Health risks for medical personnel due to magnetic fields in magnetic resonance imaging

Keywords

MR-imaging - physics - safety

Introduction

As one of the most important medical imaging methods of the last decade, magnetic resonance imaging (MRI) has become increasingly significant [1] [2] [3]. In Germany, 145 MRI examinations per 1000 inhabitants were registered in the year 2019 [4]. An estimated 50000 MRI scanners are currently in use internationally [5]. According to Modense et al., approximately 2000000 employees worldwide are exposed to high static magnetic fields as a result of medical MRI [6]. This includes not only radiologists and radiology assistants but also anesthesiologists, nursing staff, technical personnel, and cleaning staff [2], as well as employees working in research facilities with MRI systems and those who install and service MRI devices. The group with the greatest exposure is radiology assistants [7]. However, effects on personnel, primarily long-term effects, have only been minimally researched. To provide an overview of these effects and to identify gaps in the research, a systematic literature search was performed.

To prevent disruptive and harmful effects on human beings, Directive 2013/35/EU was issued. This defines the minimum requirements for protecting the safety and health of employees from risks due to physical effects (electromagnetic fields). The long-term effects of exposure to these fields were not taken into consideration in this directive since verified scientific data on this topic was not available when the directive was issued. Protection against and prevention of damaging effects when using systems involving non-ionizing radiation in medicine and dentistry as well as for industrial purposes are ensured and regulated by the “act on protection against non-ionizing radiation in humans” [8]. The scope of this law includes systems using electric, magnetic, and electromagnetic radiation in frequency ranges from 0 hertz to 300 gigahertz for medical and industrial purposes. It also regulates, for example, user requirements such as the necessity of a license or certificate of specialist training. Almost all national and international regulations on protection against electric, magnetic, and electromagnetic fields are based on recommendations of the ICNIRP (International Commission on Non-Ionizing Radiation Protection) [9].

Directive 2013/35/EU is based in part on Research Report 400-D by the Federal Ministry of Labor and Social Affairs from the year 2011 [10]. This report provides limit values and trigger thresholds for exposure to electric, magnetic, and electromagnetic fields. The limit values and trigger thresholds defined in Research Report 400-D are primarily based on the goal of protecting the human body against undesired effects from electromagnetic fields (nerve stimulation, tissue heating, etc.). These values essentially relate to short-term interactions with different types of electromagnetic fields.

The present study provides an overview of the current status of research regarding the effects of exposure of the human body to high static and low-frequency magnetic fields and high-frequency electromagnetic fields. The analysis focuses on the exposure for personnel in the field of clinical MRI. The magnetic field strength (magnetic flux density) typically used today is 1.5T to 3T. 10 ultra-high-field human MRI scanners in the range of 7T to 9.4T are currently operated in Germany in the field of research. The first 7T MRI device received clinical approval for use in patient care in 2017 [11] [12] [13]. The magnetic flux densities of MRI scanners used in research (experimental and small animal MRI) are currently up to 17.6T [12]. Magnetic flux densities of up to 28T have been used for magnetic resonance spectroscopy (MRS) [10] [14].

This review summarizes the current medical-scientific data on the effects of exposure to electromagnetic fields under consideration of the long-term exposure. The focus is on those working in the field of clinical magnetic resonance imaging.

Research method

The inclusion and exclusion criteria for the literature search are summarized in [Table 1].

Table 1 Inclusion and exclusion criteria of the systematic literature search.

	Inclusion criteria	Exclusion criteria
Language	English, German	Other languages
Target group	Human studies (employees) or (combined studies – human/experimental animal)	Only experimental animal studies
Availability	Full text is available	Access only to title or abstract

Since the study explicitly relates to the effects of electromagnetic fields on people, i.e., medical personnel, the search was limited to human studies or combined studies (human/experimental animal) within the target group. The articles that were not included due to this limitation were checked separately for relevance. Any insight relevant to this study is included in the discussion section of this article.

The databases that were used for the search are listed in [Table 2]. An expert search (expanded search, advanced search) was performed to search the databases. Boolean operators, truncation, and search phrases were also used.

