Antibiotic prescriptions among dentists across Norway and the impact of COVID-19 pandemic

Awareness of the growing problem of antibiotic resistance has steadily increased over the last two decades discussed in many studies [1‐4]. The use of antibiotics became the foundation for the treatment of infectious diseases since their discovery and has helped to save millions of lives [4]. Today, because of antibiotic use, overuse and misuse, antibiotic resistance is on the rise, which subsequently leads to the increase of morbidity, mortality, and treatment costs for infectious diseases [5].

The use of antibiotics is an integral part of practicing dentistry, both to prevent infections in vulnerable patients and to treat ongoing systemic infections of dental origin [2, 6, 7]. Dentoalveolar abscesses with systemic involvement, facial cellulitis, and osteomyelitis are examples of oral infections requiring systemic antibiotic treatment. In most cases, in combination with surgical interventions such as incision, drainage, and/or tooth extraction. Untreated or delayed treatment may in some cases lead to severe infections spreading beyond the oral cavity threatening airways and vital structures [8]. In Norway, the recommendations for treatment for odontogenic infections governed by Norwegian Directorate of Health which recommends phenoxymethylpenicillin (1 g every 6^th hour in adults for 5 days) for acute dentoalveolar infections, where there is an indication to use antibiotics, as a first choice. In case of therapeutic failure with the first drug of choice, the addition of metronidazole (400 mg every 8 hourly in adults for 5 days) is recommended. Oral diseases, such as dental caries and periodontal diseases, if not controlled and treated properly, may precede to cause acute infections in underlying tissues. Gram-positive bacteria in supragingival biofilm, such as Streptococcus spp., Lactobacillus spp., and Actinomycetes spp., are associated with the development of dental caries. Gram-negative bacteria in subgingival biofilm, such as Porphyromonas gingivalis, Actinobacillus spp., Prevotella spp., and Fusobacterium spp. have been shown to have a role in the development of periodontal diseases. The bacteria in both supragingival and subgingival biofilm have been shown to be up to 1000-fold more resistant to antibiotics compared to bacteria in suspension [9, 10]. Dentists also prescribe antibiotics prophylactically to prevent infection. This can either be due to patients with high risk factors for infection such as pronounced immunosuppression or because the planned procedure is regarded to be associated to unacceptably high risk for infection [11]. When prophylactic antibiotic is indicated, the recommendation in Norway is one dose of 2 g amoxicillin 1 h before invasive procedures.

WHO adopted a global action plan to fight antimicrobial residence (AMR) in 2015 [12]. As a result of this, the Norwegian government published the national strategy against antibiotic resistance in June 2015. In 2016, the Norwegian Ministry of Health and Care Service published an action plan against antibiotic resistance in the health service, with the goal of reducing antibiotic use in the population by 30 percent by the end of 2020 [13]. Furthermore, in 2019, the Ministry of Health published an action plan for optimizing infection control. The actions plan`s main goal is to reduce health service-associated infections and provide a better organization and structure of infection control in Norway. As a result, national recommendations for infection control and hygiene guidelines at the dental health service was implemented, and solid guidelines or recommendations in streamlining the clinicians’ decision process regarding antibiotic use was put in place [1, 14].

Studies have shown that the dentists’ prescriptions accounted for about 8–11% of total national consumptions of antibiotics in Norwegian health care [6, 15]. Inappropriate prescribing of antibiotics in dentistry is reported from several parts of the world [16‐19]. In Norway, there is a relatively low consumption of antibiotics, and it is among the three lowest prescribing countries in Europe with prescription predominately of narrow-spectrum antibiotics [15, 20].

There is an interest to know how the Covid-19 pandemic restrictions on dental care services in Norway may have had an impact on antibiotic prescribing by dentists. Because dental care services were partially closed or open with a reduce capacity during the COVID-19 pandemic, many patients chose to postpone regular checks and treatments, and it is anticipated that there might have been an increased risk of compensatory prescription of antibiotics. This is also the case because of the number of telephone consultations also increased [21]. It is necessary to continue to provide, implement, maintain, and follow up the national guidelines by well-structured organization so that antibiotics will continue to be effective for users in the future.

The main objective of this retrospective study was to monitor and evaluate the number of national antibiotic prescriptions written by dentists between 2016 and 2021 in all Norwegian counties. A further objective was to investigate the influence of demographic factors as age, gender, county, and specialty in profession on prescription of antibiotics and review differences in prescribing patterns to verify effect of governmental strategies to reduce over-prescription. A further aim was to describe the impact of the policy to restrict dental access on antibiotic prescribing during COVID-19 pandemic.

Measuring the consumption of antibiotics in any given society is a valuable information to adopt and sustain good polices that enhance reasonable use of antibiotics and preserve their effectiveness in clinical practice. There are six quantity matrices for the outpatient setting (OQM1-6) to measure consumption of antibiotics. Each matric has its advantage and disadvantage [23]. In the current study, only OQM1, OQM4 and OQM6 are provided by the Norwegian prescription database.

Previous international data show that dentists account for about 7–10% of the antibiotics prescribed in primary care [15, 24]. In the current study, the corresponding average rate was 15.6%. Previously, it was reported that the contribution of dental prescriptions to the national prescriptions in Norway between 2010 and 2016 is about 8% [6, 15]. The reported high percentage in the current study could be partly explained by the fact that antibiotic prescription seems to have increased substantially in dentistry during the COVID-19 pandemic. This was probably due to lockdown with strongly reduced availability of dental care. Since Norway is generally considered to be a country with restrictive antibiotic policy the relatively high contribution of dentistry could also be explained by the fact that the reduction of antibiotic prescriptions in the remaining primary care has been very pronounced in the study period [25]. International studies also show significant reduction in total outpatient antibiotic prescriptions issued during the COVID-19 period by physicians and other prescribers [26]. The magnitude of the reduction in the number of antibiotic prescriptions was in children, with respiratory infections [25, 26]. The result of this study shows a relative increase in prescriptions of antibiotics during the COVID-19 pandemic while other international studies show a reduction in antibiotic prescribing among dentists by 8.92% [21]. Since dental care was partially closed during parts of the pandemic period the increasing number of telephone consultations might have contributed to the observed increased in antibiotic prescription. There are studies that raised concerns about the potential for higher antibiotic prescribing rates in virtual consultation than in face- to face communication with the patients [27, 28].

