Epidemiology of visceral leishmaniasis before and after the Wenchuan earthquake in Longnan City，China，2005－2013

LU Zhao－lian，LIANG Hong－mei ，FU Xi－mei ，LIU Hai－jun，BAO Gen－shu，WU Ju－long，JING Tao，CHEN Gen

（1.Pathogens Biology Institute，School of Basic Medical Sciences，Lanzhou University，Lanzhou730000，China；2.Longnan Center for Disease Control and Prevention，Longnan746400，China；3.Shandong Center for Disease Control and Prevention，Jinan250014，China）

2.甘肃省陇南市疾病预防控制中心，陇南 746400；

3.山东省疾病预防控制中心，济南 250014

Introduction

Visceral leishmaniasis（VL），also called Kalaazar and listed as a neglected disease by World Health Organization，is a zoonotic parasitic disease caused by protozoa of theLeishmaniadonovanispecies complex（L.donovani，L.chagasi，andL.infantum）［1－3］.Leishmaniais introduced into human bodies by sandflies［4］.Clinical manifestations of human infections include recurrent fever，splenomegaly，hepatomegaly，and pancytopenia［3］.Kala－azar is endemic in Africa，Asia，Europe，and the Americas in more than 88countries，especially in India，Nepal，Sudan，Bangladesh，and Brazil［5－10］，which causes approximately 50 000deaths annually［3，11］.Two million new cases are reported annually and 350million people are at risk［11］.The hosts are human and canines and its main vectors in China arePhlebotomuschinensisandPhlebotomuswui［12］. Environmental factors that affect sandflies reproduction and increase exposure to sandflies and other animals such as dogs that are permissive with theLeishmanialife cycle play critical roles in the epidemic of Kala－azar［7，13］.

Kala－azar has been and is still an important health problemin China［14－15］.According to different epidemiological characteristics，leishmaniasis in China has been classified into three subtypes：plain，mountainous and desert subtypes.The mountainous subtype of VL occurs in the western mountainous and hilly regions of Gansu，Sichuan，Shaanxi and Qinghai provinces and patients are mostly children less than ten years old.In this instance，domestic dogs are the key reservoir.

In 1950s，it was estimated about 530 000cases spread in 17provinces or autonomous regions in China［16］.From 1951，various program policies in terms of vector control and case management were carried out in endemic areas.Firstly，through advocacy and education，rural organization established prevention and control teams to carry out survey and treatment.Until 1958，about 63million Kala－azar cases nationwide received treatment with free payment［17］.Secondly，in canine leishmaniasis endemic areas，a large number of dogs which serve as the principal source of infection were killed to prevent the prevalence of Kala－azar.In addition，from 1955，the implementation of the drug to kill sandflies in Shandong，northern Jiangsu，northern Anhui，eastern Henan and other places furthered the control of the spread of Kalaazar［17］.As a consequence，Kala－azar was nearly eliminated in the beginning of 1960s.

However，in northwestern provinces including Xinjiang，Gansu，Sichuan，and Inner Mongolia［18－19］，Kala－azar is still endemic or occurs with sporadic cases.As was reported，97.71%of cases nation－widely occurred from 2005to 2010in three provinces or autonomous regions：Xinjiang，Gansu，and Sichuan［18］.Longnan City in Gansu province is one of those important Kala－azar endemic areas.Wudu，Wen，and Tanchang counties of Longnan City have always been in high incidence rates［20］.

On May 12th，2008，a devastating earthquake occurred in Wenchuan that is located in the northwest of Sichuan Province［21］，which killed thousands of people in major cities including most areas of Sichuan and parts of Gansu and Shanxi provinces.The earthquake caused great losses of human’s lives and affected local economy，and it has also posed great harm to people’s health in those areas.In addition，the earthquake worsened people and animals’living conditions，changed insects’perch habit，and increased the number of stray dogs and movement of human population［22－23］.As an important Kala－azar endemic area，Longnan City，which is located in southern part of Gansu Province，was heavily damaged in this earthquake.Earthquake created suitable conditions for the spreading ofLeishmania.So the surveillance of Kala－azar in Longnan City before and after the Wenchuan earthquake is critical for the prevention and control of the spreading of this infectious disease.