Table 2 Selected databases.

Database	URL	Type of database
PubMed	https://pubmed.ncbi.nlm.nih.gov/	Medical database with articles from the entire field of biomedicine (access to MEDLINE)
Cochrane Library	https://www.cochranelibrary.com/	Online library includes three scientific databases (systematic reviews, Central Register of Controlled Trials, and Cochrane Clinical Answers)
ClinicalTrials	https://www.ClinicalTrials.gov/	Database of clinical studies of the U.S. National Library of Medicine

The general PICO scheme was modified to obtain a suitable search matrix for the underlying questions ([Table 3]).

Table 3 Modified PICO scheme for this study.

P	Population	Which population is being examined?	Employees (particularly in the health care industry)
I	Intervention: In this case exposure	What kind of exposure is described?	Electromagnetic fields, MRI
O	Outcome, in this case: Effects	Effects to be observed after exposure to electromagnetic fields	Effects (also long-term effects), impairment

A collection of thematically relevant key words were used for the search. Synonyms and abbreviations were taken into consideration.

All search terms were entered either as an MeSH term (e.g., “Cognition Disorders”[MeSH]) or as a term or phrase in the title/abstract (e.g., “Cognition*”[Title/Abstract]). Some MeSH terms were entered with the limitation “No Exp” for “no exploded” (e.g., “health personnel”[Mesh:NoExp]). In this case, only a search for the MeSH term itself and not its subterms was performed.

The individual search blocks from [Table 4] were then linked with the Boolean operator AND. After linking of the three search blocks, the PubMed search yielded 6428 hits. After restricting the language (1) and target group (2), 5372 hits remained for further analysis.

Table 4 Compilation of search terms (Pubmed).

	No.	Query	Hits
P	#1	"Occupational Medicine"[MeSH] OR "Occupation*"[Title/Abstract] OR "Occupational Diseases"[Mesh:NoExp] OR "Occupational Exposure"[MeSH] OR "Staff*"[Title/Abstract] OR "personnel*"[Title/Abstract] OR "Radiologists"[MeSH] OR "Medical Laboratory Personnel"[MeSH] OR "physicians"[Mesh:NoExp] OR "nurses"[MeSH] OR "medical staff"[MeSH] OR "nursing staff"[MeSH] OR "personnel, Hospital"[Mesh:NoExp] OR "Health personnel"[Mesh:NoExp] OR "Occupational Health"[MeSH] OR "Health occupations"[Mesh:NoExp] OR "employment*"[Title/Abstract] OR "workplace*"[Title/Abstract] OR "workstation*"[Title/Abstract]	872419
I	#2	"Magnetic Resonance Imaging"[Mesh:NoExp] OR "fMRI"[Title/Abstract] OR "Magnetic Resonance*"[Title/Abstract] OR "MR Tomograph*"[Title/Abstract] OR "NMR Imaging*"[Title/Abstract] OR "NMR Tomograph*"[Title/Abstract] OR "MRI"[Title/Abstract] OR "Magnetic Fields"[MeSH] OR "Magnetic Field*"[Title/Abstract] OR "Electromagnetic Field*"[Title/Abstract] OR "Electromagnetic Radiation"[MeSH] OR "Electromagnetic Radiation*"[Title/Abstract] OR "magnetic resonance"[Title/Abstract]	1079485
O	#3	"Cognition Disorders"[MeSH] OR "Cognition*"[Title/Abstract] OR "Cognition"[MeSH] OR "Cognitive*"[Title/Abstract] OR "Sensation Disorders"[MeSH] OR "sensitivit*"[Title/Abstract] OR "senes*"[Title/Abstract] OR "Sensation*"[Title/Abstract] OR "Sensor*"[Title/Abstract] OR "hearing*"[Title/Abstract] OR "Tinnitus"[Title/Abstract] OR "smell*"[Title/Abstract] OR "taste*"[Title/Abstract] OR "metallic*"[Title/Abstract] OR "Phosphenes"[MeSH] OR "phosphene*"[Title/Abstract] OR "light phenomen*"[Title/Abstract] OR "eye-hand*"[Title/Abstract] OR "Dysgeusia"[Title/Abstract] OR "vision*"[Title/Abstract] OR "visual*"[Title/Abstract] OR "Dizzi*"[Title/Abstract] OR "Dizzy*"[Title/Abstract] OR "Vertigo"[MeSH] OR "Vertigo*"[Title/Abstract] OR "spinning*"[Title/Abstract] OR "Nausea"[MeSH] OR "Nausea"[Title/Abstract] OR "Neurocognitive Disorders"[MeSH] OR "Neurocognitiv*"[Title/Abstract] OR "Sleep Disorders, Circadian Rhythm"[MeSH] OR "Sleep*"[Title/Abstract] OR "nerve stimulation*"[Title/Abstract] OR "tactil*"[Title/Abstract] OR "tissue heating*"[Title/Abstract] OR "neuropsychological Tests"[MeSH] OR "neuropsychological Tests"[Title/Abstract] OR "Embryonic Development"[MeSH] OR "embryonic development*"[Title/Abstract] OR "Congenital Abnormalities"[MeSH] OR "malformation*"[Title/Abstract] OR "Pregnancy"[MeSH] OR "pregnan*"[Title/Abstract] OR "Fertility"[MeSH] OR "Fertil*"[Title/Abstract] OR "fetal development*"[Title/Abstract] OR "fetal development"[MeSH] OR "teratogen*"[Title/Abstract] OR "Neoplasms"[MeSH] OR "Neoplasm*"[Title/Abstract] OR "cancer*"[Title/Abstract] OR "carcinog*"[Title/Abstract] OR "Blood Circulation"[MeSH] OR "Blood Circulation*"[Title/Abstract] OR "blood flow*"[Title/Abstract] OR "adverse effects"[sh] OR "adverse effect*"[Title/Abstract] OR "Time Factors"[MeSH] OR "limit value*"[Title/Abstract] OR "specific absorption rate*"[Title/Abstract]	11083102

