Introduction

At the end of December 2019, an acute respiratory disease caused by a previously unknown beta-coronavirus emerged in the city of Wuhan, Hubei province, and transmitted rapidly throughout China before the Spring Festival1. Soon after, the novel virus was isolated from patients’ respiratory epithelia, and on 12 January was temporarily named the 2019 novel coronavirus (2019-nCoV) by the World Health Organization (WHO). On 11 February, the International Commission of Virus Classification declared the virus was named severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) and, on the same day, the WHO announced that the disease caused by the infection was named coronavirus disease 2019 (COVID-19)2-4.

The most common symptoms presented by those suffering from COVID-19 include fever and cough, with less common symptoms including sputum production, headache, haemoptysis and diarrhoea1, 5, 6. Ground-glass opacity is the typical radiological finding on chest computed tomography1, 5, 7, 8. Moreover, the two major oral-related symptoms, dry mouth and amblygeustia, have been present in a relatively high proportion of COVID-19 patients, suggesting that oral symptoms can also be considered as initial symptoms of COVID-19 infection9.

Most of the cases reported in January and February had either been in contact with people from Wuhan or had been to Wuhan recently1, 8, 10, 11. The incubation period of the virus varies from 0 to 24 days1, 5, 6, and asymptomatic infections have been recorded12.

Due to the flu-like symptoms, long period of incubation, various transmission routes and asymptomatic infections, the COVID-19 epidemic has spread rapidly throughout the world by human-to-human transmission3, 13.

With the rapid transmission of the epidemic, the WHO announced that COVID-19 formed a Public Health Emergency of International Concern (PHEIC) on 31 January 2020. The WHO made the assessment that COVID-19 can be characterised as a pandemic as of mid-March.

During the COVID-19 pandemic, both dental patients and staff are at high risk of being infected in the oral therapy practice. Dentists and nurses are in direct contact with patients’ open mouths, and are exposed to both coughing and breathing. Furthermore, the high-speed gas and running water of dental handpieces generate large amounts of aerosol and droplets mixed with the patient’s saliva or blood14, 15. These fluids pollute the clinical space and the surfaces of various dental devices, increasing the risk of infection for clinic staff and subsequent dental patients16, 17.

Here, we share experiences of emergency management in our dental clinic during the COVID-19 epidemic from the end of January to mid-March, when the outbreak of the COVID-19 epidemic was growing in Beijing.

Materials and methods

Based on the guidance of National Health Commission, a series of measures have been taken to reduce the possibility of cross-infection in dental clinics, and meanwhile to provide emergency dental services.

Advance preparation in the dental clinic Personal scheduling and infection control training

Details about contact history, any symptoms of fever or cough, commuting method, and residential location should be collected as accurately as possible for staff member. According to gathered personal information and the predicted number of patients, the dental clinic director of our clinic evaluated the risk of COVID-19 infection for each individual and made the dental clinic on-duty arrangements.

Infection control training for dentists and nurses is necessary before they begin to work. Hand hygiene and the dressing and removal of medical protection suits are the most important part of training. These procedures were based on consultations with medical professionals who had experienced and worked through SARS in 2003.

Division of the dental clinic into functional areas

The ‘three zones and two passageways’ layout is the basic requirement of an infectious disease negative pressure isolation room18, 19. The three zones refer to the clean area, semi-polluted area, and polluted area, and the two passageways refer to separate passageways for patients and medical staff. During the COVID-19 epidemic, this requirement was introduced into dental clinic management. The semi-polluted area is the buffer zone from the clean area to the dental treatment room area, where dentists and nurses wash their hands, disinfect, and change their shoes and clothes before moving from one area to another. Due to the limited equipment and the original layout, our dental clinic failed to achieve positive air pressure in the clean zone, or negative air pressure in the semi-polluted and patient zones; the air pressure of all three zones was equal. The central air conditioning and ventilation systems were turned off to avoid cross-infection among the zones or even across the whole building.

