International Journal of Radiation Biology

ISSN: 0955-3002 (Print) 1362-3095 (Online) Journal homepage: http://www.tandfonline.com/loi/irab20

A Comprehensive Review of the Literature on the

Biological Effects from Dental X-ray Exposures

Vinita Chauhan & Ruth C. Wilkins

To cite this article: Vinita Chauhan & Ruth C. Wilkins (2018): A Comprehensive Review of the
Literature on the Biological Effects from Dental X-ray Exposures, International Journal of Radiation
Biology, DOI: 10.1080/09553002.2019.1547436

To link to this article: https://doi.org/10.1080/09553002.2019.1547436

© 2018 The Author(s)

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 A Comprehensive Review of the Literature on the Biological Effects from

Dental X-ray Exposures

by

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Vinita Chauhan*, Ruth C. Wilkins*

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Consumer and Clinical Radiation Protection Bureau, Healthy Environments and Consumer

Safety Branch, Health Canada, Ottawa, Ontario, Canada, K1A 1C1.

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*
Send correspondence to:
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Vinita Chauhan, Ph.D.
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Consumer and Clinical Radiation Protection Bureau
Health Canada
775 Brookfield Road, PL 6303B
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Ottawa, Ontario, Canada

K1A-1C1
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Tel: (613) 941-8516

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Fax: (613) 941-1734

E-mail: Vinita.Chauahn@hc-sc.gc.ca
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&

Ruth Wilkins, Ph.D.

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Consumer and Clinical Radiation Protection Bureau

Health Canada
775 Brookfield Road, PL 6303B
Ottawa, Ontario, Canada
K1A-1C1
Tel: (613) 941-7263
Fax: (613) 941-1734
E-mail: Ruth.Wilkins@hc-sc.gc.ca
ABSTRACT

Purpose: Routine dental X-rays are among the most common sources of ionizing radiation

exposure for healthy individuals globally, with approximately 300 examinations/1000

individuals/year as documented by the United Nations Scientific Committee on the Effects of

Atomic Radiation (UNSCEAR) global survey of medical radiation usage and exposure.

Furthermore in the United States of America, an increased use of dental radiography is evident.

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However, with the shift from using film to digital image receptors, the dose of radiation per

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routine examination has decreased. Despite this, there remains public concern of dental X-rays.

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This continuing concern highlights the need to review the literature on biological and health

effects related to exposure, from dental X-rays. Materials & Methods: This report presents
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studies investigating biological and health effects related to exposures using dental X-rays in

patients and provides a critical evaluation. Relevant studies specific to dental X-rays are
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reviewed from 1970 and onward with the bulk of data in this field resulting from
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epidemiological and biomonitoring studies. Results: While, most epidemiological studies

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suggest a possible correlation between head/neck related tumors and exposure to dental X-rays,
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evidence for causation is lacking. Biomonitoring studies suggest that exposure to low level
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radiation such as that of dental radiography may not be a factor in inducing long-term
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chromosomal damage, but may result in localized cytotoxicity in the irradiated region of the

mouth, with no long-term harm. Conclusions: In general, the total number of studies is low and

the majority of the data has been generated from poorly designed experiments. This review will

highlight shortcomings that could influence outcomes and provide a more balanced interpretation

that could impact the public perception and the level of public concern on the health effects

resulting from dental X-rays.

INTRODUCTION

Medical imaging procedures are essential for diagnosing disease, identifying injuries, and

managing patient conditions. Dental radiography is among these procedures and is an effective

means for imaging dental and maxillofacial structures to identify dental decay, infections in the

bones, root pathologies and many other dental issues.

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There are two main types of dental X-ray radiography equipment: Intraoral equipment produces

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an image by placing an X-ray film inside the mouth of the patient providing detailed information

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about the health of the teeth, jawbones, tooth root, and also confirming the presence of cavities.
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Extraoral equipment situates the X-ray image receptor exterior to the mouth, providing images of

the teeth and information on the jaw and skull. There are several types of extraoral X-ray
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equipment in dentistry, including cephalometric, panoramic, and, more recently, cone beam

computed tomography (CBCT). Each type of equipment can deliver a range of radiation doses,
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depending on the imaging technique. Cephalometric radiography captures a single image of the
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jaw and/or head, while with panoramic radiography the X-ray tube and receptor holder rotate in a
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half circle around the front of the head forming a composite image of the entire mouth in a single

image. Cone bean computed tomography (CBCT) is a technique that consists of X-ray computed
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tomography where the X-rays are divergent, forming a cone that provides 3-dimentional imaging

information.

Typical doses for each technique (Table 1) vary widely both between and within modalities,

partially due to differences in how each technique is administered. In general, individual

intraoral radiographs deliver the lowest dose. CBCT delivers a higher effective dose than
conventional radiographic techniques; however they have a lower effective dose than those

found in multi-detector CT for dental applications (Stratis et al., 2017).

As digital technologies have evolved over the years, so have dental X-ray image receptors. New

technologies are emerging that have the capability to provide improved image quality. For

example, digital radiography has become more popular in the past 10 years allowing the viewing

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of digital images on a computer screen and eliminating the need for traditional film and its

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associated processing. Under optimized settings, this can lead to shorter exposure times which

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can translate to lower doses to the patient (Okano and Sur, 2010).

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Dental X-rays are the most frequently used radiologic procedure in the US for healthy

individuals, with the frequency increasing from 54 million in 1964 to 500 million in 2006 (BEIR
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VII, 2006;Mettler, Jr. et al., 2009). Worldwide, however, there was no increase in the number of
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examinations per 1000 population reported between 1970 and 2007 in health-care level I
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countries (those with at least 1 physician for every 1000 people) (UNSCEAR, 2010). Despite the
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lower doses and the use of improved technologies, there still remains a public perception of
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increased health risks associated with exposure to dental X-rays. While there are relatively large

uncertainties associated with the low dose exposures, some of these public’s concerns of
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radiation risks may stem from how scientific information is communicated by the media.