There were 571 hits in the Cochrane Library and 1494 in ClinicalTrials.gov. Combining all three databases excluding duplicates yielded a total of 7273 hits. The title and abstract of these studies were then screened and reviewed for relevance. After the title/abstract screening, 134 studies were selected for full text screening ([Fig. 1]). Cited studies and internet sources were included in the further course of the search.

Fig. 1 Flowchart of the literature search (* = appendix 1; ** = appendix 2).

Results and discussion

Effects of static, low-frequency, and movement-induced magnetic fields

Strong static magnetic fields are capable of penetrating the human body virtually unhindered. Thus, electrodynamic interactions can have an effect on charged moving particles in the body [15] [16]. Charged particles that can be influenced magnetohydrodynamically by these interactions [15] are also found in the bloodstream. Kinouchi et al. provided a theoretical approach in the year 1996 with the help of the finite element analysis [15]. It was calculated in this study that an approximate decrease in blood volume flow of 5% or 10% can be expected at flux densities of 10T and 15T [15]. The results also show that voltages in the aorta induced by blood flow can propagate into the heart and could disrupt autonomic cardiac function [15] [17]. In the year 2003, Chakeres et al. performed 14 measurements on 25 people at different locations in the vicinity of an 8T MRI scanner inside and outside the magnetic field (high-frequency electromagnetic fields were not used) [18]. Five measurements were performed inside the magnetic field at locations corresponding to different field strengths (8; 6; 4.5; 3, and 1.5 T). Various vital functions (heart rate, electrocardiogram (EKG), systolic and diastolic blood pressure) were measured with the help of a monitoring system. The oxygen saturation and body temperature were also measured. The only statistically significant change that was identified was a slight, clinically insignificant increase in systolic blood pressure at 8T [18]. The other measured vital functions did not show any significant, clinically relevant changes in relation to exposure to different field strengths [18]. These results are in agreement with the data from Kangarlu et al., who were not able to detect any significant cardiac and cognitive effects in both pigs and human volunteers at a field strength of 8T [19]. A more recent study by Bongers et al. from the year 2018 showed that long-term exposure to static magnetic fields might be associated with the development of high blood pressure among workers manufacturing MRI devices [20]. In this study, the first and last available blood pressure measurements of workers (n = 538) were linked to the modeled cumulative exposure to static magnetic fields (facility-related exposure matrix and individual job histories). The study came to the conclusion that high cumulative exposure to static magnetic fields can result in the development of high blood pressure [20]. The strength and intensity of the exposure had a greater effect on the risk of developing high blood pressure than the total duration of exposure [20]. In this connection and in light of the constant increases in the strength of static magnetic fields in MRI, additional studies are needed to confirm the results of this study and any possible long-term effects.

