Vital Surveillances: Thirty Years of Experience of Acute Flaccid Paralysis Surveillance for Polio — China, 1993–2022

In China, real-time AFP surveillance is a mandatory initiative overseen by China CDC, with the annual submission of results to the WHO Regional Committee. The identification of AFP cases depends on both passive reporting from hospitals and active surveillance conducted by staff at county CDC. Since the inception of a nationwide infectious disease surveillance system in 1991, virtually all hospitals at or above the county level have been reporting AFP cases. County CDC personnel thoroughly investigate each AFP case, gathering stool specimens that are later transported to provincial laboratories for virus isolation. Positive isolates are subsequently forwarded to the National Poliovirus Laboratory at China CDC, recognized as a WHO regional reference laboratory, for intratypic differentiation and genome sequencing. All data are meticulously recorded in the AFP Surveillance Information Reporting and Management System.

Annually, quality indicators are computed at the national level and juxtaposed with WHO criteria. These indicators assess the sensitivity, comprehensiveness, and promptness of notification, investigation, and laboratory examinations.

The sensitive threshold for AFP surveillance set by the WHO aligns with China’s AFP surveillance guidelines, requiring the detection of at least one AFP case per 100,000 individuals under 15 years per year. Adherence to the WHO protocol for sample collection, necessitating the retrieval of two adequate stool samples within a 14-day period, stands at 80% efficiency (1). In accordance with China’s AFP surveillance guidelines, key criteria include an 80% rate for prompt investigation within 48 hours of case identification, timely receipt of stool samples within seven days, availability of poliovirus isolation results within 30 days, and the swift shipment of poliovirus-positive specimens to the national laboratory within a 30-day window.

Clinically compatible polio cases are defined as AFP cases lacking stool specimens or having inadequate stool specimens without detection of WPV or vaccine-derived poliovirus (VDPV). These cases cannot be definitively ruled out for polio by provincial expert diagnostic teams, irrespective of residual paralysis, death, or loss of follow-up.

Excluded polio cases refer to AFP cases falling into one of two categories: 1) cases presenting with eligible stool specimens wherein neither WPV nor VDPV are identified; 2) cases lacking suitable stool specimens or presenting with inadequate specimens, with no detection of WPV or VDPV, yet conclusively ruled out as polio cases by regional expert diagnostic teams, irrespective of any residual paralysis, mortality, or loss of follow-up.

Descriptive statistics were utilized to summarize the demographic characteristics of AFP cases. Data on non-polio AFP (NPAFP) detections and population statistics were sourced from the China CDC information system. The analysis was performed using Microsoft Excel (version 2019, Microsoft, Redmond, USA).

Individual-level, case-based AFP surveillance is required and is not subject to ethical review.

Table 1illustrates the results of AFP surveillance and sensitivity indicator values over the 30-year study duration. A total of 150,779 AFP cases were identified and reported, with 149,386 cases (99%) occurring in children under the age of 15. The annual reported cases of AFP varied from 1,879 in 1993 to 6,205 in 2011.

During the surveillance period, AFP surveillance identified 63 cases of WPV in 1993 and six in 1994. Additionally, five imported WPV cases were reported in 1995, 1996, and 1999. In 2011, Xinjiang reported 21 cases of WPV associated with AFP. No other instances of paralytic WPV infection were documented throughout the study period.

Among cases of AFP in individuals under 15 years of age, 140,429 (94%) were diagnosed as non-polio, 1,619 (1.1%) were clinically compatible cases that tested negative for poliovirus, and 24 cases were identified as VDPV cases. Eighty-two percent of clinically compatible cases were reported before 2000. The number of clinically compatible polio cases declined from 307 in 1994 to 42 in 1997, further dropping to fewer than 10 cases in 2007, and reaching zero in 2016, with no reported cases since, except for a slight increase in 2011 in Xinjiang attributed to enhanced AFP surveillance during an outbreak.

The surveillance sensitivity indicator for detecting NPAFP among children under 15 years of age showed an increase over the study period, rising from 0.37 cases per 100,000 in 1993 to 2.76 per 100,000 in 2012. The NPAFP detection rate in children under 15 surpassed the criterion of 1 per 100,000 for 28 consecutive years (1995–2022) and exceeded 2 per 100,000 for eleven of those years.

Of the 140,429 cases of NPAFP identified, 55,634 (40%) received definitive diagnoses. Among these, 9,505 cases were attributed to Guillain-Barré syndrome (GBS), 3,024 to non-polio enterovirus (NPEV) infection, 1,158 to transverse myelitis, and 1,116 to traumatic neuritis. The most prevalent category was classified as “others,” underscoring the diverse range of factors contributing to AFP in pediatric cases (Figure 1).

Figure 1.

Final diagnosis of NPAFP cases <15 years old in China, 1993–2022.

Abbreviation: GBS=Guillain-Barré syndrome; NPEV=Non-polio enterovirus; NPAFP=non-polio acute flaccid paralysis.

Two indicator definitions remained consistent throughout the study period: investigating within 48 hours and collecting an adequate stool sample within 14 days of paralysis. Both indicators have an established criterion of 80%. Investigation timeliness has consistently met or exceeded the 80% target annually since 1995, while stool sample timeliness achieved the 80% target in 1996 and has been maintained at over 80% ever since.

