|Year : 2022 | Volume
| Issue : 2 | Page : 81-86
Potential influence of COVID-19 on periodontal and peri-implant health – A review of literature
Rakan S Shaheen1, Layan S Alolayan2, Rayan J Al-Otaibi3, Khalid M Abu Nakha4, Abdulrahman K Alhazmi5, Meelaf S Alshahrani6, Kholood K Al-Huthali5
1 Department of Preventive, Riyadh Elm University, Riyadh, Saudi Arabia
2 College of Dentistry, King Saud Bin Abdulaziz University for Health Sciences, Riyadh, Saudi Arabia
3 Al Farabi College, Riyadh, Saudi Arabia
4 Majmaah University, Al Majma'ah, Saudi Arabia
5 College of Dentistry, Riyadh Elm University, Riyadh, Saudi Arabia
6 College of Dentistry, King Khalid University, Abha, Saudi Arabia
|Date of Submission||03-Dec-2021|
|Date of Decision||15-Jul-2022|
|Date of Acceptance||01-Aug-2022|
|Date of Web Publication||31-Aug-2022|
Dr. Layan S Alolayan
College of Dentistry, King Saud Bin Abdulaziz University for Health Sciences, Riyadh
Source of Support: None, Conflict of Interest: None
Introduction: Coronavirus disease of 2019 (COVID-19) is caused by the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) which manifests with severe respiratory symptoms. The plaque biofilm was shown to harbor SARS-CoV-2 virus and that it could be transmitted via droplets. It has been hypothesized that COVID-19 could have an influence on periodontal and peri-implant health.
Aim: This review was done to theoretically study the literature for reports that link COVID-19 to periodontal and peri-implant health.
Materials and Methods: The review was done on articles published on the Medline and Saudi Digital Library databases, and included case reports, original papers, reviews, and any other reports that link COVID-19 to periodontal and peri-implant health.
Results and Discussion: Commonly shared by COVID-19 and periodontal/peri-implant inflammation, is the increase in the pro-inflammatory mediators such as cytokines, which contribute toward exacerbating the immunological response and elevating the severity of the conditions. Furthermore, the reduced immunity due to COVID-19 can allow the periodontal/peri-implant pathogens to flourish and grow, especially when associated with poor oral hygiene owing to fatigue or bed confinement, and the negligence of maintaining routine periodontal visits due to fear of contracting COVID-19. Nevertheless, no direct cause-and-effect relationship between the SARS-CoV-2 virus and periodontal/peri-implant conditions has been ascertained, which warrants the need for further clinical studies on this topic to achieve a better understanding of it.
Conclusion: There is no direct cause-and-effect relationship between the SARS-CoV-2 virus and periodontal diseases, but the similarity of the pro-inflammatory expressions in both diseases poses an indirect risk on periodontal health.
Keywords: COVID-19, oral manifestations, periodontal disease and peri-implantitis
|How to cite this article:|
Shaheen RS, Alolayan LS, Al-Otaibi RJ, Nakha KM, Alhazmi AK, Alshahrani MS, Al-Huthali KK. Potential influence of COVID-19 on periodontal and peri-implant health – A review of literature. Saudi J Oral Sci 2022;9:81-6
|How to cite this URL:|
Shaheen RS, Alolayan LS, Al-Otaibi RJ, Nakha KM, Alhazmi AK, Alshahrani MS, Al-Huthali KK. Potential influence of COVID-19 on periodontal and peri-implant health – A review of literature. Saudi J Oral Sci [serial online] 2022 [cited 2022 Oct 4];9:81-6. Available from: https://www.saudijos.org/text.asp?2022/9/2/81/355226
| Introduction|| |
The coronavirus disease of 2019 (COVID-19) is a saga that commenced on December 31, 2019. It all started when the World Health Organization (WHO) was informed of 27 cases of “pneumonia of unknown etiology” detected in Wuhan City, China. By January 7, 2020, the causative agent of this disease was identified as a respiratory infectious condition caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). The disease spread rapidly and within a couple of months was prevalent in several countries. Consequently, it was declared a global pandemic by the WHO on March 11, 2020. Its routes of transmission have been identified as airborne and human-to-human contact which, if not caught early, causes severe damage to the lungs and other organs in the human body. Furthermore, the initial contact and colonization of the virus cells occur in