The objective of this survey is to compare the incidence rates of Kala－azar between 2005and 2013 to evaluate the epidemic status on Kala－azar in Longnan City before and after May 12thearthquake，and to determine the effect of the Wenchuan earthquake on the Kala－azar epidemic.

Materials and methods

Ethics statement

According to Law of the People’s Republic of China on the Prevention and Control of Infectious Diseases，Kala－azar belongs to category C infectious disease，and all clinical Kala－azar data must be reported to local center for disease control and prevention［24］.All patients between the ages of 0 to 15gave verbal consent to participate in the study due to limited literacy，but their legal guardian and other age groups patients wrote informed consent.The study procedures were approved by the Ethics Committee of Basic Medical College of Lanzhou University and Longnan Center for Disease Control and Prevention.

Study sites

Longnan City，including Wudu，Cheng，Tanchang，Li，Liangdang，Wen，Hui，Kang，and Xihe counties，is located in the southern part of Gansu Province.The epicenter Wenchuan located in the northwest of Sichuan Province is approximately 200kilometers away from southwest of Longnan City，which is the nearest city in Gansu Province to the epicenter（Wenchuan）（Figure 1）.

Fig.1 Location of the study site of Longnan City in Wenchuan Earthquake zone

Serum samples

Samples of leishmaniasis were collected from hospitals of various counties in Longnan City between 2005and 2013.Clinical manifestations of Kala－azar include recurrent fever，hepatosplenomegaly，general lymphadenopathy，pancytopenia，and anemia.The total populations in Longnan City were 2 724 921，which were based on the statistical data in 2005.

rK39dipstick test

Laboratory diagnosis is based on positive test for anti－rK39IgG antibodies by the Kala－azar Detect rK39dip－stick（InBios，USA）according to the manufacturer’s protocol.All cases have been definitely diagnosed since 2005and confirmed with rk39dipsticks.All patients were cured with sodium antimony gluconate and no dead cases occurred.

Data analyses

All data were analyzed by chi－square tests with SPSS 19.0software（SPSS －Chicago，IL：SPSS Inc，2010）.A value ofP＜0.05was used as the cut off for statistical significance.

Results

Kala－azar incidence variation in Longnan city

There were 825cases of Kala－azar reported between 2005and 2013in Longnan City，with average annual incidence cases of 92，an incidence rate of 3.36/100 000，and a significantly higher incidence in males than that in females（χ2＝17.122，P＜0.001）.The incidence rate of each year from 2007to 2011was higher compared to those of 2005 and 2013（P＜0.001）.The incidence rate from 2008to 2010was higher than those of 2006and 2012（P＜0.05）（Table 1）.We found that，Kalaazar cases increased from 2006，which reached a peak between 2008and 2010，and then decreased after 2011（Figure 2）.In Longnan，cases of Kalaazar mainly occurred in children between the age of 0to 9，which accounted for 67.88%of all cases，apparently higher than other age groups（χ2＝324.422，212.475，P＜0.001）.There were cases in every month，and the incidence rates fluctuated year by year.The general trend for higher incidence rates was during 2008and 2010，which was exactly the first three years after the Wenchuan earthquake.

Tab.1 Kala－azar patients’distribution by ages and gender in 2005－2013

Kala－azar incidence profile in each county of Longnan City

In Longnan City，Kala－azar only occurred in the counties of Wudu，Wen，Tanchang，Cheng，and Xihe from 2005to 2013，and mostly in Wudu（incidence rate of 60.48%）and Wen（incidence rate of 33.45%）.The Kala－azar incidence rate of Wudu was significantly different with Wen，Tanchang，Cheng，and Xihe（χ2＝64.176，376.568，490.117，496.054，P＜0.001），and Wen was significantly different with Tanchang，Cheng，and Xihe（P＜0.001）.Only three Kala－azar cases occurred in Cheng County during 2005and 2013，and only one case occurred in Xihe in that period（Ta－ble 2）.

