Correlation analysis between positivity rate of immunoglobulin G antibodies against pertussis toxin among community-based populations and reported pertussis incidence in Shandong, China: A seven-year seroepidemiological study

doi:10.21203/rs.3.rs-4855165/v1

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Correlation analysis between positivity rate of immunoglobulin G antibodies against pertussis toxin among community-based populations and reported pertussis incidence in Shandong, China: A seven-year seroepidemiological study

https://doi.org/10.21203/rs.3.rs-4855165/v1

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Background

The reported annual incidence of pertussis in China has shown a marked increase over the past decade, but it may be still underestimated. The purpose of this study was to understand the seroepidemiologic characteristics of pertussis in community-based populations and to assess the level of pertussis infection in the population.

Methods

Between 2017 and 2023, one or two cities in each of the eastern, central and western regions of Shandong Province were selected as survey sites, and a total of six age groups of healthy individuals were enrolled by multistage stratified random sampling to carry out the survey. The serum level of pertussis toxin (PT) IgG (PT-IgG) antibody was quantified by indirect enzyme-linked immunosorbent assay.

Results

A total of 9,238 subjects were enrolled, and the mean positive rate of PT-IgG antibody was 8.05% (95%CI: 7.50%~8.60%), with the highest in 2019 (10.70%, 95% CI: 9.19%~12.21%) and the lowest in 2020 (6.32%, 95% CI: 4.98%~7.66%). The highest positive rate was found in the age group of less than 3 years old (11.46%, 95%CI: 9.87%~13.05%), and the lowest rate was found in the 3 ~ 5 years group (5.40%, 95%CI: 4.28%~6.52%). There was a significant difference in the positive rate between age groups (χ² = 43.098, P < 0.001). Comparison of trends in recent infection rates and reported incidence rates in the population, that showed a very strong linear correlation in the annual distribution (r = 0.821, P = 0.023), and a extremely weak linear correlation in age distribution (r = 0.086, P = 0.872). Estimated infection rates (/100,000) among people aged ≥ 3 years ranged from 5,257 (95%CI: 3,918 ~ 6,596) to 24,449 (95%CI: 22,157 ~ 26,740) by years, with estimated infection rates in eastern region (31,544.44-fold) and in older age group (292,340.00-fold for ≥ 20 years old group, 216,388.89-fold for 17 ~ 19 years old group) differed significantly from the reported incidence rate.

Conclusions

The annual distribution trend of reported pertussis incidence rate aligns with the infection rate observed among community populations, the actual level of infection is likely to be seriously underestimated. Therefore there is a need to emphasize surveillance and consider additional booster immunizations for adolescents and adults.

Pertussis

Seroepidemiology

Antibodies against pertussis toxin

Estimated infection rate

Pertussis, a respiratory infectious diseases caused by Bordetella pertussis, remains a significant contributor important of morbidity and mortality among infants worldwide, despite the existence of vaccines for over eight decades. The implementation of whole-cell pertussis and acellular pertussis vaccines immunization strategies in childhood has undeniably led to a substantial decline in reported pertussis cases and fatalities in this demographic. However, since 1980s, pertussis has reemerged in many countries with long-standing, widespread vaccination programs [1]. The World Health Organization estimates a global incidence of approximately 24.1 million pertussis cases, with 90% occurring in developing countries [2].

In China, the incidence of pertussis prior to vaccine introduction was reported to be between 100 and 200 cases per 100,000 individuals annually [3]. The adoption of standardized immunization schedule since 1966 and the inclusion of combined diphtheria, tetanus, whole-cell pertussis vaccines (DTwP) in the Expanded Programme on Immunization (EPI) since 1978 has significantly reduced the incidence of pertussis. Nevertheless, due to the frequency of adverse reactions associated with DTwP, it was replaced by combined diphtheria, tetanus, acellular pertussis vaccines (DTaP) in 2006. Despite a DTaP coverage rate exceeding 99%, surveillance data indicate a 25-fold increase in reported pertussis cases in 2023 compared to 2009 [4].

