Swedres-Svarm Summary

For a long time, Sweden has had a favourable situation compared to many other countries when it comes to antibiotic resistance in bacteria from humans, which remains true. One contributing factor is that we have effective strategies to promote the responsible use of antibiotics and limit the spread of antibiotic resistance. Despite the favourable situation, there are problems with continuously increasing antibiotic resistance and the spread of infections in healthcare. Important examples are the recurrent outbreaks of vancomycin-resistant enterococci in hospitals and an increasing number of healthcare-associated clusters of ESBLCARBA. This emphasises the importance of continuous work with antibiotic stewardship and infection prevention and control, in healthcare as well as in the community to prevent increasing antibiotic resistance.

Antibiotic sales in human medicine in Sweden decreased sharply during the pandemic, but began to increase in 2022 and continued to increase in 2023. Despite the increase, sales remained below pre-pandemic levels. Antibiotic sales have generally decreased since the peak in 1992. The greatest decrease during this period was observed in children aged 0-4 years.

In veterinary medicine, sales of antibiotics have decreased markedly since the mid-1980s, and in recent years sales seem to have stabilised at a comparatively low level. The occurrence of resistance among bacteria from animals has generally been stable at low or moderate levels. For some substances and in some bacteria the occurrence of resistance is even declining. One example of this is a significant decline of the occurrence of ESBL-producing Escherichia coli among broilers. There are however exceptions, and for example resistance to ampicillin, sulphonamides and trimethoprim has increased in indicator E. coli from both broilers and pigs.

Key findings 2023

• Total sales of antibiotics for humans in Sweden increased by 7.3% in 2023 compared to 2022, as measured in DDD per 1 000 inhabitants per day. The increase was reflected in both outpatient and inpatient care. Antibiotic sales in dentistry decreased by 2.6% during the same period.
• Antibiotic sales in outpatient care increased during 2023 compared to 2022. Sales of antibiotics commonly used for respiratory tract infections in children especially contributed to this increase.
• Since 2020, resistance to cefotaxime in Escherichia coli and the proportion of methicillin-resistant Staphylococcus aureus (MRSA) isolated from blood are used as indicators of antibiotic resistance in Sweden. Both the proportion of MRSA and the proportion of E. coli that are resistant to cefotaxime have slowly increased over a ten-year period to the current 2.1 and 7.6% respectively. For both indicators, the increase appears to have reached a plateau in recent years.
• During the pandemic, the number of cases of most types of notifiable antibiotic resistance decreased. For most of these, clear increases are now seen, most markedly for ESBLCARBA, where 314 cases were reported, compared to 240 in 2022. Thirty-nine clusters, with between two and eight cases each, have been identified by whole-genome sequencing in 2023. For sixteen of the 39 clusters, there is one or more cases reported as healthcare-related infection in Sweden.
• Seventeen hospital-associated outbreaks of vancomycin resistant enterococci were reported in 2023.
• Resistance levels among clinical isolates from humans were not affected by the pandemic.
• Sales of antibiotics for animals are stable at a low level and are dominated by narrow-spectrum penicillin.
• MRSA is uncommon among both farm and companion animals.
• ESBL-producing E. coli is generally uncommon among farm and companion animals as well as on meat.
• ESBLCARBA-producing bacteria have not been confirmed in domestic animals in Sweden.

Sales of antibiotics

Sales of antibiotics for humans

The total sales of antibiotics for humans in Sweden increased by 7.3% in 2023 and was estimated at 10.9 DDD per 1 000 inhabitants per day. This figure encompasses all antibiotics sold on prescription to individuals and all antibiotics sold to hospitals and other health- and social care facilities.

Outpatient care

In 2023, 270 prescriptions per 1 000 inhabitants were dispensed at pharmacies in Sweden, an increase of 7.5% compared to 2022. Of the 21 regions in Sweden, four regions achieved the national long-term target of 250 or fewer prescriptions per 1 000 inhabitants and year. Antibiotic sales increased in all age groups with the highest increase in children aged 5-14 years, where sales increased by 51.9% compared to the year before. The most substantial increase occurred during the fourth quarter of 2023. This increase consisted primarily of antibiotics commonly used to treat respiratory tract infections.

The sales of antibiotics in dentistry decreased by 2.6% in 2023, and accounted for 7.2% of all outpatient antibiotic prescriptions during the year. Since 2007, the prescription of antibiotics by dentists has decreased by nearly half.

Hospitals and other health- and social care facilities

In 2023, the sales of antibiotics on requisition, including all antibiotics sold to hospitals and other health- and social care facilities, increased by 5.7% compared to 2022. Sales increased in 20 of 21 regions during the same period. As in previous years, there were large regional variations in the sale of antibiotics on requisition to the regions.

