flowers

8.49

2.88

Menzies

5.62

2.45

Fallis

3.35

1.89

Cuadros

8.75

2.91

68.34

4.09

Kraus

8.29

2.85

Tervila

1.46

1.09

14.73

3.36

Landesman

Campbell

Fixed weights

Estimate

(95% CI)

1.04

(0.48,2.28)

0.40

(0.20,0.78)

0.33

(0.14,0.74)

0.23

(0.08,0.67)

0.25

(0.13,0.48)

0.74

(0.59,0.94)

0.77

(0.39,1.52)

2.97

(0.59,15.10)

1.14

(0.69,1.91)

Characteristics of the fixed effects and random effects method are summarised

below.

Interaction: Tabs: Fixed effects:

does not allow for heterogeneity

produces a narrow confidence interval

Interaction: Tabs: Random effects:

the true effects vary randomly about the population 'average'

the between-study variance needs to be estimated

weights for each trial incorporate the between-study variance

You have seen that the two methods produce different results; in fact, the

interpretation of the fixed and random estimates is very different.

In a fixed-effects meta-analysis, it is assumed that the only reason for variation in

the individual estimates is due to sampling error.

In a random-effects meta-analysis, the summary estimate is a mean effect about

which it is assumed that the true study effects vary.

There is disagreement over whether it is appropriate to use random-effects models

to combine study estimates in the presence of heterogeneity. This is because a

single overall estimate may be unhelpful.

For example, the treatment/exposure may have an effect in some populations but

not in others. This is the case for BCG vaccination - there is strong evidence that it

protects against tuberculosis in the UK, but no evidence that it does so in India or

Malawi. So here, calculating a single overall estimate of the efficacy of BCG would be

"combining apples and pears" - combining results from a setting where the

intervention works with results from settings in which it doesn't. A more useful

statement would be, for example, that BCG works in some settings (e.g. high

latitude countries) but not in others (e.g. tropical countries with high levels of

exposure to environmental mycobacteria).

It is clear, therefore, that investigation into the sources of heterogeneity may yield

important insights. The sources of heterogeneity are biological or methodological

differences between the studies. For example, study latitude in the example of BCG

vaccination is a source of heterogeneity.

You have seen the methods that can be used to perform a meta-analysis. As always,

the results of a statistical analysis are only as good as the data from which they are

derived. One of the key issues in this area of analysis is obtaining the data.

Interaction: Button: More (card appears on right handside as a timed pop up):

In recent decades there has been a massive increase in the number of research

studies carried out. Over 2 million articles are published in the biomedical literature

each year.

A summary of the research evidence for any particular area is a difficult task.

A conventional literature review has the potential to be too subjective. It is based on

the information available to the author and is presented from the viewpoint of the

author. To avoid this occurring in 1995 guidelines on how to systematically review

the literature were developed.

A systematic review of the literature is a 'systematic assembly, critical

appraisal and synthesis of all relevant studies on a particular topic'.

Guidelines for systematic review of the literature are given below.

Interaction: Tabs: 1:

A systematic review must address a specific health care question.

The question determines which studies are relevant and how their data should be

combined.

Interaction: Tabs: 2:

The methodology of a study must serve the biology, users and providers of health

care.

The systematic review study team should therefore include expertise in the content

area and methodology.

Interaction: Tabs: 3:

In order to collate all the necessary information, collaboration with the investigators

of the primary studies is necessary.

Interaction: Tabs: 4:

Systematic reviews are retrospective, and can be affected by the same bias that

affects other retrospective studies. A good systematic review should therefore be

based on good review methodology.

Interaction: Tabs: 5:

For many reasons, review methods can vary. The review methods employed should

be described for all systematic reviews.

Interaction: tabs: 6:

Some randomised trials, case-control studies and cohort studies may be

unsatisfactory. This does not mean they should simply be excluded from a review.

They should be critically appraised, empirically studied, and the analysis improved.

Overviews of observational studies require a great deal of methodological

development.

The inclusion of studies in a systematic review should be based on:

The methods of a study, not the results

Acceptable standards should be defined before study reviews are carried out. For

example, whether individuals were blind to the treatment under study, and the

quality of the follow-up, need to be considered

The quality of a trial associated with treatment effects

The treatment benefits can be greatly exaggerated in uncontrolled trials where, for

example, randomisation was inadequate.