The reported annual incidence of pertussis in China has shown a marked increase over the past decade, it is still be underestimated. Current diagnostic criterion for laboratory confirmed pertussis case require either a positive culture or a four-fold rise in IgG titers from the acute to convalescent phase, and lack of inclusion of polymerase chain reaction (PCR) in the national case definition guideline in a reliance on clinical symptoms for reporting. This approach may not accurately reflect the true epidemiological burden of pertussis, as milder clinical presentations are often not recognized or diagnosed. This is particularly relevant for pertussis infections in vaccinated teenagers and adults with well-established immune system, who serve as important reservoirs for transmission to unvaccinated or partially protected infants and young children or partially protected infants and young children.

Shandong Province, a populated region in China, with a residents’ population exceeding 100 million, has been at the forefront of enhancing pertussis epidemiological understanding and surveillance. Since 2016, the province has proactively implemented advanced surveillance measures, including laboratory confirmation through the detection of IgG antibodies against pertussis toxin and the use of PCR for ascertainment of infectious cases, ahead of other regions in the country. This enhanced surveillance mechanism has also partly contributed to a heightened diagnostic awareness among physicians for pertussis. Consequently, the reported incidence of pertussis in Shandong Province has seen a 4-fold increase from 2016 to 2018. Despite this significant rise in reported cases, the incidence rate continues to exhibit a marked downward trend with increasing age, ranging from 0.02 to 0.14 per 100,000 individuals annually among those aged 20 years and older. The current disease surveillance system in Shandong Province, while demonstrating progress still grapples with challenges related to its activity and sensitivity, further research is imperative to elucidate the genuine epidemiological landscape of pertussis in the province.

Seroepidemiological survey represent a pivotal enhancement to pertussis surveillance activities and are instrumental in the assessment of outbreaks, a strategy that has been adopted and reviewed in various international contexts [5, 6]. In the present study, we conducted a continuous seroepidemiological survey within a randomly selected population to ascertain the seroprevalence of pertussis infection across different epidemic phase. Additionally, we sought to evaluate the correlation between the positivity rate of immunoglobulin G antibodies against pertussis toxin among community-based populations and reported pertussis incidence in Shandong from 2017 to 2023. The objective of this research is to evaluate the epidemiological characteristics and infection status of pertussis in real-word settings, and further provide evidence that can be utilized to refine the current immunization strategies and preventive interventions.

Study design and sample collection

Based on geographical layout, Shandong Province was segmented into three distinct regions, eastern (Qingdao, Yantai, Weifang, Weihai, and Rizhao), central (Jinan, Zibo, Dongying, Tai'an, and Linyi City) and western (Zaozhuang, Jining, Dezhou, Liaocheng, Binzhou, and Heze City). Each year one or two cities from each region were selected, and within these cities, a random selection process was employed to identify one county (district) as the survey sites. The participants enrolled in the study were healthy individuals who didn’t exhibits symptoms of respiratory infection and had not used antibiotics in the three months preceding the survey, and had resided in the survey site for at least 12 months. The subjects were stratified into six age-based subgroups (< 3 years, 3–5 years, 6–12 years, 13–16 years, 17–19 years, and ≥ 20 years). Within each age group, a rand sample of 30 to 50 individuals were selected, ensuring a balanced gender distribution. Serum specimens were collected from each participant, and the demography and epidemiology information such as name, gender, age, residential area, medical history, and vaccination status of pertussis were recorded in the questionnaire. A total of 9,238 datasets were collected from 2017 to 2023.

