In this study, we evaluated the capacity of clinical services for patients with STIs in Shandong Province. Specifically, we evaluated the capacity for the laboratory diagnosis of gonorrhea. We found that in the past 6 years, the hospitals that provided STI clinical services for patients had increased in number but decreased in proportion. Although the total number of registered hospitals largely increased in the past 6 years, the coverage of clinical service for patients with STIs did not increase correspondingly. In particular, the number of private hospitals increased rapidly, whereas the proportion of hospitals providing clinical services for patients with STIs was very low and decreased. Although specialized dermatological hospitals increased in proportion, their number was small and decreased. Public general Western medicine hospitals continued to play a core role in STI clinical service in Shandong Province. The proportion of hospitals providing STI clinical service remained as low as 18.53% in 2018, indicating that the availability of STI clinical services in Shandong Province has considerable room for improvement.
The availability of laboratory tests for NG was low in hospitals providing STI clinical services. Among the hospitals surveyed in 2018, over 25% could not provide smear tests for NG, over 60% could not provide culture tests, and about 85% could not provide PCR tests. With the implementation of China's Syphilis Prevention and Control Program (2010–2020), the availability of syphilis tests and screening programs was enhanced and the reported incidence of syphilis increased quickly. Nevertheless, the availability of laboratory tests for NG remained low. This situation may be one of the rational explanations for the “scissors-like differential” phenomenon exhibited by the syphilis and gonorrhea epidemic in China. In 1990s, the reported incidence of gonorrhea was much higher than that of syphilis. It kept increasing to its peak in 1999 and then decreased. A new criterion for the diagnosis of gonorrhea implemented in 2007 defined gonorrhea cases on the basis of pathogenic tests instead of clinical examination. The role of laboratory tests has been emphasized since then.
Although most hospitals could provide smear tests, female gonorrhea cases could not be diagnosed through smear testing in accordance with the criterion for the diagnosis of gonorrhea issued by the National Health Commission of China. The diagnosis of female gonorrhea cases relies on the culture or PCR tests of NG. Most female cases may be under-diagnosed and under-reported due to the low availability of culture and PCR tests. This situation may lead to the high sex ratio of reported gonorrhea cases in China.
All sexually active women aged 24 years or younger and older women who are at a high risk of gonorrhea and chlamydia infection are recommended to undergo PCR test screening . Maternal and child health hospitals should play an important role in the NG screening of females. Laboratory tests for NG are less available in maternal and child health hospitals than in specialized dermatological hospitals and general Western medicine hospitals, and the absence of improvement in the past 6 years might account for the low reported female incidence and high sex ratio of gonorrhea in Shandong Province. Although the smear test is less sensitive for women than for men, it remains the main method for NG screening even in maternal and child health hospitals in Shandong Province. Some countries with high availability for PCR tests for NG report more gonorrhea cases in males than that in females [19, 20]. However, the reasons for this difference may be different. Usually, men who have sex with men are the core high-risk population with a high incidence of gonorrhea in these countries [21–23].
We confirmed that the availability of laboratory tests for NG was related to the case reporting of gonorrhea. The distribution of hospitals with gonorrhea case reporting was consistent with that of hospitals where laboratory tests were available. The availability of culture and PCR tests had improved in class III hospitals, general Western medicine hospitals, and public hospitals from 2012 to 2018. Accordingly, the proportion of hospitals with case reporting increased significantly. An earlier study also found that the increase in the number of gonorrhea cases was related to the PCR testing rate . The diagnosis of female gonorrhea cases relies on the culture or PCR tests of NG. Insufficient laboratory tests may lead to the under-diagnosis and under-reporting of gonorrhea cases, especially female cases, in Shandong Province. In addition, although more than 74% of the surveyed hospitals could provide the smear test for NG in 2012 and 2018, less than 40% reported cases of gonorrhea. This situation indicated that the availability of laboratory tests was not an exclusive factor related to case reporting. We found by interviewing doctors that another factor leading to the under-diagnosis and under-reporting of gonorrhea might be the low awareness of clinical doctors for gonorrhea screening. Many cases of NG infection lack symptoms and most might never be diagnosed without screening. In Canada, midwives, family physicians, and generalist obstetricians tested 93.8%, 91.4%, and 88.5% of their patients, respectively . The low availability of NG screening may lead to the missed diagnosis and under-reporting of gonorrhea in China.
Many factors may affect the availability and use of laboratory tests of NG. The smear test is the most commonly used method for NG screening. It is rapid, convenient, and inexpensive. The sensitivity and specificity of the smear test are high for symptomatic males but low for females [26–28]. The culture method has high sensitivity and specificity and is the gold standard for the diagnosis of gonorrhea . However, compared with other methods, it has more stringent requirements and requires meticulous sample collection and transport and nutrient medium use [30, 31]. The PCR test offers very high detection sensitivity and specificity of above 90% and 99%, respectively. It is recommended for the detection of urogenital infections in women and men with and without symptoms . Compared with culture tests, PCR tests provide more positive results for rectal gonorrhea and pharyngeal gonorrhea . However, its higher equipment and technician requirements compared with the smear and culture tests may restrict its wide use. In California, the total proportion of gonorrhea tests performed by using the PCR test increased from 1–59% and that performed with the culture test decreased from 42–10% . By contrast, the availability of PCR tests was still as low as 15% among hospitals providing STI clinical services in Shandong Province in 2018.
The drug-resistance of NG is increasing in China and other countries [34–36]. The spread of drug-resistant NG has become a threat to controlling gonorrhea effectively worldwide and led to an increasing need for antimicrobial-susceptibility testing. The low availability of laboratory tests of NG and antibiotic abuse may further aggravate drug resistance. In a survey of 57 countries, only 14 reported having antenatal CT or NG screening policies . National-level policies that support routine screening for CT or NG infection to prevent adverse pregnancy and newborn outcomes are uncommon.
Some efforts are needed to improve the screening and reporting of gonorrhea in Shandong. First the accessibility of STI clinical services should be enhanced by integrating the prevention and management of STI into the broad agendas for HIV and sexual and reproductive health and other key platforms. Second, accessibility to innovations should be accelerated through the development of point-of-care (POC) testing. The overall rate of agreement and negative percentage agreement with the POC of NG are 97.8% and 100%, respectively, for NG compared with those of nucleic acid amplification testing (NAAT) methods . The WHO also advocated the development of POC testing as a critical step within the STI cascade and continuum of services. POC testing for urogenital infections may improve case finding and infection management and is feasible in resource-poor settings . The integration of POC testing can mitigate the transmission and burden of STIs . Third, clinician training should be strengthened, and STI interventions should be scaled up. The lack of clinician training is one of the important barriers to performing STI testing . Testing rates among university campuses increased from 7.90–17.86% through education . Finally, the quality assurance of NG laboratory tests should be strengthened. A survey showed that in Kampala, only 5% of the laboratories met or surpassed the lowest quality standards defined by the WHO/AFRO-derived laboratory strengthening tool .
This study has several limitations. First, this investigation was conducted in a province of China, and caution should be taken in generalizing the results. Second, many other factors, in addition to the availability of laboratory tests for NG, may affect the reporting and sex ratio of gonorrhea.