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Reporting quality of cohort studies in periodontology before and after the STROBE publication: a trend analysis

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Reporting quality of cohort studies in periodontology before and after the STROBE publication: a trend analysis

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Content Copyright 2022 Shira Scholten
Reporting Quality of Cohort Studies in Periodontology Before and After the STROBE
Publication: A Trend Analysis
by
Shira Scholten, D.M.D.
A Thesis Presented to the
FACULTY OF THE USC HERMAN OSTROW SCHOOL OF DENTISTRY
UNIVERSITY OF SOUTHERN CALIFORNIA
In Partial Fulfillment of the
Requirements for the Degree
MASTER OF SCIENCE
(BIOMEDICAL IMPLANTS AND TISSUE ENGINEERING)
August 2022

ii

Acknowledgements

I would like to express sincere gratitude to my faculty at the University of
Southern California who have offered endless support and encouragement during this
project. First, I am extremely grateful to Dr. Satish Kumar for the ideas in this research,
and for his guidance and endless patience throughout the process. I feel incredibly
fortunate to have had his mentorship and experience his unique and exceptional way of
thinking. I would not be where I am today without the encouragement and support of
Dr. Kian Kar, and I am grateful for his infinite wisdom and support. I would also like to
thank Yael Breziner for acting as a secondary examiner of the literature, and Dr. Chen
and Dr. Navazesh for serving as my committee members. Lastly, I would like to warmly
thank my brother, Jordan Butt, for his help interpreting my data and for sharing his
unwavering and contagious enthusiasm for scientific research.

iii

Table of Contents
Acknowledgements .......................................................................................................... ii
List of Tables ................................................................................................................... iv
List of Figures ................................................................................................................... v
Abstract ........................................................................................................................... vi
Chapter 1: Background & Introduction ............................................................................. 1
Observational Studies ................................................................................ 2
Guidelines for Reporting Quality ................................................................. 5
Aim ............................................................................................................. 8
Research Question ..................................................................................... 9
Null Hypothesis ........................................................................................... 9
Rationale .................................................................................................... 9

Chapter 2: Methods ........................................................................................................ 10
Search Results ......................................................................................... 13
Article Ratings for Quality of Reporting Assessment ................................ 15

Chapter 3: Results ......................................................................................................... 18
Statistical Analysis .................................................................................... 18
General Adherence of Articles to STROBE Checklist .............................. 18
Items With High Scores ............................................................................ 19
Items with Low Scores .............................................................................. 20
Endorsement of STROBE Criteria ............................................................ 26

Chapter 4: Discussion .................................................................................................... 26
Reporting Quality in Periodontal Literature ............................................... 27
Cohort Classification ................................................................................. 31
Title and Abstract ...................................................................................... 36
Study Limitations ...................................................................................... 37

Chapter 5: Conclusion .................................................................................................... 38
References ..................................................................................................................... 40
Tables and Figures ........................................................................................................ 49

iv

List of Tables

Table 1 Eligible studies included in analysis .................................................................. 49
Table 2: Original Unmodified STROBE 2007 Statement ............................................... 61
Table 3: STROBE checklist with additional extension ................................................... 64
Table 4: The currently accepted evidence hierarchy ..................................................... 75
Table 5: Number of citations found for each journal at each year .................................. 77
Table 6 The pool of citations found for each journal after hand selection ...................... 78
Table 7: Articles endorsing the STROBE criteria ........................................................... 85

v

List of Figures

Figure 1: Title and Abstract ............................................................................................ 21
Figure 3: Funding Information ........................................................................................ 22
Figure 2: Bias ................................................................................................................. 22
Figure 4: Study Size ....................................................................................................... 23
Figure 5: Statistical Methods Item 12c ........................................................................... 23
Figure 6: Statistical Methods Item 12e ........................................................................... 24
Figure 7: Results ............................................................................................................ 24
Figure 8: Missing Data ................................................................................................... 25
Figure 9: Title and Abstract ............................................................................................ 34
Figure 10: Search strategy ............................................................................................. 76
Figure 11: Trend in the Number of Cohort Articles Published Annually ......................... 79
Figure 12: Adherence of selected articles to the STROBE checklist ............................. 80
Figure 13: Average compliance to the STROBE checklist by year ................................ 81
Figure 14: Compliance to the STROBE checklist by journal and by year ...................... 82
Figure 15: Distribution of STROBE scores by year ........................................................ 83
Figure 16 The average percentage compliance across all articles ................................ 84

vi

Abstract

Title: Reporting Quality of Cohort Studies in Periodontology Before and After the
STROBE Publication: A Trend Analysis

Background: Observational studies are an important source of evidence in the
clinical practice of dentistry and medicine. The Strengthening of Reporting of
Observational Studies in Epidemiology (STROBE) checklist was originally created in
2007 to systematically improve reporting quality in observational research, including
cohort, case-control, and cross-sectional studies.

Aim: This cross-sectional survey evaluated cohort reports published between
2000 and 2018 in two high impact periodontology journals. The percentage of STROBE
items reported sufficiently in each article at two years prior to the 2007 STROBE
publication (2000, 2006), and two years post 2007 STROBE publication (2012, 2018)
was compared using descriptive trend analyses.

Methods: The PubMed electronic database was used to select a pool of cohort
reports in the Journal of Periodontology (JOP) and the Journal of Clinical
Periodontology (JCP) from the years 2000, 2006, 2012, and 2018. Seven cohort
articles were randomly selected from each journal at each time point, totaling in 56
articles with 4 time points, two prior to STROBE (2000, 2006), and two post STROBE
(2012, 2018). Each article was methodically rated based on the STROBE checklist and

vii

assigned a compliance score. A trend analysis of article adherence was completed and
average STROBE scores were compared across time, journals, and checklist items.

Results: Of the 85 cohort articles published in the two journals in 2000, 2006,
2012, and 2018, 56 articles were randomly selected for evaluation. The average
adherence to the STROBE checklist of all articles was 73%, and the STROBE score
was shown to increase significantly over time (the average score in 2000 of 63% versus
the average score in 2018 of 80%). The number of cohort articles published in each
year/journal was consistently low (n≤12). Categories which continue to need
improvement include item 9 “Describe any efforts to address potential sources of bias,”
and item 10 “Explain how the study size was arrived at,” and all items which involved
the management of participants lost to follow-up (items 12, 13, and 14).

Conclusion: The quality of cohort reports published in periodontology has
improved significantly between the years of 2000 and 2018, but many items of the
STROBE guidelines remain unmet across all years. Due to limitations of an
uncontrolled before-after trend analysis, it cannot be concluded whether the increased
adherence is due to the publication of the STROBE guidelines, or due to a progressively
positive trend in reporting quality over time. It was clear, however, that publications that
explicitly recognized the STROBE guidelines tended to have higher average ratings.
While this study has limitations, the checklist items which need improvement based on
our findings have also been highlighted in comparable reviews in periodontology and
implant dentistry. Most notable shortcomings include attempts to address bias,

viii

explanation of sample size calculations, reports of participation and follow up, and
reports indicating the number of participants with missing data. Based on the results of
this trend-analysis, an increase in quality of cohort studies in periodontology is still
needed, and adherence of observational studies to STROBE should be required by all
journals. Journals in periodontology may benefit from additional mechanisms in place
to increase adherence to reporting guidelines, such as requirements that authors submit
written descriptions of how each checklist criteria has been met in a prospective article
prior to publication.

1
Chapter 1: Background & Introduction

With the contemporary emphasis on evidence-based dentistry and
periodontology, the quality of published research has never been more important.
Scientific evidence, along with the clinician’s personal experience, patient preferences,
and clinical circumstances, is used daily by clinicians to support decisions in treatment
planning and to explain these decisions to patients and peers. While literature shows
that the quantity of publications has increased annually (Elwood, 2016), the quality of
evidence may not be developing in the same direction. For a clinician to cautiously
gather information and incorporate evidence-based dentistry into his/her practice, it is
imperative to understand research design classifications and the inherent limitations of
each category.

2

Observational Studies

Evidence-based dentistry and medicine categorizes research into two main study
design groups: (1) experimental and (2) observational. For a study to be categorized as
experimental, a procedure or intervention is part of a study design, and is administered
to the participants methodically by the researcher. The assignment of the participant to
receive the treatment or not can be random (in a randomized controlled trial/RCT), or
non-random (in a non-randomized controlled clinical trial). Randomized controlled trials
(RCTs) are at the top of the evidence hierarchy, and are accepted to be the most
reliable study design in terms of minimizing bias and confounding variables. While
randomized controlled trials (RCTs) are widely accepted to have valuable advantages in
terms of the accepted hierarchy of research validity, there are many disadvantages to
this model. Most notably, many experimental models cannot be implemented ethically
and must therefore be investigated using an observational approach. Observational
studies observe participants and report outcomes without intervention. Observational
studies are often criticized for running a higher risk of containing bias, or confounding
factors that are unaccounted for. Due to the complexity of dental research and
epidemiology, however, observational studies are necessary. A well-designed
observational study can attempt to minimize certain types of bias, control for
confounding variables and significantly increase the validity of the results (Concato,
2004).
Observational studies can be further categorized into analytical studies (such as
cohort, cross-sectional, and case-control studies), and descriptive studies, such as case
reports or case series reports. Descriptive studies such as case reports simply involve

3

the observation of an occurrence or observation, and are considered the lowest grade
of evidence within the category of observational studies. An argument can be made
that much of the criticism that observational research receives is based on observations
and data from the lower forms of observational research such as descriptive studies
(Concato, 2004). Case series reports have even been described by Dekkers as a
“neglected design,” however this format is often used to present rare disorders and
diseases that present too rarely to examine using a higher form of study (Dekkers et al.,
2012). Another group of observational studies includes analytical studies, which can be
subdivided into cross-sectional, case-control, and cohort studies. Many authors in
epidemiology state that all analytical studies must incorporate a control group (Grimes
and Schulz, 2002). It should be noted, however that in the STROBE criteria, this
distinction is only explicitly made for case-control studies (Vandenbroucke et al., 2014).
Cross-sectional studies involve the collection data from a representative sample at a
single time point. One major disadvantage of cross-sectional study is the difficulty in
determining the order of the exposure and the outcome, which can lead to confusion
regarding the cause and effect. Case-control studies involve the comparison of groups
with and without the defined outcome, whereas case-control studies initially sample
groups based on outcomes. The major distinction of cohort studies, is that patients are
pooled based on initial exposures, and then evaluated for outcomes. Cohort studies are
defined by the authors of the STROBE criteria as studies which follow exposed patients
from a defined start time until a pre-determined end time. Researchers often contrast
exposed and non-exposed cohorts, which allows for the calculation of relative risk,
showing how each individual variable effects the probability of the outcome. According

4

to the authors of the STROBE criteria, however, a control group is not a defining
component to a cohort study (Dekkers et al., 2012) (see “Cohort Classification” section
for more information).
Cohorts are considered the highest form of clinical evidence within the subgroup
of observational studies. Therefore, in areas of research where randomized controlled
trials are not appropriate, cohorts may be the best option for ethical or logistical
reasons.