Time-varying, low-frequency magnetic fields (100–1000 Hz) and movement in a static magnetic field as well as movement along a field gradient can induce eddy currents [21] [22] [23]. In the case of constant movements (constant speed of movement), the strength of the induced electrical fields in the body can be estimated [24]. There are natural field strengths from 5–50 mV in the human body [25]. The induction of electrical fields exceeding certain threshold values can thus result in sensory effects and health risks [25]. Furthermore, the interaction of strong static magnetic fields with moving, charged particles in the fluids and cells of the body can result in temporary sensory disruption. This is the result of magnetic induction due to the development of Lorentz forces. In a static magnetic field, it is assumed that Lorentz forces act, for example, on ionic currents in the vestibular endolymph fluid and in the hair cells [3] [26]. [Table 5] shows the frequency of maximum sensitivity (maximum effect) for certain physiological effects. Schaap et al. examined the occurrence of temporary symptoms in 361 employees in 14 hospitals and research facilities [27]. The scanner strength ranged from 0.5 to 11.7T. The study showed that defined symptoms (vertigo, nausea, tinnitus, magnetophosphenes, and metallic taste) associated with exposure to static magnetic fields occurred in 16–39% of work shifts. The symptoms correlated positively with an increasing magnetic flux density. Vertigo, which can present a safety risk, was observed in 6% of employees [7]. In 2015, Schaap et al. published a study on the exposure of MRI employees to magnetic fields and the occurrence of vertigo [28]. In this study, the exposure was not estimated but rather was calculated with wearable magnetic field dosimeters. The clearest connection between vertigo and exposure was seen in the case of movement-induced time-varying magnetic fields [28]. However, there are also studies that have shown that subjects experience vertigo even without movement in the MRI scanner [29] [30], which can be caused by ionic currents in the endolymph in the semicircular canals [3] [26] [30] [31]. Particularly when the presence of an employee is required during a medical intervention, episodes of vertigo present a risk for the employee as well as for the patient [3] [32]. In light of the constant increases in the magnetic flux densities of MRI systems, an increase in related symptoms can also be expected [27].

Table 5 Frequency of maximum sensitivity to certain physiological effects in the low-frequency range (modified according to FB 400-D).

Frequency of max. sensitivity	Physiological effect	Interaction site
˂˂ 1 Hz	Metallic taste sensations	Taste receptors of the tongue (changes in ionic gradients)
˂ 0.1–2 Hz	Vertigo, nausea Electric fields in tissue induced by blood flow	Inner ear (vestibular apparatus) Irritation of nerves and muscles (disruption of autonomic cardiac function)
~ 20 Hz	Magnetophosphenes	Retina
~ 50 Hz	Tactile and painful sensations Loss of muscle control Impaired autonomic cardiac function	Peripheral nerves Peripheral nerves, muscles Heart

The effects mentioned above are summarized as sensory effects. They can disrupt sensory organs and cause minimal changes in brain function among employees. However, in general, they are generally considered harmless since they are usually very brief. The health effects include the stimulation of nerve and muscle tissue at higher field strengths. The frequency of the maximum sensitivity for peripheral nerve and muscle stimulation is approximately 50 Hz. At a frequency of 50 Hz, the international basic threshold value is an electrical field strength of 20 mV/m [25]. Starting at a threshold of 50 mV/m, phosphenes are released and starting at electrical field strengths of 4000–6000 mV/m, irritation of the peripheral nerve cells and muscle cells occurs [25]. Starting at approximately 12,000 mV/m, cardiac function can be impaired (additional contractions and even ventricular fibrillation) [33].

