ENDODONTICS Potential Errors and Misuse of Statistics in Studies

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Potential Errors and Misuse of Statistics in Studies

ENDODONTICS Potential Errors and Misuse of Statistics in Studies

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on leakage in endodontics

1

Department of Conservative Dentistry, School of Dentistry, University of Granada, Granada; 2Department of Conservative

Dentistry, School of Dentistry, University of Seville, Seville; and 3Department of Statistics and Operations Research, Faculty of

Pharmacy, University of Granada, Granada, Spain

Abstract

Lucena C, Lopez JM, Pulgar R, Abalos C,

Valderrama MJ. Potential errors and misuse of statistics in

studies on leakage in endodontics. International Endodontic

Journal, 46, 323331, 2013.

Aim To assess the quality of the statistical methodology used in studies of leakage in Endodontics, and

to compare the results found using appropriate versus

inappropriate inferential statistical methods.

Methodology The search strategy used the descriptors root filling microleakage, dye penetration,

dye leakage, polymicrobial leakage and fluid filtration for the time interval 20012010 in journals

within the categories Dentistry, Oral Surgery and

Medicine and Materials Science, Biomaterials of the

Journal Citation Report. All retrieved articles were

reviewed to find potential pitfalls in statistical

methodology that may be encountered during study

design, data management or data analysis.

Results The database included 209 papers. In all

the studies reviewed, the statistical methods used

Introduction

The practice of Endodontics involves decision-making

on materials, techniques, procedures and treatment

options. Today, in the era of evidence-based dentistry,

many of these decisions are based on the review of

Campus de Cartuja s/n, University of Granada, E-18071

Granada, Spain (Tel: ++34 958 242949; fax: +34 958

240908; e-mail: clucena@ugr.es).

outcome variable, but in 41% of the cases, the chisquare test or parametric methods were inappropriately selected subsequently. In 2% of the papers, no

statistical test was used. In 99% of cases, a statistically significant or not significant effect was

reported as a main finding, whilst only 1% also

presented an estimation of the magnitude of the

effect. When the appropriate statistical methods were

applied in the studies with originally inappropriate

data analysis, the conclusions changed in 19% of the

cases.

Conclusions Statistical deficiencies in leakage studies may affect their results and interpretation and

might be one of the reasons for the poor agreement

amongst the reported findings. Therefore, more effort

should be made to standardize statistical methodology.

Keywords: confidence intervals, endodontics, leakage, statistical bias.

Received 17 April 2012; accepted 18 July 2012

the main considerations in this process is that the scientific literature should be sound, reliable and unbiased

(Eckert et al. 2003). The standardization and quality of

reporting of biomedical research is, therefore, an important obligation of the healthcare community.

However, a growing number of articles are emerging in the dental and statistical literature warning of

flaws in research reports (Baccaglini et al. 2010).

According to Kim et al. (2011), 51.5% of 307 articles

published in 10 dental journals between 1995 and

2009 contained at least one statistical error. Most of

323

these deficiencies are encountered in the areas of Epidemiology, Periodontology, Implantology and Orthodontics (Galgut & OMullane 1998, BeGole 2000,

Galgut 2003, Tu et al. 2004, 2005), but until now,

little has been published on the prevalence of flawed

statistical analysis in Endodontics.

The inappropriate application of statistical methods

to research data is an error of sufficient magnitude to

raise serious questions about the validity of the

conclusions reached (Elenbaas et al. 1983). Nevertheless, in dentistry, most of the papers published on this

question have listed only the types of statistical mistakes committed, but have made no attempt to determine whether both the correct and incorrect statistical

tests lead the investigators to the same conclusions.

Fardi et al. (2011) identified the 100 top-cited articles

published in journals dedicated to Endodontics, analysing

the subject areas to highlight noteworthy trends and to

reflect major advances during the last 50 years. This

review shows that one of the main topics covered is leakage. Although the number of citations that an article

receives is not necessarily a measure of its quality, it does

reflect recognition by the scientific community and the

influence of the article in generating changes in dental

practice or further research (Fardi et al. 2011).

