key: cord-303557-bbbq6ylr
authors: Tong, Michael Xiaoliang; Hansen, Alana; Hanson-Easey, Scott; Xiang, Jianjun; Cameron, Scott; Liu, Qiyong; Liu, Xiaobo; Sun, Yehuan; Weinstein, Philip; Han, Gil-Soo; Bi, Peng
title: China's capacity of hospitals to deal with infectious diseases in the context of climate change
date: 2018-04-16
journal: Soc Sci Med
DOI: 10.1016/j.socscimed.2018.04.021
sha: 
doc_id: 303557
cord_uid: bbbq6ylr

OBJECTIVES: Infectious diseases are a major cause of morbidity and mortality in China. The capacity of hospitals to deal with the challenge from emerging and re-emerging infectious diseases due to climate change is of great importance to population health. This study aimed to explore the capacity of hospitals in China to deal with such challenges. METHODS: A cross-sectional questionnaire survey was utilized to gauge information regarding capacity of hospitals to deal with infectious diseases in the context of climate change among 611 clinical professionals whose roles pertained to infectious disease diagnosis, treatment and management in Anhui Province of China. Descriptive analysis and logistic regression analysis were performed on the data. RESULTS: More than 90% of participants believed climate change would have an adverse influence on population health and infectious disease control in China. Most indicated that their hospitals were well prepared for emerging infectious diseases at present, and they considered that logistical support in hospitals (e.g. administrative and maintenance services) should be strengthened for future capacity building. The majority of participants suggested that effective prevention and control measures, more interdisciplinary collaborations, more funding in rural areas for health care, and improved access to facilities enabling online reporting of infectious diseases, were extremely important strategies in building capacity to curb the population health impact of emerging and re-emerging infectious diseases due to climate change in China. CONCLUSIONS: Clinical professionals recognized that climate change will likely increase the transmission of infectious diseases. Although rural health care and hospitals’ logistical support need to be improved, most professionals believed their hospitals to be capable of dealing with emerging diseases. They thought that interdisciplinary and cross-regional collaborations, together with necessary resource support (e.g. improved facilities for rural health care) would be important control strategies.

Currently there are roughly 7 million cases of reported infectious diseases in China, which result in approximately 17,000 deaths annually (National Health and Family Planning Commission of the PRC, 2016) . Previous studies have found the incidence of infectious diseases has been sharply reduced due to great improvements in health care services (Hipgrave, 2011) . However, the emergence and re-emergence of some climate-sensitive diseases, such as malaria, dengue and hemorrhagic fever with renal syndrome (HFRS) have occurred in recent decades in China (Huang et al., 2012; Xiang et al., 2016; Zhang et al., 2010b) . Malaria was a serious public health problem during the 1970s with an incidence of approximately 2800 per 100,000 population . In 2001, the incidence was only 2 per 100,000 with about 20,000 cases reported . However, malaria cases in China increased to 64,178 in 2006 (Zhou et al., 2007) dengue cases were reported prior to 1977, but frequent outbreaks have occurred during the last few decades in China (Lai et al., 2015) . HFRS, a serious zoonotic disease caused by hantaviruses, can be transmitted to humans by contact with infected rodents or their excreta . The disease is frequently reported in China where roughly 90% of the world's cases occur (Xiao et al., 2014) . Although the incidence of HFRS significantly declined during the 1990s, there has been an increasing trend since 2008 (Xiao et al., 2014; Zhang et al., 2014) . The possible reasons for the emergence and re-emergence of these infectious diseases may be linked to climate change, population movement, rapid urbanization and increased surveillance efforts (Tong et al., 2015; Wu et al., 2016) .

