Oral complications associated with metal ion release from oral piercings: a systematic review

Purpose This systematic review explored dental complications associated with metal ion release from oral piercings using the Preferred Reporting Items for Systematic Reviews and Meta-analyses guidelines. Methods Item retrieval from October 2022 to December 2022 from databases, such as Cochrane Central Register of Controlled Trials, Medline, PubMed, Embase, Scopus and Web of Science, using predefined search terms was undertaken by two independent reviewers. Data were extracted and risk of bias was assessed using the Joanna Briggs Institute (JBI) critical appraisal checklist. From 1509 identified studies, 25 were included for analysis. Results Of the 25 studies, 20 included both clinical examination and questionnaire-based data. The remaining five studies were deemed low quality based on the Joanna Briggs Institute criteria. The average time piercings were worn ranged between 5 and 48 months. Most studies did not investigate complications from metal ion release. Only two studies examined the direct effects of metal ion release and showed that metal ions may cause hypersensitivity reactions and mucosal changes. Other soft tissue complications were reported, with gingival recession noted in 16 out of 25 studies, especially due to lip piercings. Studies reporting other complications were as follows: swelling (9), pain (8), infection (6), bleeding (6), inflammation (5), alterations to speech, eating and/or swallowing (5), changes to taste or metallic taste (5), and mucosal changes (4). Ten studies reported tooth chipping from tongue piercings. Conclusion Oral piercings leach metal ions into surrounding tissues which may cause local mucosal changes. Furthermore, oral piercings cause damage to both soft and hard oral tissues, particularly gingival recession for lip piercings and tooth chipping for tongue piercings. Thus, to prevent such adverse injuries, dental professionals should discourage patients against oral piercings. Supplementary Information The online version contains supplementary material available at 10.1007/s40368-023-00831-0.


Introduction
Oral piercings are a form of body jewellery that are inserted into the oral or peri-oral tissues (Ziebolz et al. 2009).They have a long history, having been practised in diverse ancient cultures as part of ceremonial and religious practices (Vozza et al. 2014;Hennequin-Hoenderdos et al. 2016;Chadwick et al. 2005;Covello et al. 2020).However, over the last two decades, oral piercing has evolved into a common practice amongst young people in the Western world (Ziebolz et al. 2009;Vozza et al. 2014;Chadwick et al. 2005) with approximately 5.2% of young adults having oral piercings (Hennequin-Hoenderdos et al. 2016).Oral piercings are placed into the tongue, lips, cheeks or frena (Chadwick et al. 2005;Levin et al. 2005).Tongue piercings are commonly a barbell, with balls at either end of a rod, whilst lip piercings may be a ring or a labret, which is a rod with one ball and one flat disc (Ziebolz et al. 2009;Chadwick et al. 2005;Levin et al. 2005).
Common short-term complications after placing an oral piercing include pain, swelling of the site, and secondary bleeding (Ziebolz et al. 2009;Chadwick et al. 2005;Levin et al. 2005;Inchingolo et al. 2011).These problems are often self-limiting and of short duration.Erythema and haematoma can also occur, whilst tongue oedema may cause airway obstruction (Ziebolz et al. 2009;Levin et al. 2005).Changes to speech, swallowing patterns and mastication have also been reported (Kapferer et al. 2010;Firoozmand et al. 2009;Vieira et al. 2011).Less frequently, the generation of a galvanic current flow between barbell tongue piercings and metal dental restorations has been noted (Chadwick et al. 2005).Long-term complications from oral piercings include damage to gingival tissues, fractures of enamel and dentine, and allergic reactions, especially to nickel (Ziebolz et al. 2009;Hennequin-Hoenderdos et al. 2016;Levin et al. 2005).Abrasion of the enamel, fractures of tooth structure, and gingival recession, particularly affect the mandibular anterior teeth, are common long-term complications (Kapferer et al. 2010;Firoozmand et al. 2009;Kapferer et al. 2012;Vilchez-Perez et al. 2009).
The majority of piercings are made from metal, including surgical-grade stainless steel, titanium, platinum, silver or gold (Ziebolz et al. 2009;Walsh et al. 2008;Masood et al. 2023).When oral piercings come in contact with oral fluids such as saliva, they may corrode and leach out metal ions into the surrounding tissues (Domingo et al. 2019).The released ions can then cause allergic reactions, with nickel reported as the most common allergen (Vozza et al. 2014;Levin et al. 2005;Lupi et al. 2010).Other metals, such as chromium and cobalt, have been also reported to cause hypersensitivity reactions (Domingo et al. 2019;Lupi et al. 2010).Surface defects on the piercing surface may be a location where corrosion begins (Domingo et al. 2019).In addition to causing local reactions in the oral mucosa, released ions may enter the systemic circulation.Systemic complications of oral piercings include bacteraemia and infections at distant sites, including infective endocarditis and brain abscesses (Domingo et al. 2019).Whether other systemic reactions, including toxicity from released heavy metals, occurs from oral piercings is unclear.
Despite a range of serious complications caused by leaching of metal ions from oral piercings, no reviews of the literature on this topic have been conducted.A recent systematic review examined only the complications of oral piercings on hard and soft tissues (Passos et al. 2022).Therefore, the aim of this review is to investigate the oral complications as a result of metal ions released from oral piercings.The null hypothesis for this review is that the oral complications will be associated with the release of the metal ions from oral piercings.