Given the importance of the statistical methodology in

terms of the validity of the findings of any research and

the fact that the subject of leakage represents an area of

significant interest within endodontics, the goals of the

present study were to analyse the quality of statistical

methodology used in the literature with respect to leakage in Endodontics, and to compare the results using

appropriate versus inappropriate inferential statistical

methods.

The database selected for the search was the ISI Web of

Science (WoS), using the Science Citation Index

Expanded (SCI-E). The search was limited to the categories Dentistry, Oral Surgery and Medicine and Materials Science, Biomaterials of the Journal Citation Report

(JCR) for the time interval 20012010. For descriptors,

we used the non-MeSH term root filling combined by

pairs with the non-MeSH terms microleakage, dye

penetration, dye leakage, polymicrobial leakage and

fluid filtration. The results were filtered according to

the type of document articles, thus excluding other

types of publications, such as proceedings papers and

abstracts for meetings and congresses, because of the

insufficient information provided in these documents.

324

The records were imported to the bibliography-management program ProCite, version 5 for Windows,

eliminating all duplicates. Two researchers from the

Conservative Dentistry Department of the University of

Granada (Spain) independently screened the database,

selecting only the documents related to leakage in

Endodontics. Doubtful cases were decided by consensus.

A detailed evaluation was made of the articles to

assess the quality of the statistical methodology used

and to find potential pitfalls in the implementation and

reporting of research methodology that may be

encountered during the study design, data management, statistical analysis or documentation of the

statistical tests applied. For this purpose, we used guidelines specified in previous studies (Strasak et al. 2007,

Baccaglini et al. 2010, Clark & Mulligan 2011).

The study design included whether the working

hypothesis was clearly defined, whether an a priori

effect and sample size was considered, or whether the

participants were randomly assigned to either an exposure treatment or a control group. Next, the method of

evaluating the leakage was recorded: qualitatively

(as success or failure, according to an ordered scale

and at which level of severity) or quantitatively (mm,

percentages, etc.), and the category (qualitative or

quantitative) assigned to the outcome variable leakage.

The description of basic data made by the authors

was examined (the descriptor of central tendency was

recorded as mean, median or both), as well as

whether the distribution of the data (normal or nonnormal) had been specified. A note of whether the

authors stated that they had performed a test of

normality on data was made or if they explicitly

mentioned the distribution. For articles that did not

describe the distribution of data, it was assumed to be

non-normal, unless sufficient information was

provided to reveal that the data were normally

distributed (Qualls et al. 2010).

The inferential statistical tests used were noted and

compared against standards (Qualls et al. 2010, Lucena

et al. 2011) used to test categorical or continuous data

(normally or non-normally distributed).

Documentation stage

All statistical methods applied were checked to confirm

whether they were described clearly and correctly, and

ascertained whether the raw data were presented to

enable a reader to recalculate the results presented

(Strasak et al. 2007, Clark & Mulligan 2011). In addition, whether the magnitude of the effect had been

estimated was also considered (by means of confidence

intervals CIs-, odds ratios, etc.).

this question ranges from 11 to 32, implying an average

of just over 21 articles per year, appearing in 20

journals. Three journals accounted for 83% of the total,

whilst the remaining 17% were distributed amongst 17

journals.

All articles were laboratory studies. These documents

referred mainly to apical leakage (n = 129). Some of

the studies concerned coronal leakage (n = 30) and 50

articles examined both coronal and apical leakage from

root canals.

Statistical re-analysis

For all the studies that, according to the standards

mentioned, had employed inappropriate methods to

analyse their data, and in which the authors had

provided raw data, statistical methods were applied

that were more appropriate to the nature of the data

presented. Finally, to estimate the magnitude of the

effect, the odds ratios or CIs were calculated in all the

studies in which it was possible to apply them.

