A shifting pattern of parasitic diseases in China
Published estimates from China’s Ministry of Health indicated that by the early 1990s
China exhibited some of the world’s highest prevalence rates of parasitic and other
tropical diseases [1]. The findings included estimates that more than 0.5 billion
people were infected with ascariasis, whereas approximately 200 million people suffered
from trichuriasis and hookworm infection [2, 3]. In the more than two decades since
the first published estimates of China’s parasitic infections, the nation has undergone
impressive economic development, with its GDP growth roughly increased by 10% annually
and massive reductions in the numbers of Chinese living in extreme poverty [4]. Indeed,
the World Bank notes that China was successful in achieving all of its Millennium
Development Goals [4]. As a result, today China is the second largest economy globally
next to the United States.
In addition to rapid economic growth that promotes urbanization, significant change
in agricultural practice, and improved sanitation, China has undertaken extensive
parasite control measures [5]. These changes have translated into impressive reductions
of China’s neglected parasitic diseases and other neglected tropical diseases (NTDs)
during recent decades. Based on several national surveys for parasitic diseases performed
by Ministry of Public Health and other public health agencies in 1994 [1, 2], 2005
[6], and 2010 [7], as well as the data from Global Burden of Disease (GBD) 2016 [8],
the overall trends of China’s major neglected parasitic infections are shown in Fig
1.
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Fig 1
The overall trends of China’s major neglected parasitic infections since 1990 based
on information either from (A) several national surveys performed by Ministry of Public
Health and other sources [1, 2, 6, 7] or (B) the GBD 2016 [8]. The second graphs on
the right are the amplified graphs for those parasitic diseases with low prevalence
on the bottom. GBD, Global Burden of Disease.
Overall there is general concurrence between both referenced data sets. Briefly, China’s
major neglected parasitic diseases have declined dramatically, especially soil-transmitted
helminth infections (STHs), schistosomiasis [5], and malaria [9], and lymphatic filariasis
has been eliminated [10]. However, the prevalence of some food-borne trematode infections
and cysticercosis has significantly increased [11]. Although autochthonous malaria
has been nearly eliminated in China, imported malaria and other parasitic infections
have been brought into China from Africa or other endemic countries as trade activities
and traveling have increased during the past decades, especially after the newly launched
Belt and Road Initiative.
Declining of endemic STHs and schistosomiasis
The major STHs—ascariasis, trichuriasis, and hookworm infection—have been historically
widespread in China and have had a major role in interfering with economic and social
advancement [12]. Based on a nationwide survey of human parasites in China conducted
in total 1,477,742 persons in 1994, the prevalence rate of ascariasis, hookworm infections,
and trichuriasis was 47.0%, 17.2%, and 18.8%, with estimates of a total infected population
of 531 million, 194 million, and 212 million, respectively [1, 13]. However, China’s
economic growth has not occurred evenly with an East to West poverty gradient, resulting
in dramatic declines in the former and remaining high STHs prevalence rates in the
southwest provinces where the economy has not progressed [14]. For example, recent
estimates indicate that the highest prevalence rates of STHs currently occur in the
southwestern provinces of Guangxi, Guizhou, Sichuan, and Yunnan, where poverty is
widespread, as well as the South China Sea Province of Hainan [7].
Schistosomiasis caused by the infection of Schistosoma japonicum has had an important
role in the history of modern China. Prior to the Great Leap Forward in the 1950s,
it was highly endemic in 12 provinces of the Yangtze River valley, with 11.6 million
infected individuals and over 100 million people under threat of infection [15, 16].
Since then, China has implemented comprehensive national campaigns to control the
prevalence of schistosomiasis in humans and livestock, through the liberal use of
molluscicides and destroying snail habitats, mechanization to replace water buffalo
with tractors, and large-scale mass chemotherapy of both humans and livestock with
praziquantel [17]. According to the Ministry of Health, the number of infected human
cases has dropped to 54,454 in 2016 with no new acute cases reported [18]. However,
these estimates are significantly lower than the GDB 2016, which reported schistosomiasis
prevalence of 1,067,203 in 2016 in China, possibly due to the different cited sources
[8]. We are working to understand the basis of this discrepancy. There are also concerns
about snail repopulation along the Yangtze and its tributaries, and human disease
reemergence as a consequence of climate change and large hydroelectric projects such
as the Three Gorges Project and the South-to-North Water Diversion Project in China
[19, 20].