Protocol and registration
This systematic review used The Preferred Reporting Items for Systematic Reviews and Meta-analysis (PRISMA) guidelines (Page et al. 2021).The protocol for this review was registered on PROSPERO (CRD42022336112).

Eligibility criteria, screening and selection
The eligibility for inclusion was based on the PICO criteria as described in Table 1 with (P) human participants; (I) intervention or oral metal piercings used; (C) comparison: allergy or hypersensitivity reactions and/or ion release from oral piercings; (O) outcome: incidence of hard and soft tissue injuries/complications from oral piercings and incidence of dental complications from metal ion release from oral piercings.The PICO research question for this systematic review was "Is there an association between metal ions released from oral piercings and oral complications?"

Search strategy
Cochrane Central Register of Controlled Trials (CENTRAL), Medline (via EbscoHost), PUBMED (National Library of Medicine), Embase (via Elsevier), Scopus and Web of Science databases were searched using combinations of the following key terms: (mouth* OR oral OR lip OR tongue OR labial OR buccal OR frenulum OR mucosa OR gingiva AND (piercing* OR body piercing OR jewellery (disease OR injury OR Adverse material reactions/hypersensitivity Incidence of dental complications from metal ion release from oral piercings Reviews, abstracts, letters to the editor, editorials Study design: Nonrandomised control trials, cohort studies and case-control studies Publication year: no restrictions Language: papers in English or with English-language abstract available complications) AND (allergy OR toxicity OR adverse reaction OR hypersensitivity) AND (release of metal ions OR metal ion release OR metal ions).The search was conducted from October 2022 to December 2022.Additional hand searches of article reference lists as well as Google and grey literature searches were conducted using the same keywords to identify literature not accessible via standard databases, as given in the supplemental data table.

Data collection and analysis
Studies reporting complications from oral or perioral piercings were identified.After screening of titles and abstracts, the reference lists of applicable studies were examined to identify any additional sources.The studies were imported into End-note™ software (Clarivate, U.S.A), and duplicate articles were removed.The first level of selection was undertaken using titles and abstracts, by applying the inclusion and exclusion criteria outlined in Table 1.Subsequently, full text versions were retrieved, and a second level of selection was performed, using the same criteria.Study characteristics included in the data collection forms were as follows: author/s, year published, country where research was undertaken, study design, total number of subjects, participant characteristics (gender, mean age, type of piercing, mean period piercing worn), postpiercing oral complications, whether metal ion release was reported, conclusions and key findings.These findings were tabulated using Excel spreadsheets.For synthesis, studies were grouped into whether metal ion release was reported or not.Inter-rater reliability between the two independent assessors (M.M and S.Z) during the data extraction stages (identification, screening, eligibility, and inclusion) was calculated as a percentage.Inter-rater reliability agreement for selection and outcome was evaluated using Cohen's kappa using the Statistical Package for the Social Sciences version 24.0 software (IBM Corp., Armonk, NY, USA).