This review will focus on the studies pertaining to health and biological effects related

specifically to dental X-ray exposures to patients since 1970, as exposures prior to this date were

substantially higher and not representative of current dental practice. However, the information

presented here is also broadly relevant to low dose medical exposures of the head and neck. A
comprehensive literature search was conducted using various engines e.g. PubMed, Google

Scholar, MEDLINE, Embase and Scopus. Included in this report are epidemiological

investigations and biomonitoring-based studies on human patients, however, no data is currently

available from animal-derived studies specific to dental radiography. In reviewing these studies,

commonalities with respect to cohort recruitment, study design and data management and

analysis were considered and overarching conclusions were drawn. In all studies, shortcomings

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of the research and study designs were examined and are discussed in order to highlight

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drawbacks that may have influenced the outcomes.

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STUDIES ON HEALH EFFECTS
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Epidemiological Studies
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All epidemiological studies considered in this review were population-based case controls, with
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data collected from individuals with cancers of the head and neck (case) compared to those who
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were cancer-free (controls). Patients were typically obtained from population-based cancer
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registries such as the Surveillance, Epidemiology, and End Results (SEER) Program (Hankey et
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al., 1999) or medical records from hospitals. The control populations were either matched
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patients or neighborhood residents with similar socioeconomic status, age, race and sex.

Pertinent data was collected from both cohorts including information on lifestyle, age, race,

gender, frequency of dental and medical visits, and job history including tasks, occupational

illness and/or injury. Depending on the rigour of the interview process between studies,

questions may have been posed about head trauma, head X-rays, family history of cancer

(including brain, head and neck and thyroid), as well as intake of tobacco, alcohol, vitamin
supplements, and certain foods (Preston-Martin et al., 1983;Preston-Martin et al., 1989). It

should be noted that case-control studies have inherent issues that may skew results leading to a

positive association. These may include issues of case and control misclassification, low

participation rates, recall and information bias and survival bias. The strength of such types of

studies is only realized when large sampling sizes are used, the selection of cases and controls is

unbiased and information is available on potential confounders, diagnostic and/or therapeutic x-

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rays of head, neck, and chest, radiotherapy (to any part of the body), and the number of

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exposures. In general the majority of the studies were lacking in the above factors. Most

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importantly, the studies were not able to provide detailed information on the type of dental

procedure, number of dental X-ray examinations and the total number of exposures, thereby
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challenging the ability to estimate dose. A summary of the results and detailed methodologies for

all studies is provided in Table 2.

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The first case control study relating to dental X-rays was conducted in the late seventies. In this
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study, male laryngeal cancer patients were recruited to assess the relationship between exposure
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to dental X-rays and the development of cancer (Hinds et al., 1979). The study was derived from
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a low sample size using a total of 47 laryngeal cancers, all in Caucasian males, identified through
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a cancer surveillance system. The method of data collection was inconsistent and not blinded to

the interviewer. Some cases were interviewed by clinical personnel while controls were

interviewed in their home by a different interviewer. It was also not known whether the cases

and controls were interviewed by the same individual using a standardized format. Therefore

possibilities of bias exist. Furthermore, the necessary details to estimate of the dose of radiation

received by an individual based on the number of dental X-ray examinations were not recorded.
As a consequence of the low sample size and lack of information on the dosimetry no

conclusions on the relationship between dental X-ray exposure and the development of laryngeal

cancer could be drawn from this study.

In the late eighties and early nineties Preston-Martin et al. conducted a series of studies on the

risks associated with dental X-rays (Preston-Martin et al., 1985b;Preston-Martin et al.,

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1980;Preston-Martin et al., 1983;Preston-Martin et al., 1985a;Preston-Martin et al.,

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1988;Preston-Martin et al., 1989). These studies were the first epidemiological investigations to

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assess the correlation between dental X-rays and the development of tumors in the brain and

parotid glands. Following this, several other groups also examined the effects of dental X-rays on
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meningioma development (Neuberger et al., 1991;Ryan et al., 1992;Rodvall et al.,

1998;Longstreth et al., 2004;Claus et al., 2012;Lin et al., 2013). The results and details of these
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studies have been summarized in a recent meta-analysis which included seven case-control
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studies involving 6,174 patients and 19,459 controls that reported development of meningioma.
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Overall, it was found that exposure to dental X-rays had no effect on brain cancer risk. When
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different types of examinations including full-mouth, bitewing, panoramic and lateral

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cephalometric were analyzed individually, there was a slight increase in risk relative to control
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groups with exposure to dental bitewing X-rays but with no other type of examination (Xu et al.,

2015). However as only two of the seven studies reported risk with dental bitewing, statistical

power is lacking to support the increased risk. It was noted that there was substantial

heterogeneity in cohort selection, study design, information collection, and determination of

exposure among the included studies. The results were also derived from studies with a number

of shortcomings, the most notable of these being recall bias. Furthermore, information on the
type of dental equipment, loading factors and film used or the frequency and the type of dental

X-rays were not accurately documented in most studies. With respect to data analysis, odds

ratios were presented without confidence intervals, which are meaningless in terms of

significance and therefore voids any conclusions that may have been drawn from the data. A

commentary by Tetradis et al. also proposed that the association between meningiomas and

dental exposure observed by Clause et al. may have been due to increased numbers of dental X-

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rays taken for referred facial pain from meningiomas or the presence of head trauma (Tetradis et

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al., 2012).