Laboratory testing

Specimens were assayed for immunoglobulin G antibodies against pertussis toxin utilizing the Enzyme-linked immunosorbent assay method at the laboratory of Shandong Provincial Center for Disease Control and Prevention, using the Anti-Bordetella pertussis toxin ELISA (IgG) commercial kit (EUROIMMUM Medizinische Labordiagnostika AG, Germany), adhering strictly to the manufacturer’s protocols. The interpretation of the antibodies against Bordetella pertussis toxin of class IgG (PT IgG) was based on current publications and guidelines. The established cut-off for a positive result was set at level 40 IU/mL. Specimens with PT less than 40 IU/mL was considered to show no evidence of past Bordetella pertussis infection. Levels ranging from 40 to less than 100 IU/mL were interpreted as indicative of exposure to the pathogen within the 2 years preceding sample collection. And PT IgG levels exceeding 100 IU/mL was classified as an acute infection or recent vaccination, which would have occurred within the past year.

Reported incidence of pertussis

Data on pertussis case were sourced from National Notifiable Disease Reporting System (NNDRS). To calculate the incidence rate of pertussis, the number of reported cases was divided by the total population, with the rate expressed per 100,000 individuals, the population figures used as the denominator in these calculations were obtained from Shandong Statistical Yearbook [7].

Estimated incidence of pertussis

The estimation of pertussis infection incidence was in accordance with the methodologies outlined in established literature [8–9]. It was shown that following a pertussis infection, PT IgG levels typically decline to 100 IU/mL within an average of 58.6 days. Utilizing the 100 IU/mL threshold, the incidence of infection was calculated using the formula: 365.2/58.6 × the proportion of subjects with PT IgG levels at or above 100 IU/mL To ensure the accuracy of incidence assessment, it was necessary to account for potential interference from recent vaccination with pertussis-containing vaccines. Consequently, the incidence estimation excluded individuals who had received such vaccinations within the past 12 months. Considering the current immunization schedule in China, which includes 4 doses of pertussis vaccine administered at 3, 4, 5, and 18–24 months of age, the incidence estimation of pertussis infection in this study was limited to the population aged three years and older.

Statistical analysis

Data analysis was performed using Microsoft Excel 2020 and IBM SPSS Statistics 26 software. Quantitative variables were summarized by means along with their corresponding 95% Confidence Interval (CI), and qualitative variables were presented as percentages. The chi-squared test was used to test the rate or the composition ratio of the population across different time periods, regions, age groups, and gender. A significant level of P < 0.05 was used to determined statistical significance. Spearman correlation coefficient r was used to determine the linear correlation relationship between the positive rate of PT-IgG antibodies and the reported incidence rate of pertussis.

A total of 9,238 blood specimens were collected from healthy individuals from 2017 to 2023. The analysis of these specimens revealed that 744 cases tested positive for anti-PT IgG antibodies, yielding a mean positive rate of 8.05% (95% CI: 7.50%~8.60%). Within this positive group, 246 cases were identified as indicating acute or recent pertussis infections, corresponding to a mean infection rate of 2.66% (95% CI: 2.33%~2.99%). The majority of specimens, 8,494 in total, yielded negative results for anti-PT IgG concentration, representing 91.95% of the sample population (95% CI: 91.40%~92.50%). Additionally, 4,509 specimens had anti-PT IgG concentrations below the lower detection limit of the assay, constituting 48.81% of the total specimens collected (95% CI: 47.79%~49.83%) (Table 1).

Time correlation

The analysis of anti-PT IgG antibody positivity rates and recent infection rates revealed that both metrics reached their peak in 2019, with a positivity rate of 10.70% (95% CI: 9.19%~12.21%) and a recent infection rate of 4.17% (95% CI: 3.19%~5.15%). Conversely, the lowest rates were observed in 2020, with a positivity rate of 6.32% (95% CI: 4.98%~7.66%) and a recent infection rate of 1.26% (95% CI: 0.65%~1.87%), with significant differences in both rates across between years (χ² = 23.909, P < 0.001; χ² = 31.566, P < 0.001) (Table 1).