Malaria
China’s indigenous malaria, mostly caused by Plasmodium vivax, was effectively controled
after several decades of nationwide efforts, which included the screening and treatment
of patients, integrated vector control, and a nationwide surveillance and reporting
systems [9]. As a result, outstanding progress has been made toward the elimination
of malaria in China. Since the National Malaria Elimination Program was launched in
2010, China’s malaria incidence has declined from 64,178 cases in 2006 [21] to 2,718
cases in 2012 [22] and has remained at low levels (Fig 2A). However, there has been
a significant rise in imported cases from Africa and southeast Asia, especially since
the launch of Belt and Road Initiative. In 2016 alone, there were 3,321 malaria cases
reported; 3,317 of them were imported from Africa or other endemic countries with
only 3 cases of indigenous malaria [23]. There was no indigenous malaria case reported
in China in 2017; all of the malaria cases were imported [24]. This is associated
with a shift in malaria species from predominantly P. vivax to P. falciparum in addition
to P. ovale and P. malariae (Fig 2B) [24]. Moreover, although the total cases of malaria
have been significantly reduced, the severe malaria cases and deaths remain at similar
levels due to the increased proportion of imported P. falciparum malaria [16, 23].
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Fig 2
The dynamic changes of malaria prevalence in China since 2006 [21–24, 53–57].
(A) Imported and Domestic malaria cases presented in different years. (B) Infected
Plasmodium species reported in China since 2006.
Increasing food-borne helminth infections
The prevalence of foodborne parasitic diseases has risen sharply during the last two
decades, such that these diseases have emerged as important illnesses affecting food
safety and public health in both urban and rural foci [11]. Paradoxically, the rise
in China’s foodborne parasitic infections may partly reflect rising incomes, with
resultant increased access to meat or exotic foods, together with urbanization [25].
Clonorchiasis and paragonomiasis represent two key food-borne trematode infections
in China. With regard to the former, approximately 15 million people are infected
nationwide [11, 26], representing an 80% increase compared with the infections identified
in the first national survey of parasitic diseases in 1994 [2]. Today, China accounts
for 85% of global clonorchiasis. The geographical distribution shows a north-south
polarized distribution with the highest infection rates in the southern provinces
of Guangdong and Guangxi, or in the northern provinces of Heilongjiang and Jilin [26].
Due to its identification as a strong carcinogen, infection of Clonorchis sinensis
has become an important cause for liver cancer in these endemic areas [11]. With regards
to paragonimiasis, the current national infection rate is 1.7%, with an estimated
infected population of 22.3 million with 200,000 disability-adjusted life year (DALY)
lost[6, 25, 27].
Two important food-borne zoonoses from pigs include trichinellosis and taeniasis-cysticercosis.
For trichinellosis, the infected population is estimated over 20 million, with 40
million people at risk in China, and more than 2 billion Chinese yuan (CNY) spent
on inspection and quarantine of pigs annually [25, 28]. Taeniasis-cysticercosis caused
by Taenia solium is also widespread. The prevalence of cysticercosis in China increased
from 0.01% in 1994 to 0.58% in 2004, so that the most recent estimate indicates that
the infected population was about 7 million [6]. Tibet in Western China exhibits the
highest Taenia infection rate of 19.2% [6, 29]. Echinococcosis is also endemic in
western China, with an estimated 170,000 infections, of which more than 98% occur
in Xinjiang, Qinghai, Gansu, Sichuan, Inner Mongolia, and Ningxia [30].
Belt and Road Initiative and imported parasitic diseases
In 2013, Chinese President Xi Jinping launched the landmark Belt and Road Initiative
to enhance trade, infrastructure, and economic outreach from China to and from Asia,
Africa, and Europe [31]. The new initiative is being touted as one of the most ambitious
economic and foreign policy initiatives undertaken by China since its liberation in
1949 (Fig 3).
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Fig 3
Map of China’s proposed Belt and Road Initiative including a land route (One Road;
red unbroken line) and a sea route (One Belt; blue dotted line) reaching from China
to Asia, Europe, and Africa.
Original figure made with data from China Xin Hua news agency and public domain world
map available here: https://commons.wikimedia.org/wiki/File:BlankMap-FlatWorld6.svg
[52].
With respect to Africa, currently there are an estimated 3 million Chinese already
working there through more than USD$100 billion in capital investments made at the
World Economic Forum in Davos [32]. In terms of emerging parasitic diseases, however,
a significant downside of increased investments and trade in Africa has been an increase
in imported parasitic infections including intestinal schistosomiasis (caused by Schistosoma
mansoni), loiasis, African trypanosomiasis, cutaneous leishmaniasis [33–37], and falciparum
malaria.