It is widely known that the global average combined land and ocean surface temperatures have increased by 0.85°C over the period from 1880 to 2012 (Intergovernmental Panel on Climate Change, 2013). The Intergovernmental Panel on Climate Change (IPCC) indicates that the global average surface temperature will increase by 1.0-3.7°C by 2081-2100 compared to 1986-2005 , and other climatic variations, such as changes in rainfall patterns and relative humidity will also occur (Intergovernmental Panel on Climate Change, 2013). Climate change has, and will continue to, impact the transmission of vector and rodent-borne diseases by affecting the growth and development of the vectors or hosts, shortening the incubation period of the pathogens within the vectors, and impacting human behaviour (e.g. more time spent outdoors) (World Health Organization, 2012). The projected temperature increase and change in rainfall patterns may bring about an increase in cases of infectious diseases such as malaria, dengue and HFRS Zhang et al., 2010a; Zhou et al., 2010) . In China, annual average land surface air temperature has increased by 0.5-0.8°C over the past 100 years, and is projected to increase by 2.3-3.3°C by 2050 as compared to 2000 (China National Development and Reform Commission, 2007) . Extreme climate events, such as extremes in temperature, drought in north China, and flooding in south China, may become more frequent and intensive (China National Development and Reform Commission, 2007) . The variations in temperature, rainfall, humidity and extreme events posed by climate change could facilitate infectious disease transmission and result in the possible increase in cases of infectious diseases in China (Tong et al., 2015) .

In the Chinese health care system, both the clinical health sector and preventive medicine (public health system) play important roles in the protection of population health. In the clinical health system, hospitals provide patient diagnosis, treatment and management. In the public health system, the Centers for Disease Control and Prevention (CDC) work to protect and improve public health and safety, and focus on disease prevention, control and surveillance; and cases of notifiable diseases are reported by clinical professionals to the local CDC (He, 2005) . Therefore, hospital clinical staff and CDC public health professionals perform different roles, and may have different views on infectious disease control and prevention. Given that the ability of the public health system (i.e. CDCs) to deal with emerging and re-emerging infectious diseases in the context of climate change has been extensively studied (Tong et al., 2017a; Tong et al., 2016) , a similar investigation of the clinical health system where diseases are diagnosed and treated, is warranted. This study will contribute to a better understanding of infectious disease diagnosis, treatment, prevention and control in the face of climate change in China, and may also benefit disease control in other countries .

The study employs a cross-sectional questionnaire survey among clinical professionals to explore China's capacity of hospitals to deal with infectious diseases in the context of climate change. Further, the study explores participants' views on capacity building in the hospital sector to curb potential emerging and re-emerging infectious diseases due to climate change in China.

A questionnaire was administered to clinical professionals in November 2015. The questionnaire instrument design was informed by previous studies and relevant literature on climate-sensitive diseases (National Development and Reform Commission of the PRC, 2015; Semenza et al., 2012; Tong et al., 2016; Wei et al., 2014) . The questions asked about clinical professionals' thoughts on climate change, disease occurrence, the capacity of hospitals to deal with infectious diseases, and strategies to build the capacity of the hospital sector and curb the health impacts of climate change related to infectious diseases. An open-ended question was included to explore in greater depth, participants' understandings of disease control, diagnosis, treatment and management in the context of climate change. The questionnaire is included in Appendix A.

The study site of Anhui Province was selected because it has a high incidence of infectious diseases, especially malaria and HFRS (Bi et al., 2005; Jiao et al., 2013 ; The People's Government of Anhui Province, 2015). Anhui Province is located in East China (see Fig. 1 ), and has a warm-temperate, semi-humid monsoonal climate with an average annual temperature between 14 and 17°C, and annual precipitation between 800 and 1800 mm (The People's Government of Anhui Province, 2015).

Participants were clinical professionals from three major hospitals in Anhui. A total of 68 clinical professionals were surveyed in two general hospitals in the capital city of Anhui. A further 543 were surveyed in an infectious diseases hospital in a prefectural-level city. The clinical professionals included both doctors and nurses whose roles pertained to infectious disease diagnosis, treatment, and management.

Investigators administered the questionnaire in the three hospitals. To maximize the response rate, the principal researchers selected six key senior contacts from hospitals to assist with the distribution of questionnaires to potential participants. The process of participation was voluntary, and no incentives were offered. There are 650 clinical professionals relating to infectious diseases in the three major hospitals, and for ease of administration, the entire population was used as sample. In total, 650 questionnaires were distributed, and after omitting incomplete questionnaires, 611 were analyzed, with a response rate of 94%.