Between 2017 and 2023, a total of 155,979 cases of pertussis were reported in China, with reported incidence rate (per 100,000, the same below) of 0.75 (10,390 cases), 1.59 (22,057 cases), 2.15 (30,027 cases), 0.32 (4,475 cases), 0.68 (9,611 cases), 2.71 (38,295 cases), and 2.92 (41124 cases) for each respective year. At the same period, 23,940 cases were reported in Shandong Province, representing 15.35% of the national level. The reported incidence rates ranged from 0.51 to 5.68, with specific rates of 3.75 (3,729 cases), 5.68 (5,770 cases), 5.04 (5,063 cases), 0.51 (516 cases), 0.55 (563 cases), 5.18 (5,263 cases), and 2.99 (3,036 cases) for each year. The recent infection rate of pertussis among healthy populations in Shandong Province exhibited a fluctuating upward trend and showed a very strong linear correlation with the reported incidence rate of pertussis in Shandong Province (r = 0.821, P = 0.023) for the corresponding year. Additionally, there was a strong linear correlation with the reported incidence rate of pertussis across China (r = 0.750, P = 0.052) (Table 1, Fig. 1).

Population distribution

The survey subjects, spanning 2 months to 81 years of age, were categorized into age groups, each containing a range of 1,407 to 1,643 individuals. The lowest antibody positivity rate was observed in 3 ~ 5 years old group at 5.40% (95% CI: 4.28–6.52%), followed by the 6 ~ 12 years old group with a positivity rate of 7.00% (95% CI: 5.77–8.23%). The highest positivity rate was found in the under 3 years old age group, at 11.46% (95% CI: 9.87%~13.05%), followed by the 17 ~ 19 years old group at 8.67% (95% CI: 7.20%~10.14%). The positivity rates for the 13 ~ 16 years old and ≥ 20 years old age groups were 8.47% (95% CI: 7.07%~9.87%) and 7.53% (95% CI: 6.22%~8.84%), respectively. Significant differences in antibody positivity rates were noted among all age groups (χ² = 43.098, P < 0.001). Among the recent infected individuals, the infection rate in the under 3 years old age group was the highest at 4.10% (95% CI: 3.11%~5.09%), while the 3 ~ 5 years old and 6 ~ 12 years old groups had relatively lower infection rates of 1.72% (95% CI: 1.08%~2.36%) and 1.70% (95% CI: 1.07%~2.33%), respectively. A significant difference in recent infection rates was observed between age groups (χ² = 26.214, P < 0.001) (Table 1).

The reported incidence rate of pertussis in Shandong Province showed a decreasing trend with age over the period from 2017 to 2023. The average reported incidence rates of pertussis in the age groups < 3, 3 ~ 5, 6 ~ 12, 13 ~ 16, 17 ~ 19, and ≥ 20 years were 56.89, 16.90, 7.96, 0.42, 0.05, and 0.09 from 2017 to 2023, respectively. These rates showed an extremely weak correlation with the recent infection rates surveyed among healthy subjects (r = 0.086, P = 0.872) (Table 2).

The ratios for male/female were 1.05:1 (4,742:4,496), with antibody positivity rates and recent infection rates (male/female) of 8.22% (95% CI: 7.44%~9.00%) / 7.87% (95% CI: 7.08%~8.66%), 2.70% (95% CI: 2.24%~3.16%) / 2.62% (95% CI: 2.15%~3.09%), respectively. No significant differences were found between the male and female groups for either antibody positivity rates (χ² = 0.383, P = 0.536; χ² = 0.050, P = 0.824) (Table 1).

Regional distribution

The number of survey subjects in each region ranges from 2,734 to 3,543, with the lowest antibody positivity rate observed in the eastern region (7.21%, 95% CI: 6.24–8.18%), and relatively high in the central region (9.46%, 95% CI: 8.41–10.51%). There was a statistically significant difference in antibody positivity rates between regions (χ² = 11.804, P = 0.003). The recent infection rates in the eastern, central and western populations were 2.30% (95% CI: 1.74–2.86%), 3.04% (95% CI: 2.42–3.66%), and 2.62% (95% CI: 2.04–3.20%), respectively, and the difference in recent infection rates between the regions was not statistically significant (χ² = 2.996, P = 0.224).