Splash treatment room

The splash treatment room is specially prepared for certain kinds of dental procedures that apply high-speed rotating dental drills or ultrasonic vibrating dental cleaners. The splash treatment room is isolated and should be located in a remote area of the department far away from the other dental treatment areas, with good ventilation, a buffer area and reasonable passageway management. All unrelated items should be removed or stored in a cabinet to keep the surfaces clean and smooth. Together, this makes disinfection of the splash treatment room more effective. Povidone-iodine solution at a concentration of 0.5%–1% is highly recommended as mouthwash before dental treatment, as it may provide a protective oropharyngeal hygiene measure for individuals at high risk of exposure to oral and respiratory pathogens, including SARS-CoV and MERS-CoV20. Moreover, we employ rubber dam and suction in the splash treatment room to reduce saliva splashing (Figure 1).

Dental professionals with personal protective equipment (PPE) and use of the rubber dam and suction in the isolated treatment room.

Contingency plan: isolated treatment room for patients at high risk of COVID-19

The isolated treatment room is prepared for patients who have been evaluated as at high risk of COVID-19, and who concurrently need an emergency oral treatment. Because of the limited space in our dental clinic, one splash treatment room will be temporarily transformed into the isolated treatment room. Environmental disinfection will be more stringent and no further treatment will be performed in the same room for at least 4 hours.

Adjustment of the medical process Preview triage first and then registration

It was a convention that registration came first in the former medical process. However, given the epidemic, we have adjusted the procedure so that dental nurses preview and evaluate the patients in advance. The aim of this change is to evaluate the COVID-19 risk in prospective patients to arrange the treatment order and time, reducing the possibility of cross-infection.

Patient evaluation

Patient evaluation was determined to be an important part of cross-infection control. Dentists and nurses should be able to identify a suspected case of COVID-19 or an individual at high risk. Based on the Guideline for the Diagnosis and Treatment of Novel Coronavirus Pneumonia (5th edition) by the National Health Commission of the People’s Republic of China, we designed a questionnaire to administer for patient evaluation (Table 1).

Table 1. Patient questionnaire before dental treatment

There are four main categories of the dental patient evaluation. Patients (category A) with no fever, no symptoms listed, and who reply ‘no’ to all questions about epidemiological history are able to receive dental treatment immediately. Patients (category B) who have a fever of more than 37.3°C, but who answer ‘no’ to all questions about epidemiological history, will be recommended to visit the Fever Clinic immediately. Patients (category C) who answer at least one ‘yes’ to the questions about epidemiological history, but who have no fever and no other symptoms will be recommended to undergo medical isolation for 14 days at home. Patients (category D) who answer at least one ‘yes’ to the questions about epidemiological history, and who have a fever of more than 37.3°C or any respiratory symptoms will be treated as high-risk patients or suspected COVID-19 infections. The contingency plan of a suspected case in hospital will be enabled, and the patient will be isolated before undergoing chest computed tomography and laboratory detections.

Limitation or delay of non-emergency patients

On 30 January 2020, the Beijing Municipal Health Commission released a notice about how to carry out dental work during the epidemic. According to the notice, conventional dental service was to be interrupted, except for dental emergencies such as acute toothache, tooth trauma, maxillofacial trauma or infection.

Supply protocol of personal protective equipment

Providing personal protective equipment (PPE) to healthcare personnel plays an essential role in avoiding occupational exposure and infection21. However, the hospital has extremely limited PPE inventory, with a supply shortage of N95 respirators and protective suits.

The US Centers for Disease Control and Prevention has recommended gloves, gowns, respiratory protection and eye protection as standardised PPE for the COVID-19 infection control of healthcare personnel22. In early February 2020, the National Health Commission of the People’s Republic of China issued ‘Introduction of medical protection equipment application in the prevention of COVID-19’ and other policies (http://www.nhc.gov.cn/jkj/s7916/202002/485e5bd019924087a5614c4f1db135a2.shtml). According to these policies, the hospital management has developed a PPE supply protocol based on the COVID-19 infection risk of different jobs. Herein, we have detailed the supplemental supply protocol for dental clinics (Table 2). Our management strategies, as a temporary emergency plan, have extracted the greatest benefits from extremely limited resources to meet the emergency need. In our opinion and experience, there is neither medical necessity nor economic feasibility to supply all dental staff with N95 respirators and protective suits. We even used swimming goggles as eye protection at the beginning of the epidemic.