All returned questionnaires were entered using EpiData 3.1 software (Lauritsen, 2008) to create a database. Statistical analyses were performed with Stata 13.1 (StataCorp, 2013). Participants' demographic characteristics were descriptively analyzed. Binary logistic regression was used to explore the association between binary responses and demographic variables. Ordinal logistic regression was used to explore the association between ordinal responses and demographic variables. The demographic variables were age, gender, professional level, length of employment, education, and occupation. The binary responses were "yes", and "no/unsure". The ordinal responses were "very concerned", "concerned", "slightly concerned", and "not concerned"; or "extremely important", "very important", "important", "less important" and "not important". Data were analyzed with a two-sided test and p-values less than 0.05 were considered statistically significant. Table 1 shows the demographics of the participants. In this study, 44% of the clinical professionals who participated were doctors, and 46.3% were nurses. While ages ranged from 20 to 70 years, 64.6% of professionals were aged below 30 years, with the mean age being 28.4 years. Of the participants, 70.1% were female. Junior level professionals accounted for 43.9%, intermediate level professionals 19.8% and senior level 4.6% of the total participants. Over 40% of the participants had worked in hospitals more than five years. More than 60% held a university degree or higher qualifications, especially the doctors who were mostly highly educated with a bachelor of medicine degree or above (see Supplementary Table S1 in Appendix B).

As shown in Table 2 , more than 75% of the professionals were either very concerned or concerned about climate change. There was a statistically significant association between age group, professional level and the concern about climate change (see Supplementary Table S2 in Appendix B). Those who were over 30 years (OR = 1.993, 95% CI: 1.006-3.948, p = 0.048) and the senior staff (OR = 3.411, 95% CI: 1.372-8.482, p = 0.008) were more likely to be concerned about climate change. Furthermore, 71% of the professionals agreed with the statement that the weather was becoming warmer, especially nurses and the professionals who had been employed more than ten years (see Supplementary Table S3 in Appendix B) .

Nearly all (95.6%) believed climate change would have an adverse influence on population health. Furthermore, 94.9% and 91.3% of professionals agreed that predicted increasing temperatures and changes in precipitation patterns would affect infectious disease transmission. Specifically, 83.8%, 74.3%, and 69.9% of professionals were either extremely or very likely to believe that there was an association between climate change and malaria, dengue, and HFRS, respectively. Table 3 shows that about 20% of participants thought that there had been an increasing number of patients with malaria, dengue, and HFRS, and roughly 45% and 30% of professionals thought that climate change and population migration, respectively, were contributing factors. More than 81% of participants believed that malaria and HFRS hospital-reporting protocols were in place, and 75.8% believed so for dengue.

In terms of the diagnostic capability of hospital laboratories, 76.9% of professionals responded that their hospitals were 'always' or 'mostly' able to rapidly provide diagnostic tests for malaria, 67.3% for dengue, and 76.6% for HFRS, respectively. Some 84% of participants rated diagnostic and treatment capacity as excellent/good for malaria and HFRS, while 75% thought this was the case for dengue. Moreover, if an unusual cluster of cases was noticed, most professionals would take actions such as discussing with colleagues and laboratory technicians, informing the public health officer, and consulting with the CDC. In addition, there were no significant differences in these perceptions of infectious diseases between doctors and nurses.

Clinical professionals' perceptions of the current capacity of their hospitals to deal with infectious diseases are shown in Table 4 . Specifically, 95.3% of participants agreed that they had sufficient staff to deal with disease outbreaks. Also, more than 90% believed that their staff were well informed about current infectious disease trends, and that the quality of reported data from their hospitals to the CDC was excellent. However, 96.5% of professionals thought that logistical support in hospitals (for example administrative and maintenance services) needed to be strengthened. Overall, 94.2% either agreed strongly or somewhat that hospitals were well prepared for the threat of a serious emerging disease. There were no significant differences between perceptions of doctors and nurses regarding the current capacity of the hospital. Additionally, 95.5% agreed that more research on the health impacts of climate change was needed.

To build capacity to meet the challenge of emerging and re-emerging infectious diseases due to climate change, 75.9% of participants thought that prevention and control measures were extremely important strategies, and 73.7% believed more collaboration with their local CDC was extremely important (Table 5) . Furthermore, multivariate ordinal logistic regression analysis showed that compared to those under 30 years, professionals aged over 30 years were more likely to indicate that prevention and control measures are extremely important (OR = 2.261, 95% CI: 1.061-4.818, p = 0.035). Senior level staff were more likely to believe that more collaboration with the CDC was extremely important (OR = 13.760, 95% CI: 1.636-115.700, p = 0.016); while doctors were less likely to believe so (see Supplementary Table S4 in Appendix B). About 70% believed more funding was required for rural health care and that improving the accessibility of the online infectious disease reporting system for rural hospitals was also extremely important. More than 65% of those surveyed believed that the health impacts of emerging and re-emerging infectious diseases due to climate change could be addressed with strategies such as: better response mechanisms; strengthening the 