Results

The search strategy applied retrieved 371 papers, 209 of

which adhered to the predetermined criteria. Therefore,

the final database consisted of 209 original research articles on leakage in Endodontics, published between 2001

Table 1 summarizes the frequencies of the most

common errors found in the papers reviewed. In most

studies (n = 200), leakage was assessed using either a

quantitative measurement scale or a qualitative one,

although in nine papers more than one method was

used. Thus, in three cases, both a qualitative scale and

quantitative method were applied, whilst another three

combined two different quantitative methods, two articles compared three different quantitative methods,

and, finally, one study compared four different quantitative methods. Therefore, the total number of leakage

tests considered was 222. Table 2 presents their distribution according to the type of scale of the outcome

variables used to evaluate the amount of leakage.

Statistical error type

Study design

No clear a priori statement or description of the Null Hypothesis under investigation

No a priori sample-size calculation/effect-size estimation (power calculation)

Failure to use and report randomization or method of randomization not clearly stated

Failure to report drop-out subjects from the study

Failure to use and report blinding if possible

Failure to report initial equality of baseline characteristics and comparability of study groups

Analysis of study data

Failure to examine/specify for the normality of continuous data

Failure to use an inferential test, giving only a description of the data

Documentation of study data

Failure to provide data with enough detail to enable the reader to recalculate all results

Failure to specify which test was applied

Presentation of study data

No a priori significance level definition

Reporting P = NS or P < 0.05 instead of reporting exact P-values

Reporting median without its respective standard deviation

Recording Odds Ratio for treatment group differences

Recording Confidence Intervals for treatment group differences

Frequency

Percentage

209

209

209

209

209

209

178

205

1

198

43

15

85.2

98.0

0.5

94.7

20.6

7.2

192

209

158

4

82.3

1.9

209

209

181

6

86.1

2.9

209

204a

182

26

90

66

114

16

2

1

31.6

55.9

8.8

7.7

1.1

a

In five studies there were no data of significance.

325

Number of

studiesa

Leakage measurement

Qualitative

01 scale (success or failure)

02 scale

03 scale

04 scale

05 scale

13 scale

Total

Quantitative

Millimetres, micrometers

or nanometres

Percentages or ratios

Fluid movement (in mL min 1,

lL min 1, etc.)

Bacterial or glucose concentrations

(in mmol mL 1, UI mL 1, etc.)

Mean of days without leakage

Filtration area (in mm2)

Electrical conductance (in k)

Total

21

7

2

4

4

2

40

56

10

79

12

20

2

3

182

N = 222

Table 3 summarizes the inferential statistical tests

used in the articles. In 26 articles, authors evaluated

the leakage using a qualitative scale and treated the

Fishers test was correctly applied. In the remaining

15 (58%) articles, the chi-square test was inappropriately employed.

In 14 of the studies reviewed (6% of the total),

leakage was assessed using a qualitative measurement

scale, but these measurements were used to generate

count outcome variables. In 93% of these cases

(n = 13), the authors selected nonparametric tests

with a non-normal distribution, but in 7% (n = 1),

parametric tests of significance were used on nonnormal data.

Finally, in 182 cases, leakage was measured quantitatively; the ANOVA test was appropriately applied in

15 (8%) and the KruskalWallis test in 88 (48%). In

the remaining 75 (41%) articles, a parametric test of

significance was applied to data that were non-normally distributed, or a nonparametric test was applied

to normally distributed data. In four studies (2%) with

a quantitative measurement of leakage, no test of statistical inference was used.

In short, the above results show that in 127 cases

(57%) the authors selected an appropriate test of statistical inference, but in the remaining 95 cases, an

incorrect statistical test (41%) or no statistical test

(2%) was applied. The percentage of articles that used

the appropriate test of statistical inference varied

depending on the journal (Table 4).