Table 2. Supplemental supply protocol for dental clinic staff Dental staff PPE Triage nurses and disinfection nurses Surgical cap, eye protection, face shield, surgical mask, latex examination gloves, isolation gowns, plastic shoe covers Dentists and nurses in the conventional treatment room Surgical cap, eye protection, face shield, surgical mask, latex examination gloves, isolation gowns, plastic shoe covers Dentists and nurses in the splash treatment room Surgical cap, eye protection, face shield, surgical mask (+N95 respiratory protection), latex examination gloves, isolation gowns, plastic shoe covers Dentists and nurses in the isolated treatment room Surgical cap, eye protection, face shield, surgical mask (+N95 respiratory protection), double surgical gloves, protective suits, isolation gowns, plastic shoe covers PPE, personal protective equipment. Clinic environmental disinfection

Infection control measures were helpful in the containment of SARS as well as avian influenza in the past23. Environmental disinfection plays a much more important part in preventing COVID-19 cross-infection in the dental office, as dental procedures will generate large amounts of droplets and aerosols. Our set environmental disinfection standards for different areas are detailed in Table 3.

Table 3. Environmental disinfection standard Area Location Disinfection method Disinfection frequency Conventional treatment room and splash treatment room Dental instruments Autoclave sterilisation Every case Dental chair and side table Wipe with 75% alcohol-containing disinfectant wipes or 1,000 mg/L chlorine disinfectant solution Every case Air Aerosol spray with 10% sodium hypochlorite solution; ultraviolet disinfection lamp for 30 minutes; room ventilation through windows Every single case Floor Mop the floor with 1,000 mg/L chlorine disinfectant solution Twice a day Clean and semi-polluted area Office equipment Wipe with 75% alcohol-containing disinfectant wipes or 1,000 mg/L chlorine disinfectant solution Twice a day Air Aerosol spray with 10% sodium hypochlorite solution; ultraviolet disinfection lamp for 2 hours; room ventilation through windows Twice a day Floor Mop the floor with 1,000 mg/L chlorine disinfectant solution Twice a day Waiting and registration area Infrared thermometer Wipe with 75% alcohol-containing disinfectant wipes or 1,000 mg/L chlorine disinfectant solution Every case Registration table Wipe with 75% alcohol-containing disinfectant wipes or 1,000 mg/L chlorine disinfectant solution Every 2 hours Chairs

Wipe with 75% alcohol-containing disinfectant wipes or 1,000 mg/L chlorine

disinfectant solution

Twice a day Air Aerosol spray with 10% sodium hypochlorite solution; room ventilation through windows Twice a day Floor mop the floor with 1,000 mg/L chlorine disinfectant solution Twice a day Online dental care and consultation services

Online medical care is increasingly popular in China with the development of communication and use of the smartphone. It is also useful for outpatient education and management. Dental professional staffs in our clinic provide online medical care services for free by instant messaging APP or phone. Online medical consultations are playing an important role during the COVID-19 epidemic24.

Results Dental patient evaluation in our clinic

All dental patients visiting our clinic were notified before treatment. In general, patients with COVID-19 who are in the acute febrile phase of the disease are not recommended to visit the dental clinic. From 31 January to 15 March, there were 94 visitors to our clinic in total. The number of patients (category A) was 92, and they received dental treatment. There were two patients in category B, who were recommended to visit the Fever Clinic immediately and ruled out COVID-19. No patients in category C or category D were identified in our clinic.

The number of visitors and consultations

From 31 January to 15 March, there were 94 visitors to our clinic in total, a sharp decrease from the 3,803 visitors in the same period last year. Two cases of maxillofacial trauma, four cases of fascial space infection, 39 cases of acute toothache (of which 13 cases received treatment), two cases of chronic toothache, and 47 cases of other conditions (mainly asking for a prescription for medication) were seen (Table 4).