the oral cavity, nose, and eyes, by projected droplets. The incidence of the viral infection can be determined by performing a polymerase chain reaction (PCR) test on a swab taken from the nose or the oropharynx. In some cases, a dysregulated immune reaction induces the overproduction of early response pro-inflammatory cytokines, such as tumor necrosis factor (TNF), interleukin-6 (IL-6), and IL-1β, resulting in a “cytokine storm.” Subsequently, this raises the risk of vascular hyperpermeability, multi-organ failure, and death. The SARS-CoV-2 targets the lung cells through angiotensin-converting enzyme receptor-2 (ACE-2) which leads to activation of the cytokine storm, immunity suppression, and respiratory epithelium injury. ACE-2 and transmembrane protease serine 2 both exist in salivary glands, facilitating the viral entrance into the cell. However, the clinical symptoms of COVID-19 appear only after an incubation period of approximately 5.2 days, and manifest as fever, fatigue, myalgia, dry cough, sore throat, and/or diarrhea. The main complications that represent a state of severe illness are pneumonia, blood clots, sepsis, septic shock, and acute respiratory distress syndrome. The risk mortality factors include old age, gender, and underlying comorbidities. As reported in the literature, the mean age was 69 years old; the predisposed gender was male representing 70% of deaths, and underlying comorbidity in 48% of the cases. Among these comorbidities, 30% of them had hypertension, 19% had diabetes mellitus, and 8% had heart disease.
Periodontal diseases are defined as those chronic inflammatory conditions that affect the tissues surrounding teeth such as gingivitis and periodontitis. It is known that microbial products produced by the periodontal diseases can spread through the bloodstream affecting other systemic organs. Moreover, those microbial products can augment the development of systemic diseases such as diabetes mellitus, atherosclerotic heart disease, and cerebrovascular disease. Similarly, poor oral hygiene can exacerbate complications of systemic diseases such as diabetes, chronic kidney disease, and liver disease. The main pathogens associated with periodontal diseases such as Porphyromonas gingivalis, Tannerella forsythia, and Treponema denticola, as well as other species such as Prevotella, Desulfobulbus, Selenomona, and Aggregatibacter which manifested in the metagenome of patients severely infected with SARS-CoV-2. In fact, Staphylococcus showed the highest reads, in which 1659 reads were identified, whereas Prevotella showed 493 reads and 463 reads with Fusobacterium. Another study noted that Prevotella, Fusobacterium, and Veillonella are generally associated with severe cases of COVID-19. Poor oral hygiene, age, smoking, diabetes, medication, hereditary, and obesity have been also associated with increased risk of periodontal diseases. Thus, this review was conducted to theoretically investigate and study the current literature for reports that link COVID-19 to periodontal and peri-implant health.
| Materials and Methods|| |
This study was an online review of scientific articles published until the year 2021. The study was conducted from June 2021 to the end of August 2021 after obtaining approval from the institutional review board of a dental college in Riyadh under the registration number SRP/2021/59/453 and the approval number SRP/2021/59/453/439. The research question was “Is there a link between COVID-19 and periodontal/peri-implant health?”. To address the focused question, the MEDLINE/PubMed and Saudi Digital Library databases were viewed and searched using various combinations of the following keywords: “COVID-19,” “periodontal,” “peri-implant,” “gingival disease,” “periodontitis,” “peri-implantitis,” “oral manifestations,” and “SARS-CoV-2.” Inclusion criteria were determined to select all research papers that were found under the categories of “original papers,” “reviews,” and “case reports” that link COVID-19 to periodontal and peri-implant health. All articles included were published as full-text articles in the English language. Exclusion criteria were applied on articles that do not ink COVID-19 to periodontal and/or peri-implant health and non-English articles. Finally, 21 articles were selected in addition to six-related articles.