Discussion

In natural disasters，such as earthquake，various precipitating factors in favor of diseases will be created，which in turn provide a suitable condition for propagation of the vectors and the transmission of the parasites.An earthquake that erupted in Bam of Iran on December 26，2003，brought nearly 4.4times higher of anthroponotic cutaneous leishmaniasis overall cases five years after the earthquake than the cases registered before the earthquake in a same time length［25－27］.In January 2010，an earthquake in Haiti likely contributed to the subsequent start of the cholera epidemic that began in October 2010［28－30］.

Tab.2 Kala－azar incidence profile in each county of Longnan in 2005－2013

Fig.2 Kala－azar annual incidence rate in Longnan City（1/100 000）in 2005－2013

On May 12th2008，a devastating earthquake occurred in southwest China，more than 69 000 people were confirmed dead，more than 374 000 were seriously injured，and more than 18 000were reported missing.Longnan City，one of the most important leishmaniasis epidemic areas in China，was badly damaged in this natural disaster.That earthquake had a huge impact on the local environment and ecology.In the first three years after the earthquake during 2008and 2010，the Kala－azar incidence of Longnan City remained in a high level.The statistical data indicated that the May 12thearthquake provided favorable conditions for the epidemic of Kala－azar，although the reasons of Kala－azar prevalence in Longnan were more complex.

Firstly，Longnan Kala－azar epidemic region of Gansu Province in China belongs to canines’source endemic areas and dogs are the main infection sources.After the earthquake，a large number of stray dogs which served as a principal source of infection became unsupervised［31］，which deteriora－ted the situation.Secondly，the earthquake happened in late spring and early summer when local temperature and humidity was suitable for the propagation of vector sandflies.Moreover，it was estimated that approximately one million children and adolescents were affected by the devastating earthquake，including those who were displaced，transferred，physically injured.With the original houses being destroyed，a large number of victims lived in crowded temporary shelters，which doubled the chance of exposure to insect vectors.Additionally，with the commencement of reconstruction work［32］，a large number of domestic and international workers came into the disaster area，increased the number of susceptible population.From all of the above reasons，the earthquake created complicated natural environment and social circumstances，which probably contributed to the spread of the Kala－azar epidemic.

From 2005to 2013，825Kala－azar cases were reported in this area，and the average annual cases were 92，which accounted for approximately one fourth of all Chinese Kala－azar cases each year［18］.Our data showed that all age groups were affected，but children less than nine years old were more susceptible.It should be noticed that，however，incidence rate among adult was higher than statistical data among 1987to 1991［33］.Before 1990s，the incidence rate in Wen was higher than those in other counties of Gansu Province［33］.However，the cases in Wudu accounted for 59.67%of total cases in Longnan City in recent years，which were significantly higher than those in Wen，and higher than annual cases recorded from 1987to 1991in Wudu.In Wen and Wudu counties，complex mountainous landform，warm and humid climate provided a suitable condition for propagation of the vectors and the transmission of the parasites.

This study provided direct evidence that humanitarian community and local government should closely monitor the epidemic of VL after earthquake.They should collaboratively take effective containment measures to ensure no major epidemics of epidemic diseases and minimize the losses caused by secondary disasters after the earthquake including plague.The rising number of pet dogs in recent years made the prevention and control of Kala－azar more difficult.Besides，Longnan is adjacent to northern Sichuang Province and Gannan of Gansu Province which belong to Kala－azar endemic areas.Thus，there were cases of Kala－azar from people outside the region were reported every year by local center for disease control and prevention.As the economic and cultural center in Longnan City，Wudu attracts large number of immigrant population，which increase the chances of Kalaazar cross infection.In recent years，although there were only sporadic Kala－azar cases in Longnan，measures of Kala－azar control and prevention should be implemented for pre－warning of its outbreak.

To our knowledge，this is the first report of close investigation of the epidemic of Kala－azar after the 2008earthquake.Examination of the epidemiological characteristics will be critical for the surveillance of visceral leishmaniasis and helpreduce of costs of the visceral leishmaniasis infection.

Acknowledgements

We gratefully acknowledge Longnan Center for Diseases Control and Prevention，Gansu，in China for providing all data on insect－borne diseases.

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