Table 4. The number of visitors or consultations (2020.01.31–2020.03.15) Total number Trauma Fascial space infection Acute toothache Chronic toothache Other causes Outpatient 94 2 4 39 2 47 Online consultation 189 2 6 40 47 94

As of 15 March, dental professionals have completed approximately 189 free online dental consultations via messaging apps (QQ, Wechat) and telephone. These professionals offer medication guidance or emergency treatment advice at home, and evaluate the necessity of receiving further treatment in the dental clinic (Table 4).

The number of visitors to our clinic and new confirmed cases of COVID-19 in Beijing each day from 26 January to 15 March

Figure 2 shows the number of visitors to our clinic and new confirmed cases of COVID-19 in Beijing each day from 26 January to 15 March. There were no visitors to our clinic from 26 January to 30 January, due to clinic closure during the spring holidays. Ten patients visited the clinic on 31 January, the first day post-holiday. There were 44 visitors in total from 31 January to 6 February, and an average of 24 new COVID-19 cases were confirmed in Beijing during this period, indicating a growth peak. In response, a series of prevention management strategies was issued gradually by the government; people were restricted at their homes to reduce the risk of infection, contributing to no visitors to the clinic between 7 February and 19 February. With the COVID-19 epidemic slowly becoming controlled, the average number of new confirmed COVID-19 was 2, and there were less than 5 visitors to our clinic each day from 20 February to 15 March.

Number of dental outpatients in our clinic and new confirmed COVID-19 in Beijing (2020.01.31–2020.03.15).

No infections because of dental treatment

As of 15 March, we have not provided dental emergency treatment for patients who have been evaluated as at high risk of COVID-19. Also, no dental institute throughout Beijing, including our clinic, provided dental therapy to a confirmed case of COVID-19. There has been no reports of a dental staff member or patient being infected through dental treatment in China.

Discussion

As a novel coronavirus, SARS-CoV-2 is very similar to the virus that caused the SARS outbreak (SARS-CoV) of 2003. Both coronaviruses belong to a large family of single-stranded RNA viruses, in which MERS-CoV is also included25, 26. Compared with SARS and MERS, COVID-19 has spread more rapidly, due in part to increased globalisation and the origin of the epidemic. The outbreak originated in Wuhan, one of the most important transportation hubs in China, shortly before the Spring Festival when the maximum passenger flow volume would occur27.

Transmission routes and high-risk dental practice

Dental professionals are most concerned with the transmission routes of SARS-CoV-216. Conventional transmission routes of SARS-CoV and MERS-CoV include respiratory droplets and direct contact26, 28, but the importance of indirect contact transmission (involving contamination of inanimate surfaces) is uncertain26. In contrast, it has been reported that SARS-CoV-2 has been detected not only in respiratory droplets from coughs and sneezes, but also in the gastrointestinal tract, saliva and urine; the transmission routes of 2019-nCoV may therefore consist of fomite transmission alongside the conventional routes of respiratory viruses. There is also increasing evidence that the virus may spread through faecal−oral transmission and through the conjunctiva29, 30, indicating the importance of hand hygiene in dental practice.

Most dental therapies are invasive and involve contamination through a short range of face-to-face positions; as a result, dental professionals will directly encounter respiratory droplets and contaminates from an open mouth. Dental pulp, gingiva, oral mucous and alveolar bone are all involved in the process of oral treatment, which can lead to the outflow and exudation of respiratory secretions, saliva, blood and tissue fluid. At the same time, stimulation and limited swallowing movements during treatment lead to the increase and retention of saliva and nasopharyngeal secretions in the oral cavity.

Dental procedures involving sandblasting devices, high-speed rotating dental drills and ultrasonic vibrating dental cleaners promote the vaporisation of saliva, blood and tissue fluid in the oral cavity, and generate large amounts of droplets and aerosols, which can remain suspended in the air for an extended period of time31. Droplets and aerosols floating in the clinic air contain many bacteria, fungi, viruses, tooth fragments and dental filling materials, which are an important source of air pathogen transmission in dental clinics that may contribute to the explosive COVID-19 epidemic.