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As the thyroid gland is highly susceptible to radiation induced carcinogenesis, particularly in
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children, a series of studies have investigated the effects of dental radiation on thyroid cancer

risk (Ron et al., 2012;Ron et al., 1995). Memon et al. conducted a population-based case control
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interview study among 313 patients with thyroid cancer, matched controls and information on
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confounders such as nationality, gender, and age (Memon et al., 2010). The results of this study
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showed that exposure to dental X-rays was associated with an increased risk of thyroid cancer.
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However, the study was based on self-reporting by the participants as no dental X-ray records
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had been maintained at the dental clinics. More recently, employing data from the US Radiologic
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Technologists, Neta et al. found a 13% increase in thyroid cancer risk for every 10 reported

dental radiographs using a prospective cohort study design (Neta et al., 2013). This study ran

from 1983 to 2006 and included data from almost 150,000 patients who were radiological

technologists who had undergone dental examinations in the past, with detailed information on

confounding factors. However, information on the type of procedure (e.g. full mouth, panoramic,

bitewing) was not available, with only the approximate number of times/year they had the
procedure being reported. It should be noted, however, that these results were driven by dental

X-rays received prior to 1970 when doses from dental X-ray procedures were much higher

(Johnson and Goetz, 1986) . No detailed radiation exposure assessment was conducted to enable

quantitative evaluation of risk. Furthermore, in 2015, Zhang et al. found a borderline increase

risk for thyroid cancer associated with a having more than one dental X-ray per year (OR 2.20,

95% CI: 1.03-4.73) (Zhang Y, 2015). This study was conducted in Connecticut in 2010-2011,

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and included 462 histologically confirmed incident thyroid cancer cases and 498 population

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based controls. The study examined all types of medical diagnostic procedures including dental

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radiography. Participants were questioned on frequency and type of dental procedure they

underwent and information on confounding factors was available. However, similar to earlier
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studies, recall bias must be considered as a shortcoming and information on the radiation doses

to the thyroid gland was not available. The data analysis was based solely on the number of X-
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ray procedures received/participant therefore conclusions should be interpreted with caution.
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In 2004, Hujoel et al. conducted a study using enrollees of a dental insurance company to
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investigate the relationship between antepartum dental radiographs and infant low birth weight
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(Hujoel et al., 2004). Cases consisted of 117 women with low birth weight infant and controls
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comprised pregnancies resulting in normal birth weight infants (4468 participants). The authors

hypothesized that pregnant woman exposed to dental X-rays may be at risk for delivering low

birth weight infants (<2500g). The study was performed with women aged 12-45 between 1993

and 2000 of singleton births. For each woman, the date and type of each dental radiograph taken

was abstracted from the dental utilization database. Doses were assigned to each type of

radiographic exposure, and summed. Doses were estimated based on a nationwide 1993 (U.S.
N.E.X.T) dental survey evaluation of X-ray trends and published thyroid radiation doses. It was

noted that thyroid shields were not used during the procedures for the participants recruited. For

each of the enrollees, infant birth dates were recorded, however no information was collected on

critical items that could bias the study outcomes including information on smoking status,

previous non-dental radiation exposures, and whether the participant had a normal functioning

thyroid. Not all information was available from the participants on other confounders such as

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existing disease. It was shown that 10% of the cohorts had dental radiography during pregnancy

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and birth weights of infants were reduced by up to 5%. The authors indicate that low dose

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radiation can cause thyroid dysfunction, which disrupts fetal development which may be the

rationale for the observed low birth weight infants. This article was reviewed critically
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highlighting the association was indirect and not causally related and the lack of information on

critical confounding factors, such as overall oral health of the mother and recall of dental
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procedures, make it difficult to interpret the data (Boice, Jr. et al., 2004;Brent, 2005).
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Furthermore, studies that followed by others did not support the above findings. Al-Attas et al.
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showed that, in a study with 47 cases and 58 control mothers, there was no association between
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the use of dental radiography in any trimester of the pregnancy and birth weight (Al-Attas S.,
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2014). Mortazavi et al. examined using large sample size of 1,200 newborns, whose mothers had
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been either exposed or not exposed to dental radiography in Iran. It was shown that the children

of mothers who had received dental radiography during their pregnancy showed no significant

decrease in their birth weight (Mortazavi et al., 2013).

Summary of Epidemiological findings:

In general, at such low doses, the detection of significant adverse health effects will always be a
challenge, even with well-designed epidemiological studies with strong statistical power.

However, when designing future studies the following criteria should be taken into

consideration in order to ensure high confidence results:

1) Selection Bias: The selection and number of controls is an important determinant to the

study design and if not appropriate, blinded and matched, may skew the outcomes.

2) Statistical power: One of the most important limitations of each of the evaluated studies

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is lack of statistical power. The studies have recruited a small number of participants

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(<40) to elucidate correlations. It is recommended for any type of epidemiological study

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the sample size and power of association be large in order to obtain reliable statistical

inference.
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3) Questionnaires: These should be well designed, clear and not open for misinterpretation

by the respondent. It should also be designed to collect information on confounders along

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with adequate detail to accurately determine the dose of radiation exposure.
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4) Interview bias: Interviewers should be blinded as to the status of the patient (i.e. case or
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control), thereby ensuring impartiality.

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5) Accurate Dose estimates/Recall bias: As there are currently limited databases available
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for diagnostic dental imaging procedures, it is difficult to obtain accurate dental exposure
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records. As such, researchers have had to rely on patient self-reporting, which has

potential for recall bias leading to inaccurate data collection. Without accurate dental

records and dose per procedure information, dose-response trends have to be

approximated by the recall of the frequency of dental visits and type of X-ray procedures

performed. It is recommend that future studies obtain complete information on the dental

history of the patient, including type of procedure, specifications of the instrument used,
 settings, loading factors, number of visits, age of first visit etc.

6) Data interpretation: Standard statistical methods for the analysis of case-control studies

are based on odds ratios, which calculate relative risk for each categorical risk factor

(Breslow and Day, 1980a). However, there are limitations of the odds ratio in detecting a

diagnostic outcome which have been described and reviewed by (Pepe et al., 2004). Odds

ratios, especially without confidence intervals, are not the best statistical method for

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classification of outcomes. Other approaches such as multi logistic regression are more

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suitable.