From 2017 to 2023, the recent infection rate of pertussis among healthy populations in all regions of Shandong Province displayed a fluctuating upward trend. When compared to the reported incidence rates of pertussis in each region, correlations were observed between the two metrics. Specifically, the correlation coefficients were as follows: eastern region (r = 0.487, P = 0.268), central region (r = 0.500, P = 0.253), and western region (r = 0.786, P = 0.036). These correlations were categorized as medium or strong, indicating a linear relationship between the recent infection rate and the reported incidence rate in each respective region (Table 3).

Estimated infection rate of pertussis

From 2017 to 2023, among the 7,702 individuals aged 3 years and older, the recent infection rate of pertussis was 2.38% (95% CI: 2.04%~2.72%) (183 individuals). Utilizing the known attenuation time of antibodies concentration after pertussis infection and the detection threshold of assay, the estimated infection rate (/100,000, the same below) was 14,807 (95% CI: 14,014 ~ 15,601). The estimated infection rates for each year showed significant variability, with the highest rate record in 2019 (24,449, 95% CI: 22,157 ~ 26,740) and the lowest in 2020 (5,257, 95% CI: 3,918 ~ 6,596). The estimated infection rates of pertussis in each year were found to be approximately 4,766.40 ~ 31,633.33 times higher than the reported incidence rates, with an average multiplier of 9,312.58 times the reported incidence rate (Table 4).

In examining the age distribution of the estimated infection rates, it was observed an upward trend with age, The estimated infection rates for the 3 to 5 years old group and the 6 to 12 years old group were 10,697 (95% CI: 9,170 ~ 12,225) and 10,621 (95% CI: 9,131 ~ 12,111), respectively. These rates were relatively lower compared to the infection rates observed in older age groups. The infection rate began to rise significantly from 12 years old, with the highest estimated infection rate recorded in the ≥ 20 years old group, at 19,475 (95% CI: 17,515 ~ 21,435). The disparity between estimated infection rate and reported incidence was the most pronounced in the older age group. The exceed incidence was 29,2340.00-fold for the 17 ~ 19 years old group and 216,388.89-fold for the ≥ 20 years old group (Table 4).

Regarding the regional distribution, the central region exhibited the highest estimated infection rate with 18,412 (95% CI: 16,874 ~ 19,951). Conversely, the eastern region exhibited the lowest estimated infection rate, at 11,356 (95% CI: 10,060 ~ 12,651). The largest difference between estimated infection rate and the reported incidence was observed in the eastern region with a ratio of 31,544.44-fold (Table 4).

The number of reported cases of pertussis in Shandong Province has experienced a notable increase from 2008 to 2023, with a particularly significant surge following the strengthen surveillance of pertussis carried out in 2016 province wide. The reported incidence rate in 2022 (5.18/100,000) was 46 times higher than that in 2008 (0.11/100,000), marking a pronounced trend known as the "reappearance of pertussis" [10]. The current case reporting system in China primarily relies on clinical symptoms, which may lead to underreporting due to lack of laboratory confirmation, especially among adolescents or adults with atypical symptoms or those who do not seek medical care. Consequently, the actual incidence of pertussis is likely to be significantly underestimated. Anti-PT IgG is a pertussis-specific antibody, and a single serum sample with a titer exceeding the established threshold is generally acknowledged as an indicator of recent infection or vaccination within the past 12 months [11]. This serological marker has been utilized in many countries to characterize the epidemiology of pertussis and estimate the infection rate within populations [8, 12–14]. The surveillance data from this study revealed a very strongly linear correlation (r = 0.821, P = 0.023) between the annual distribution trend of the positive rate of pertussis antibody among healthy populations in Shandong Province and the reported incidence rate. These findings suggest that conducting a seroepidemiological survey of PT IgG antibody among healthy populations can provide a more accurately assessment of the actual infection level of pertussis.