Sales of antibiotics for animals

In 2023, reported sales of antibiotics for animals from pharmacies in Sweden were 9 069 kg, of which around 55% were narrow-spectrum penicillins. Sales of antibiotics that should be used with special restrictions (fluoroquinolones, third generation cephalosporins and polymyxins) have decreased considerably since 2013. During the same decade, the proportion of products for the treatment of individual animals has been around or over 90% of the total sales.

Since the withdrawal of growth-promoting antibiotics from the Swedish market in 1986, the total sales of antibiotics corrected for population sizes over time have decreased by more than two thirds. During the 1990s, sales of veterinary products for medication of groups of animals decreased, and in the past decade there has also been a decrease in sales of products for use in individual animals.

Comparing sales of antibiotics in human and veterinary medicine

In 2023, a total of 64.4 tonnes of antibiotics were sold for human use and 8.9 tonnes were sold for animal use (excluding products for intramammary or intrauterine use). Measured as milligrams of active substance per kilogram biomass, the corresponding sales were 91.2 and 11.6 milligrams per kilogram, respectively.

Notifiable resistance

ESBL-producing Enterobacterales

ESBL-producing Enterobacterales in humans has been subject to mandatory notification since 2007. It is the most common type of notifiable antibiotic resistance.

Results 2023, Enterobacterales with ESBL

• Number of reported cases: 10 895 (previous year 9 611), relative change +13%.
• Number of bloodstream infections: 897 (previous year 818).
• As in previous years, Escherichia coli was the most common species, (83%), followed by Klebsiella pneumoniae, (11%).
• The proportion of E. coli from blood cultures that are resistant to third-generation cephalosporins were 7.6% as in 2023.

Results 2023, Enterobacterales with ESBL CARBA

• Number of reported cases: 314 (previous year 240), relative change +31%.
• Number of bloodstream infections: 21(previous year 14).
• Among Enterobacterales with ESBLCARBA, E. coli was the most common species, (61%) followed by Klebsiella pneumoniae (28%).
• Thirty-nine clusters or pairwise linked cases of ESBLCARBA were identified by whole-genome sequencing in 2023 (2-8 cases per cluster). Of the 39 clusters, 19 clusters had at least one case prior to 2023. For 16 of the 39 clusters, there is one or more cases reported as healthcare-related infection in Sweden.
• The number of E. coli from blood cultures resistant to meropenem was 3 out of 10 719, compared to 3 out of 10 541 in 2022.

ESBL-producing Enterobacterales are generally rare among animals in Sweden. Previously, the occurrence in intestinal samples from broilers was high but it has decreased in recent years. In 2023, the occurrence of ESBL-producing E. coli in intestinal samples from fattening pigs and broilers, as well as samples of pig and cattle meat was investigated with selective methods. Such bacteria were isolated from 1% of the intestinal samples from pigs and broilers, respectively but such bacteria were not isolated from any of samples of pig meat or cattle meat.

Bacteria that produce ESBLCARBA have not been confirmed in domestic animals in Sweden.

Methicillin-resistant Staphylococcus aureus (MRSA)

Community-acquired infection has long been the most common type in humans, accounting for half of the cases. In 2015, community-acquired infection was divided into family/ household-related infection and community-acquired infection. Family/house-hold-related infections and community acquired infections accounted for 27% and 21% of the cases, respectively.

Results 2023

• Number of reported cases: 3 547 (previous year 3 340), relative change +6%.
• Number of bloodstream infections: 103 (previous year 96).
• The proportion of MRSA among Staphylococcus aureus isolated from blood has Increased to 2.1%, compared to 1.9% in 2022.

The occurrence of MRSA in animals in Sweden is still low, which limits the spread from animals to humans. MRSA was found sporadically in horses, dogs, and cats. The increase of MRSA cases, compared to previous years, seen in horses in 2020 and 2021 was partly explained by outbreaks in equine hospitals. In 2023 there were 12 cases, and no outbreaks. In companion animals, the same types of MRSA as in humans dominate, indicating a human source of MRSA in these animals.

Methicillin-resistant Staphylococcus pseudintermedius (MRSP)

In 2023, the number of reported cases of methicillin-resistant Staphylococcus pseudintermedius (MRSP) in animals was around the same level as in previous years. In total 46 cases of MRSP were notified to the Swedish Board of Agriculture, including 44 from dogs and two from cats. All but one isolates were available for further investigations. When MRSP first occurred among animals in Sweden, the sequence type ST71 dominated. However, for several years the isolates of MRSP have been more diverse with several sequence types occurring. MRSP in humans is not notifiable.

Streptococcus pneumoniae with reduced susceptibility to penicillin (PNSP)

Results 2023

• Number of reported cases: 152 (previous year 146), relative change +4%.
• Number of bloodstream infections: 7 (previous year 9).
• The proportion of S. pneumoniae with reduced susceptibility to penicillin (PNSP) among bloodstream infections decreased to 5.8% from 7.7% 2022.