5

Guidelines for Reporting Quality

Cohort study designs fall within a widely accepted “hierarchy” of research
designs (Table 4). Knowledge of this “hierarchy of evidence” theoretically should
provide the tools for clinicians to efficiently navigate to the most reliable information.
Creating a hierarchy of research design types theoretically allows readers to gauge the
utility of an article for a specific need. Most research, however, regardless of its place
on the hierarchy, is neither conducted nor reported acceptably, often due to problems
such as poor study design and bias (Loannidis et al., 2014). To improve scientific
research publications and increase the transparency of information available to
clinicians, references have been published with reporting guidelines on the EQUATOR
Network. The EQUATOR Network can be accessed publicly online at equator-
network.org, and is an international initiative to improve reporting quality of health
research by providing reporting guidelines for the most common types of study designs.
The first resource to be featured on the EQUATOR was published in 1996 for the
assessment of randomized clinical trials: “The Consolidated Standards for Reporting
Trials” (CONSORT) (Moher et al., 2001). Checklists with a similar goal have been
published for systematic reviews, including the widely used “Assessment of Multiple
Systematic Reviews” (AMSTAR) checklist (Shea et al., 2007), and the Glenny checklist
(Glenny et al., 2003). The use of these statements has been shown to improve the
quality of research in major medical journals based on comparative evaluations of
articles before and after their respective checklist publication (Moher et al., 2001) (Kelly
et al., 2016) (Hopewell et al., 2016).

6

The original STROBE (Strengthening of Reporting of Observational Studies in
Epidemiology) statement from 2007 is the second article to be displayed on the
EQUATOR website, and was created to improve reporting of analytical observational
studies and create a way to measure the quality of these studies (von Elm et al., 2007).
Currently, there are no long-term trend analyses examining the adherence of cohort
studies to the STROBE criteria over time in periodontology journals, although there
have been a few similarly designed publications in other areas of medical research. For
example, a trend analysis in a nephrology journal examined the quality of evidence
before and after the STROBE statement, concluding that no significant evidence for
change in the quality of reporting between 2002-2013 could be found (Rao et al., 2016).
This trend analysis included only 11 pre-STROBE articles and 26 post-STROBE
articles, and the authors noted that significant improvements in scores were shown in
articles from 2011 to 2013 compared to previous years (Rao et al., 2016). In a
dermatology journal, observational studies were examined for adherence based on the
STROBE criteria and grouped into two pre-STROBE periods and one post-STROBE
period. The authors concluded that, based on their evaluations, reporting quality of the
observational studies was increasing steadily over time, with the STROBE statement
playing an insignificant role in this improvement (Bastuji-Garin et al., 2013). This article,
however, only includes one cohort of post-STROBE articles with publication dates
rangeing from 2008-2010. It is possible that the STROBE statement has impacted
journals to a greater extent in later years, after which many journals began to officially
require the these reporting guidelines (such as the Journal of Clinical Periodontology),
and authors may have developed a greater awareness.

7

It is still not fully clear how effectively the publication of the STROBE criteria in
2007 has affected improvement of reporting quality in observational studies in medical
and dental journals. In high impact periodontology journals such as the Journal of
Periodontology (JOP) and the Journal of Clinical Periodontology (JCP), cross-sectional
surveys of have been performed to analyze the quality of reporting at a single time
point, which examined the reporting of both observational studies and randomized
controlled trials (Bushehri, 2015; Kumar et al., 2018b). To this date, there is no long-
term trend analysis of the quality of reporting of cohort studies in periodontology, and no
publication which demonstrates the impact of the 2007 STROBE publication on the
quality of reporting in periodontology.

8

Aim

This report is a longitudinal study evaluating cohort reports published at four time
points (with a time span of 18 years) in two high impact periodontal journals (Journal of
Periodontology and Journal of Clinical Periodontology). Seven cohort articles were
randomly selected from each journal in 2000, 2006, 2012, and 2018 totaling 56 articles
with 4 time points selected every 6 years starting at the year 2000. This time frame was
selected to examine articles published in two separate years prior to the 2007 STROBE
publication (2000, 2006) and two separate years after the STROBE publication (2012,
2018).

9

Research Question: How has the quality of reporting changed in two high impact
periodontology journals after the publication of the STROBE statement in 2007?

Null Hypothesis: There is no difference in the publication quality of cohort studies
in selected periodontology journals from 2000 to 2018, before and after STROBE was
published.

Rationale

The STROBE publication was originally created in 2007, and publications from 7
years before, 1 year before, 5 years after, and 11 years after the release of the checklist
were analyzed. The 4
th
timepoint of 2018 was selected due to this being the latest year
available at the beginning of this project in 2019. The selection of Journal of
Periodontology and Journal of Clinical Periodontology was based on the consistently
high impact factors these journals have had in periodontology from 2000-2019. The
selection of four time points allowed for the evaluation of the quality of reporting over
time so that the temporal trends in reporting could be estimated in addition to the
influence of the STROBE publication.

10

Chapter 2: Methods

A search was initially conducted using the PubMed electronic database selecting
cohort articles published in the Journal of Periodontology and the Journal of Clinical
Periodontology at the years 2000, 2006, 2012, 2018. The following search shows an
example of the search conducted for the year 2000:

1) “J Periodontol."[Journal] AND ("cohort studies"[MeSH Terms] OR ("cohort"[All
Fields] AND "studies"[All Fields]) OR "cohort studies"[All Fields] OR "cohort"[All
Fields]) AND ("2000/01/01"[PDAT]: "2000/12/31"[PDAT])
2) "J Clin Periodontol"[Journal] AND ("cohort studies"[MeSH Terms] OR
("cohort"[All Fields] AND "studies"[All Fields]) OR "cohort studies"[All Fields] OR
"cohort"[All Fields]) AND ("2000/01/01"[PDAT]: "2000/12/31"[PDAT])

The same MeSH (Medical Subject Heading) terms were used for the years 2000,
2006, and 2012 as shown in the following search criteria:

2006:
1) “J Periodontol."[Journal] AND ("cohort studies"[MeSH Terms] OR ("cohort"[All
Fields] AND "studies"[All Fields]) OR "cohort studies"[All Fields] OR "cohort"[All
Fields]) AND ("2006/01/01"[PDAT] : "2006/12/31"[PDAT])
2) "J Clin Periodontol"[Journal] AND ("cohort studies"[MeSH Terms] OR
("cohort"[All Fields] AND "studies"[All Fields]) OR "cohort studies"[All Fields] OR
"cohort"[All Fields]) AND ("2006/01/01"[PDAT] : "2006/12/31"[PDAT])

11

2012:
1) “J Periodontol."[Journal] AND ("cohort studies"[MeSH Terms] OR ("cohort"[All
Fields] AND "studies"[All Fields]) OR "cohort studies"[All Fields] OR "cohort"[All
Fields]) AND ("2012/01/01"[PDAT] : "2012/12/31"[PDAT])
2) "J Clin Periodontol"[Journal] AND ("cohort studies"[MeSH Terms] OR
("cohort"[All Fields] AND "studies"[All Fields]) OR "cohort studies"[All Fields] OR
"cohort"[All Fields]) AND ("2012/01/01"[PDAT] : "2012/12/31"[PDAT])

2018
1) “J Periodontol."[Journal] AND ("cohort studies"[MeSH Terms] OR ("cohort"[All
Fields] AND "studies"[All Fields]) OR "cohort studies"[All Fields] OR "cohort"[All
Fields]) AND ("2018/01/01"[PDAT] : "2018/12/31"[PDAT])
2) "J Clin Periodontol"[Journal] AND ("cohort studies"[MeSH Terms] OR
("cohort"[All Fields] AND "studies"[All Fields]) OR "cohort studies"[All Fields] OR
"cohort"[All Fields]) AND ("2018/01/01"[PDAT] : "2018/12/31"[PDAT])

The use of the PubMed electronic database allowed for journals fitting the
inclusion criteria to be identified methodically, although the search was accompanied
with additional hand searching of the two journals. No additional cohort articles were
identified from hand searching.

12

Inclusion Criteria

Only cohort studies from the years 2000, 2006, 2012, and 2018 in the Journal of
Periodontology and the Journal of Clinical Periodontology published in the English
language were included. There was no topic related restriction, and both retrospective
and prospective cohort articles were included.
Due to the heterogeneity in the definition of a cohort study, there will undoubtedly
be controversy surrounding the classification of many articles. To maintain consistent
with the STROBE guidelines, for the purposes of this paper, studies that meet the
criteria defined by authors of the original STROBE statement in Dekkers et al., were
grouped as cohort articles.

Exclusion Criteria

All studies that were not of a cohort study design were excluded. Examples of
study designs excluded are other forms of observational analysis such as cross-
sectional and case-control studies, as well as descriptive studies such as case series
and surveys. Experimental studies such as randomized controlled trials were also
excluded, as well as systematic reviews/meta-analyses, and consensus reports.

13

Search Results

Using the MeSh terms previously specified, PubMed’s electronic database was
used to find a total of 471 articles from the years 2000, 2006, 2012, 2018 combined.
Table 5 shows the number of citations found for each journal at each year (total = 471).
All citations and abstracts of cohort studies from the four selected journals were
retrieved for the years 2000, 2006, 2012, and 2018 and imported into EndNote X6
software (Thomson Reuters, Philadelphia, USA).
Endnote was used to remove the citations that were not from the years 2000,
2006, 2012, and 2018. For example, 2019 citations were included in the PubMed
search that had been published online late in 2018 were removed. A duplications test
was run using Endnote’s “find duplicates” feature. Duplicate articles were deleted
according to date (the article published at the earliest date was retained). After the
removal of duplicate articles and incorrect years, the abstracts of 389 remaining articles
were read, and any article incorrectly classified as a cohort article was removed by
hand. Table 5 shows the number of citations found for each journal at each year after
the completion of these procedures (n=85). Figure 2 shows the number of cohort
articles published annually in JOP and JCP, which remained consistently low (9-12
cohort articles per journal per year). Initial screening for cohort articles was performed
by the primary evaluator (S.S.), and any uncertainties were addressed by the secondary
reviewer (S.K).

14

The online website designed for research randomization (www.randomizer.org)
was again used to randomly produce 7 numbers between 1 and x for each journal and
year (x=number of cohort articles in the journal/time point). Randomizing the articles
used from different time points removed selection bias and increased the quality of
evidence. The method was used to select the final 56 cohort articles (ArRejaie et al.,
2019; Auyeung et al., 2012; Beliveau et al., 2012; Bergström et al., 2000; Bonino et al.,
2018; Broadbent et al., 2006; Buchmann et al., 2000; Buduneli et al., 2006; Carrillo-de-
Albornoz et al., 2012; Collares et al., 2018; Costa et al., 2012a; Costa et al., 2012b;
Costa et al., 2018; Covani et al., 2012; Cunha-Cruz et al., 2006; de Castilhos et al.,
2012; Duarte et al., 2018; Erley et al., 2006; Fugazzotto, 2012; Hanookai et al., 2000;
Heaton et al., 2018; Holtfreter et al., 2012; Hughes et al., 2006; Hujoel et al., 2000;
Keller et al., 2012; Kocher et al., 2000; Kumar et al., 2018a; Lahdentausta et al., 2018b;
Linden et al., 2012; Machtei et al., 2000; Miyamoto et al., 2006; Morelli et al., 2018;
Moreno Rodríguez et al., 2018; Nascimento et al., 2019; Nilsson et al., 2018;
Pattrapornnan et al., 2012; Payne et al., 2000; Persson et al., 2000; Pitiphat et al.,
2006; Robinson et al., 2000; Roos-Jansaker et al., 2006; Schwartz-Arad et al., 2000;
Shimazaki et al., 2006; Soikkonen et al., 2000; Suda et al., 2000; Swierkot et al., 2012;
Tanaka et al., 2018; Thomson et al., 2006; Tilakaratne et al., 2000; Tonetti et al., 2000;
Van der Velden et al., 2006; Venza et al., 2006; Wolf et al., 2006) to be included for this
paper (see table 1 for a chart of included studies). Figure 1 includes a flow chart
detailing the article selection process for the final 56 cohort articles included for
analysis.