Given the current immunization program for the pertussis in China, the antibody levels in young children are likely influenced by both vaccination and natural infections. Anti-PT IgG antibodies tend to sharply decrease following a pertussis infection for 1 ~ 2 years. Therefore, surveillance data among individuals aged ≥ 3 years can be used to estimate the clinical infection rate rather than vaccination. The findings of this study revealed that the average recent infection rate among the ≥ 3 years population in Shandong Province was 2.38% over recent years, with the estimated infection rate of 14,807 per 100,000 individuals. In stark contrast, the average annual reported incidence for the same population was a mere 1.59 per 100,000 individuals. This significant discrepancy suggests that the actual infection rates of pertussis in Shandong Province substantially exceed those reported by physicians based on clinical findings. Similar observations have been reported in other regions of China. Research conducted in Beijing, Chongqing and Tianjin found that the infection rates were more than 6,000/100,000 among individuals over 5 years old [9], 7,290/100,000 [15], and 10,852/100,000(4 ~ 83 years old) [16], respectively.

Several factors contribute to the substantial discrepancies between reported pertussis cases and the estimated incidence of infection. Firstly, the current statutory infectious disease reporting system in China notified passively based on typical clinical diagnosis, and some general practitioners do not take a great attention and awareness of pertussis, that makes it difficult to be definitive diagnosed for mild cases, atypical patients, and mixed infections with multiple pathogens. Secondly, the increase in pertussis testing such as PCR and ELISA, following recognition of early epidemic cases has led to identification of previously undetected infections, resulting in a further increase in reported cases and awareness among general practitioners [17–18]. However, these diagnostic methods have not been widely adopted in medical institutions in China due to the absence of national diagnostic standards and lack of uniform criteria for interpreting test results across different countries. In a survey of the laboratory diagnostic capacity for pertussis in Grade Ⅱ and Ⅲ medical institutions of Shandong Province in 2018 revealed that only 3.7% (20/543) of medical institutions conducted laboratory testing. These institutions accounted for 67.44% (3,891/5,770) of the total pertussis cases reported in the province. The eastern region, with no institutions conducting testing out of 156 surveyed (0, 0/156), was found to have significant insufficient in testing capacity compared to central region (4.76%, 8/168) and the western region (5.48%, 12/219) [19]. Our study shows that there was no significant difference in the recent infection rate among populations in the eastern (2.30%), central (3.04%) and western (2.62%) population (χ² = 2.996, P = 0.224). However, the reported incidence in the eastern part (0.76/100,000) was significantly lower than that in the other two regions (χ² = 6,230.387, P < 0.001). This disparity suggests that lack of laboratory diagnosis may be a significant factor contributing to the underrecognition of pertussis. Furthermore, adolescents and adults infected with pertussis often exhibit asymptomatic, mild or persistent coughing [20], which may lead to a neglect of medical treatment. This can have a detrimental effect on the identification and control of cases, ultimately exacerbating the spread of the disease. In China, the reported cases of pertussis were dominated by infants and young children, with substantial proportion of cases occurring in children under 3 years old. From 2011 to 2017, this demographic accounted for 82.46% of reported cases [21], and from 2018 to 2021, the proportion decreased to 72.31% [22]. In recent years, some countries have reported a rapid increase in pertussis cases among adolescents and adults, such as the European Union, where cases over 15 years of age accounted for 62% of the total number of reported cases in 2018 [23]. This shift highlights the underreporting of pertussis among middle-aged individuals, which is a concerning issue as it suggests that the true burden of the disease in this demographic may be significantly higher than reported [24]. In Shandong Province, this trend is also evident, with the proportion of reported cases among children under 3 years old decreasing from 73.61% (2,745/3,729) in 2017 to 24.97% (758/3,036) in 2023. However, the proportion of cases among individuals ≥ 20 years old has remained relatively stables, averaging 1.96%. The results of this study revealed that the estimated infection rate of pertussis increased with age, and the largest discrepancy between estimated and reported incidence observed in the older age groups. Specifically, the estimated infection rate was 292,340.00-fold higher in the 17 ~ 19 years old group, and 216,388.89-fold higher in the ≥ 20 years old group compared to the reported incidence. This suggests that the lack of awareness of pertussis infected in adolescents and adults, as well as insufficient surveillance for adult cases, are key factors contributing to the underreporting of pertussis in these age groups.