Risk bias assessment reporting
The Joanna Briggs Institute (JBI) critical appraisal checklist for non-randomised experimental studies was used to rate the studies in terms of their risk of bias (Porritt et al. 2014).Two independent reviewers (M.S and S.Z) screened the articles, and any discrepancies were resolved by discuss with the third author (L.W).

Literature results
From the database searches, a total of 1506 articles were identified, whilst three additional articles were found via hand-searching and checking reference lists.During the first level of selection, 254 duplicates were removed, and 1155 records excluded due to irrelevant titles and/or abstracts.A total of 100 papers were screened for eligibility.Case reports and series were excluded (n = 53) and articles with participants of mean age above 25 years of age were excluded (n = 17).This resulted in 30 articles that met the second level of inclusion criteria for this review.
From the 30 articles selected for inclusion, 5 articles were excluded when applying the selection criteria and through discussion amongst the reviewers.Three articles included only English abstracts.For these, it was difficult to assess study methodology against the JBI criteria, and so they were excluded.Two articles were not included due to being irrelevant, with one discussing Candida infections and another looking solely at temporomandibular disorders, which is outside the inclusion criteria.This reduced the final number of studies to 25.
The Preferred Reporting Items for Systematic Reviews and Meta-analysis (PRISMA) flowchart is shown in Fig. 1.No papers reported an objectionable risk of bias.

Inter-rater reliability agreement
The inter-rater reliability percentages for the two assessors were as follows: identification 98.8% (1509/1527 studies), screening 98.4% (1255/1276 studies), eligibility 100% (100/100 studies) and inclusion 83.3% (25/30 studies).It was agreed that two studies discussed the outcome of complications related to metal ion release from oral piercings.Discrepancies were resolved via discussion and agreement reached.The kappa scores were as follows: for inclusion 76.09% agreement (kappa 0.516) and for outcome 96.15% agreement (kappa 0.8999).

Outcomes from included studies
The included studies consisted of 14 cohort, 6 case-control and 5 cross-sectional studies.Three studies were published between 2020 and 2015, 12 studies between 2014 and 2009 and 10 studies, 2008 and 2003.From the 25 included studies, the greatest number of articles published was from Brazil (n = 4).Other locations studies for studies are shown in Table 2.
The majority of the studies included had more female participants than males, and only three studies had more male participants than females (Levin et al. 2005;Firoozmand et al. 2009;Campbell et al. 2002).One study examined only male participants (Ziebolz et al. 2012) and one study did not specify the gender distribution of subjects (Stead et al. 2006).In terms of the mean age of participants, the most common age was 22 years old (n = 6) and the youngest mean age was 14 years old (Domingo et al. 2019).There were 7 studies that examined tongue piercings only, whilst 3 examined lip piercings only, and 15 studies examined both tongue and lip piercings (Table 2).Five studies examined piercings in other oral locations such as the cheek or frenum in addition to tongue and lip piercings.The average period that piercings were worn ranged between 5 and 48 months.
In terms of post-piercing oral complications, reported soft tissue problems included damage to gingival tissues, and mucosal changes, such as atrophy, hyperplasia or local lichenoid reactions.Hard tissue complications were toothrelated, such as fracture or chipping.Gingival recession was the most common soft tissue complication reported in 16 out of 25 studies.Tooth fracture or chipping was noted in 10 studies.Other commonly reported complications included: swelling (n = 9), pain (n = 8), infection (n = 6), bleeding (n = 6) and inflammation (n = 5).Alterations to speech, eating and/or swallowing were noted in five studies.Changes to taste, or a metallic taste were reported in five studies.Four studies reported mucosal changes or atrophy from oral piercings.
Most studies did not report complications resulting from metal ion release.Only two studies examined the direct effects of metal ion release on surrounding oral tissues (Domingo et al. 2019;Lupi et al. 2010).One study explored different piercing materials, such as titanium, stainless steel and Teflon, in terms of the rate of gingival recession and tooth chipping from these various types of oral piercings (Hickey et al. 2010).