15

Article Ratings for Quality of Reporting Assessment

The cohort studies selected for analysis were scored using the criteria described
in the original STROBE statement of 2007. While the STROBE checklist contains a
total of 22 item numbers, items 1, 6, 12, 13, 14, and 16 are further subdivided into two
or more sections with separate conditions, a method described in detail by Bushehri et
al. These sections were each given their own additional score, leading to a total of
thirty-four items in the STROBE statement which were used to score all articles.
Many items published in the initial STROBE checklist are subjective in nature,
and notable expansions of the STROBE statement have been published attempting to
rectify this (Cheng et al., 2016). When additional explanation and elaboration was
required to score an item, a detailed explanation of every item on the STROBE checklist
by Vandenbroucke et al. 2014 was referred to. A chart containing the original STROBE
checklist as well as additional explanations previously formulated by Bushehri et al.
(Bushehri, 2015) was created, and an additional column was added to the chart to
provide further explanations (Table 3). This process decreased subjectivity and
attempted to produced consistent and standardized data collection for all papers
reviewed by adding reporting guidelines to each of the thirty-four items in order to create
an objective scoring system, allowing for a dichotomous yes/no answer. The score for
each article was calculated by adding the total number of items scored with 1. The
percentage of items adequately addressed was calculated for each journal by dividing
the numerical score by 34 (X/34), and multiplying by 100%.

16

All scoring was completed using a Microsoft Excel spreadsheet, and for each of
the 34 parts, a score of 1 was added for “yes,” and a score of 0 for “no.” After the
completion of inter and intra-evaluator calibration, each article was scored by primary
reviewer (Shira Scholten [SS]), and secondary reviewer (Yael Breziner [YB]).

Calibration protocol:

Due to the qualitative nature of some of the checklist items, the intra and inter-
evaluator calibration sessions were designed to increase the consistency of checklist
responses. After the 56 articles for analysis were removed from the 85 total cohort
articles from the two journals and four time points, the remaining 29 articles were placed
into one group, and three articles were randomly selected from this group using an
online website designed for research randomization (www.randomizer.org). Three
numbers were randomly generated between 1 and 61, and these numbers
corresponded to the chosen articles. These articles were used for the calibration
process, and were evaluated using the STROBE checklist. Intra-evaluator calibration
(calibration of the 1
st
evaluator only) was performed by reading the three articles once,
and then reading the same articles five weeks later. Results were compared and a
Kappa analysis was run to measure agreement with a Kappa score of 0.925. Areas of
concern were checked by 3
rd
evaluator Satish Kumar (SK). Inter-evaluator calibration
(between the 1st and 2nd evaluator) was performed in a similar manner using three
different articles, and areas of discrepancy were discussed and resolved. A Kappa
analysis for inter-evaluation was performed with a score of 0.8968.

17

18

Chapter 3: Results

Statistical Analysis

The STROBE scores of cohort studies in each pool of journals was evaluated
using descriptive statistics. This evaluation was based on the scoring system
developed by Bushehri et al. which generated a numerical score (X) out of 34 possible
points. The percentage of items adequately addressed was calculated for each journal
by dividing the numerical score by 34 (X/34) multiplying by 100%. This allowed for
comparison of compliance averages across time and between journals, and this data
was used to complete descriptive statistics. The standard error of each group was
calculated by dividing the standard deviation by the square root of the sample size.
Studies which explicitly cited the STROBE criteria from 2012 and 2018 were noted and
grouped for analysis.

General Adherence of Articles to STROBE Checklist

Compliance scores for each of the 56 article were calculated and converted into
percentages (Figure 2). No article was fully adherent to the checklist, and the average
overall adherence was 73%.
The average adherence to STROBE across the selected years (2000, 2006,
2012, 2018) was compared (Figure 3), with 2012 calculated to have the highest mean
compliance of 81% overall, and 2000 calculated to have the lowest mean compliance of
63%. The overall trend is an increase in STROBE compliance from 2000 to 2018,

19

although 2012 and 2018 have almost the same average scores. The distribution of
scores across all years was highly variable with an overall positive trend in scoring
(Figure 5).

The average STROBE compliance was also measured and compared between
JOP and JCP. The percentage adherence of both JOP and JCP tended to increase
with time, with JOP scores increasing by an average of 13% between 2000 and 2018,
and JCP scores increasing by an average of 21% between 2000 and 2018. JOP
showed consistent steady improvement, and each year the average score increased by
a small increment. The average compliance of JCP was irregular, with a great
improvement in the average score between 2006 and 2012, and the highest percentage
of compliance in 2012 (Figure 4).

Items With High Scores

Average adherence to each item in the STROBE checklist was calculated across
all selected articles (Figure 7).

The following items had a 100% rate of compliance across all journals and all years:

• Item 11 quantitative variables
• Item 18 Key Results

20

The following items had a rate of compliance 95% or greater across all journals and all
years:

• Item 1b Title and Abstract
• Item 2 Background and Rationale
• Item 3 Introduction/Objectives
• Item 5 Methods: Setting
• Item 8 Data Source/Measurement
• Item 15a Outcome Data
• Item 16b Main Results
• Item 20 Interpretation

Items with Low Scores

The following items had an average rate of compliance 30% or less throughout all
years:

• Item 12e Statistical Methods
• Item 13c Results

21

The following items had an average rate of compliance of 50% or less throughout all
years:

• Item 1a Title and Abstract
• Item 9 Bias
• Item 10 Study Size
• Item 13c Statistical Methods
• Item 13b Results
• Item 14b Descriptive Data

Some critically deficient items of the checklist improved in score over time.

For example checklist Item 1a
(left) showed a dramatic
improvement over time, and
many JOP and JCP publications
now properly indicate the
study’s design in the title and/or
the abstract. This has the most
significant improvement of any checklist item, with the Journal of Clinical Periodontology
increasing by 100% from 2000 to 2018.

0%
20%
40%
60%
80%
100%
2000 2006 2012 2018
Average Compliance to
STROBE
Item 1a: Title and Abstract
Journal of
Periodontology
Journal of Clinical
Periodontology
Figure 1: Title and Abstract

22

Another checklist item
which showed dramatic
improvement over time for both
journals was Item 22: funding
information, which increased
from 29% to 100% in the
Journal of Clinical

Periodontology from 2000 to 2018. Based on the STROBE criteria, the ”role of the
funders for the present study” must also be discussed. Some leniency was given for
this category in the grading, and it was not required that details be provided regarding
the exact part of the research the funding was provided for. Some checklist items, on
the other hand, showed
inconsistent improvement.
The score addressing bias
(checklist item 9), on the other
hand, remained constantly low
in both journals and showed no
temporal improvement. Journal
of Clinical Periodontology
tended to have slightly higher
ratings for item 9, especially after the year 2006. Generally articles that did not include
0%
20%
40%
60%
80%
100%
2000 2006 2012 2018
Average Compliance to
STROBE
Item 9: Bias
Journal of
Periodontology
Journal of Clinical
Periodontology
0%
20%
40%
60%
80%
100%
2000 2006 2012 2018
Average Compliance to
STROBE
Item 22: Funding Information
Journal of
Periodontology
Journal of Clinical
Periodontology
Figure 2: Funding Information
Figure 3: Bias

23

the word “bias” were screened for other attempts to address this item such as the
discussion of “human error”. It was easier as the reviewer to give credit for this section,
however, if the word bias is used, and there is a paragraph clearly and explicitly
addressing this issue. This demonstrates the importance of utilizing the checklist as an
author in order to ensure that attempts to address each section is explicitly
communicated in a way preferred by the scientific community.

Study size calculations
(item 10) were also poorly
reported over time, however the
Journal of Clinical
Periodontology showed a
greater improvement. When
mentioned, study size
calculations were sometimes incomplete, but credit was given if any calculation was
attempted, with leniency regarding the sophistication of the calculation.

Item 12c was consistently
weak, and less than 50% of
journals explained how missing
data was addressed. Most
articles stated that there was
missing data without making
0%
20%
40%
60%
80%
100%
2000 2006 2012 2018
Average Compliance to
STROBE
Item 10: Study Size
Journal of
Periodontology
Journal of Clinical
Periodontology
0%
20%
40%
60%
80%
100%
2000 2006 2012 2018
Average Compliance to
STROBE
Item 12c: Statistical Methods
Journal of
Periodontology
Journal of Clinical
Periodontology
Figure 5: Statistical Methods Item 12c
Figure 4: Study Size

24

any attempt to address this problem statistically. Some authors made no mention of
missing data. A notable exception to this is JCP in 2012 with 86% adherence.

When sensitivity analysis
was described in an article, this
article was adherent to item
12e. Sensitivity analysis was
generally weak, and less than
40% of articles described any
sensitivity analysis, until 2018
when both journals improved tremendously in this category.

Authors using a flow
diagram to depict the level of
participation at each stage of
the study were given credit for
item 13c of the results section.
If a table rather than a flow chart
was provided, credit was given.
Articles generally scored poorly in this category, although JCP showed great
improvement after 2006.

0%
20%
40%
60%
80%
100%
2000 2006 2012 2018
Average Compliance to
STROBE
Item 12e: Statistical Methods
Journal of
Periodontology
Journal of Clinical
Periodontology
0%
20%
40%
60%
80%
100%
2000 2006 2012 2018
Average Compliance to
STROBE
Item 13c: Results
Journal of
Periodontology
Journal of Clinical
Periodontology
Figure 6: Statistical Methods Item 12e
Figure 7: Results

25

The number of participants
with missing data for each
variable of interest (Item 14b)
was generally poorly reported
with some improvement shown
after the year of 2006.
Participant drop out leading to
missing data is a common cause
of bias in observational studies,
should be explicitly addressed.