Furthermore, a variety of instruments, assistant equipment and the surrounding environment would all be contaminated by bodily fluids of the patients. Once contaminated by the environment, hands can self-inoculate the mucous membranes of the nose, eyes and mouth. Poor hand hygiene will also increase the risk infection of COVID-1932.

As a result, routine dental procedures will probably accelerate the spreading of SARS-CoV-2. Certain management procedures should be performed to control the transmission routes and prevent COVID-19 infection in the dental clinic.

Post-epidemic management

The ‘emergency only’ policy of the dental clinic is appropriate to implement during the epidemic threshold period to reduce the cross-infection risk, but is executed at the expense of the dental treatment of numerous patients. Fortunately, the COVID-19 epidemic is stabilising and becoming more controlled in Beijing as of mid-March, and new confirmed cases have only been imported from epidemic areas overseas like Italy and Iran. However, it has been predicted that the epidemic may be in a relatively low period at present, and has the potential to worsen again in the following months. Therefore, we plan to progressively expand the dental services offered in the clinic so that along with dental emergencies (acute toothache, tooth trauma, maxillofacial trauma or infection), secondary dental demands can also be satisfied (Table 5).

Table 5. Dental disease classification based on degree of emergency Degree of emergency classification or dental diseases Dental diseases, symptoms, dental service demand Dental clinic visitation advice Emergency Acute toothache Tooth trauma Maxillofacial trauma or fascial space infection TMJ dislocation Persistent bleeding Etc. Immediate clinic visit Secondary emergency Interrupted orthodontic treatment Chronic toothache Dental filling Root canal therapy Etc. Appointment registration or online consultation Optional treatment Orthodontic demand Dental implant demand Dental hygienic treatment Prosthodontic demand Etc. Post-epidemic appointment registration or online consultation

Dental professionals determine the priority of dental diseases by classification according to symptoms, diseases, severity degree and the potential of COVID-19 infection risk.

It has been predicted that there will be a rise in dental clinic visitors post-epidemic, along with large numbers of individuals with previously interrupted treatment. Therefore, it is highly recommended that no dental professional is absent from the workforce during the 2 months post-epidemic. Moreover, the supply of some imported medicines and instruments should be reserved in advance, as imported goods may be interrupted due to the spreading of COVID-19 overseas.

Conclusions

Early public preventive measures were key to limiting the spread of the epidemic. There were 25 provinces that began the first-level response to this major public health emergency at 21:00 hours on 25 January, covering a total of 1.2 billion people. The number of new confirmed COVID-19 cases nationwide varied from 18 to 29 daily between 9 March and 15 March. We have, therefore, achieved phase achievements in mid-March. Based on guidelines from the National Health Commission and the Chinese Stomatological Association, dental professionals have continued to provide dental treatment during the COVID-19 epidemic. As of 15 March, there has been no report of a dental staff member or patient being infected through dental treatment in China.

By experiencing SARS in Beijing in 2003, and now COVID-19, we are reminded that every emerging infectious disease is a challenge to the whole of mankind. The importance of standard precautions for any patient and disinfection for the healthcare environment cannot be overemphasised in the dental office during the COVID-19 epidemic, due to the virus’ rapid human-to-human transmission routes of respiratory, direct and indirect contact. To protect dental staff and promote disinfection, we have offered emergency dental treatment in clinic and consultation services online. Hence, this report relays useful lessons for dental professionals or hospital managers during both the present COVID-19 era and future epidemics.

Acknowledgements

The authors appreciate Professor Zhao Wenfeng and head nurse Wang Liying for sharing their experiences and providing guidance after their own contributions to the SARS epidemic in 2003.

Funding

None.

Conflicts of interest

The authors declare no conflicts of interest.

Author contributions

Research concept and design: Chao Wang, Li Miao, Hongchen Liu. Collection and assembly of data: Yanjie Xiong, Chao Wang. Data analysis and interpretation: Chao Wang, Li Miao, Zhigang Wang. Writing the article: Chao Wang, Yang Jiao. Critical revision of the article: Hongchen Liu, Zhigang Wang, Yang Jiao. Final approval of the article: Hongchen Liu, Chao Wang.