Acute effects of electromagnetic fields on cognition and behavior

The acute effects of electromagnetic fields on cognition and behavior are summarized in [Table 6]. While eye-hand coordination was affected in the first study by De Vocht et al. [34], coordination speed was reduced in a second study [35]. These differences could be affected by exposure differences or also a relatively small test group size. This study also showed that there are exposure-effect relationships for visual and auditory working memory, eye-hand coordination speed, and visual tracking tasks. It was unclear whether the effects on neurological behavior are triggered in the majority of cases by the static magnetic field or the speed of movement within the stray field [36]. In contrast, a study by Chakeres et al. was not able to show a relationship between exposure to static magnetic fields of 0.05T and 8T and cognitive function [37]. Not only employees working with MRI but also those involved in the manufacture of such devices have high levels of exposure to the described electromagnetic fields. In a study of people manufacturing and installing MRI systems, De Vocht et al. were able to show that the occurrence of vertigo, concentration problems, metallic taste, and tinnitus was significantly higher but cognitive function was not affected [38]. Since the cognitive tests were performed immediately before and after a shift, De Vocht et al. concluded that cognitive impairment is only of an acute and temporary nature and disappears relatively quickly following exposure [38]. A further study by Vocht et al. showed mild effects on the visual sensory domain and hand-eye coordination in test persons in the immediate vicinity of the MRI system, but this was not significant with respect to the control group [39]. The studies by Van Nierop et al. essentially showed that movement in the static magnetic field had a negative effect on concentration, memory, attention, and visual acuity [40] [41].

Table 6 Acute effects of electromagnetic fields on cognition and behavior.

Field strength	Literature source	Cognitive effects
0.7T Static magnetic field with and without movement of the subject	De Vocht et al. [37]	4% reduction of speed and precision 16% reduction of visual contrast sensitivity at close range
Scatter field of 0.6–1 T for 1.5T and 3T MRI	De Vocht et al. [38]	Negative exposure-effect relationships for visual and auditory working memory (eye-hand coordination speed and visual tracking tasks)
Static magnetic field of 0.05T and 8T (Without movement)	Chakeres et al. [42]	No relationship between exposure to a static magnetic field and cognitive ability
Variable	De Vocht et al. [35]	Vertigo, trouble concentrating, metallic taste, and tinnitus significantly more common in the exposure group Number of defined symptoms significantly higher with an increased duration of exposure, magnetic flux density, and speed of movements No significant impairment of cognitive ability like motor response
1600 mT, 800 mT, and 0 mT (static and induced time-varying magnetic fields)	De Vocht et al. [36]	Slight and insignificant effects on the visual-sensory domain and eye-hand coordination
Head movement in the scatter field of a 7T scanner at 0.5T and 1T or without exposure at 0T	Van Nierop et al. [43]	Negative effect on concentration and attention as well as impairment of visual-spatial orientation Effect on attention and concentration particularly in the case of high working memory performance
Head movement in the scatter field of a 7T scanner (1T in front of the bore of a 7T scanner with or without 2.4T/s motion-induced exposure)	van Nierop et al. [44]	Static magnetic fields in combination with motion-induced, time-varying magnetic fields significantly affect verbal memory performance and visual acuity Attention and concentration negatively affected Sole exposure to a static magnetic field did not show any significant effects