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7) Confounding factors: These are not often adjusted for, or insufficient data is available to

draw accurate conclusions. These adjustments are normally achieved by unconditional

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multiple logistic regression which, with currently accessible analytical tools, should be

applied to all epidemiological data (Breslow and Day, 1980b) .

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Cell-based Studies
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In light of the concerns regarding epidemiological studies, cell-based investigations become

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important as they are not hindered by many of the issues described above. Over the past decade
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the majority of these studies have examined cytogenetic modulations (micronuclei formation)
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and cytotoxicity-induced effects (karyorrhexis, pyknosis and karyolysis) in the oral mucosa

following dental X-ray exposure. Cytotoxicity assays normally assess short-term changes in the

vicinity of the exposure that could eventually result in degenerative nuclear changes which might

lead to cell death. Cell death is transient in the sense that, once the cell dies, the surrounding

tissue will regenerate with no lasting effects. Concurrent to assessing these short-term changes,

studies also detect long-term chromosomal damage using the buccal cell micronucleus (MN)
assay (Thomas et al., 2009;Bonassi et al., 2011a). The MN assay is widely used to identify

irreversible chromosomal damage. MN formation occurs in dividing cells which are most likely

to be found in the basal layer and move to the surface through turnover of the epithelial layer. As

this turnover is rapid (7-16 days), MN formation can be detected in exfoliated cells within this

time-frame subsequent to the exposure (Thomas et al., 2009). The majority of the cell-based

studies harvest oral mucosa cells from the cheeks of their subjects before, and 10 days following

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exposure to dental X-rays and then assess the cells for cytotoxic damage and MN formation.

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Specific details on type of dental procedure and specifications of the dental instrument used in

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each study are provided in Table 3.

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Over the course of the past 12 years, these methods have been used to asses cytogenetic changes

associated with dental X-ray exposures at the cellular level after panoramic radiography. MN and
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nuclear cytotoxic changes were examined in harvested oral mucosa cells obtained from the
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cheeks of healthy adults before and 10 days post-procedure. These studies have shown that the
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frequency of nuclear alterations, indicative of apoptosis (karyorrhexis and condensed chromatin)

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are significantly higher following dental X-ray procedures but, in most cases, no statistically
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significant increase in the number of MN was observed (Cerqueira et al., 2004;Ribeiro and
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Angelieri, 2008;Popova et al., 2007;Angelieri et al., 2010). A follow-up study, in 2008, by

Cerqueira et al. conducted in epithelial gingival cells showed significant cytogenetic effects

following dental X-ray exposures (Cerqueira et al., 2008). In contrast to their previous study in

2004, the results indicate a higher MN induction in epithelial cells harvested from the gingiva.

Significant cytotoxic nuclear alterations were also observed indicative of apoptosis similar to

those found in oral mucosa cells. In 2011 Ribeiro et al. performed a study examining genetic
damage in oral mucosa cells of patients after exposure to digital radiography performed using

panoramic radiographs and lateral and frontal cephalometric X-rays (Ribeiro et al., 2011). The

results of this work were similar to previous studies in terms of evidence for cytotoxicity and a

lack of MN formation. More recently, two new studies have emerged both using similar analysis

of MN in buccal cells following panoramic radiographic exposures. The first study of 60 subjects

found a small but significant increase in MN after exposure to dental X-rays (Al-Attas S.,

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2014;Waingade, 2012) while another study found a significantly higher increase in both the

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frequency of MN and the percent of cells with MN after a similar exposure (Arora et al., 2014).

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Similarly, by using exfoliated cells from the lateral border of the tongue from men aged 18-40,
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da Silva et al. observed no genotoxicity at the chromosome level following one or two panoramic

radiographs, however the number of cells undergoing apoptosis was increased post-exposure (da
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Silva et al., 2007). A cytotoxic effect was more evident in patients who required a repeat
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radiograph exposure due to error in the first procedure, but no evidence of permanent cellular
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damage was observed. The authors do acknowledge that the sample size in this study was small,
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and any effects of alcohol, tobacco or other genotoxic agents, which could produce changes in
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the oral mucosa, were not accounted for.

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With the introduction of CBCT, research has shifted to examine biological markers of damage

induced by this new technology. This technology, which offers three-dimensional (3D) imaging

of dental structures, is administered at higher doses than bitewing, root end or panoramic X-rays.

In 2010, Carlin et al. assessed DNA damage and cellular death in exfoliated buccal mucosa cells

from adults following CBCT (Carlin et al., 2010). Exfoliated oral mucosa cells were collected
immediately before and 10 days after CBCT in healthy adults and evaluated for DNA damage,

using the MN test, as well as other indicators of cell death. Prior to CBCT exposure, the

frequency of MN cells was small (0.04%) with no statistically significant increases observed

following the CBCT procedure. However, nuclear alterations in the form of karyorrhexis,

pyknosis, and karolysis were shown to increase by more than two fold. These results are in line

with those shown previously, indicating the potential for ionizing radiation to induce localized

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temporary cellular damage.

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The above studies which have been conducted in adults have predominately shown no permanent

cellular effects associated with dental X-ray exposures. However, children are thought to be
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more susceptible to adverse health effects from exposure to radiation, mainly because they are

developing and have shown altered DNA repair capacity (Frush, 2011). The following studies
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have examined DNA damage (MN formation) and cellular death in exfoliated buccal mucosa
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cells from healthy children following dental radiography (Angelieri et al., 2007;Carlin et al.,
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2010;Ribeiro et al., 2008;Carlin et al., 2010;Ribeiro et al., 2008;El-Ashiry et al., 2010;Agarwal

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et al., 2015). Overall these studies indicate no increased susceptibility in these endpoints among
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children as compared to adults. In 2011, Lorenzoni et al. performed a comprehensive cytogenetic

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biomonitoring study in children following a complete set of radiographs for orthodontic

planning. This included lateral and posteroanterior cephalographics, panoramic, full periapical

exams and bitewing exams. The MN test indicated no increase in chromosomal damage,

however, a significant increase in nuclear alterations related to cytotoxicity was observed similar

to results observed in adult patients (Lorenzoni et al., 2012). The study was repeated with CBCT

and similar findings were observed (Lorenzoni DC, 2013).