0%
20%
40%
60%
80%
100%
2000 2006 2012 2018
Average Compliance to
STROBE
Item 14b: Missing Data
Journal of
Periodontology
Journal of Clinical
Periodontology
Figure 8: Missing Data

26

Endorsement of STROBE Criteria

Publications citing the STROBE criteria in 2012 and 2018 were noted so that a
separate analysis could be completed which compared these publications to their
counterparts that did not explicitly endorse STROBE. Table 7 shows the articles that
explicitly mentioned the STROBE criteria:
Studies which formally recognized the STROBE guidelines tended to have
significantly higher ratings based on our scoring system. The average adherence of the
five articles listed in Table 7 to the STROBE criteria was 83.5%, which was greater than
the average compliance of all compared groups (other than JCP 2012, which had an
average of 88%). It is worth noting that the Journal of Clinical Periodontology has listed
adherence to the STROBE criteria as a requirement for all observational studies under
their “Research Reporting Guidelines,” although it is unclear when the journal published
these requirements.
Chapter 4: Discussion

Many articles have suggested that there is a need for increased adherence to the
STROBE statement within periodontology journals such as the Journal of
Periodontology and the Journal of Clinical Periodontology (Bushehri, 2015; Costandi,
2015), as well as within other medical subspecialties (Rao et al., 2016; Swords et al.,
2019).
This study analyzed the reporting of cohort studies published in the Journal of
Periodontology and the Journal of Clinical Periodontology in 2000, 2006, 2012, and
2018. The quality of reporting was quantified using 34 items from the STROBE

27

checklist and then calculating the percentage of adherence of each article. The results
were compared between the journals, across time, and among the checklist items
suggesting some areas of reporting are improving in the periodontal literature, and
some areas still need improvement.

Reporting Quality in Periodontal Literature

Randomized controlled clinical trials have classically been viewed as the “gold
standard” of primary evidence, and many publications in periodontology have reviewed
the reporting quality of these studies (Cairo et al., 2012; Kumar et al., 2018b; Lieber et
al., 2020; Wu et al., 2020). RCTs are in no way immune to investigative bias. A recent
cross-sectional analysis published in the Journal of Clinical Periodontology evaluated
196 articles in periodontology and oral implantology, and showed that of these articles,
69.9% of these articles had a “pre-determined spin strategy.” (Wu et al., 2020).
Secondary research such as systematic reviews must also be carefully evaluated due to
the heterogeneity of the studies within the reviews, which can lead to weaknesses of
data combination and statistical analysis. Based on recent data collected at the
University of Southern California, systematic reviews from periodontology and implant
dentistry have consistently not met all criteria from the Assessment of Multiple
Systematic Reviews (AMSTAR) and Glenny et al. checklists (Alsharah, 2020). A lack of
transparency in reporting has been noted not only in systematic reviews and
interventional studies, but also recently in observational studies (Bushehri, 2015;
Costandi, 2015). The STROBE guidelines were published to systematically improve the
quality of observational research.

28

The temporal improvement of reporting quality in observational research in
periodontology has been examined in the literature. In 2012, a consensus report was
published in the Journal of Clinical Periodontology examining the quality of reporting in
implant dentistry for both observational and experimental studies. A group of clinicians
(group 2) at the 8th European Workshop on Periodontology assessed four systematic
reviews, and two of these publications evaluated reporting quality of observational
research in periodontology(Meijer and Raghoebar, 2012; Rocchietta and Nisand, 2012).
These two articles included (1) a long term systematic review by Meijer and Raghobar,
which used the STROBE statement to examine all types of observational studies
published from 1990-2010 and (2) a report by Rocchietta and Nisland which evaluated
reporting quality of implant risk factor research in periodontology from 2007-
2011(Tonetti and Palmer, 2012). In the first review, the authors reported an
improvement in adherence of descriptive studies such as case series to the STROBE
criteria from 46% in 1990 to 70% in 2010 (Meijer and Raghoebar, 2012). This review
does not include any cohort articles, and the time periods addressed fall mainly before
the publication of STROBE in 2007.
The second article by Rocchietta and Nisland evaluated reporting quality of
implant risk factor research in periodontology from 2007-2011, and the authors
concluded that 97% of the articles found by hand sifting through PubMed were case
series studies, many of which were incorrectly labeled. The authors based their
analysis on the only three cohort articles that were found to meet their search criteria,
and these three articles were found to have many weaknesses, including inappropriate
and inconsistent measurements of exposure (Tonetti and Palmer, 2012). It is important

29

to note the significant differences in study design, sample size, and goals compared to
our study. Our study evaluates 56 cohort articles from four different years in two
periodontology journals, and we used a different scoring calculation system. While our
methods are too heterogenous to allow for comparison, these articles highlight many of
the same shortcomings in observational studies that we found, such as lack of bias
minimization, improper statistical management of confounding variables, inadequate
sample size calculations, and inappropriate management/reporting of subjects lost to
follow up.
Two recent cross sectional surveys at the University of Southern California
analyzed the quality of observational reporting in periodontology and implant dentistry in
the years 2013 (Costandi, 2015) and 2014(Bushehri, 2015). The first study (Costandi,
2015) evaluated 59 analytical studies published in JOP from 2013. Costandi et al. used
a similar dichotomous scoring system, but did not separate the subcategories, so the
score calculation was based on 22 items rather than 34. The second study, (Bushehri,
2015) evaluated 51 analytical articles published in 2014 JCP, using a modified checklist
based on 34 items with explanations of each criteria based on Vandenbroucke et al.’s
elaboration document (Vandenbroucke et al., 2014). This checklist and scoring method
was adapted for our study with additional explanations from Vandenbroucke et al. when
appropriate. Both articles reviewed cohort, cross-sectional, and case-control studies
from a single year in a single journal, whereas our study analyzed cohorts from two
journals at four time points. Nevertheless, some data comparisons can be made. For
example, our average yearly percentage compliance of cohort articles ranged from 61%
(JCP 2000) to 87% (JCP 2012), so the mean adherence of JCP 2014 cohort articles to

30

STROBE calculated at 74% by Bushehri et al. was not surprising. These reviews
suggested good reporting of introduction/background, data sources and measurements,
outcome data, category boundaries, and key results interpretations, which was also
consistent with our findings. Interestingly, Costandi et al. reported poor scores in JOP
2013 for item 22 (disclosure of source of funding) whereas Bushehri et al. reported good
scores in JCP 2014 for item 22. Upon closer examination, this may be due a slight
difference in interpretation of item 22 between these two authors. Costandi et al. stated
that no credit was given for this item if the authors did not explicitly describe the “role of
funders for the present study.” Alternatively, Bushehri et al. did not discuss her
interpretation of this checklist item, and it is possible more leniency was granted to
authors who disclosed funding information without a clear indication of the exact nature
and role of the funding. For our analysis, leniency was provided in this category if
authors made some effort to disclose funding information, so it could be argued that the
upward trend in this category may be different if the articles were graded based on the
interpretation of Costandi et al. The differences in the findings of Costandi et al. and
Bushehri et al. may also be in part due to the changes in adherence between the years
2013 (evaluated by Costandi et al.) and 2014 (evaluated by Bushehri et al.). This is
also consistent with our findings, as JCP began requiring adherence to the STROBE
criteria and showed a far greater improvement in concrete checklist items such as study
design labelling and funding disclosure. Both Bushehri et al. and Costandi et al.
performed a hand search of the literature and found 15 (JCP, 2014), and 11 (JOP,
2013) cohort articles. These numbers are consistent with the trend in number of cohort
articles found in our study to be published per journal per year (figure 2), which ranged

31

from 9-12 cohorts. Cohort studies are often costly and time-consuming (Grimes and
Schulz, 2002), so it is expected that publication of this study design is relatively
uncommon.

Cohort Classification

In general, a cohort is the strongest research design available for the evaluation
of risk factors, which may be of particular interest in periodontology due to the
multifactorial association between periodontal disease and systemic illnesses. In fact,
99% of associations between systemic conditions and periodontitis have been studied
using observational studies only, with many authors questioning the validity of these
associations (Mark Bartold and Mariotti, 2017). The authors of this review, however, fail
to differentiate between different types of observational studies, which may lead to an
overly critical view of the legitimacy of research demonstrating associations between
periodontitis and systemic conditions. A cohort study design is considered to have the
highest level of scientific rigor, followed by a cross-sectional, case-control, and case
series study design. It is true, however that most observational studies published in
periodontics and implant dentistry have case series designs which are weak study
designs for testing a hypotheses. In a study evaluating reporting quality of implant risk
factor research in periodontology from 2007-2011, the authors concluded that 97% of
the articles found by hand sifting through PubMed were case series studies, many of
which were incorrectly labeled (Rocchietta and Nisand, 2012).

32

Errors in the cataloging of study designs in the PubMed database are not unique
to periodontology journals, and have been previously reported for observational studies
(Bushehri, 2015; Costandi, 2015; Rocchietta and Nisand, 2012), as well as systematic
reviews and meta-analysis (Alsharah, 2020; Wilczynski and Haynes, 2009). Based on
an article published in 2014, 72% of articles labeled as “case series” in leading
neurosurgery journals from 2008-2012 were labeled incorrectly, and more than half of
the cohort articles were mislabeled as “case series” articles (Esene et al., 2014). Many
authors in JCP and JOP chose to avoid the decision by labeling the article “cohort or
case-control” or “cohort or case series” rather than choosing a single category. In fact,
it was reported that only three cohort studies have been published in periodontology
journals from the years of 2007-2011 addressing the risk factors of diabetes, smoking,
and periodontitis (Rocchietta and Nisand, 2012). According to these authors, 101 out of
104 papers about risk factors in periodontitis retrieved from a PubMed search were
hand sorted and classified as case series or cross-sectional studies. This contrasts
with the finding of other publications, including Bushehri et al, who determined that 14
cohort articles and 25 cross-sectional study designs were published in Journal of
Periodontology and Journal of Clinical Periodontology in the year 2014 alone (Bushehri,
2015). These contrasting trends may be in part due to the ineffectiveness of hand-
categorizing articles, and the lack of consensus in epidemiology regarding the definition
of cohort articles. This problem may be circumvented if authors were required to
categorize their study design and document the definition(s) used to create this label.

33

Mislabeling of observational studies within databases may be in part due to the
heterogeneity cohort study definitions between different publications, journals, and
textbooks. According to a publication Dekkers et al. (Dekkers et al., 2012), one of the
main distinguishing factor is that in a true cohort study, an absolute risk estimation can
be calculated (subjects with outcome/total subjects exposed). This is because case
series articles choose samples of the population based on previous outcomes, whereas
cohort studies choose samples for the article based on previous exposures. The
distinction between an outcome and an exposure is critical to conceptualize with this
definition. For example, a case series may include patients with a specific consequence
to a treatment, whereas a cohort study has one or more groups with a specific exposure
or treatment and examined this population over a specific period of time (Mathes and
Pieper). This definition leads to a major controversy regarding the number of subject
groups required for an article to be classified as a “cohort”. According to some authors
including Dekkers et al., various textbooks in epidemiology (Rothman et al.), and the
STROBE guidelines (Vandenbroucke et al., 2014; von Elm et al., 2007), a study with a
single cohort can be classified as a cohort study as long as the group of exposed
patients are examined from a defined start time, and followed over a clearly defined
timeline. It must be noted that this differs from many journals and publications,
including (Bryant et al., 2009; Ergina et al., 2009; Kooistra et al., 2009; Song and
Chung), who maintain that at least two groups must be present so that one group may
serve as an external control. It should be noted however, that if a study has only one
cohort, the group within the cohort that does not experience the outcome measured can
serve as the “internal control.” (Mann, 2003)

34

Consistency in the definition and labeling of cohort articles is an important factor
in maintaining a transparent hierarchy of evidence. Because cohort studies are
considered the highest form of evidence within the category of observational studies,
frequent mislabeling a case series as a cohort article within a database makes it more
time consuming and tedious for readers to locate articles such as cohorts, which often
have a higher epidemiological significance. According to our results, authors of cohort
articles both JOP and JCP have greatly improved the score of item 1a “Title and
Abstract,” which involves correctly indicating the study design.