Of the millions of studies carried out, only a small percentage is published. It is well

known that there is strong publication bias in favour of studies with the more

'positive' or 'interesting' results. The people behind this bias are listed on the tabs

below.

Interaction: Tabs: Investigators:

If an investigator obtains the result they expected at the start of their research they

are more likely to submit their findings for publication than if they feel the results are

'negative'.

Whatever the study results, a good quality study should be reported.

If the editor of a journal is enthusiastic about the findings of a study, or if the study

area has a currently high profile, then it is more likely to be sent for review.

Interaction: Tabs: Referee:

A referee is more likely to favour studies with a 'positive' result, which appear more

interesting than studies with a so-called 'negative' result.

This problem has been made worse by the following issues. Click each one for

details:

Small studies

The 'magical' P = 0.05 cut-off

Interaction: Hyperlink: Small studies (card appears on right handside):

Studies have been too small

Small studies can show a significant effect by chance. They are then more likely to

be published than a non-significant study. This is known as publication bias

We saw earlier that a random-effects meta-analysis gives studies more equal

weights than a fixed-effects analysis does. If a random-effects summary estimate

differs from the fixed-effects estimate, this is a sign that the average estimate from

the smaller studies differs from the average of the large ones.

Given that small studies are more subject to publication bias than large ones, this is

clearly a disadvantage of random-effects analysis.

Publication bias

Studies which produce negative or non-significant effect estimates are often

considered less important and less appealing to scientific journals. As a consequence

one problem that arises in drawing conclusions from a number of published studies is

that the studies may not be truly representative, they are more likely to be the ones

which showed strong positive effect estimates.

Interaction: Hyperlink: The 'magical' P = 0.05 cut-off (card appears on right

handside):

Too much emphasis on the 'magical' cut-off value, P < 0.05

The emphasis should be on the confidence intervals that reflect the precision of the

study estimate.

A solution to overcome the problem of publication bias has been to establish

registers of all studies carried out in a particular subject area.

It has also been proposed that journals consider studies for publication "blind" of the

actual results. It is clear that the active discouragement of studies that do not have

power to detect an important effect would reduce the problem.

Publication bias is not so great a problem for larger studies, for which there tends to

be general agreement that the results are of interest, whatever they are.

For more information on publication bias, see the Dickersin and Berlin paper in your

Reader.

We have seen that:

than (non-systematic) literature reviews.

The Cochrane Collaboration, which started in 1993, is an attempt to address these

issues. It aims to produce systematic, periodically updated reviews of randomised

controlled trials. These are available in electronic form (via CD-ROM), which means

that reviews can be updated as new evidence becomes available or mistakes have

been identified. Already, some hundreds of systematic reviews are available as part

of the Cochrane Collaboration, and at least 150,000 studies are indexed in the

database of randomised trials.

The Cochrane Collaboration have also carried out systematic reviews and meta

analyses of observational studies

Section 8: Summary

The main points of this session will appear below as you click through the step card

opposite. Click on any of the list entries below to go back to that page.

Why use meta-analysis?

Individual studies are often too small to obtain a precise estimate of effect.

The objective of meta-analysis is to combine evidence from several studies.

Common use in research

Systematic reviews and meta-analysis (the quantitative analysis of such reviews) are

now accepted as an important part of medical research. While the analytical methods

are relatively simple, there is still controversy over appropriate methods of analysis.

Increasing importance

Systematic reviews are substantial undertakings, and those conducting such reviews

need to be aware of the potential biases that may affect their conclusions. However,

the explosion in medical research information and the availability of reviews on-line

mean that summaries of research findings are likely to be of increasing importance

to the practice of medicine.

Fixed-effects versus random-effects

If it is correct to assume that the only reason for variation in the study estimates is

due to sampling error, then you can apply the fixed-effects method in a metaanalysis.

If the study effects vary randomly about the population average, the random-effects

method should be applied. The variation in study effects can be assessed using a test

for heterogeneity.

Helping the decision process

Meta-analysis cannot tell a researcher what to do, but it can help with the decisionmaking process.

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