Climate change poses a significant threat to global population health (Intergovernmental Panel on Climate Change, 2014). Clinical professionals are at the frontline of health care provision to the population and are likely to witness firsthand the health impacts of a changing climate (Blashki et al., 2012) . They, therefore, provide a unique perspective on the health impacts of climate change and an indepth understanding of local community health (Blashki et al., 2012) . To the best of our knowledge, this study is the first of its kind to gauge clinical professionals' perceptions of the capacity of China's hospitals to manage infectious diseases under climate change and to provide insight for policymakers, practitioners and medical educators regarding climate change adaptation in the health sector.

Concern about climate change was acknowledged by most professionals, especially among senior staff and the group aged over 30 years. The majority of professionals, particularly nurses and those with longer terms of employment indicated that the weather was getting warmer. Nearly all respondents indicated climate change would adversely affect population health, and most indicated it would facilitate infectious disease transmission. Less than 10% of participants thought climate change was unlikely to be associated with malaria incidence compared to 12% for dengue and HFRS. The results were consistent with our previous studies among CDC staff who indicated climate change was more likely to have an influence on malaria than HFRS, whilst the perception of an association between climate change and dengue was not as strong as in a previous study conducted in Guangdong (Tong et al., 2016) . This is likely due to Guangdong having the highest incidence of dengue in China, whilst in Anhui there are fewer dengue cases reported (Lai et al., 2015) . Moreover, compared with previous studies among CDC public health professionals in other provinces (Tong et al., 2017a) , the hospital clinical professionals in this study were more likely to indicate that climate change would have an influence on HFRS. This could be due to the relatively high number of HFRS cases in Anhui Province, and hence firsthand knowledge of the disease and its determinants. Additionally, another study conducted among health experts in Europe also indicated their perceptions of the negative impact of climate change on vector-borne, food-borne, water-borne and rodent-borne diseases (Semenza et al., 2012) . Despite 94.2% of participants agreeing strongly or somewhat that hospitals were currently well prepared for the threat of a serious emerging disease, climate change may present new challenges for health sectors such as increased incidence in certain climate-sensitive diseases, or diseases either not previously seen in the area, or not seen for some time. Such an influx in cases could stretch the coping capabilities of the present system. This may explain why the public health and clinical health sectors share concerns about potential emerging and re-emerging climate-sensitive diseases.

The majority of professionals indicated that climate change and population migration were considered as the most significant factors associated with the increase of these infectious diseases. This is in line with other studies that indicated the impact of climate change and migration would affect infectious disease transmission (Gao et al., 2012; McMichael, 2015; Sang et al., 2015) . Higher temperatures and changing precipitation patterns can contribute to the increasing M.X. Tong et al. Social Science & Medicine 206 (2018) 60-66 population of vectors/rodents and more frequent contact with humans. Simultaneously, population movement can facilitate disease transmission from one region to another. In China, currently it is estimated that approximately 245 million people have migrated from poor rural areas to gain work in the cities (National Health and Family Planning Commission of the PRC, 2017). This "floating population" (highly mobile population) of internal migrants chiefly work in insecure lowwage jobs. Moreover, they often lack health insurance and defer seeking timely medical treatment, which could have a negative influence on infectious disease control (Qin et al., 2014) . Future infectious disease control and prevention should be cognizant of climate change impacts and population movements on the transmission of these diseases. In addition, building a more comprehensive national health insurance system covering the internal migrant population's health expenses in any part of China may provide benefits for population health (Qin et al., 2014) . Most professionals claimed that there was a hospital protocol in place for the reporting of notifiable diseases and believed that the capacity for disease diagnosis and treatment was either excellent or good, especially for malaria and HFRS. As Anhui historically has a high incidence of malaria and HFRS (Chen and Qiu, 1993; Gao et al., 2012) , professionals are more likely to have experience and confidence in dealing with these diseases, whereas historically there has been a low incidence of dengue in the Province. The majority of professionals believed that their hospital laboratories were able to provide rapid diagnostic test results for malaria, dengue and HFRS. Additionally, most professionals purported they would take comprehensive actions if they detected an unusual cluster of cases. This indicates there is a strong likelihood that outbreaks of emerging or re-emerging diseases would be detected early by the clinical professionals or the CDC. This detection of unusual trends could aid in curbing transmission if preventive measures are activated early.