Despite this improvement in
adherence of cohort articles to item
1a of the STROBE checklist, cohort
articles remain difficult to locate
through a PubMed search, and
require hand selection. For the purposes of this paper, a significant amount of time
was spent hand-sifting through abstracts to find cohort studies, for all years, including
2012, and 2018. This is in part due to the low quantity of cohort articles being published
relative to the high number of case series studies (Meijer and Raghoebar, 2012;
Rocchietta and Nisand, 2012). Mainly, however, this appears to be due to a high
quantity case series articles being mislabeled as cohort articles. Even if the reporting
quality of cohort articles is improving every year, if most articles published are case
series studies, many of which may be incorrectly labeled as cohorts, would a time-
pressed clinician spend the time to sort through the “noise” to locate cohorts?
0%
20%
40%
60%
80%
100%
2000
2006
2012
2018
Average Compliance to
STROBE
Item 1a: Title and Abstract
Journal of
Periodontology
Journal of
Clinical
Periodontology
Figure 9: Title and Abstract

35

By not requiring the correct categorization of observational studies as “cohort,”
“case-control,” “cross-sectional,” or “case series,” dental journals are making it difficult
for users to reap the benefits of the improvements in reporting quality and increased
adherence to the STROBE criteria. It is no surprise that cohort articles have been
shown to demonstrate the greatest adherence to the STROBE criteria compared to
other types of observational study literature (Bushehri, 2015; Costandi, 2015), but if a
PubMed search for cohort articles yields 471 articles, and only 85 of these articles are
truly cohort by design, will a typical reader will have time to hand sift through each
article looking for a cohort study design? If journal editors and authors do not correctly
differentiate between cohorts and case series designs, it is probably unreasonable to
expect this of the average consumer. Future studies are needed to better understand
the trends in the mislabeling of observational studies and how this is impacting
consumption of the periodontal literature among clinicians.

36

Title and Abstract

In a time when information is overabundant, an ineffective search engine or
system of categorization will inhibit the consumption of quality information. The
STROBE criteria was designed to increase reporting quality and transparency of
reporting, and based on current literature and the data produced by this trend analysis,
the quality of reporting of cohorts is improving over time. An argument could be made
that the first item in the STROBE criteria (Item 1a Title and Abstract), is the most
important, because if the study design is not indicated with “a commonly used term in
the title or abstract,” search engines may produce inconsistent results. Unless high
quality reporting becomes more identifiable and accessible, with current search
engines, an improvement of reporting quality produced may not translate to an
improvement of reporting quality consumed. JCP increased in rating for this section by
100% from 2000 to 2018, which may be due in part to the requirement of adherence to
the STROBE criteria for observational studies. All periodontology and implantology
journals may consider following suit and officially endorsing the applicable research
reporting guidelines found on the EQUATOR network. While it may not be realistic to
completely ensure that all studies to adhere 100% to all checklist items, accurate
indication of the study’s design in the title or abstract should be a stringent requirement
with no exceptions.

37

Study Limitations

This study was designed to methodically assess the reporting quality of cohort
articles over time in two high impact periodontology journals. It should be noted,
however, that the authors of the STROBE criteria stated explicitly that the use of the
checklist as a tool to assess the reporting quality of research is “inappropriate (da Costa
et al., 2011).” While the STROBE criteria was not originally created as an assessment
tool to rate previously published literature, it is now widely used for this purpose in
medical and dental literature (Bastuji-Garin et al., 2013; Bushehri, 2015; Rao et al.,
2016). It is important to remember that the goal of this paper is not to criticize the
methods or results of previously published research. Some articles may have lost
points from criteria which was met but not clearly reported, and human error in grading
is always a possibility. The quality of reporting is subjective by nature and the STROBE
criteria was adapted to minimize subjectivity, bias, and error in article ratings. To further
attempt to minimize human error, intra-examiner, and inter-examiner calibration was
performed by a primary and secondary reviewer, with input from a third reviewer in case
of any disagreements or confusion.
This study was designed to identify trends, but does not offer significant insight
as to what factors are responsible for affecting changes in the trend. Therefore, it
cannot be concluded whether the average increased adherence to the STROBE
guidelines over time is due to the publication of the STROBE guidelines, or due to a
progressively positive trend in reporting over time. Additionally, a larger pool of articles
would allow for more sophisticated statistical analyses. Further studies evaluating

38

adherence to the STROBE guidelines over a longer period with a larger pool of articles
are needed.
Chapter 5: Conclusion

Randomized controlled trials continue to be viewed as the “highest” form of
evidence, however, observational studies allow for research in some areas that cannot
be observed with RCTs. While cohort studies are generally accepted to be the highest
form of observational study design, the number of cohort studies being published in the
Journal of Periodontology and the Journal of Clinical Periodontology remains low, and
the reporting quality is still imperfect.
While this study has limitations, the checklist items which need improvement
based on our findings have also been highlighted in comparable reviews in
periodontology and implant dentistry. Most notable shortcomings include attempts to
address bias, explanation of sample size calculations, reports of participation and follow
up, and reports indicating the number of participants with missing data.
While there is an overall positive trend in reporting quality of cohort studies, it is
imperative that authors continue to improve the quality of reporting, following widely
accepted criteria such as the STROBE criteria. The Journal of Clinical Periodontology
does state that STROBE is a requirement prior to publishing an article, however editors
and peer-reviewers may not be taking the time to review the article’s adherence to
every section of the STROBE statement, as this could be a time-consuming process.
JCP’s endorsement of the STROBE criteria may have contributed to the greater
adherence compared to JOP, but there are still greater measures that should be taken

39

to increase adherence. Many scientific journals now require authors to submit a
designated form which describes how each section of the reporting guidelines are met
prior to accepting a manuscript, such as Clinical Oral Implants Research. While this is
likely not a foolproof method, it may be an effective way to reinforce adherence
practically and efficiently, making the authors accountable during the submission
process. It is recommended that editors and publishers of journals in periodontology
improve the quality of reporting of scientific articles published, by improving the
screening process in a way that increases adherence to the respective reporting
guidelines in the EQUATOR network.

40

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49

Tables and Figures
Table 1: Eligible studies included in analysis
Number

Article Title Author Publication Journal
1 Actinobacillus
actinomycetemcomitans
in Destructive
Periodontal Disease.
Three-Year Follow-Up
Results
Rainer
Buchmann,
Rüdiger F.
Müller, Achim
Heinecke,
Dieter E.
Lange
2000 Journal of
Periodontology
2 Herpesviruses and
Periodontopathic
Bacteria in Trisomy 21
Periodontitis
Delaram
Hanookai,
Hessam
Nowzari,
Adolfo
Contreras,
John L.
Morrison,
Jørgen Slots
2000 Journal of
Periodontology
3 Outcome Variables in
Periodontal Research:
Means and Threshold-
Based Site Changes
Eli E. Machtei,
Millicent
Schmidt,
Ernest
Hausmann,
Sara Grossi,
Robert
Dunford,
Glenn Davies,
Julie
Chandler,
Robert J.
Genco
2000 Journal of
Periodontology
4 2-Year Observation of
Attachment Loss in a
Rural Chinese
Population
Reiko Suda,
Caifang Cao,
Kohji
Hasegawa,
Shi Yang,
Ryuji Sasa,
Motoyuki
Suzuki
2000 Journal of
Periodontology

50

5 A 10-Year Prospective
Study of Tobacco
Smoking and
Periodontal Health
Jan
Bergström,
Sören
Eliasson, Jan
Dock
2000 Journal of
Periodontology
6 Non-Surgical
Periodontal Therapy
and Tooth Loss. A
Cohort Study
P.P. Hujoel,
B.G. Leroux,
H. Selipsky,
B.A. White
2000 Journal of
Periodontology
7 Immediate Versus Non-
Immediate Implantation
for Full-Arch Fixed
Reconstruction
Following Extraction of
All Residual Teeth: A
Retrospective
Comparative Study
Devorah
Schwartz-
Arad, Nathan
Gulayev, and
Gavriel
Chaushu
2000 Journal of
Periodontology
8 Periodontal Disease
Status During
Pregnancy and 3
Months Post-Partum, In
a Rural Population of
Sri-Lankan Women
Tilakaratne A,
Soory M,
Ranasinghe
AW, Corea
SMX,
Ekanayake
SL, De Silva
2000 Journal of
Clinical
Periodontology
9 Radiographic
periodontal attachment
loss as an indicator of
death risk in the elderly
K. Soikkonen,
J. Wolf, T.
Salo, R. Tilvis
2000 Journal of
Clinical
Periodontology
10 Initial extractions and
tooth loss during
supportive care in a
periodontal population
seeking comprehensive
care
Maurizio S.
Tonetti,
Patricia
Steffen,
Veronique
Muller-
Campanile,
Jean Suvan,
Niklaus P.
Lang
2000 Journal of
Clinical
Periodontology
11 Disease progression in
periodontally treated
and untreated patients
– a retrospective study
Thomas
Kocher,
Jörgen König,
Uwe Dzierzon,
Hassem
Sawaf, Hans-
Christian
Plagmann
2000 Journal of
Clinical
Periodontology

51

12 The association of
cigarette smoking with
alveolar bone loss in
postmenopausal
females
Jeffrey B.
Payne,
Richard A.
Reinhardt,
Pirkka V.
Nummikoski,
David G.
Dunning,
Kashinath D.
Patil
2000 Journal of
Clinical
Periodontology
13 A retrospective
radiographic outcome
assessment study of
intra-bony defects
treated by osseous
surgery or by bone graft
procedures
G. Rutger
Persson,
Hanne Falk,
Lars Laurell
2000 Journal of
Clinical
Periodontology
14 A controlled study of
relative periodontal
attachment loss in
people with HIV
infection
P.G.
Robinson, A.
Boulter, W.
Birnbaum,
N.W. Johnson
2000 Journal of
Clinical
Periodontology
15 Statin Use and Tooth
Loss in Chronic
Periodontitis Patients
J. Cunha-
Cruz, B.
Saver, G.
Maupome,
P.P. Hujoel
2006 Journal of
Periodontology
16 Gingival Recession
Treatment With
Connective Tissue
Grafts in Smokers and
Non-Smokers
Kenneth J.
Erley, Gary D.
Swiec, Robert
Herold,
Frederick C.
Bisch, Mark E.
Peacock
2006 Journal of
Periodontology
17 Compliance as a
Prognostic Indicator:
Retrospective Study of
505 Patients Treated
and Maintained for 15
Years
Takanari
Miyamoto,
Takashi
Kumagai,
Judith A.
Jones,
Thomas E.
Van Dyke,
Martha E.
Nunn
2006 Journal of
Periodontology
18 The Influence of
Current and Former
Yoshihiro
Shimazaki,
2006 Journal of
Periodontology