Leakage

measurement

Outcome

variable

Conditions

of application

Ordinal scale

(n = 40)

As a categorical variable

(n = 26)

As a continuous variable

(n = 14)

Expected number

in a cell 5 (n = 26)

Variables without normal

approximation (n = 14)

Quantitative

measurement

(n = 182)

As a continuous variable

(n = 182)

approximation (n = 16)

approximation (n = 162)

leakage measurement in

which no test of statistical

inference was used

Test of

significance

used

Fisher

Chi-square

Parametric

test

Nonparametric

test

Parametric

test

Nonparametric

test

Parametric

test

Nonparametric

test

Number

of works

11

15

1

13

15

1

74

88

4

Numbers in italics refer to studies that used the appropriate test of statistical inference.

a

In nine studies more than one type of evaluation was used.

326

Journal

J Endod

Oral Surg Oral Med

Oral Pathol Oral Radiol Endod

Int Endod J

Quintessence Int

Aust Endod J

J Appl Oral Sci

J Can Dent Assoc

Am J Dent

Dent Mater J

J Biomed Mater

Res B Appl Biomater

J Dent

J Oral Rehab

Dent Mater

Eur J Oral Sci

J Adhes Dent

J Biomater Appl

J Biomed Mater Res A

J Am Dent Assoc

J Prosthet Dent

Med Oral Patol

Oral Cir Bucal

Published

worksa

Correct

works

(%)b

96

40

47

55

37

5

4

4

4

3

2

2

84

60

75

75

50

100

50

0

2

2

1

1

1

1

1

1

1

1

100

0

100

0

100

0

0

0

0

100

a

Number of articles on leakage in Endodontics published in

the time interval 20012010.

b

Percentage of articles that used the appropriate test of statistical inference.

Documentation stage

Amongst the 91 cases that had selected an inappropriate test of statistic inference, only 16 provided

raw data enabling a statistical re-analysis to be performed. With respect to the presentation of the study

results, only three of the 209 articles reviewed provided a measure of the magnitude of the difference,

by means of an odds ratio (two articles) or CIs (one

case).

Statistical re-analysis

The change of the statistical methodology with

respect to the one previously applied (n = 16) gave

results that differed from those originally presented in

11 studies (69% of the sample) and represented a

substantial alteration of the final conclusions in three

of them (19% of the recalculated studies). In eight of

the recalculations (50%), a lower P-value was

obtained, although the initial conclusions remained

valid. In five cases (31% of the sample), it was not

possible to compare the results generated in the

authors had not provided exact P values (only

reporting P = NS or P < 0.05).

Of the 91 studies that had selected inappropriate

statistical tests, none provided data with enough

detail to allow CIs to be calculated, whilst in 10 cases,

it was possible to calculate the odds ratio. Amongst

these, four were negative studies based on significance

testing (studies that produced statistically nonsignificant results) and six were positive (studies producing

statistically significant results). The re-analysis of

these negative studies focused on interpreting the

odds ratio rather than P-values and revealed that the

intervention had been beneficial in one study. In this

latter case, the application of the appropriate statistical test predicted this effect, giving statistically

significant results (P = 0.021). In the remaining three

cases, the odds ratio did not reflect beneficial intervention effects. Amongst six studies with positive results,

the odds ratio calculation revealed that the significant

differences were clinically relevant in five studies,

whilst in the remaining one the statistically

significant effect was minor and of negligible clinical

importance.

Amongst 127 studies that had selected appropriate

statistical tests, none provided data with enough

detail to allow CIs to be calculated, and only in three

cases was it possible to calculate the odds ratio. The

interpretation of the results on the basis of calculating

the odds ratio in the studies with statistically significant differences (n = 2), revealed significant treatment

effects. In the remaining paper that reported negative

results based on significance testing, no substantial

changes with regard to the original interpretation of

the results were necessary after calculating the odds

ratio.

Discussion

Studies of leakage in Endodontics have a long and

controversial history, with both supporters and

detractors (Oliver & Abbott 2001, Susini et al. 2006,

Editorial Board of the Journal of Endodontics 2007,

De-Deus 2008). Thus, the relationship of in vitro

leakage to clinical success or failure of endodontic

treatment has been widely debated (Oliver & Abbott

2001). Furthermore, the inconsistency apparent

amongst the results of different studies means that

the value of virtually any endodontic technique may

be supported or disputed (Editorial Board of the

Journal of Endodontics 2007).

