Resurgence and atypical patterns of pertussis in China

Abstract

•The resurgence of pertussis in the latest one decade and atypical plunges and surges occurred after COVID-19 outbreak are described.•During the late stage of the pandemic, the precise adjustment of non-pharmaceutical interventions (NPIs) adopted for COVID-19 control could not stop pertussis transmission, but might provide favorable conditions for this infection.•The dominant position of erythromycin-resistance Bordetella pertussis expressing ptxP1 allele (ERBP-ptxP1) in clinical isolates has been replaced by ERBP-ptxP3 in the atypical epidemic, from 2020-2022. Dear Editor, A previous study reported that the cases of pertussis was reduced in the first two years following the COVID-19 outbreak due to the non-pharmaceutical interventions (NPIs) in China.1Geng Y. Zhang L. Impact of non-pharmaceutical interventions during COVID-19 pandemic on pertussis, scarlet fever and hand-foot-mouth disease in China.J Infect. 2022; 84: e13-e15https://doi.org/10.1016/j.jinf.2021.12.023Abstract Full Text Full Text PDF PubMed Scopus (12) Google Scholar With the shift of the prevention and control strategies against COVID-19, atypical surge of pertussis in the latest two years was observed. Therefore, we summarized the the variable epidemiology of pertussis in the last one decade in China and discussed the factors contributing to the dynamic changes. Following the exclusive administration of acellular vaccines (ACVs) within China's national immunization program (NIP) for children, a marked increase in reported pertussis cases has been observed. This uptrend, particularly evident from 2016 to 2019 (Fig. 1), saw reported cases surpass 30,000 in 2019, echoing infection levels from the late 1980s. This rise, diverging from expected natural cyclic patterns, has been recognized as a resurgence of pertussis across China, a view broadly supported by national health experts.2Chinese Preventive Medicine AssociationVaccine and Immunology Branch of the Chinese Preventive Medicine Association. Expert consensus on the China Pertussis Initiative.Zhonghua Liu Xing Bing Xue Za Zhi. 2021; 42: 955-965https://doi.org/10.3760/cma.j.cn112338-20210308-00186Crossref Scopus (4) Google Scholar Additionally, there is consensus among these experts that the reported cases might significantly underestimate the actual scope of the epidemic. Key factors identified as contributing to this increase include enhanced disease awareness, improved surveillance and diagnostic capabilities, notably through the adoption of polymerase chain reaction (PCR) testing, and the relatively brief duration of immunity conferred by ACVs.2Chinese Preventive Medicine AssociationVaccine and Immunology Branch of the Chinese Preventive Medicine Association. Expert consensus on the China Pertussis Initiative.Zhonghua Liu Xing Bing Xue Za Zhi. 2021; 42: 955-965https://doi.org/10.3760/cma.j.cn112338-20210308-00186Crossref Scopus (4) Google Scholar, 3Pertussis vaccines: WHO position paper - September 2015..Wkly Epidemiol Rec. 2015; 90: 433-458PubMed Google Scholar The advent of COVID-19 at the end of 2019 and subsequent NPIs aimed at outbreak control have also impacted the epidemiology of other infectious diseases due to the emergence of immunity gaps.4Cohen R. Ashman M. Taha M.K. et al.Pediatric Infectious Disease Group (GPIP) position paper on the immune debt of the COVID-19 pandemic in childhood, how can we fill the immunity gap?.Infect Dis Now. 2021; 51: 418-423https://doi.org/10.1186/s12889-023-16009-8Crossref PubMed Scopus (2) Google Scholar Over the four years of the COVID-19 pandemic, China's prevention and control strategies evolved from strict containment to a dynamic zero-case policy, culminating in an almost complete reopening at the onset of 2023.5Tang S. Wang X. Tang B. et al.Threshold conditions for curbing COVID-19 with a dynamic zero-case policy derived from 101 outbreaks in China.BMC Public Health. 2023; 23: 1084https://doi.org/10.1016/j.idnow.2021.05.004Crossref Scopus (122) Google Scholar This period saw significant atypical shifts in the epidemiology of pertussis (Fig. 1). Unlike the pre-COVID-19 pattern of gradual increases from January to August, followed by a swift decline, 2020 (1,141 cases) began with numbers comparable to January 2019 (1,260 cases) but then saw a sustained drop, creating a sharp decline in the annual trend. This was followed by a notable increase through 2021 and into 2022, reaching a peak in August 2022 (5,355 cases), with numbers then quickly diminishing by February 2023 (538 cases). The pattern observed in 2022 mirrored pre-pandemic years, yet monthly figures reached new heights not seen since 2010, culminating in the highest reported cases over the past three decades. This rebound coincided with the implementation of dynamic zero-case policies for COVID-19 control. With the initiation of "Class B infectious disease Class