General oral manifestations
Many systemic viruses manifest themselves in the oral cavity and COVID-19 is not an exception. An observational clinical study done in 2021 by Gomes et al. of 70 participants who tested positive for COVID-19 concluded that the particles of SARS-CoV-2 RNA were found in the dental biofilm of 13 participants. This, therefore, supports the hypothesis that the oral cavity can carry SARS-CoV-2 RNA and aid in its transmission. However, the oral manifestations of COVID-19 patients vary and might include oral pain, desquamative gingivitis, ulcers, and blisters. The literature had previously labeled cutaneous manifestations in 375 cases of COVID-19. Among these, three cases reported intraoral manifestations that vary from ulcers in the palatal mucosa, to localized erythema in the palate and gingival margins. In addition, vesiculobullous lesions, hyposalivation, dry mouth as well as smell and taste dysfunction have also been observed in COVID-19-infected patients. As it is known, the oral cavity is occupied by different types of microorganisms including bacteria that cause pneumonia (i.e., Chlamydia pneumoniae) making patients with periodontal diseases prone to develop pneumonia through aspiration of oral pathogens into the respiratory tract. Not only the aspiration of pathogens but also the secretion of several cytokines from periodontitis can promote adhesion and colonization of respiratory pathogens. It has been reported that symptoms get worse when associated with poor oral hygiene. A randomized controlled trial conducted in Japan examined 417 patients who were provided with oral care after every meal and compared with a control group. They reported that 19% of the control group contracted pneumonia compared with 11% who received oral care. Moreover, the control group was at double risk of postpneumonia mortality in comparison with the group who received oral care. Similarly, a cohort study revealed that the total incidences of pneumonia were significantly reduced over a 12-year follow-up period in patients who received periodontal therapy. There is evidence in the literature that periodontal treatment leads to a fall in the levels of IL-17 in the gingival crevicular fluid (GCF) of patients with periodontal diseases which may aid in reducing the risk of complications. Furthermore, improved oral hygiene can significantly decrease the incidence of ventilator-associated pneumonia in intensive care unit (ICU) patients. A systematic review concluded that for every 10 pneumonia-related deaths among the elderly, one of them can be prevented by improving oral hygiene. This, consequently, highlights the importance of oral hygiene and dental care in reducing the chances of encountering pneumonia-related complications, especially in those over the age of 70.
COVID-19 and periodontal diseases
The interaction between respiratory infections and the oral cavity has been well established by many studies. For instance, patient morbidity due to respiratory infections was 4-fold higher in patients with 10 or more teeth with periodontal pockets than in those without periodontal pockets. Although the exact pathological association between COVID-19 and periodontal disease is not known yet, many proposed theories have shown their reliability. The virus may enter the systemic circulation from periodontal pockets, as they provide a favorable environment for the viral load through GCF, or through periodontal capillaries. Interestingly, like saliva sensitivity, GCF too has shown sensitivity for SARS-CoV-2 detection. Hence, GCF could be a potential mode of transmission, although no direct association between virus levels in GCF and periodontal disease has been established yet. Moreover, alteration in the process of cytokine release has been proposed as one of the major pathological mechanisms between COVID-19 and periodontal diseases. It has been shown that the salivary glands of a COVID-19-infected patient contain ACE-2 receptors higher than in the lungs, which could also indicate that the oral cavity might be a potential reservoir for the virus. Porphyromonas gingivalis, Eikenella corrodens, Fusobacterium nucleatum, Aggregatibacter actinomycetemcomitans, Peptostreptococcus, Clostridium, and Actinomyces are all oral microflora and facultative bacteria that have been known as etiologic agents for periodontal disease and have also been isolated from infected lung fluids. In the presence of comorbidities that are associated with COVID-19 severity (e.g., diabetes mellitus, hypertension, chronic