Our analysis has brought to light several critical issues. First, the estimated incidence of pertussis infections across all age groups significantly exceeds the rates reported by physicians based on clinical diagnosis, emphasizing the inadequacy of the current surveillance system, relies primarily on case reporting, and highlights the utility of seroepidemiology as a complementary tool to enhance disease surveillance alongside existing programs. Secondly, there is a notable discrepancy between the age-specific profile of the reported incidence and the estimated infection profile among community-based populations. The highest reported prevalence is observed among young children under the age of 6, which is characterized as hyper-endemic. While the infection rates detected among the population are lowest in the 3 to 12 years old group, with rates increasing with age and reaching a peak in the population over 20 years old. This suggest that there is a need to focus on surveillance efforts and consider additional booster immunizations for adolescents and adults. Additionally, the use of laboratory confirmation through PCR or serological testing has emerged as pivotal diagnostic methods, which offer great sensitivity and rapid results for case diagnosis and assessing the infection rates within the population, and that is essential for accurately depicting the true prevalence of pertussis.

IgG pertussis toxin IgG

Ethics approval and consent to participate

This study was registered and approved by Institutional Review Board of Shandong Center for Disease Control and Prevention (2015WS0271). This is a cross-sectional study with human subjects, before sample collection, all participants included in this study signed an informant consent. To preserve the confidentiality the data is not exposed to any third party except investigators.

Consent for publication

Not applicable.

Competing interests

The authors have no competing interests to declare that are relevant to the content of this article. The authors declare they have no financial interests.

Author details

Division of Expanded Immunization Program, Shandong Provincial Center for Disease Control and Prevention; Shandong Academy of Preventive Medicine; Shandong Provincial Key Laboratory of Infectious Disease Control and Prevention, No. 16992 Jingshi Road, Jinan 250014, P. R. China

Funding

This work was supported by the Taishan Scholar Program of Shandong Province (grant number Tstp20221164 and ts201511105).

Author Contribution

All authors participated in the design, implementation, analysis, and critically revising for important academic content of the study. Yan Zhang conceptualized this study, tested laboratory samples and verified results, carried out the initial analyses, interpreted results, drafted the manuscript, and approved the final manuscript as submitted. Li Zhang conceptualized this study, supervised data collection, interpreted the results, reviewed and revised the manuscript, and approved the final manuscript as submitted. All authors reviewed the manuscript.

Acknowledgement

We are grateful to the efforts made by staff of centers for disease control and prevention in sixteen cities of Shandong Province involved in this study. We also thank those participants who took part in the study and provided the samples.

Data Availability

Data is provided within the manuscript or supplementary information files.

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Tables 1 to 4 are available in the Supplementary Files section.

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Correlation analysis between positivity rate of immunoglobulin G antibodies against pertussis toxin among community-based populations and reported pertussis incidence in Shandong, China: A seven-year seroepidemiological study

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Abstract

Background

Methods

Results

Conclusions

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Background

Methods

Study design and sample collection

Laboratory testing

Reported incidence of pertussis

Estimated incidence of pertussis

Statistical analysis

Results

Time correlation

Population distribution

Regional distribution

Estimated infection rate of pertussis

Discussion

Conclusion

Abbreviations

Declarations

Author details

Funding

Author Contribution

Acknowledgement

Data Availability

References

Tables

Additional Declarations

Supplementary Files

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