Summary of Cell-based studies:

In general, the results from the cell-based studies described above predominantly indicate that

there are no cytogenetic changes associated with exposures from dental X-rays. However there is

some indication of a localized cytotoxic response in the tissue. The most recent studies that do

show increased MN formation may be the result of improvements to and standardization of the

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MN assay for biomonitoring, thereby, increasing the ability to measure small changes with

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greater confidence (Holland et al., 2008). However, these minute cellular changes may not pose

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any long term adverse health effects. Furthermore, as with the epidemiological studies, there are

some possible concerns and limitations to these cellular assays as listed here:
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1) Confounding factors: confounding factors such as age, smoking and alcohol consumption,

are all known to be associated with increased frequencies of chromosome aberrations and
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therefore, MN (Nefic et al., 2013;Fenech, 1998;Bonassi et al., 2011b). This can lead to large
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inter-individual variation in background levels which are difficult to control for and can skew
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results and bias outcomes. Robust statistical methods must be employed to appropriately
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analyze this type of data.

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2) Sensitivity: Due to large variations in the background levels of MN, the sensitivity of the
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assay may be insufficient to detect changes after very low doses of radiation (Ceppi et al.,

2010). New technologies have emerged over the years that may have greater sensitivity to

detect effects at lower doses.

3) Sample size: Results from many of the studies were derived from low sample numbers (<40)

and in some cases, these were divided into multiple treatment groups. For detecting small

changes with statistical confidence, larger sample sizes would be required.

4) Scorer bias: It is not clear from the studies whether the scorers were blinded to the sample

identification. Future studies should control for selection and information collection bias by

randomizing data and ensuring evaluators are blinded to the process.

5) Dosimetry: Dose estimates, if available were based on equipment settings with no evidence

of actual physical dose measurements to the area of sampling. In addition, the reporting of

dosimetry outputs was inconsistent across studies, making it difficult to compare results.

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Future studies should measure the physical doses to the area of sampling, thereby ensuring

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proper dose estimates.

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CONCLUDING REMARKS
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Dental X-rays account for most of the collective population dose to the head and neck from
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diagnostic radiography in healthy individuals. The question remains whether low-dose exposure
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to ionizing radiation could lead to a detectable increase in the risk of developing cancer.
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Epidemiological investigations have attempted to address this question; however not

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successfully, as these studies are challenged by inherent limitations in design, dosimetry, lack of
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information on confounding factors and most importantly sampling and recall bias, which are of

particular importance when trying to detect small changes after such a low dose. Genetic effects

from dental radiography have also been assessed by investigating MN formation and cytotoxicity

markers, but these studies have shortcomings related to the use of biomonitoring assays that are

not sensitive to detect changes at low doses and a statistical analysis approach that does not

account for confounding factors. Overall, the scientific literature on the possible biological
implications of dental X-rays is insufficient and, based on decades of research on low dose

ionizing radiation (<10 mGy), there is no clear indication of health effects. Studies using higher

doses of radiation (i.e skull radiographs, sinus radiograph or head computed tomography) and

extensive work with Japanese atomic bomb survivors have not provided evidence of increased

cancer risk below 0.1 Gy. However, more mechanistic studies are needed and research efforts

should be put forth to developing innovative approaches for interpolating dose-response between

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data from epidemiological investigations and incremental doses above background and the

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correlation to long-term health effects. At such low doses, the detection of significant adverse

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health effects will always be a challenge, even with well-designed epidemiological studies with

strong statistical power, Ultimately what is of relevance is the detection of early biological
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signatures that may be indicative of a long-term adverse health effect. As new technologies

evolve these may prove valuable in detecting minute changes in biological tissue and future
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studies should be centered on identifying key events that are associated with an adverse outcome.
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Until, this time, the public should rest assured that clinicians ensure that each radiographic
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examination is appropriately justified as beneficial, and any required exposures are optimized to
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ensure the lowest reasonable radiation dose is used without compromising diagnostic
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information (Annals of the ICRP, 2007b;Annals of the ICRP, 2007a;European Commission,

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2004).
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FUNDING
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Health Canada A-Based funds #8R1055

DISCLOSURE STATEMENT

No conflicts to report.

BIOGRAPHICAL NOTE

Vinita Chauhan and RuthWilkins are research scientists at Health Canada.

ACKNOWLEDGEMENT

The authors are grateful to Matthew Rodrigues, Richard Smith, Christian Lavoie and Narine

Martel for critical review of the manuscript.

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Table 1. Typical doses from radiographic examinations

Examination Effective Dose Area Product References

Dose (μS) (mGycm2)
Intraoral
Bitewing (4 images) 5 35.9 (Ludlow et al.,
2008;Poppe et al.,
2007b)
Extraoral
Panoramic 9-24 76.4 (Ludlow et al.,
2008;Poppe et al.,
2007a;Granlund et al.,

t
ip
2016)
Cephalometric 2-6 32 (Ludlow et al.,
2008;Holroyd, 2011)

cr
Cone beam CT
Large Field of View 212 1229 (Ludlow et al.,
2015;Granlund et al.,

us
2016)
Medium Field of View 177 683 (Ludlow et al., 2015)
Small Field of View 84 an 61 (Ludlow et al., 2015)
M
e d
pt
ce
Ac
 Table 2: Summary of epidemiological studies

Reference Dental Study Population Instrument Dose Disease Outcome Measure on

Procedure which

Outcome is

Based

t
Hinds et al No 47 males with Information No indication of Laryngeal Possible relationship of Relative risk

ip
(1979) indication laryngeal cancer from not provided exposure, cancer laryngeal cancer with with p value

cr
Pierce King or Kisap however cases exposure to dental x-

us
counties between report a mean of rays among heavy

1976-1977 compared 14.3 dental x-ray smokers

to neighborhood
an
visits and controls

controls a mean of 12.3

M
visits over subject

lifetime
d

Preston- Full mouth 101 (of the total 185) Information No indication Intracranial Dental x-rays Odds ratio
e