Discussion
This systematic review aimed to examine the incidence of hard (teeth) and soft tissue complications relating to oral piercings, with a particular focus on complications caused by metal ion release.To the author's knowledge, this is the first systematic review that examines metal ion release from oral piercings and the subsequent complications.The results of this review showed that metal ion release can occur from oral piercings when subject to the oral environment.They may corrode and release metal ions into surrounding oral tissues, causing local soft tissue reactions.Oral piercings are made from a variety of metals, such as surgical stainless steel, titanium, platinum, or gold, as mentioned above (Masood et al. 2023).Two included studies examining metal ion release investigated piercings made from surgical stainless steel only (Domingo et al. 2019;Lupi et al. 2010).Stainless steel piercings were found to cause a high incidence of tooth chipping (Hickey et al. 2010).One study that examined different oral piercing materials showed that titanium piercings cause greater gingival recession (Hickey et al. 2010).Teflon or acrylic piercings showed lower levels of dental complications, and the change in composition avoided the problem of metal allergy (Hickey et al. 2010;Dougherty et al. 2005).
Complications caused by metal ion release were reported by two studies (Domingo et al. 2019;Lupi et al. 2010); Domingo et al. (2019) examined both lip and tongue piercings, and reported the presence of metal particles, such as aluminium, tungsten and molybdenum, in keratinocytes at sites where the oral mucosa was pierced.Lupi et al. (2010) investigated only tongue piercings, and noted concentrations of iron, nickel, and chromium in tongue mucosal keratinocytes.These metal ions may exert local cytotoxic effects on keratinocytes (Lupi et al. 2010), which may result in local mucosal changes, such as atrophic, "hyperplastic, leukoedematous, erythematous, and/or erosive lesions" (Domingo et al. 2019).Interestingly, the rate of metal ion release is also influenced the surface quality of the piercings, where surface defects can be a site of metal corrosion (Masood et al. 2023;Domingo et al. 2019); Domingo et al. (2019) noted surface defects on both used and unused piercings.
Of the 25 articles included for analysis, there were no articles published prior to 2002 that examined lip or tongue piercings and related dental complications.The majority of the included studies had more female participants than males, indicated a higher prevalence of oral piercings in females (Walsh et al. 2008;Dougherty et al. 2005;Kapferer et al. 2007;Samoilenko et al. 2019;Simoes et al. 2014;Tomaževič et al. 2017).There may also be a higher willingness of females to participate in studies, and they may seek oral health input more readily than males (Dougherty et al. 2005;Kapferer et al. 2007).
The included studies generally reported that tongue piercings cause significantly more dental complications than lip piercings (Ebrahim et al. 2008).Pain, difficulty speaking and eating problems were reported more often with tongue piercings (Kapferer et al. 2010;Firoozmand et al. 2009;Vieira et al. 2011).These were similar findings to the 2022 systematic review by Passos et al.Immediately after piercing placement, common complications included pain, swelling, bleeding and irritation (Kapferer et al. 2007;Samoilenko et al. 2019;Ebrahim et al. 2008).One study showed that 86% of subjects with oral piercings experienced these complications (Kapferer et al. 2007).Pain was reported to occur in between 58.3 and 69% of cases and swelling in between 47.2 and 52% of cases (Kapferer et al. 2007;Samoilenko et al. 2019).Furthermore, mucosal changes were reported in 6 of the 25 studies included for analysis.Atrophy or depapillation around the oral piercing was the most common mucosal change with tongue piercings (Oberholzer et al. 2010).Hyperplasia or tissue overgrowth at the pierced site was seen mainly in tongue piercings, at a prevalence of 16.2% to 33.3% (Vieira et al. 2011;Samoilenko et al. 2019).Complete resolution was achieved when the piercings were removed (Vieira et al. 2011).