52

Smoking on Gingival
Bleeding: The
Hisayama Study
Toshiyuki
Saito, Yutaka
Kiyohara, Isao
Kato, Michiaki
Kubo, Mitsuo
Iida, Yoshihisa
Yamashita
19 Salivary Histamine
Level as a Predictor of
Periodontal Disease in
Type 2 Diabetic and
Non-Diabetic Subjects
Mario Venza,
Maria Visalli,
Maria
Cucinotta,
Domenico
Cicciu`, Pietro
Passi, Diana
Teti
2006 Journal of
Periodontology
20 Periodontitis and
Plasma C-Reactive
Protein During
Pregnancy
Waranuch
Pitiphat,
Kaumudi J.
Joshipura,
Janet W. Rich-
Edwards,
Paige L.
Williams,
Chester W.
Douglass,
Matthew W.
Gillman
2006 Journal of
Periodontology
21 Changes in Periodontal
Disease Experience
From 26 to 32 Years of
Age in a Birth Cohort
W. Murray
Thomson,
Jonathan M.
Broadbent,
Richie
Poulton,
James D.
Beck
2006 Journal of
Periodontology
22 Effects of smoking and
gingival inflammation on
salivary antioxidant
capacity
Nurcan
Buduneli,
Levent
Kardesler,
Hasan Isik, C.
Steadman
Willis Ill,
Samuel I.
Hawkins,
Denis F.
2006 Journal of
Clinical
Periodontology

53

Kinane, David
A. Scott
23 Dental restorations: a
risk factor for
periodontal attachment
loss?
Jonathan M.
Broadbent,
Karen B.
Williams, W.
Murray
Thomson,
Sheila M.
Williams
2006 Journal of
Clinical
Periodontology
24 Nine- to fourteen-year
follow-up of implant
treatment. Part II:
presence of peri-implant
lesions

Roos-
Jansåker AM,
Lindahl C,
Renvert H,
Renvert S

2006 Journal of
Clinical
Periodontology
25 Investigation of
periodontal destruction
patterns in smokers and
non-smokers
Badiah
Baharin,
Richard M.
Palmer, Paula
Coward, Ron
F. Wilson
2006 Journal of
Clinical
Periodontology
26 Prognostic factors in the
treatment of
generalized aggressive
periodontitis: II. Effects
of smoking on initial
outcome
Francis J.
Hughes,
Mahnaz Syed,
Bindhu Koshy,
Nagihan
Bostanci, Ian
J. McKay,
Michael A.
Curtis,
Wagner
Marcenes,
Raymond E.
Croucher
2006 Journal of
Clinical
Periodontology
27 Fcγ receptor
polymorphisms and
periodontal status: a
prospective follow-up
study
D.L. Wolf,
A.M.
Neiderud, K.
Hinckley, G.
Dahlen, J.G.J.
van de Winkel,
P.N.
Papapanou
2006 Journal of
Clinical
Periodontology
28 Java project on
periodontal diseases.
The natural
U. Van der
Velden, F.
Abbas, S.
2006 Journal of
Clinical
Periodontology

54

development of
periodontitis: risk
factors, risk predictors
and risk determinants
Armand, B.G.
Loos, M.F.
Timmerman,
G.A. Van der
Weijden, A.J.
Van
Winkelhoff,
E.G. Winkel
29 Evaluation of
Periodontal Status and
Effectiveness of Non-
Surgical Treatment in
Patients With Type 2
Diabetes Mellitus in
Taiwan for a 1-Year
Period
Ling Auyeung,
Pei-Wen
Wang, Rue-
Tsuan Lin,
Ching-Jung
Hsieh, Pei-Yu
Lee, Rui-Yeh
Zhuang,
Hsueh-Wen
Chang
2012 Journal of
Periodontology
30 A 10-Year Evaluation of
Implants Placed in
Fresh Extraction
Sockets: A Prospective
Cohort Study
Ugo Covani,
Giacomo
Chiappe,
Mario Bosco,
Bruno
Orlando,
Alessandro
Quaranta, and
Antonio
Barone
2012 Journal of
Periodontology
31 Influence of Obesity
and Bariatric Surgery
on the Periodontal
Condition
Andre´ Luiz
Pataro,
Fernando
Oliveira Costa,
Sheila
Cavalca
Cortelli, Jose´
Roberto
Cortelli, Ana
Carolina
Dupim Souza,
Mauro
Henrique
Nogueira
Guimaraes
Abreu,
Marcelo
Gomes
2012 Journal of
Periodontology

55

Girundi, Jose´
Eusta´quio
Costa
32 Periodontal Risk
Assessment Model in a
Sample of Regular and
Irregular Compliers
Under Maintenance
Therapy: A 3-Year
Prospective Study
Fernando
Oliveira Costa,
Luı´s Ota´vio
Miranda Cota,
Eugenio Jose´
Pereira Lages,
Ana Paula
Lima Oliveira,
Sheila
Cavalca
Cortelli, Jose´
Roberto
Cortelli, Telma
Campos
Medeiros
Lorentz, Jose´
Eustaquio
Costa
2012 Journal of
Periodontology
33 Increased Risks of
Preterm Birth and a
Low-Birth-Weight Baby
in Thai Human
Immunodeficiency
Virus-Positive Pregnant
Women with
Periodontitis
Pakkaporn
Pattrapornnan,
Timothy A.
DeRouen,
Yupin
Songpaisan
2012 Journal of
Periodontology
34 Mucositis, Peri-
Implantitis, Implant
Success, and Survival
of Implants in Patients
with Treated
Generalized Aggressive
Periodontitis: 3- to 16-
Year Results of a
Prospective Long-Term
Cohort Study
Katrin
Swierkot, Peer
Lottholz, Lavin
Flores-de-
Jacoby,
Reiner Mengel
2012 Journal of
Periodontology
35 A Retrospective
Analysis of Implants
Immediately Placed in
Sites with and Without
Periapical Pathology in
Sixty-Four Patients
Paul A.
Fugazzotto
2012 Journal of
Periodontology

56

36 Benefits of early
systemic antibiotics in
localized aggressive
periodontitis: a
retrospective study
Dennis
Beliveau,
Ingvar
Magnusson,
John A.
Bidwell,
Edward F.
Zapert,
Ikramuddin
Aukhil,
Shannon
M.Wallet,
Luciana M.
Shaddox
2012 Journal of
Clinical
Periodontology
37 Gingival changes during
pregnancy: III. Impact of
clinical, microbiological,
immunological and
socio-demographic
factors on gingival
inflammation
Ana Carrillo-
de-Albornoz,
Elena Figuero,
David Herrera,
Pedro Cuesta,
Antonio
Bascones-
Martinez
2012 Journal of
Clinical
Periodontology
38 Peri-implant disease in
subjects with and
without preventive
maintenance: a 5-year
follow-up
Fernando
Oliveira Costa,
Satoshi
Takenaka-
Martinez, Luis
Otavio
Miranda Cota,
Sergio Diniz
Ferreira,
Geraldo Lucio
Magalhaes
Silva, Jose
Eustaquio
Costa
2012 Journal of
Clinical
Periodontology
39 Association between
obesity and periodontal
disease in young
adults: a population-
based birth cohort
Eduardo
Dickie de
Castilhos,
Bernardo
Lessa Horta,
Denise
Petrucci
Gigante,
Flavio
Fernando
2012 Journal of
Clinical
Periodontology

57

Demarco,
Karen Glazer
Peres, Marco
Aurelio Peres
40 A comparison of
periodontal status in the
two regional,
population-based
studies of SHIP and
INVEST
Birte
Holtfreter,
Ryan T.
Demmer, Olaf
Bernhardt,
Panos N.
Papapanou,
Christian
Schwahn,
Thomas
Kocher, Moise
Desvarieux
2012 Journal of
Clinical
Periodontology
41 Chronic periodontitis
and the subsequent risk
of trigeminal neuralgia:
a 5-year follow-up study
Joseph J.
Keller, Jau-
Jiuan Sheu,
Herng-Ching
Lin
2012 Journal of
Clinical
Periodontology
42 All-cause mortality and
periodontitis in 60—70-
year-old men: a
prospective cohort
study
Gerard J.
Linden, Katie
Linden, John
Yarnell, Alun
Evans, Frank
Kee, Chris C.
Patterson
2012 Journal of
Clinical
Periodontology
43 Prospective study of the
impact of peri-implant
soft tissue properties on
patient-reported and
clinically assessed
outcomes
Francesca
Bonino, Bjorn
Steffensen,
Zuhair Natto,
Yong Hur,
Lucrezia
Paternò
Holtzman,
Hans-Peter
Weber
2018 Journal of
Periodontology
44 Metabolic syndrome
and periodontitis: A
structural equation
modeling approach
Gustavo G.
Nascimento,
Fábio R. M.
Leite, Karen
G. Peres,
Flávio F.
Demarco,
Marcos B.
2018 Journal of
Periodontology

58

Corrêa, Marco
A. Peres
45 Periodontal profile
classes predict
periodontal disease
progression and tooth
loss
Thiago Morelli,
Kevin L. Moss,
John S.
Preisser,
James D.
Beck, Kimon
Divaris, Di Wu,
Steven
Offenbacher
2018 Journal of
Periodontology
46 Peri-implant soft tissue
status and crestal bone
levels around adjacent
implants placed in
cigarette smokers and
never smokers: Five-
year follow-up results
Aws S.
ArRejaie,
Khulud
Abdulrahman
Al-Aali,
Mohammed
Alrabiah,
Sameer A.
Mokeem,
Fahim Vohra,
Tariq
Abduljabbar
2018 Journal of
Periodontology
47 Effect of compliance
during periodontal
maintenance therapy
on levels of bacteria
associated with
periodontitis: A 6-year
prospective study
Fernando
Oliveira Costa,
Thaís Riberal
Vieira, Sheila
Cavalca
Cortelli, Luís
Otávio
Miranda Cota,
José
Eustáquio
Costa, Maria
Cássia
Ferreira
Aguiar, José
Roberto
Cortelli
2018 Journal of
Periodontology
48 Periodontal
reconstructive surgery
of deep intraosseous
defects using an apical
approach. Non-incised
papillae surgical
approach (NIPSA): A
Jose A.
Moreno
Rodríguez,
Antonio J.
Ortiz Ruiz,
Raúl G.
Caffesse
2018 Journal of
Periodontology

59

retrospective cohort
study
49 Smoking Confounds the
Periodontal Diagnostics
Using Saliva
Biomarkers

Laura
Lahdentausta,
Susanna Paju,
Paivi Mantyla
et al.
2018 Journal of
Periodontology
50 Longitudinal evaluation
of periodontitis and
development of
cognitive decline among
older adults
Helena
Nilsson, Johan
Sanmartin
Berglund,
Stefan
Renvert
2018 Journal of
Clinical
Periodontology
51 Clinical and
microbiological effects
of scaling and root
planing, metronidazole
and amoxicillin in the
treatment of diabetic
and non-diabetic
subjects with
periodontitis: A cohort
study
Poliana
Mendes
Duarte, Magda
Feres, Lina
Lameh Smeili
Yassine,
Geisla Mary
Silva Soares,
Tamires
Szeremeske
Miranda,
Marcelo
Faveri, Belen
Retamal-
Valdes,
Luciene
Cristina
Figueiredo
2018 Journal of
Clinical
Periodontology
52 Proximal restoration
increases the risk of
clinical attachment loss
Kauê Collares,
Flávio F.
Demarco,
Bernardo L.
Horta, Marcos
B. Correa
2018 Journal of
Clinical
Periodontology
53 Relationship of
toothbrushing to
metabolic syndrome in
middle-aged adults
Akihiko
Tanaka, Kenji
Takeuchi,
Michiko
Furuta, Toru
Takeshita,
Shino Suma,
Takashi
Shinagawa,
2018 Journal of
Clinical
Periodontology