obstructive pulmonary disease, cardiovascular disease, and cerebrovascular disease), the periodontal condition may also be exaggerated consequently. At the same time, periodontal disease could also increase COVID-19 severity, yet this is to be investigated. Furthermore, studies have shown that mortality risk was higher among COVID-19 patients with periodontal disease. Clinically, an association between gingival bleeding and COVID-19 infection was noticed in three cases among different Saudi cities, which also raised the potential negative impact of COVID-19 on the periodontium. As studies have demonstrated a relationship between the severity of COVID-19 and other systemic diseases, it has been hypothesized that a possible association between such a virus and oral diseases, such as periodontitis, may be present. Initially, periodontitis-associated biomarkers may alter the mucosal surfaces to allow for more secretions and expression of receptors that create favorable sites for adhesion and colonization of respiratory pathogens. Two possible mechanisms could explain the association between periodontitis and COVID-19 which are via a direct pathway and/or an indirect one. The direct pathway could be through the high expression of ACE-2 and CD147 receptors in cases of periodontitis that will be used by the virus to infect the cells. The indirect pathway takes place through overexpression of several cytokines and serum levels of IL-1 beta, IL-6, IL-7, IL-10, IL-17, IL-2, IL-8, IL-9, GM-CSF, G-CSF, interferon (IFN)-gamma, TNF alpha, MIP1A, MIP1B, MCP1, and IP10. Not only COVID-19 but also periodontal disease has been recognized as a cytokine storm-generating disease [Figure 1]. In fact, periodontitis can be developed due to pro-inflammatory cytokines induced by periodontopathic bacteria that are, in turn, involved in many respiratory diseases. In addition, Galectin-3, a pro-inflammatory protein that is elevated in cases of severe periodontitis, also showed a correlation with SARS-CoV-2 according to some studies. From another perspective, periodontitis could cause ulceration of the gingiva, reducing the protective function of the oral epithelium, thereby exposing patients to a higher risk of SARS-CoV-2 invasion. It has been reported that periodontitis was associated with a higher risk of COVID-19 complications., A recently published case–control study, done in the State of Qatar, found that periodontitis cases were considerably linked with increased levels of blood biomarkers which may have worsened the COVID-19 outcomes which led to a higher risk of ICU admission, need for ventilation, and even death. Hence, it is safe to say that recent studies have not only found an association between the presence of periodontitis and COVID-19 but also the exacerbation of COVID-19 respiratory distress if periodontitis was manifested. Not only periodontitis but also necrotizing periodontal diseases (NPD) have shown a particular association along with COVID-19. The high bacterial loads of Prevotella intermedia, a major etiological bacterial species for NPD, were manifested in SARS-CoV-2 analyses. Thus, it has been proposed that SARS-CoV-2 infection may predispose individuals to develop NPD through bacterial co-infections. All of this had led to the suggestion that nonsurgical periodontal therapy could help in reducing the systemic spread of COVID-19, which has also been proposed in the literature.,
|Figure 1: Indirect pathway of the association between periodontitis and COVID-19|
Click here to view
COVID-19 and peri-implantitis
Studies published in the literature correlating a relationship between COVID-19 and peri-implantitis are limited. However, the infectious and inflammatory links that connect peri-implant diseases with other systemic conditions were the basis to hypothesize the relationship between COVID-19 and peri-implantitis. In fact, peri-implantitis is a bacterial infectious disease that demonstrates a strong inflammatory response regulated by IL-6. This alteration in the process of cytokine release could be one of the major causes behind the relation since COVID-19 cases show elevated IL-6 levels as well., As a result, it seems to be evident that the viral nature of COVID-19 and the emotional stress encountered during the peak of the pandemic had a negative impact on the periodontal tissues and consequently, peri-implant tissues. Moreover, peri-implant procedures that generate high amounts of droplets and aerosols could exert a significant role in the relationship between the two conditions.