Regarding the capacity of hospitals to deal with disease risks, most participants believed they were well prepared for the threat of a serious emerging disease. Of particular note, participants indicated there was a need to strengthen the hospital's logistical support. This is in line with another study conducted by Xu and Chu in 2010 focusing on logistics capacity in hospitals, which advocated that a reliable logistical support system is one of the most important components in modern health care systems and should be given higher priority to sustain and promote better health care services in the long-term (Xu and Chu, 2010) . Currently, the main obstacles to improving hospitals' logistical support in China are the lack of high-quality staff and regulatory frameworks for logistics management within hospitals (Lin, 2012) . Promoting specialized training for logistics staff and implementing management and quality control guidelines would be important.

Moreover, the problems in rural areas were highlighted, especially regarding the funding for rural health care support and accessibility to an online reporting system. The Severe Acute Respiratory Syndrome (SARS) outbreak demonstrated that rural health care was the weakest component of China's disease control and prevention system (Knobler et al., 2004) . More resource allocation to rural areas would be a vital step in advancing China's capacity building in response to emerging infectious diseases due to climate change.

In this study, older and senior staff were more likely to indicate that primary prevention measures and interdisciplinary collaboration were important, compared with the younger or non-senior staff. Such differences could be due to the rich working experience of the groups, who may have a better understanding of the infectious disease control and prevention strategies. Most participants also suggested a need for improved environmental health, more health education programs and financial support to improve vector/rodent-borne disease control, diagnosis, treatment and management in the context of climate change. Some studies have made future predictions about the effect of climate variation on dengue and malaria (Caminade et al., 2014; Ebi and Nealon, 2016) , although there are many confounding factors to consider. Although some participants in this study indicated that changes have already been noted, it would be useful in future studies to gain an insight into stakeholders' perceptions of when global warming would reach a point where there is a marked effect on the burden of climate-sensitive diseases.

Some limitations of this study deserve mention. Firstly, this study was conducted in one province. The results may not be generalizable to clinical professionals in other provinces of China. Secondly, as dengue is an emerging and uncommon disease in Anhui, participants in this region may be less likely to have hands-on experience in dealing with dengue cases, and feel less confident about dengue diagnosis and treatment. Lastly, the study was conducted among three major hospitals in cities, and results may not be generalizable to rural areas, townshiplevel hospitals or village-level clinics. Nevertheless, these findings may provide information for policymakers and clinical professionals pursuing initiatives to strengthen the capacity for hospitals to cope with a potential increase over time, in cases of climate-sensitive infectious diseases.

This study revealed that most clinical professionals thought climate change would have an impact on infectious diseases, and believed climate change and population migration were significant factors associated with infectious disease transmission. Health professionals in our study thought that the overall capacity of the hospital healthcare system to deal with infectious diseases was excellent. However, logistical support should be strengthened in hospitals and more climate change related research is needed. Issues that could be addressed include prevention and control measures, collaboration with the CDC, inhouse staff training and improved healthcare systems in rural areas. The multiple direct and indirect impacts of climate change will continue to threaten the health of the Chinese population. These findings may help health policymakers develop organizational adaptation policies to address the adverse impact of climate change on health.

The authors declare no conflicts of interest.

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This work has been funded by the Department of Foreign Affairs and Trade through the Australian Development Research Awards Scheme under an award titled 'How best to curb the public health impact of emerging and re-emerging infectious diseases due to climate change in China' [Project ID: 66888] and the National Basic Research Program of China (973 Program) [Grant No. 2012CB955504]. The views expressed in the publication are those of the authors and not necessarily those of the Department of Foreign Affairs and Trade or the Australian Government. The Commonwealth of Australia accepts no responsibility for any loss, damage or injury resulting from reliance on any of the information or views contained in this publication. We thank the Anhui Medical University, Anhui Provincial Hospital, the Second Hospital of Anhui Medical University and Fuyang No.2 People's Hospital getting involved in this study for their assistance in the distribution and return of questionnaires. All survey participants are greatly appreciated for their valuable contributions.

Supplementary data related to this article can be found at http://dx. doi.org/10.1016/j.socscimed.2018.04.021.M.X. Tong et al. Social Science & Medicine 206 (2018) 60-66