60

Yoshihiro
Shimazaki,
Yoshihisa
Yamashita
54 Evaluating periodontal
disease
misclassification
mechanisms under
partial mouth recording
protocols
Brenda
Heaton,
Praveen
Sharma, Raul
I. Garcia,
Thomas
Dietrich
2018 Journal of
Clinical
Periodontology
55 Site-level risk predictors
of peri-implantitis: A
retrospective analysis
Purnima S.
Kumar,
Shareef M.
Dabdoub,
Rachna
Hegde,
Nanditha
Ranganathan,
Angelo
Mariotti
2018 Journal of
Clinical
Periodontology
56 Saliva and serum
biomarkers in
periodontitis and
coronary
artery disease
Lahdentausta
LSJ, Paju S,
Mäntylä P,
et al.
2018 Journal of
Clinical
Periodontology

61

Table 2: Original Unmodified STROBE 2007 Statement – checklist of items that should be addressed in
reports of observational studies
Section/Topic Item
No
Recommendation
Title and Abstract
Title and Abstract #1 (a) Indicate the study’s design with a commonly used
term in the title or the abstract

(b) Provide in the abstract an informative and balanced
summary of what was done and what was found
Introduction
Background/ratio
nale
#2 Explain the scientific background and rationale for the
investigation being reported
Objectives #3 State specific objectives, including any pre-specified
hypotheses

Methods
Study Design #4 Present key elements of study design early in the
paper
Setting #5 Describe the setting, locations, and relevant dates,
including periods of recruitment, exposure, follow-up,
and data collection
Participants #6* (a) Cohort study—Give the eligibility criteria, and the
sources and methods of selection of participants.
Describe methods of follow-up

(b) Cohort study—For matched studies, give matching
criteria and number of exposed and unexposed
Variables #7 Clearly define all outcomes, exposures, predictors,
potential confounders, and effect modifiers. Give
diagnostic criteria, if applicable
Data sources/
measurements
#8* For each variable of interest, give sources of data and
details of methods of
assessment (measurement). Describe comparability of
assessment methods if there is more than one group
Bias #9 Describe any efforts to address potential sources of
bias
Study size #10 Explain how the study size was arrived at
Quantitative
Variables
#11 Explain how quantitative variables were handled in the
analyses. If applicable,
describe which groupings were chosen and why
Statistical
methods
#12
*
(a) Describe all statistical methods, including those
used to control for confounding

(b) Describe any methods used to examine subgroups
and interactions

(c) Explain how missing data were addressed

62

(d) Cohort study—If applicable, explain how loss to
follow-up was addressed

(e) Describe any sensitivity analyses

Results
Participants #13 (a) Report the numbers of individuals at each stage of
study—e.g., numbers potentially eligible,
examined for eligibility, confirmed eligible, included in
the study, completing follow-up, and
analyzed

(b) Give reasons for non-participation at each stage

(c) Consider use of a flow diagram
Descriptive Data #14
*
(a) Give characteristics of study participants (e.g.,
demographic, clinical, social) and information
on exposures and potential confounders
(b) Indicate number of participants with missing data
for each variable of interest
(c) Cohort study—Summaries follow-up time (eg,
average and total amount)
Outcome Data #15
*
Cohort study—Report numbers of outcome events or
summary measures over time
Main Results #16 (a) Give unadjusted estimates and, if applicable,
confounder-adjusted estimates and their
precision (eg, 95% confidence interval). Make clear
which confounders were adjusted for and
why they were included.
(b) Report category boundaries when continuous
variables were categorized
(c) If relevant, consider translating estimates of relative
risk into absolute risk for a meaningful time period
Other Analyses #17 Report other analyses done—e.g., analyses of
subgroups and interactions, and sensitivity

Discussion
Key Results #18 summarize key results with reference to study
objectives
Limitations #19 Discuss limitations of the study, taking into account
sources of potential bias or imprecision. Discuss both
direction and magnitude of any potential bias
Interpretation #20 Give a cautious overall interpretation of results
considering objectives, limitations, multiplicity of
analyses, results from similar studies, and other
relevant evidence
Generalizability #21 Discuss the generalizability (external validity) of the
study results

Other Information

63

Funding #22 Give the source of funding and the role of the funders
for the present study and, if applicable for the original
study on which the present article is based

*Original checklist provides information for cohort, case-control, and cross-sectional
studies. This checklist has been modified to include only information for cohort studies.

64

Table 3: STROBE checklist with additional extension from Bushehri et al. and Vandenbroucke et al.
**note: checklists and extensions quoted directly from source

Section/Topic Ite
m
No
Recommendatio
n
Bushehri et al.
extension
Additional
Extension
Adapted from
Vandenbroucke
et al.
Title and
Abstract

Title and
Abstract
#1 (a) Indicate the
study’s design
with a commonly
used term in the
title or the
abstract
If the study design
was not specifically
stated, then
this item will be scored
= 0
• When incorrect
terms are used to
describe the study
design (i.e.,
retrospective/prospecti
ve), this was
recorded as not being
complete.
–NA–

(b) Provide in
the abstract an
informative and
balanced
summary of
what was done
and what was
found
–NA– Must include
descriptions of:
(1) what was
done (2) what
was found (3)
specific study
population(s) (4)
explanation of
measurement(s)
used (4)
description of
results.

Introduction

65

Background/
rationale
#2 Explain the
scientific
background and
rationale for the
investigation
being reported
–NA– Must include
descriptions of
(1) gaps in
literature to be
addressed by
this research (2)
description of
the research
topic (3) the
purpose of the
research.
Objectives #3 State specific
objectives,
including any
pre-specified
hypotheses
–NA– Objectives
stated in the
background
section must be
re-stated with an
explanation
included. The
explanation
must include
information
regarding
populations,
exposures,
limitations, and
parameters.
Any subgroup or
analysis added
after data
collection/planni
ng must be
identified and
clearly stated.

Methods
Study
Design
#4 Present key
elements of
study design
early in the
paper
• Presented early in
the materials and
methods section
or at the end of the
introduction.
• Ill defining terms
(“retrospective” or
“prospective) to
describe cohort
studies will be scored
= 0
• Correct terminology
–NA–

66

to define study design:
cohort;
cross-sectional; case-
control.
Setting #5 Describe the
setting,
locations, and
relevant dates,
including
periods of
recruitment,
exposure,
follow-up, and
data collection
• When the authors
did not report the
setting/location
but referred the reader
to a previously
published study
then the item scored =
1
• When the authors
did not report the
setting/location
and did not refer the
reader to a previously
published
study then the item
scored = 0
• When the
information is reported
in the article but not
necessarily in the
materials and methods
section, the
item is rated as
complete.
–NA–
Participants #6* (a) Cohort
study—Give the
eligibility criteria,
and the sources
and methods of
selection of
participants.
Describe
methods of
follow-up
–NA– This section
must separately
describe (1)
what was
planned and (2)
what was
carried out so
that departure
from the original
plan can be
evaluated. The
explanations
must allow for
evaluation of

67

control of bias
and confounding
variables.

(b) Cohort
study—For
matched
studies, give
matching criteria
and number of
exposed and
unexposed
–NA– Eligibility criteria
must be clearly
stated and
labeled. The
larger group
from which the
study population
was chosen
must also be
stated.
Variables #7 Clearly define all
outcomes,
exposures,
predictors,
potential
confounders,
and effect
modifiers. Give
diagnostic
criteria, if
applicable
Authors should clearly
declare all the
‘candidate
variables” in the
methods section and
not selectively report
the ones included in
the final analysis.
All confounders,
modifiers,
outcomes
predictors,
exposures, and
risk factors must
be defined.
Methods of
measurement
must be
described. An
explanation
should be
included of how
these factors
may affect the
outcome.
Data
sources/
measurements
#8* For each
variable of
interest, give
sources of data
and details of
methods of
assessment
(measurement).
Describe
comparability of
assessment
methods if there
–NA– The source of
data, and the
training of those
required for data
collection should
be described.

68

is more than one
group
Bias #9 Describe any
efforts to
address
potential
sources of bias
• Authors are recorded
as having made
attempts address
sources of bias if they
reported any tools to
do this; standard
deviation (SD) or
validated scoring
systems.
Articles that did
not include the
word “bias” were
screened for
different
verbiage
attempting to
address this.
Study size #10 Explain how the
study size was
arrived at
–NA– Calculations or
estimates of the
sample size
needed for a
sufficiently
narrow
confidence
interval must be
shown.
Imprecise
estimations are
acceptable if
calculation is
attempted.
Quantitative
Variables
#11 Explain how
quantitative
variables were
handled in the
analyses. If
applicable,
describe which
groupings were
chosen and why
Did the authors
explain how
quantitative variables
were handled in the
analyses?
• If applicable:
Did they describe
which groupings were
chosen for quantitative
variables?
Did they describe why
the quantitative
groups were chosen?
–NA–

69

Statistical
methods
#12
*
(a) Describe all
statistical
methods,
including those
used to control
for confounding
• Unless the authors
stated which
confounders they
controlled for and why,
this item was not
recorded as
complete.
–NA–

(b) Describe any
methods used to
examine
subgroups and
interactions
–NA– Subgroups from
the study may or
may not be
analyzed. If
analyzed, the
authors must
state which
subgroup
evaluations
were planned in
advanced.

(c) Explain how
missing data
were addressed
• Authors should
report the number of
missing values
for each variable of
interest and, if
possible, the
reason for missing
values.
–NA–

(d) Cohort
study—If
applicable,
explain how loss
to follow-up was
addressed
–NA– Any subjects
lost to follow up
must be
addressed,
including a
description of
the methods for
accounting for
this.

(e) Describe any
sensitivity
analyses
–NA–

Results
Participants #13 (a) Report the
numbers of
individuals at
each stage of
study—e.g.
numbers
–NA– The quantity of
participants
eligible for the
study, the
number at each
recruitment

70

potentially
eligible,examine
d for eligibility,
confirmed
eligible, included
in the study,
completing
follow-up,
andanalyzed
stage, the
number that
completed the
study, and the
number used in
data analysis
must be shown.

(b) Give reasons
for non-
participation at
each stage
–NA– Reasons for loss
of participants at
every step must
also be
included.

(c) Consider use
of a flow
diagram
–NA– A flow chart
showing the
quantity of
participants or
percentage of
remaining
participants at
each stage
should be
included.
Descriptive
Data
#14
*
(a) Give
characteristics
of study
participants (e.g.
demographic,
clinical, social)
and information
on exposures
and potential
confounders
• Authors should
summarize continuous
variables for
each group in the
study by giving mean
and standard
deviation.
• For asymmetrical
distribution, the
median and
percentile range
should be reported.
–NA–
(b) Indicate
number of
participants with
missing data for
each variable of
interest
–NA– An explanation
of how missing
data may have
affected the
influence of
variables must
be included.
(c) Cohort
study—
Summarize
–NA– The document
must include the
average and

71

follow-up time
(eg, average
and total
amount)
total follow up
time for all
populations.
Outcome
Data
#15
*
Cohort study—
Report numbers
of outcome
events or
summary
measures over
time
–NA– The
number/percent
age of
participants in
each outcome
category should
be clearly
reported.
Main
Results
#16 (a) Give
unadjusted
estimates and, if
applicable,
confounder-
adjusted
estimates and
their
precision (e.g.,
95% confidence
interval). Make
clear which
confounders
were adjusted
for and
why they were
included.
–NA– Potential
confounders
should be
shown and
accounted for
statistically,
including an
evaluation of
how this
confounder may
have affected
results.