327

important and this parameter should continue to be

used as a factor to rank and evaluate new materials

(De-Deus 2008, Wu 2008). Consequently, there is a

need to try to create a standard method that is reliable

and reproducible and that relates to clinical outcomes

(Editorial Board of the Journal of Endodontics 2007).

Concerning this point, it is important to note that

the reliability of any research depends on the internal

validity of the study, which refers to the qualitative

characteristics of the methodology employed (Pandis

et al. 2011). Several papers have discussed methodological aspects that can influence the outcome of

in vitro leakage (Pommel et al. 2001, Camps & Pashley 2003, Karagenc et al. 2006, Rechenberg et al.

2011). Given the importance of the statistical methodology in terms of the validity of the findings of any

research, it is particularly striking that, to date, no

study has determined the prevalence or the exact

implications of possible errors or misuse of statistics

on the validity of these studies.

In the present review, the authors have found a

high prevalence of statistical errors, most of which

are committed during the planning stage and the statistical-analysis phase (Table 1). It should be noted

that errors in the analysis phase can be corrected if

the study design is sound, but flaws in the study

design can lead to data that are unusable.

A recent review (Pandis et al. 2011) concluded that

reporting on sample-size calculations in dental

research is low, ranging from 0% to 28% amongst

dental speciality publications. In this study, only 2%

of the studies employed sample-size estimation. However, an appropriate sample size is crucial for highquality statistical work, to detect any differences

between study groups. Inadequate sample size often

leads to type-II errors, in which the null hypothesis is

falsely accepted. Thus, a previous study (Schuurs

et al. 1993) concluded that the value of many

endodontic leakage studies is limited because of the

inadequate power of the statistical test applied, as a

result of sample sizes that are unjustifiably small.

With respect to the analytical phase, the present

data are in agreement with the findings of previous

studies (Altman 1991, Tu et al. 2004, 2005, Abt

2010a,b) that one of the most frequent methodological errors is to select an incorrect statistical test. For

example, the chi-squared test is applied to analyse

ordinal-scaled data that appear as frequencies or

number of observations in every category. Application

of this test requires observations to be independent,

328

more than 20% of the cells should have an expected

cell frequency 5 (Kim et al. 2011). To satisfy these

requirements, a sufficiently large sample size is necessary. However, 15 articles were found to violate the

above conditions. In these cases, Fishers test or the

chi-squared test with Yates correction would have

been more appropriate options.

This review also shows that one-way analysis of

variance is one of the most egregiously misused

statistical methods (Kim et al. 2011). For the proper

use of a one-way ANOVA, the populations must be

independent, normally distributed and have the same

variance. With respect to the issue of distribution,

normality tests should always be used as a prerequisite to the application of parametric or nonparametric

tests, but invoking the central limit theorem, the nonnormal distribution of the variable does not always

involve the rejection of the parametric test (Cohen

2001), since, even if the variables do not follow a

normal distribution, their means may do so, provided

that the sample has been taken randomly from the

population and the sample size is sufficiently large.

When these conditions are not satisfied, a transformation of the variable would make sense. This could

lead to an approximately Gaussian distribution, and

the variances would equalize. Examples of such transformations are the square-root transformation for

Poisson data, the Box-Cox transformation for regression analysis, and the arcsine transformation for

proportions. Another common situation in practice

occurs when there are several independent Gaussian

variables, and one has a different variance. In this

situation, the procedure required is to perform, first,

an ANOVA amongst the remaining variables and then

to apply a hypothesis test between the means of two

variables with different variances, using the Welch

approximation to degrees of freedom. However, as

shown in Table 4, in 75 of the 196 cases with count

variables, these conditions were not met, and

consequently, the statistical methodology applied was

considered to be incorrect.

The article that used a nonparametric test on

normal data has also been classified as incorrect

because in this case a parametric test, being more

powerful and versatile, would have been the correct

option.