Strategy to effectively control the neglected parasitic diseases in China
As highlighted above, there are three major themes to China’s neglected parasitic
infections: (1) as nationwide control performed in China, STHs and schistosomiasis
have significantly declined, however, STH infections still remain highly prevalent
in China’s southwest due to persistent poverty; (2) increases in food-borne helminth
infections in northern and southern provinces; and (3) imported tropical infections,
led by falciparum malaria. In addition, China is becoming increasingly urbanized with
population shifts leading to the establishment of new megacities—by some estimates,
60% of China’s population will live in urban areas, with the creation of multiple
megacities by the year 2030 [38]. By this time, one-quarter of the world’s 100 largest
cities will be in China. Unchecked urbanization has the capacity to promote the emergence
of urban STHs and schistosomiasis, malaria, and leishmaniasis[39]. Based on these
trends of parasitic infections in China, the following strategies should be considered
to strengthen the control of these infections.
Comprehensive control measures
For the future control of STHs, there is an urgent need to continue implementing mass
drug administration approaches using albendazole and mebendazole, especially to China’s
less-developed southwestern provinces and Hainan. However, high rates of post-treatment
reinfection and variable efficacies of benzimidazole anthelminthics, including the
possible emergence of anthelminthic resistance [40, 41], suggest the need for alternative
technologies, including better drugs or even anthelminthic vaccines [42]. For schistosomiasis
in China, enormous strides have been made through a multipronged approach highlighted
above, but there is a need to reinforce and strengthen these measures to achieve its
elimination as a public health problem. For food-borne helminth infections, a comprehensive
control approach should be deployed, for example, the establishment of case report
network, including a traceable system for the infection source; a surveillance and
supervision system for the entire food industry chain; and public education and awareness
for disease infection and control methods [43, 44].
International monitoring and surveillance network
For the importation of malaria and other NTDs, there is a need to expand monitoring
and disease surveillance, especially among the estimated 3 million Chinese workers
in Africa and the more than 430,000 Africans living in Guangdong province for academic
study, business, and trade [45]. In parallel, there is a need to establish tropical
disease control and surveillance centers in the major urban areas of China, such as
the one established at the Friendship Hospital in Beijing [34], which plays important
roles in screening, diagnosis, and treatment of imported tropical diseases. Conversely,
within Africa, China’s national aid can be partly redirected to the healthcare sector
with an emphasis on NTD surveillance and treatments. Currently, the healthcare sector
accounts for only 2.1% of China’s total investment in Africa, and only a small percentage
of this amount goes towards basic and clinical research and training [46, 47]. Expansions
in public health and medical research support for African countries would promote
both disease reductions there and in imported tropical diseases to China.
The Belt and Road Initiative also has implications beyond Africa [48]. In the Middle
East, a wide range of NTDs are emerging in the conflict zones of Syria, Iraq, Libya,
and Yemen, which will be further disseminated through roadmapped trade routes. Shown
in Table 1 are some of the major NTDs we can anticipate emerging in China as a consequence
of Belt and Road trade [48, 49].
10.1371/journal.pntd.0006946.t001
Table 1
Major NTDs and malaria in countries along the Belt and Road Initiative.
Diseases
East Africa
South-Southeast Asia
Middle East
Russia-Kazakhstan-Central Asia
West China (One Road start)
East China (One Belt start)
Malaria
√
√
Visceral leishmaniasis
√
√
√
√
Cutaneous leishmaniasis
√
√
√
Schistosomiasis
√
√
√
Food-borne helminthiasis
√
√
Echinococcosis
√
√
√
STHs
√
√
√
MERS
√
Dengue and arbovirus
√
√
Abbreviations: MERS, middle east respiratory syndrome; NTD, neglected tropical disease;
STH, soil-transmitted helminth infection.
Concluding comments
Shown in Fig 4 are some of the modern 21st century forces that are likely to affect
the future of China’s human parasitic infections. They include continued disease prevalence
reductions due to further decrease in poverty (especially rural poverty) but also
new factors that could promote disease emergence, including the rise of urbanized
helminth infections as noted elsewhere; continued food insecurity, especially in terms
of its impact on food-borne trematodiases and other helminth infections; and China’s
Belt and Road initiative in terms of its reintroduction of malaria and other tropical
infections. Finally, although not discussed in detail here, we’ll need to consider
the impact of China’s aging population on parasitic infections. For instance, it was
noted that the elderly are disproportionately affected by hookworm infection in some
areas of China [50]. Also, more attention needs to be paid to the possible effects
of climate change on the emerging or reemerging NTDs, especially on vector-borne and
snail-borne disease [51]. It will be important to continue active surveillance for
parasitic infections in order to better understand the dynamic state of China’s human
parasitic infections.
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Fig 4
Dynamic forces that affect China’s neglected tropical diseases (NTDs).