(b) Report
category
boundaries
when
continuous
variables were
categorized
–NA– Must denote
how continuous
variables affect
the category
analysis. Data
range, mean,
and median of
all categories
must be
demonstrated.
If not all factors
are present,
score = 0.
(c) If relevant,
consider
translating
estimates of
• Only relevant when
there is convincing
evidence of causal
association.
If the author
presents
relative/absolute
risk but does not

72

relative risk into
absolute risk for
a meaningful
time period
convert this into
clinically
relevant terms,
score = 0.
Other
Analyses
#17 Report other
analyses done—
e.g. analyses of
subgroups and
interactions, and
sensitivity
–NA– Other analyses
may include
analysis of
subgroup
interactions.
This must be
presented and
interpreted with
great caution.
The author must
clearly state if
the analysis of
subgroups was
an a priori
objective.

Discussion
Key Results #18 Summarize key
results with
reference to
study objectives
–NA– The summary of
key findings
must be
presented with
caution and not
extrapolated to a
greater extent
than reasonable.
Limitations #19 Discuss
limitations of the
study,
considering
sources of
potential bias or
imprecision.
Discuss both
direction and
magnitude of
any potential
bias
–NA– Discussion of
limitations must
include a
summary of
potential factors
introducing bias,
and the impact
of these
potential biases.

73

Interpretatio
n
#20 Give a cautious
overall
interpretation of
results
considering
objectives,
limitations,
multiplicity of
analyses, results
from similar
studies, and
other relevant
evidence
–NA– Over
extrapolation
and over
interpretation,
must be
avoided.
Original
hypotheses and
objectives
should be
addressed, and
implications of
the study for
clinical use may
be cautiously
suggested. The
authors should
present a short
literature review
to contextualize
the data from
this study. If not
all these factors
are present,
score = 0.
Generalizabi
lity
#21 Discuss the
generalizability
(external
validity) of the
study results
–NA– Internal and
external validity
must be
addressed with
a cautious
interpretation
from the author.
Information such
as setting,
eligibility criteria,
location,
exposures, and
follow up should
be present to
help the reader
make his/her
own judgment.

Other
Information

74

Funding #22 Give the source
of funding and
the role of the
funders for the
present study
and, if
applicable for
the original
study on which
the present
article is based
–NA– If the funding
source was
mentioned and
the role of those
funding the
study was
described, credit
was given.
Credit was given
to those who did
not describe the
role of the
funders in detail.

75

Table 4: The currently accepted evidence hierarchy
1 Systematic Review and Meta -Analysis
2 Large Randomized Controlled Trials
3 Small Randomized Controlled trials
4 Non-randomized trials
5 Cohort Studies
6 Case-control studies
7 Case series and descriptive studies
8 Expert Opinion

76

Figure 10: Search strategy

77

Table 5: Number of citations found for each journal at each year (total =471)
Journal of
Periodontology
Journal of
Clinical
Periodontology
2000 n=67 n=33
2006 n=62 n=51
2012 n=104 n=64
2018 n=36 n=54
total n = 269 n = 202

78

Table 6 The pool of citations found for each journal after hand selection of articles (total=85).
Journal of
Periodontology
Journal of
Clinical
Periodontology
2000 n=11 n=9
2006 n=12 n=11
2012 n=12 n=12
2018 n=9 n=9

79

Figure 11: Trend in the Number of Cohort Articles Published Annually

0
10
20
30
40
50
60
70
80
90
100
2000 2006 2012 2018
Number of Cohort Articles Published Annually
Journal of Periodontology Journal of Clinical Periodontology

80

Figure 12: Adherence of selected articles to the STROBE checklist

0% 10% 20% 30% 40% 50% 60% 70% 80% 90% 100%
1_JOP 2000 Buchman
3_ JOP 2000 Machtei
5_ JOP 2000 Schwartz Arad
7_ JOP 2000 Hujoel
2_ JCP 2000 Payne
4_JCP 2000 Robinson
6_JCP 2000 Tilakaratne
1_ JOP 2006 Venza
3_ JOP 2006 Cunha Cruz
5_ JOP 2006 Pitiphat
7_ JOP 2006 Thomson
2_JCP 2006 Hughes
4_JCP 2006 Van Der Velden
6_ JCP 2006 Broadbent
1_ JOP 2012 Swierkot
3_JOP 2012 Patero
5_JOP 2012 Costa
7_ JOP 2012 Auyeung
2_ JCP 2012 Keller
4_JCP 2012 De Castilhos
6_JCP 2012 Carrillo
1_JOP 2018 Bonino
3_JOP 2018 Nascimento
5_JOP 2018 Costa
7_JOP 2018 Lahdentausta
2_ JCP 2018 Duarte
4_JCP 2018 Tanaka
6_ JCP 2018 Kumar
% Compliance with STROBE Criteria
% of Adherence of All 58 Articles to the STROBE Checklist

81

Figure 13: Average compliance to the STROBE checklist by year. **error bars = +/- standard error

0%
10%
20%
30%
40%
50%
60%
70%
80%
90%
Total Average 2000 2006 2012 2018
Average Compliance
Average Overall Compliance to STROBE Checklist

82

Figure 14: Compliance to the STROBE checklist by journal and by year. **error bars = +/- standard error.

0%
10%
20%
30%
40%
50%
60%
70%
80%
90%
100%
2000 2006 2012 2018
% Compliance
% Overall Compliance
Journal of Periodontology
Journal of Clinical Periodontology

83

Figure 15: Distribution of STROBE scores by year

0%
10%
20%
30%
40%
50%
60%
70%
80%
90%
100%
1994 2000 2006 2012 2018 2024
Distribution of STROBE Scores By Year

84

Figure 16 The average percentage compliance across all articles was calculated for each criteria within
the STROBE checklist

85

Table 7: Articles endorsing the STROBE criteria
Year Journal of Periodontology Journal of Clinical
Periodontology
2012 none (Carrillo-de-Albornoz et al.,
2012) Carrillo-de-
Albornoz, A., et al.
Gingival changes
during pregnancy:
III. Impact of clinical,
microbiological,
immunological and
socio-demographic
factors on gingival
inflammation

2018
(Nascimento et al., 2018)
Nascimento, G.G., et al.,
Metabolic syndrome and
periodontitis: A structural
equation modeling
approach.

(Collares et al., 2018)
Collares, K., et al.,
Proximal restoration
increases the risk of
clinical attachment loss.

(Lahdentausta et al.,
2018b) Lahdentausta,

86

(Lahdentausta et al.,
2018a) Lahdentausta, L.,
et al., Smoking confounds
the periodontal diagnostics
using saliva biomarkers
L.S.J., et al., Saliva and
serum biomarkers in
periodontitis and coronary
artery disease.

Abstract (if available)

Abstract Background: Observational studies are an important source of evidence in the clinical practice of dentistry and medicine. The Strengthening of Reporting of Observational Studies in Epidemiology (STROBE) checklist was originally created in 2007 to systematically improve reporting quality in observational research, including cohort, case-control, and cross-sectional studies.
Aim: This cross-sectional survey evaluated cohort reports published between 2000 and 2018 in two high impact periodontology journals. The percentage of STROBE items reported sufficiently in each article at two years prior to the 2007 STROBE publication (2000, 2006), and two years post 2007 STROBE publication (2012, 2018) was compared using descriptive trend analyses.
Methods: The PubMed electronic database was used to select a pool of cohort reports in the Journal of Periodontology (JOP) and the Journal of Clinical Periodontology (JCP) from the years 2000, 2006, 2012, and 2018. Seven cohort articles were randomly selected from each journal at each time point, totaling in 56 articles with 4 time points, two prior to STROBE (2000, 2006), and two post STROBE (2012, 2018). Each article was methodically rated based on the STROBE checklist and assigned a compliance score. A trend analysis of article adherence was completed and average STROBE scores were compared across time, journals, and checklist items.
Results: Of the 85 cohort articles published in the two journals in 2000, 2006, 2012, and 2018, 56 articles were randomly selected for evaluation. The average adherence to the STROBE checklist of all articles was 73%, and the STROBE score was shown to increase significantly over time (the average score in 2000 of 63% versus the average score in 2018 of 80%). The number of cohort articles published in each year/journal was consistently low (n≤12). Categories which continue to need improvement include item 9 “Describe any efforts to address potential sources of bias,” and item 10 “Explain how the study size was arrived at,” and all items which involved the management of participants lost to follow-up (items 12, 13, and 14).
Conclusion: The quality of cohort reports published in periodontology has improved significantly between the years of 2000 and 2018, but many items of the STROBE guidelines remain unmet across all years. Due to limitations of an uncontrolled before-after trend analysis, it cannot be concluded whether the increased adherence is due to the publication of the STROBE guidelines, or due to a progressively positive trend in reporting quality over time. It was clear, however, that publications that explicitly recognized the STROBE guidelines tended to have higher average ratings. While this study has limitations, the checklist items which need improvement based on our findings have also been highlighted in comparable reviews in periodontology and implant dentistry. Most notable shortcomings include attempts to address bias, explanation of sample size calculations, reports of participation and follow up, and reports indicating the number of participants with missing data. Based on the results of this trend-analysis, an increase in quality of cohort studies in periodontology is still needed, and adherence of observational studies to STROBE should be required by all journals. Journals in periodontology may benefit from additional mechanisms in place to increase adherence to reporting guidelines, such as requirements that authors submit written descriptions of how each checklist criteria has been met in a prospective article prior to publication.

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Asset Metadata

Creator Scholten, Shira (author)

Core Title Reporting quality of cohort studies in periodontology before and after the STROBE publication: a trend analysis

School School of Dentistry

Degree Master of Science

Degree Program Biomedical Implants and Tissue Engineering

Degree Conferral Date 2022-08

Publication Date 07/22/2022

Defense Date 05/18/2022

Publisher University of Southern California (original), University of Southern California. Libraries (digital)

Tag cohort,compliance,dentistry,Epidemiology,Evidence,implant,OAI-PMH Harvest,periodontics,periodontology,quality,reporting,STROBE

Format application/pdf (imt)

Language English

Contributor Electronically uploaded by the author (provenance)

Advisor Chen, Casey (committee member), Kar, Kian (committee member), Kumar, Satish (committee member), Navazesh, Mahvash (committee member)

Creator Email sbutt@usc.edu,shirascholten@gmail.com

Permanent Link (DOI) https://doi.org/10.25549/usctheses-oUC111375391

Unique identifier UC111375391

Legacy Identifier etd-ScholtenSh-10934

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Type texts

Source 20220728-usctheses-batch-962 (batch), University of Southern California (contributing entity), University of Southern California Dissertations and Theses (collection)

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