This survey shows the important influence of the

statistical test adopted, with respect to the results and

interpretation of any research, given that a change in

the conclusions was necessary in 19% of the studies

both the correct and the incorrect statistical tests lead

to the same conclusion, of course the P-values will be

different, (in this review, this circumstance arose in

50% of the recalculations). Therefore, the misuse of

statistics in data analysis may lead to erroneous

conclusions and make the research findings difficult

to replicate. This highlights the need for the raw data

to be reported, at least during the editorial review

process, prior to the acceptance of an article. The

final decision on acceptance should be taken only

after screening by a statistical expert provided by the

Journal. Journals could also publish online extended

version of articles including the entire body of data as

supporting information, thus allowing readers to

perform alternative analyses.

In relation to the presentation and interpretation

of study results, in 91% of the articles reviewed, only

P-values are reported and used to draw conclusions concerning intervention effectiveness. However, it has long

been recognized that over-reliance on P-values is often

misleading (Rothman 1978, Pandis et al. 2011). Thus,

an intervention may be found to be not statistically significant because of inadequate sample size, even though,

if the intervention were applied to the population, it

might have a very important clinical effect. Conversely, a

statistically significant effect could be small and of very

little clinical importance (Petrie et al. 2002). A recent

publication (Vavken et al. 2009) showed that a high

proportion of statistically significant results (31%) do not

reflect relevant treatment effects.

In this context, a more appropriate presentation of

the results would be to quote the exact P-values and

the CIs. Thus, the reader would have the possibility of

interpreting the results from a broader perspective

(Gardner & Altman 1986, Goodman 1999, Abt 2011,

Pandis et al. 2011). Nevertheless, in accordance with

previous findings (Pandis et al. 2011), it is crucial to

note that there is very limited adoption of CI reporting

in the literature on leakage in Endodontics. In this

review, only one of 90 studies that used parametric

tests included CIs. This pattern of data interpretation

may have important implications for the implementation of research findings in clinical practice (Pandis

et al. 2011, Polychronopoulou et al. 2011).

In this study, amongst all the papers reporting

positive results on the basis of the inferential test, the

use of the odds ratio reflected large treatment effects

in 75% of them. Conversely, amongst five studies

with negative results (no significant differences), the

use of the odds ratio indicated that the intervention

(20%). Therefore, it was verified that the use of the

odds ratio could help avoid an erroneous interpretation in one study, at least.

The limitations of this review include the fact that

only a specific topic (leakage) was included, perhaps

introducing selection bias; however, articles from

20 different journals were examined, and therefore,

the inclusion of more topics, although this would

have increased outcome precision, would not be

expected to alter the conclusions.

The availability of statistical software packages and

the lack of a system to validate the competence of

persons who perform the statistical analysis could

explain this prevalent misuse of statistics in dental

research (Altman et al. 2002, Kim et al. 2011).

Although the errors in research methods are mainly the

authors responsibility, a clear attitude taken by the

editorial boards of dental journals is also required to

minimize this problem in forthcoming years. Authors

and editors should have the same goal, to seek the highest standards of science. Therefore, researchers may

benefit greatly from involving expert statistical help at all

stages of a research project. Editorial boards could also

contribute by creating detailed guidelines on how to conduct and report statistical methods, by applying stronger

statistical reviewing policies and by encouraging the publication of the full and transparent reporting of research

(i.e. extended version of articles including the raw data

used in research articles) (Altman 2002). If journals are

willing to implement this policy, they should suggest it

explicitly to authors. With respect to the consequences of

statistical mistakes, as they can go unnoticed for a long

time, their impact is not easy to quantify.

Conclusions

Statistical deficiencies found in studies of leakage in

Endodontics may affect their results and interpretation

and might be one of the reasons for the poor agreement

amongst the reported findings. The standardization of

statistical methodology should be more widely implemented and assistance from a statistical expert is highly

recommended.

Acknowledgements

We thank David Nesbitt and Glenn Harding for the

English version of the text. This research was supported

by Ministerio de Ciencia e Innovacion (Spain) grant

MAT2009:09795.

329

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