Effects of long-term exposure to static and low-frequency fields

There are only a few studies or minimal data regarding the long-term effects of occupational exposure to strong static magnetic fields [45]. When analyzing acute effects in relation to neurocognition, neurobehavior, and sensory effects, it is necessary to examine whether regularly occurring reactions could result in long-term impairment [46]. In a retrospective cohort study, Bongers et al. examined the effect of occupational exposure to strong static magnetic fields in a manufacturing facility for MRI devices [46]. The goal of this study was to examine the relationship between exposure to strong static magnetic fields and the accident risk for employees. A connection between exposure to static magnetic fields and an elevated accident risk was seen. In addition, the occurrence of accidents or near accidents on the way to work (less on the way home) was also dependent on occupational exposure and recent exposure to static magnetic fields. Huss et al. confirmed this observation among radiology assistants [47]. An elevated risk for commuting accidents was seen in this study when study participants when study participants worked more frequently on or near an MRI device in the year before the accident. The risk increased with an increase in the number of exposure days per year. In addition, a higher magnetic flux density resulted in an increase in the risk. A limiting factor of this study was the low return rate of the questionnaire (~ 30%) and the possibility that persons had accidents in the time period prior to the study period but were categorized as accident-free in the study.

Huss et al. showed that sleep quality among other factors could be a reason for the previously observed increase in accident risk [48]. Employees in the scanner room during image acquisition also reported an increase in sleep disturbances.

Pregnant employees in clinical MRI

There are a number of studies examining the benefits and risks of MRI examination of pregnant patients [3] [49] [50] [51].

However, in relation to long-term effects and safety for pregnant employees in the field of MRI, the study by Kanal et a. from the year 1993 is often the only study cited [42] [43]. In this study, a survey of employees at MRI facilities was used to record various parameters like duration of pregnancy, premature births, miscarriages, birth weight, cycle duration, etc. [42]. 1915 questionnaires were included in this study and 1421 pregnancies (in 770 women) were registered. Of the 1421 registered pregnancies, 280 involved employees who were magnetic resonance imaging workers at the time of pregnancy. Kanal et al. concluded that there are no particular deviations regarding pregnancy parameters, i.e., no increased risk for pregnant employees and their unborn children [42]. This study is often cited in connection with risks in the field of MRI with respect to pregnant employees [44] [51] [52] and in national and international regulations [21] [53]. According to these regulations, it is not recommended for pregnant employees to be present in the scanner room. However, working in the control room is not prohibited as cited by the German Commission on Radiological Protection in their report from 2003 [54] [55]. Mühlenweg et al. point out that the lack of limit values results in pregnant employees being allowed to enter the MRI room in many hospitals and practices when scans are not being performed based on the recommendation of standard IEC 60601–2-33:2010/A2 [54]. In the USA, according to the “ACR Guidance Document on MR Safe Practices: 2013” by Kanal et al., pregnant employees are allowed to work in the scanner room even during scans during the entire pregnancy [53].

Epidemiological studies

There is no explicit epidemiological data for the field of clinical MRI. This was also explicitly noted by Bongers et al. in a retrospective study from the year 2014, which examined the health consequences of long-term exposure to static magnetic fields [56]. In 2005, Feychting et al. stated the need for studies on the long-term effects of exposure to static magnetic fields [45]. Epidemiological studies regarding chronic exposure to static magnetic fields have also been recommended by other organizations [16] [57] [58]. Low-frequency fields have been repeatedly connected to neurodegenerative diseases (amyotrophic lateral sclerosis (ALS), Alzheimerʼs, Parkinson's). However, the results are inconclusive [59] [60] [61] [62] [63]. Low-frequency magnetic fields have continued to be categorized by the International Agency for Research on Cancer (IARC) of the World Health Organization (WHO) as class 2B “possibly cancer-causing” based on the results of epidemiological studies showing an elevated risk for pediatric leukemia at magnetic flux densities of over 0.3–0.4 µT [64] [65]. However, the mechanism of action is currently not known, and the results could not be confirmed in animal experiments [64] [65].

Conclusion

Magnetic fields can result in sensory and cognitive disturbance. However, this disturbance is typically transient. A possible predisposition for high blood pressure and sleep disturbances were shown as long-term effects. Pregnancy parameters in pregnant employees do not deviate from the standard. However, there are only very few publications on the long-term effects on pregnant employees. Thus, there is a significant need for research here.

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