Another finding in the current study is the use of the narrow spectrum phenoxymethylpenicillin was the most common choice among dentists in Norway which is an important core in the country’s conservative prescriptions practice. However, although phenoxymethylpenicillin (Pc-V) represents a dominating proportion of the prescription it would be expected to be even higher since it is the first choice of treatment for dental infections according to Norwegian national recommendations. The only situation in general dentistry requiring clindamycin is in the case of penicillin allergy. Thus, the amount of prescribed clindamycin is not likely to correspond to true type 1 penicillin allergies but could be rather the effect of an overestimation of penicillin allergy and perhaps negligence of the recommendations. In cases of severe odontogenic infections with suspected anaerobic bacteria addition of metronidazole to Pc-V is advocated. Another possible explanation for the relatively high clindamycin prescription could be that it is chosen for these more severe infections. A previous study showed a reduction in the prescription of antibiotics by dentists between 2010 and 2016 by 4.3% [15]. In contrast, this study shows that antibiotic utilization between 2016 and 2021 in dentistry has increased in general and particularly among the main antibiotics used in dentistry in Norway, i.e., Pc-V followed by amoxicillin, clindamycin, and metronidazole.

An unexpected finding was the prescription of co-amoxiclav which had significantly increased among Norwegian dentists during the 5 years study period especially among general dentists. In 2017, the co-amoxiclav compound Augmentin received marketing authorization to be prescribed in Norway. This composite compound contains two different active substances, amoxicillin and clavulanic acid causing more pronounced ecologic disturbance to the normal microbiota compared to the narrow spectrum Pc-V. While amoxicillin is an active against both against Gram-positive and Gram-negative bacteria, clavulanic acid has no antimicrobial effect but binds irreversibly covalent to beta-lactamase [29]. This inactivation of beta-lactamases renders the compound effective against beta-lactamase producing bacteria. The Antibiotic Center for Primary Medicine (ASP) recommends Augmentin in general practice only for treatment infections with Haemophilus influenza or Moraxella catarrhalis with resistance to amoxicillin, in some cases with chronic obstructive pulmonary disease, and for patients with pneumonia, otitis, or sinusitis. However, according to the Felleskatalog (Encyclopedia of pharmaceutical preparations marketed in Norway), Augmentin is also used for skin and soft tissue infections, including dental infections, infections in bones and joints. The question arises whether the increase in prescription of Augmentin is due to differences in susceptibility among oral bacteria with becomes more resistance that led to treatment failure with conventional antibiotics, or attitudes toward antibiotic prescribing influenced by dentists coming to Norway from abroad, or because of differences in educational guidelines. Before 2021 the recommendations in Norway to use a 600 mg Pc-V dose four times daily for the treatment of dental infections. This dose may have been too low considering that these infections has both soft and hard tissue engagement. Insufficient effect of the recommended antibiotic treatment could also have been a driver for the choice of more broad-spectrum alternatives. To reverse the trend of prescribing broad-spectrum antibiotics, arrangement of audits in antibiotic prescription for dental and oral infections, especially among these who graduated from outside of Norway should be considered by the health authorities.

The results that the population in Agder county of Norway received most antibiotics in Norway, while Trondelag, Troms and Finnmark were significantly lower is in accordance with a previous study [30]. The reason for this finding is not completely clear. It has been suggested that socioeconomic factors could have an impact on antibiotic prescription [31‐33]. Statistics provided by NAV (the Norwegian Labour and welfare administration) indicated that Agder has some of the highest level of unemployment in 2021 compared to Trondelag, Troms, and Finnmark. Interestingly, also in Sweden the highest prescription of antibiotics in dentistry is seen in the most southern part of the country [24].

Less prescription was seen from July through September. This could be explained by the fact that dental offices have limited opening hours during this period or because of patients postpone their dental appointments during this period because of summer vacation [34]. Female dentists significantly prescribed fewer antibiotics than that of male dentists, which has been shown in other studies as well [30]. There are studies that shows gender gap in compliance with public policy rules [35]. The results also show that younger dentists prescribe fewer antibiotics than their older counterparts. It seems that the younger dentists are more restrictive and following guidelines updates, more carefully than otherwise older generations. It seems that preservation of antibiotics, sustainability issues and impact on future generations are issues that young people tend to me more aware of than older generations.

There were marked differences in patterns of consumption of antibiotic attributed to dental prescriptions in last 5 years. It seems that the impact of COVID -19 pandemic, probably because reduced access to dental care, resulted in the increased use of antibiotic prescription compared to an otherwise downward trend. Reduced access to dental service is an important factor which can lead to unnecessary over prescribing of antibiotics. It highlights the essential role of good oral health and availability of dental care in the global efforts to manage antibiotic resistances. The trend of increasing broad-spectrum prescription does not seem to have an apparent association to the pandemic and may be an early warning sign of undesired trends in antibiotic prescription in dentistry. Health authorities are advised to arrange a series of audits in antibiotic prescription for dental and oral infections, especially among these who graduated from outside of Norway.