Martin et intra-oral matched pairs of not provided meningiom associated with with p value
pt

al (1980) dental x- woman patients and as increase in

ce

rays neighborhood controls meningioma risk

residents of Los associated with early

Ac

Angeles county with exposure to full-mouth

intracranial X-ray series (16-20

meningioma's from intraoral films used)

1972-1975
Preston- Five or 105 matched pairs of Information Potential to be Intracranial Dental x-rays Odds ratio

Martin et more full men and not provided exposed to 315 R meningiom associated with with p value

al (1983) month neighborhood controls during full mouth as increase in intracranial

intra-oral in Los Angeles county examinations meningioma

dental x- with meningioma from development,

ray series 1972 to 1979 especially early

t
exposure (before age

ip
of 20) and multiple

cr
exposures in early

us
years (≥5 full mouth x-

ray series before 1945)

Burch et al No 215 cases of brain Information

an
No indication Brain Non-significant minor Relative risk

(1987) indication tumors in adults in not provided cancer elevation in the risk for with 95% CI
M
Southern Ontario glioma in those ever

between 1979 and exposed to dental x-

d

1982 with individually rays

e

matched hospital
pt

control series
ce

Preston- Details of 408 patients (269 Information Total cumulative Benign/ma Cumulative exposure Relative risk

Martin et lifetime benign tumors, 139 not provided parotid dose lignant of the parotid gland with 95% CI
Ac

al (1988) history of malignant) from Los varied from 0 to tumors of from diagnostic

dental care Angeles county with >50 rad the parotid radiograph associated

(full mouth tumor of the parotid gland with dose-related

or gland compared to increase in risk of

panoramic neighborhood controls malignant tumours.

 dental from 1976-1984 Benign tumors showed

radiograph a weaker positive

y or association

medical

radiograph

y to

t
the head )

ip
Preston- Full mouth 272 men with primary Information No indication Gliomas or Glioma risk increased Odds ratio

cr
Martin et intra oral brain tumor and not provided meningiom with an increase in the with 95% CI

us
al (1989) dental x- matched neighbour as frequency (from never

rays (~18 controls from 1980- to yearly) of full-mouth

intraoral 1984
an examinations

films) after age 25; a similar

M
trend was seen for

meningiomas. Both
d

glioma and
e

meningioma risk also

pt

increased with an
ce

increase in the

frequency of exposure
Ac

to dental x-rays of any

type before age 25,

although these trends

did not reach statistical

significance.
Neuberger No 7 cases and matched Information No indication Brain Positive correlation of Odds ratio

et al indication with 25 controls of a not provided cancer brain cancer with with 90% CI

(1991) brain cancer cluster in reported exposure to

Missouri from 1973- dental x-rays

1982

Wingren et No 185 female papillary or Information No indication Papillary Increased risks were Odds ratio

t
al (1995) indication mixed cancer cases not provided thyroid seen for women who with 95% CI

ip
cancer had worked as

cr
dentist/dental

us
assistant

Ryan et al Ordinary 110 subjects with Information No indication Gliomas or No excess risk for Odds ratio

(1992) dental x- glioma and 60 with not provided

an meningiom glioma associated with with 95% CI

rays and meningioma and 417 as exposure to diagnostic

M
panoramic controls from 1987- dental x-rays, however

full mouth 1990 statistically significant

d

x-rays increased risk

e

associated with dental

pt

x-rays for meningioma

ce

in males and not in

females
Ac

Rodvall et Dental 192 cases of glioma, 99 Information No indication Gliomas or No clear indication Relative risk

al (1998) radiograph cases of meningioma not provided meningiom that dental with 95% CI

y and and 42 cases of as radiography is related

frequency acoustic neurinoma to the development of

between 1987-1990 tumours of the central

 with a control group of nervous system,

343 subjects however there is risk

of meningioma with no

risk associated with

gliomas

Wingren et No 186 thyroid cancer Information Average number Female High risk for papillary Odds ratio

t
al (1997) indication cases in two Swedish not provided of radiographs papillary thyroid cancer was with 95% CI

ip
case-control studies on has been thyroid found in the

cr
determinants for 1.8/person/year cancer occupation group of

us
thyroid cancer from versus 1.65 in the dentist/dental

1977-1989 compared US and 0.25 in the assistants

to population controls UK
an
Longstreth Posterior 200 case-control study Information No indication Intracranial The full mouth series Odds ratio
M
et al bitewings, of residents of not provided meningiom (>6 over a lifetime) with 95% CI

(2004) full mouth Western Washington as was associated with a

d

series and State with intracranial significant risk of

e

lateral meningioma between meningioma, no dose-

pt

cephalome 1995-1998; two response relation was

ce

tric and control subject observed

panoramic matched to each case

Ac

radiograph patient based on age

s and gender
Hujoel et Full mouth 1117 women with low- Information Exposure of Low birth Dental radiography Odds ratio

al (2004) series, (21 birth weight infants not provided higher than 0.4 weight during pregnancy is with 95% CI

radiograph (<2500 g). Four control mGy during infants associated with low

s, 1.6 mGy pregnancies resulting gestation birth weight

to thyroid), in normal birth weight occurred in 1.9%

periapical infant (>2500g) were of the mother

t
dental used for each case with low birth

ip
radiograph (4468) between 1993- infants. 3% of the

cr
(0.08 2000 mothers with low

us
mGy), 4 birth infants

bitewings received doses

(0.22
an
higher than 0.4

mGy), mGy
M
cephalome

tric
d

radiograph
e

(0.46 mGy
pt

to thyroid,
ce

panoramic

radiograph
Ac

, 0.12 mGy

Ma et al No 1742 population-based Information No indication Breast Increased risk among Odds ratio