Hence, considering more conservative approaches such as crestal sinus floor elevation, placement of short dental implants instead of lateral window sinus lifting or advanced bone augmentation, and using adjunctive modalities such as photodynamic therapy was highly recommended. Yet, the cytokine alteration in peri-implant diseases and its potential role in the severity of COVID-19 is still unclear and should be further investigated.
| Discussion|| |
The present study had theoretically investigated the potential influence of COVID-19 on periodontal and peri-implant health. Several studies reported in the literature have concerned the role of COVID-19 on health as well as emotional, economic, and educational systems. The fact that COVID-19 has a strong negative impact on the overall health of a person and has a human-to-human mode of transmission, preludes the fact of a potential association with periodontal health. The primary receptor and portal of SARS-CoV-2 entry into the cell are ACE-2, which is highly expressed in the oral mucosa, especially the epithelial cells of the tongue and the salivary glands. This, in turn, derives one conclusion that ACE-2 may act as a reservoir for the virus. Furthermore, COVID-19 patients' saliva is full of SARS-CoV-2 particles during the infection period. As gingival ulceration could reduce the protective function of the oral epithelial cells, ulcerated gingiva exposes the patient to an elevated risk of invasion by SARS-CoV-2 via salivary secretion. In addition, poor oral hygiene leads to the accumulation of periodontopathic bacteria that will be aspirated via respiratory epithelial cells through the expression of ACE-2. Literature has also shown that epithelial cells of periodontal pockets express high levels of CD147. Therefore, SARS-CoV-2 infection through the CD147 route is possible in cases of inflamed periodontal and peri-implant tissues. Both SARS-CoV-2 and periodontal diseases have shown an overexpression of cytokines making it a shared character between them, and recent findings have pointed toward the fact that it could result in systemic inflammation and aggravate pulmonary inflammation. As mentioned previously, levels of blood biomarkers such as white blood cells, D-dimer, and C-reactive protein were significantly elevated in COVID-19 patients with periodontitis, which highlights the systemic association between the two diseases. There are two possible mechanisms that could explain the association between periodontitis and COVID-19, i.e., direct and indirect pathways. The direct one could be through the high expression of ACE-2 and CD147 receptors in cases of periodontitis that are used by the virus to infect the cells. The indirect pathway takes place through overexpression of several cytokines and serum levels of IL-1 beta, IL-6, IL-7, IL-10, IL-17, IL-2, IL-8, IL-9, GM-CSF, G-CSF, IFN-gamma, TNF alpha, MIP1A, MIP1B, MCP1, and IP10. Studying and understanding the effects of COVID-19 on the oral cavity, especially the periodontal tissues, has become a promising area in dental research. Due to the significant association between general and dental health, this review embarked on highlighting the potential impact of COVID-19 on periodontal health as reported in the available literature. Through this review, it is believed that modifying treatment protocols would seem mandatory during the current pandemic, especially that dental practice involves close person-to-person contact and aerosol-producing procedures which triggered some level of fear among practitioners. Several measures in dental practice have been recommended, such as using hydrogen peroxide mouthwash before any dental procedure, cautious use of aerosol-generating handpieces, keeping regular maintenance visits, and reinforcing infection control protocols. In fact, dental practitioners were found to be well trained and exposed to hygiene practices and sanitization of their clinics during the COVID-19 pandemic. Not only awareness of infection control but also a high level of knowledge about the COVID-19 origin, incubation period, and mode of spread and prevention was reported among health-care workers. This review of the literature has some limitations in which clinical and observational studies currently published correlating COVID-19 and its direct impact on periodontal and peri-implant health were few.
| Conclusion|| |
Currently, available literature suggests a potential influence of COVID-19 on periodontal and peri-implant health. Other than the high expression of ACE-2 and CD147 there is no direct cause-and-effect relationship between the SARS-CoV-2 virus and periodontal diseases; however, the deterioration of the patient's periodontal and peri-implant conditions indirectly due to the similarity of the pro-inflammatory expressions (IL-1 beta, IL-6, IL-7, IL-10, IL-17, IL-2, IL-8, IL-9, GM-CSF, G-CSF, IFN-gamma, TNF alpha, MIP1A, MIP1B, MCP1, and IP10) present in both diseases were reported.
However, further studies are warranted on this topic to achieve a better understanding. Therefore, we recommend future research to further examine to which extent COVID-19 would affect periodontal and peri-implant health through in vivo clinical studies.
We would like to thank Dr. Tahani Alrahbeni, Dr. Deema Alshammary, Dr. Omar Al-Kadhi, and Dr. May Alkhudairi.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
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