B management" for COVID-19 in early 2023, leading to nearly full societal reopening, the pattern of pertussis cases in 2023 resembled that of 2021, but with a significantly steeper increase in the latter half of the year, culminating in a pronounced peak. The numbers of reported cases in November and December reached 6,410 and 9,126, which made a very prominent peak end in Fig. 1. The numbers of reported cases continued to increase throughout the year with a peak in winter, which formed an obvious characteristic of off-season outbreak. The unusual pertussis epidemic patterns observed in the last four years relate to various factors, including heightened attention to respiratory infections post-COVID-19 outbreak and the broad acceptance of nucleic acid testing methods like PCR. The inclusion of such testing in national diagnostic criteria of pertussis at the end of 2023 is likely a significant factor in the observed surge. Other factors should be involved. First, similar to off-season epidemics of other pathogens, such as invasive group A streptococcus infection,6Ledford H. Why is strep A surging - and how worried are scientists?.Nature. 2022; 612: 603https://doi.org/10.1038/d41586-022-04403-yCrossref PubMed Scopus (7) Google Scholar the build-up of susceptible populations due to decreased exposure and interrupted vaccination efforts during the pandemic is related to the surge of pertussis. Second, the precise adjustment of NPIs may cause this atypical surge. Because the natural characteristics of pertussis, including susceptible persons, disease course, incubation period and infectious period, epidemic season and region, are quite different from those of COVID-19. The NPIs adopted for COVID-19 control could not stop pertussis transmission, but might provide favorable conditions for this infection.7Yao K. Deng J. Beware of atypical epidemiological changes of infectious diseases.Zhonghua Shi Yong Er Ke Lin Chuang Za Zhi. 2023; 38 (DOI:): 829-832https://doi.org/10.3760/cma.j.cn101070-20230914-00193Crossref Scopus (0) Google Scholar Third, the absence of booster vaccinations for older demographics may play a role in the pandemic of pertussis in China. In the national immunization program, no booster is recommended for children more than two years old. Fourth, the erythromycin-resistance Bordetella pertussis (ERBP) strains emerged in China. Furthermore, the bacterial strains expressing ptxP3 allele with higher virulence had been found acquired this resistance.8Wu X. Du Q. Li D. et al.A cross-sectional study revealing the emergence of erythromycin-resistant Bordetella pertussis carrying ptxP3 alleles in China.Front Microbiol. 2022; 13901617https://doi.org/10.3389/fmicb.2022.901617Crossref Scopus (8) Google Scholar The continuous monitoring discovered that the dominant position of ERBP expressing ptxP1 allele (ERBP-ptxP1) in clinical isolates has been replaced by ERBP-ptxP3 in the atypical epidemic, from 2020-2022. The proportion of ERBP-ptxP1 and ERBP-ptxP3 in 2019 were 91.6% (109/119) and 0% (0/119), which in 2022 were 19.6% (18/92) and 80.4% (74/92), respectively (not published data). Similar changes have been confirmed in Shanghai, China.9Cai J. Chen M. Liu Q. et al.Domination of an emerging erythromycin-resistant ptxP3 Bordetella pertussis clone in Shanghai, China.Int J Antimicrob Agents. 2023; 62 (Epub 2023 Apr 30.)106835https://doi.org/10.1016/j.ijantimicag.2023.106835Crossref Scopus (4) Google Scholar The ERBP-ptxP1 lineage has been found in neighboring countries, which attracted regional public health attention.10Feng Y. Chiu C.H. Heininger U. et al.Emerging macrolide resistance in Bordetella pertussis in mainland China: Findings and warning from the global pertussis initiative.Lancet Reg Health West Pac. 2021; 8100098https://doi.org/10.1016/j.lanwpc.2021.100098Abstract Full Text Full Text PDF Scopus (20) Google Scholar The ERBP-ptxP3 has a stronger potency to break through immune selection pressure and is more likely to have a wider spread. This shift towards higher resistance and virulence in China underscores the urgent need for intensified international surveillance and public health initiatives. The pertussis continues to pose a significant public health challenge in China, with a record 15,275 cases reported in January 2024. Therefore, it is imperative to enhance disease surveillance, clinical management, immunization practices, and vaccine development to effectively address this ongoing challenge.2Chinese Preventive Medicine AssociationVaccine and Immunology Branch of the Chinese Preventive Medicine Association. Expert consensus on the China Pertussis Initiative.Zhonghua Liu Xing Bing Xue Za Zhi. 2021; 42: 955-965https://doi.org/10.3760/cma.j.cn112338-20210308-00186Crossref Scopus (4) Google Scholar This work was supported by the National Natural Science Foundation of China [81973100].

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