(2008) indication case patients and 441 not provided cancer women who received with 95% CI

control subjects from dental x-rays without

neighbourhood in Los lead apron protection

 Angeles County before age of 20

Memon et No 313 patients with Information Not indicated, Thyroid Exposure to dental x- Odds ratio

al (2010) indication thyroid cancer and not provided however dose- cancer rays was associated with 95% CI

matched control response data with an increased risk

subjects in Kuwait was based on of thyroid cancer with

t
number of dental a dose-response

ip
X-rays pattern

cr
categorized as 1-

4, 5-9 and 10+

us
Claus et al Self- 1433 case-control Information No indication Intracranial Exposure to some Odds ratio

(2012) reported study of residents of not provided

an meningiom dental x-rays with 95% CI

bitewing, North Carolina, San as performed in the past,

M
full mouth Francisco Bay and when radiation

series and Texas from 2006-2011 exposure was greater

d

panoramic diagnosed with than in the current era,

e

dental x- intracranial appears to be

pt

rays meningioma; control associated with an

ce

group of 1350 increased risk of

individuals matched on intracranial

Ac

age, sex and geography meningioma

Mortazavi No 1200 mothers with Information No indication Infant birth No statistical Odds ratio

et al indication their first-term labor not provided weight significant with 95% CI

(2013) (vaginal or caesarean) no differences

whose newborns’ between the mean

history had been weight of newborns

 registered whose mothers had

in neonates’ screening been exposed to

program in Shiraz were dental radiography vs

interviewed and non-exposed

surveyed

Lin et al Periapical 4123 benign brain Information No indication, Malignant No significant Odds ratio

t
(2013) radiograph tumor cases and 16 not provided indicates or benign association was found with 95% CI

ip
y, bitewing 492 controls without frequency of x- brain between malignant

cr
tumours (study 1) and rays tumours brain tumours and

us
197 malignant brain dental diagnostic X-

tumour ray. Small increase

cases and 788 controls

an risk of developing

without malignant benign brain tumours

M
tumours (study 2) from

Taiwan National Health

d

Insurance claim data

e

Neta et al Full mouth 75494 radiologic Information 0.1-0.7 mGy Thyroid 13% increase in Odds ratio
pt

(2013) intra oral, technologists who not provided cancer thyroid cancer risk for with 95% CI
ce

panoramic, were followed up for every 10 reported

bitewing thyroid cancer by the dental radiographs

Ac

American registry of

radiologic

technologists between

1926-1982
Zhang et al Full mouth 462 histologically Information No indication Thyroid Borderline increase Odds ratio

(2015) intra oral confirmed incident not provided cancer risk for thyroid cancer with 95% CI

series, thyroid cancer cases associated with a

panoramic and having more than one

exams 498 population-based dental X-ray per year

controls

t
Al-Attas Restorativ 47 cases and 58 Information No indication Infant birth No association Odds ratio

ip
(2014) e controls of women not provided weight between maternal with 95% CI

cr
treatment, who gave single live dental health or dental

us
periodonta birth in Jeddah city care with low birth

l, weight infants

endodonti
an
c,
M
extraction,

TMJ
d

CI=confidence interval
e
pt
ce

Table 3: Summary of in vitro studies

Ac

Reference Dental Cell Type Instrument Instrument End Point Outcome

Procedure details* Analysis

Cerqueira Panoramic Oral mucosa Siemens Orthophos 71 kV, 15 mA, Micronucleus P>0.05 in micronucleated

et al dental cells from 14s, 110 assay, oral mucosa cells before
2
(2004) radiography healthy adults mGy/cm , pyknosis, and after dental x-rays.

(n=31) effective dose karyolysis P<0.05 increase in nuclear

 21.4 Sv karyorrhexis alterations related to

cytotoxicity karyorrhexis,

pyknosis and karyolysis

da Silva et Panoramic Tongue Rotography Plus 60-85 kV, 10 mA, Micronucleus Increase in the number of

al (2007) dental epithelial cells 14-17s, dose on and nuclear anomalies (except

radiography from healthy the lateral cytotoxicity micronuclei in exfoliated

t
adult males border of the assays cells of the lateral border

ip
collected 10 tongue was of the tongue, effect was

cr
days after 0.057 mSv pronounced when

us
exposure (n=42) patients were exposed to

repeat radiographs

Angelieri Panoramic Exfoliated Siemens Orthophos

an
71 kV, 15 mA, Micronucleus P>0.05 in micronucleated

et al dental buccal mucosa 14s, 110 assay, oral mucosa cells before
M
2
(2007) radiography cells from mGy/cm , pyknosis, and after dental x-rays.

healthy children entrance dose karyolysis P<0.05 increase in nuclear

d

(n=17) 0.08 R karyorrhexis alterations related to

e

cytotoxicity karyorrhexis,
pt

pyknosis and karyolysis

ce

Ribeiro Panoramic Exfoliated Siemens Orthophos 71 kV, 15 mA, Micronucleus P>0.05 in micronucleated

and dental buccal mucosa 14s, 110 assay, oral mucosa cells before
Ac

2
Angelieri radiography cells from mGy/cm , pyknosis, and after dental x-rays.

(2008) healthy adults entrance dose karyolysis P<0.05 increase in nuclear

(n=39) 0.08 R karyorrhexis alterations related to

cytotoxicity karyorrhexis,

pyknosis and karyolysis

Ribeiro Panoramic Exfoliated Siemens Orthophos 71 kV, 15 mA, Micronucleus Both groups exhibited no

et al dental buccal mucosa 14s, 110 assay, effects in micronucleus

2
(2008) radiography cells from mGy/cm , pyknosis, formation after exposure.