Vancomycin-resistant enterococci (VRE)

Results 2023

• Total number of reported cases: 260 (previous year: 236), relative change +10%.
• The number of cases of VRE can vary greatly between years depending on the number and magnitude of hospital outbreaks.
• Number of reported cases of E. faecium with vancomycin resistance: 250 (previous year: 227), relative change +10%
• Number of reported cases of E. faecalis with vancomycin resistance: 10 (previous year: 4)
• There were six cases infected with both E. faecium and E. faecalis.
• Number of bloodstream infections: 5 (previous year: 5)
• Seventeen clusters were reported during the year with 2-35 cases each. Out of these, five were large hospital-related outbreaks with 10-35 cases each. In 2022, sixteen hospital related outbreaks were reported.
• The proportion of VRE among bloodstream infections is low at, 0.7% for E. faecium resistant to vancomycin and 0.0% for E. faecalis resistant to vancomycin.

Zoonotic pathogens

Salmonella is rare in animals in Sweden. Furthermore, only a few of the notified cases involve antibiotic resistant strains. Resistance to fluoroquinolones is rare. Among 107 isolates from animals in 2023, 90% were susceptible to all antibiotics tested.

For Salmonella species isolated from human faeces, the highest occurrence of resistance was to fluoroquinolones, (24%). No resistance to carbapenems was reported. Isolates from human invasive infections with Salmonella are markedly more resistant, probably due to the large proportion of cases acquired abroad.

Campylobacter from animals in Sweden are generally susceptible to relevant antibiotics, and resistance to erythromycin, for example, is most uncommon. In Campylobacter jejuni from humans, resistance to ciprofloxacin was 56% and resistance to tetracycline was 26% in 2022, and 1.9% of the isolates were resistant to erythromycin.

Infections, either in humans or i in animals, caused by Salmonella and Campylobacter are usually not treated with antibiotics. In humans, only a small proportion of the isolates, most of which are related to serious infections, are tested for antibiotic susceptibility.

Human clinical isolates

All data for these compilations are collected automatically via Svebar, a collaboration between the clinical microbiology laboratories and the Public Health Agency.

Escherichia coli: Resistance in blood isolates to ceftazidime and cefotaxime was 6.6 and 7.6% respectively. The number of reported E. coli ESBL from blood was 670 cases in 2023.

Resistance to ciprofloxacin is now 15% and 11%, respectively, in isolates from blood and urine. This needs to be considered when choosing empirical treatment for febrile urinary tract infection.

When E. coli from urine are divided by age and gender, some differences in resistance are seen. Most prominent is the high ciprofloxacin resistance (17-21%) seen among men 20 years and older.

Klebsiella pneumoniae: resistance in blood isolates to cefotaxime and ceftazidime was 9.6 and 8.6% respectively. The number of reported K. pneumoniae ESBL from blood was 144 cases in 2023. As for E. coli, resistance to ciprofloxacin is now relatively high at, 11-13% in isolates from urine and blood.

Staphylococcus aureus: Resistance to cefoxitin (which is indicative of MRSA) in isolates from blood and samples from skin and soft tissue was 2.1% and 2.4% respectively. The number of reported MRSA from blood was 103 cases in 2023.

Enterococcus faecalis and Enterococcus faecium: Vancomycin resistance in isolates from blood remains low (0.0% and 0.7%, respectively) and high-level aminoglycoside resistance is still on a lower level compared to 2017.

Clostridioides difficile: The incidence has been relatively stable since 2018 and was now 60 cases per 100 000 inhabitants and year. No isolates were tested for antibiotic resistance in 2023.

Animal clinical isolates

Bacteria causing clinical disease in animals are mostly susceptible to antibiotics relevant for treatment. Respiratory pathogens from farm animals and horses are generally susceptible to benzylpenicillin, but resistance occurs, for example in Pasteurella multocida from calves. Penicillin resistance is common in Staphylococcus pseudintermedius from dogs and occurs in S. aureus from horses and S. felis from cats. However, in S. schleiferi from dogs penicillin resistance is uncommon. Resistance to commonly used antibiotics in E. coli occurs in all animals but is most prominent in enteric isolates from young pigs. Susceptibility testing for guidance in antibiotic therapy is warranted, especially for staphylococci, E. coli, and Brachyspira spp.

Indicator bacteria from healthy animals

Antibiotic resistance in E. coli from the intestinal flora of healthy animals serves as an indicator of the presence of resistance in an animal population. The prevalence of acquired resistance in such commensal bacteria also indirectly indicates the magnitude of the selective pressure from the use of antibiotics in an animal population. The prevalence of resistance in indicator bacteria from animals in Sweden is low, and the situation is favourable in an international perspective. As an example, in the latest investigations of indicator E. coli from broilers and pigs, 69% and 73% respectively, were susceptible to all tested substances.