Definitions for three indicators were modified over the study period. The timeframe for receipt of stool samples by provincial CDCs was adjusted from ten days in 1993 to seven days in 1995. Similarly, the timeline for isolation results being available at provincial CDC laboratories was altered from 45 days in 1993 to 30 days in 1995, then to 28 days in 2003, and finally to 14 days in 2015. Despite more stringent criteria, China’s AFP surveillance system achieved and maintained 80% targets in 1996 and 1997. The indicator tracking poliovirus-positive specimens shipped to the national polio laboratory (NPL) fluctuated between 35% and 100%, with the timeframe changing from 30 days in 1997 to 14 days in 2003 (Figure 2).

Figure 2.

Timeliness indicators of AFP surveillance in China, 1993–2022.

Since 1995, China’s AFP surveillance system has consistently met both the WHO and national sensitivity criteria. From 1993 to 2022, the system identified 95 cases of WPV and 24 cases of vaccine-derived poliovirus among over 150,000 AFP cases. Through thorough investigations, these cases were found not to be polio-related. Maintaining accurate and sensitive polio surveillance is crucial for preserving a polio-free status in both pre- and post-global polio eradication efforts. This study represents the initial account of the results generated by the AFP surveillance system over the years leading up to China’s polio-free certification in 2000 and the subsequent years thereafter.

The AFP surveillance system’s detections of WPV have been crucial for upholding the polio-free status. For instance, in Xinjiang in 2012, AFP surveillance identified 21 WPV cases, which, through subsequent investigations, were determined to be import-related with evidence of local transmission. The prompt detection facilitated a swift response that safeguarded China’s polio-free status (9).

AFP surveillance identified 24 VDPV cases, some of which were previously documented (10-11). Following WHO recommendations, response measures were implemented for each VDPV case. Given the continued use of live poliovirus vaccines, the emergence of VDPVs capable of transmission and causing paralysis is expected, underscoring the importance of AFP surveillance in identifying paralytic cases indicative of VDPV outbreaks. As the global eradication of polio progresses, AFP surveillance will play a pivotal role as an essential element of a robust polio surveillance system.

AFP surveillance, although critical, may not suffice for comprehensive poliovirus detection, as it lacks the ability to identify polioviruses in asymptomatic children. An incident in Shanghai during 2020–2021 illustrated this limitation, where two circulating VDPV (cVDPV) type 3 were detected in a non-paralyzed child and an environmental sample, which genetic analysis revealed genetically linked (12). Despite the evidence of poliovirus circulation, no paralysis cases were reported. Similarly, a child diagnosed with a primary immunodeficiency (PID) without paralysis was found to harbor an VDPV, namely iVDPV, in stool samples (13). Silent infections like these are beyond the scope of detection by AFP surveillance; however, they can contribute to poliovirus transmission. Therefore, supplementary surveillance methods are imperative, including environmental (wastewater) surveillance and poliovirus monitoring in children newly diagnosed with PID. The evolution of AFP surveillance into an integrated disease surveillance system holds promise for sustained polio control and may yield benefits in managing other infectious diseases (14).

In order to enhance quality assurance, our AFP surveillance system underwent enhancements and modernizations concurrent with advancements in surveillance practices and program development. Initially, from 1991 to 1993, AFP cases were documented on paper and in written correspondence. Subsequently, spanning the years 1994 to 2003, case data for AFP were managed at the local level before being transmitted to China CDC via monthly email communications. Between 2004 and 2011, AFP surveillance transitioned to a client-server Internet platform that facilitated data analysis, with provincial CDC personnel submitting case details on a monthly basis. By 2012, the AFP surveillance mechanism had been integrated into China’s national disease reporting framework, operating as a real-time online system (4).

The evaluation of AFP surveillance quality relies on two key performance indicators: the NPAFP detection rate and the percentage of AFP cases with adequate stool specimens. A NPAFP rate of ≥1/100,000 is deemed sufficiently sensitive for poliovirus detection. The benchmark for AFP cases with adequate stool specimens is set at ≥80%. Our research reveals a swift and sustained enhancement in surveillance indicators. Amid the COVID-19 lockdown from 2020 to 2022, certain timeliness indicators may have been adversely affected in selected PLADs; nonetheless, national annual indicators consistently met the 80% benchmark. The rapid decline in polio-compatible cases early on signifies improvements in stool sample collection and laboratory diagnosis procedures, signaling the need for continued enhancements. Despite unchanged surveillance guidance since 2006, there persists a subset of AFP cases lacking specific diagnoses or final classifications. The fluctuating proportion of positive samples forwarded to the NPL throughout the study period underscores the necessity for ongoing refinements.

Our study is constrained by the fact that definitions for VDPV cases were modified in 2016, likely resulting in potential underestimation of VDPV cases prior to the alteration. Furthermore, the relatively low counts of “No. of AFP cases” and “<15 NPAFP” in 1993 could be attributable to the nascent stage of the AFP surveillance system at that time.

In conclusion, AFP surveillance has been pivotal in China’s effort to attain and uphold polio-free status, identifying 119 polio cases among 150,000 AFP cases over a 30-year period. The significance of AFP surveillance remains paramount, even post global polio eradication. Key performance indicators, such as the NPAFP rate and the proportion of AFP cases with sufficient stool specimens, have consistently met both WHO and national standards, demonstrating the effectiveness of China’s AFP surveillance system in detecting polioviruses. Given the ongoing risks associated with WPV and cVDPV importation and transmission, maintaining a highly sensitive and timely AFP surveillance system will be essential to upholding polio eradication efforts in China and worldwide (15).

No conflicts of interest.

All provincial and local Centers for Disease Control and Prevention in China.