healthy children entrance dose karyolysis Increase in cytotoxicity

and adults (n- 0.08 R karyorrhexis endpoints was observed

34) (karyorrhexis, pyknosis

t
and karyolysis) in both

ip
groups following exposure

cr
Popova et Panoramic Exfoliated No indication No indication Micronucleus CBCT and conventional

us
al (2007) dental buccal cells assay radiographs P>0.05

radiography from healthy micronucleus frequency,

adults (n=32)
an P<0.05 karyorrhexis,

pyknosis and karyolysis

M
Cerqueira Panoramic Epithelial Siemens Orthophos 65-90 kV, 15 mA, Micronucleus P<0.05 increase in

et al dental gingival cells 14s, 110 assay, chromosomal damage

d

2
(2008) radiography from healthy mGy/cm , pyknosis, and nuclear alterations
e

adults (n=40) effective dose karyolysis

pt

21.4 Sv karyorrhexis

ce

Carlin et Cone beam Buccal mucosa i-CAT CBCT scanner 70-80 kV, 10 mA, Micronucleus P>0.05 micronucleus

al (2010) computed cells harvested 0.7-0.8s, assay, frequency, P<0.05

Ac

tomography from healthy entrance dose pyknosis, karyorrhexis, pyknosis

adults (n=19) 0.046 R karyolysis and karyolysis

karyorrhexis

Angelieri Panoramic Comparison Siemens Orthophos 71 kV, 15 mA, Micronucleus Lateral border of the

et al dental between 14s, assay, tongue is more sensitive

 2
(2010) radiography epithelial cells 110mGy/cm , pyknosis, to cytotoxic insults

harvested from entrance dose karyolysis combined with

buccal mucosa 0.08 R karyorrhexis continuous cigarette

and lateral smoke exposure

border of the

tongue in

t
healthy adults

ip
(n=32)

cr
Angelieri Lateral and Exfoliated oral Siemens Orthophos 71 kV, 15 mA, Micronucleus P>0.05 micronucleus

us
et al frontal mucosa cells 14s, assay, frequency, P<0.05
2
(2010) cephalometric from healthy 110mGy/cm , pyknosis, karyorrhexis, pyknosis

x-ray and adults (n=18)

an
effective dose karyolysis and karyolysis

panoramic x- 21.4Sv karyorrhexis

M
ray

El-Ashiry Panoramic Exfoliated Orthopantomograph 70 kV, 24 mA, Micronucleus P>0.05 micronucleus

d

et al dental buccal mucosa 16s, 110 and frequency, P<0.05

e

2
(2010) radiography cells from mGy/cm , cytotoxicity karyorrhexis, pyknosis
pt

healthy children entrance dose assays and karyolysis

ce

(n=20) 0.08 R

Ribeiro et Cephalometric Exfoliated oral Rotography Plus 70-80 kV, 10 mA, Micronucleus P>0.05 micronucleus
Ac

al (2011) mucosa cells 0.7-0.8s, assay, frequency, P<0.05

from healthy entrance dose pyknosis, karyorrhexis, pyknosis

adults (n=30) 0.046 R karyolysis and karyolysis

karyorrhexis

Waingade Panoramic Buccal epithelial Gendex Orthoralix 60-80 kV, 10 mA, Micronucleus P<0.047 Micronucleated
et al radiography cells from system 9200 12s, output dose assay cell frequencies

(2012) healthy subjects rate: 0.325 m

(n=60) Gy/s

Arora et Panoramic Nonkeratinized Gendex Orthoralix 74 kV, 10 mA, Micronucleus P<0.05 of Micronuclei

al (2014) radiography buccal cells and system 12s, output dose assay frequency in buccal cells,

keratinized rate 0.325 m No statistically significant

t
epithelial Gy/s at 70 kV, 10 increase was found of

ip
gingival cells mA Micronuclei frequency in

cr
from healthy gingiva cells

us
adults (n=53)

Agarwal Panoramic Exfoliated Kodak 8000 C 65-90 kV, 15 mA, Micronucleus P>0.001 no significant

et al radiography buccal mucosa system

an
13s, 110 assay, number of MN in buccal
2
(2015) cells (n=20) mGy/cm , karyorrhexis, epithelial cells, P<0.001
M
pediatric effective dose pyknosis and combined frequency of

patients, 21.4 mSv laryolysis karyorrhexis, pyknosis

d

and laryolysis was

e

observed
pt

Lorenzoni Lateral Exfoliated Rotograph Plus Rotograph Plus Micronucelus P>0.05 no statistically
ce

et al, cephalograph, buccal cells equipment equipment: LAT: assay, significant differences

(2012) posteroanterior from healthy Spectro 70X 80kV, 10 mA, cytotoxicity were observed in Mni
Ac

cephalograph, children (n=25) selectronic 1.3S, 0.003 mSv assay: formation after exposure,

panoramic equipment PA: 85kV, 10 mA, pyknosis, p<0.05 increase in

radiograph, full 1.6 s, 0.03 mSv, karylolysis, karryorrhexis, pyknosis

mouth intra- PAN: 70 kV, 10 karyorrhexis and karyolysis was

oral x-ray mA, 17s, 0.03 observed following

 mSv radiation exposure

Spectro 70X

selectronic

equipment:

anterior

periapical: 70 kV,

t
8mA, 0.4 s, 0.008

ip
mSv, round

cr
collimation

us
posterior

periapical and
an
bitewing: 70 kV,

8 mA, 0.45 s,
M
0.008 mSv,

round
d

collimation
e

Lorenzoni Cone beam Exfoliated oral i-CAT CBCT scanner/ 120 kV, 46.72 Micronucleus CBCT and conventional
pt

et al, computed mucosa cells Rotography plus mAs, 40 assay, radiographs P>0.05
ce

(2013) tomography, from healthy seconds/ 70-80 pyknosis, micronucleus frequency,

conventional children (n=25) KV, 10 mA, 0.7- karyolysis P<0.05 karyorrhexis,

Ac

radiograph 0.8s, entrance karyorrhexis pyknosis and karyolysis

dose 0.046 R

*as described in the publication