Most studies showed that tongue piercings are associated with tooth injuries such as chipping or fractures (Firoozmand et al. 2009;Ziebolz et al. 2012;Oberholzer et al. 2010).The study by Tomaževič et al. (2017) showed that dental damage of any type, such as enamel fractures, enamel-dentin fractures, and complicated crown-root fracture, occurred twice as frequently in people with tongue piercings (76.5%) compared to community controls (32.1%).About 59% of people with tongue piercings had enamel fractures (Tomaževič et al. 2017).The majority of teeth with enamel damage (92%) were molars and premolars (Campbell et al. 2002).This may be explained by the habit of patients playing with, biting, or knocking the piercing against their teeth (Campbell et al. 2002).Of subjects with fractured teeth, this habit of playing with the piercing was noted in some 51.6% of cases (Hickey et al. 2010).
Lip or labial piercings cause more gingival recession (Kapferer et al. 2010;Firoozmand et al. 2009;Kapferer et al. 2012;Vilchez-Perez et al. 2009;Plessas et al. 2012).As such, labial piercings have been shown to be more damaging to periodontal tissues (Kieser et al. 2005;Lopez-Jornet and Camacho-Alonso 2006;Slutzkey et al. 2008).In contrast, Pires et al. (2010) noted that subjects with tongue piercings are at 11 times increased risk of developing lingual anterior gingival recession.This is supported by Dougherty et al. (2005) who reported that tongue piercings were commonly associated with the presence of calculus, which may lead to higher levels of periodontal disease.The systematic review and meta-analysis by Passos et al. showed that 33% of individuals with oral piercings had gingival recession.The problem of gingival recession is primarily related to the position of the piercing.Studies examining this issue showed that piercings placed at the CEJ caused a greater rate of buccal gingival recessions, (Kapferer et al. 2007) whilst lip piercings placed coronally to the CEJ had a lower incidence of lower lip buccal recession (Kapferer et al. 2012).This important finding regarding piercing placement is something which body piercing professionals should consider when advising patients about possible long-term complications.
The rate of oral complications may be related to piercing length and the wear period.The barbell rod or stem length on tongue piercings appears to be directly proportional to the risks of gingival recession and tooth chipping (Campbell et al. 2002).Longer stems cause more recession due to the greater ease of the barbell piercing coming into direct contact with the gingival tissues (Campbell et al. 2002;Hickey et al. 2010).Similarly, several studies also reported a higher prevalence of gingival recession and tooth chipping with longer wear periods (Campbell et al. 2002;Plessas et al. 2012;Ebrahim et al. 2008).Interestingly, one study found that the greatest incidence of complications occurred within 2 years and involved 57.6% of cases (Lopez-Jornet and Camacho-Alonso 2006).
Multiple studies reported limitations to their study design.The main limitation reported was convenience sampling, where the participants were recruited specifically for participation in the study (Stead et al. 2006;Dougherty et al. 2005;Kieser et al. 2005;Ebrahim et al. 2008).Some studies did not have a control group (Domingo et al. 2019;Plessas et al. 2012), which prevents comparisons with the experimental group.Lastly, the majority of studies included a questionnaire in the study design, with four studies relying solely on the information collected from the survey to draw conclusions (Kapferer et al. 2010;Stead et al. 2006;Hickey et al. 2010;Ebrahim et al. 2008).Memory bias is a key limitation that may influence the results from questionnairebased studies (Stead et al. 2006;Kapferer et al. 2007;Pires et al. 2010).Despite these limitations, the included studies have a consistent and recurring message that oral piercings frequently cause hard and soft tissue complications.Thus, education of patients and increasing their awareness of these risks is imperative, and a key responsibility of healthcare professionals.

Conclusion
The findings of the present systematic review evaluating the oral complications associated with metal ion release from oral piercings reveal the following: -Oral piercings are associated with complications involving hard and soft dental tissues.-Oral piercings leach metal ions into surrounding tissues which may cause local mucosal changes.-Additionally, the evaluated studies showed that tongue piercings are commonly associated with tooth fractures, whilst lip piercings result in a greater incidence of gingival recession.

Fig. 1
Fig. 1 PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-analysis) flowchart for selection of studies

Table 1
Inclusion and exclusion criteria adopted in the literature search

Table 2
Characteristics of included studies