Prevalence of intestinal helminths in domestic goose (Anser domesticus) in Qingyuan, Guangdong Province, China

1 State Key Laboratory of Veterinary Etiological Biology, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, Gansu Province 730046, China. 2 College of Veterinary Medicine, South China Agricultural University, Guangzhou, Guangdong Province 510642, China. 3 Institute of Animal Health Supervision, Qingyuan, Guangdong Province 511515, China. 4 College of Animal Science and Technology, Yunnan Agricultural University, Kunming, Yunnan Province 650201, China.


INTRODUCTION
Meat of domestic goose (Anser domesticus) is an important part of Chinese cuisine worldwide, especially in People's Republic of China (PRC). China is the largest producer of goose in the world, and Guangdong is one of the largest goose breeding and consumption provinces in China (Shi et al., 2003;Yang, 2003). 66 million geese are bred for human consumption in Guangdong province in 2009, which represents approximately 7.6% of the total goose production in China (He et al., 2010). Qingyuan city is one of the most important goose breeding bases in Guangdong province, and goose industry plays an important role in the district's economy.
Parasites cause significant economic losses globally as a consequence of deaths of infected animals, chemical *Corresponding author. E-mail: xingquanzhu1@hotmail.com. Tel: +86 931 8342837. Fax: +86 931 8340977. treatment of infected animals, and reduced egg and meat production (Urquhart et al., 1996;Weng et al., 2005). Parasitic infections may have a symptomless but insidious manifestation in geese, whether they are reared in modern commercial farms or in family-type small-holder farms and the production performance may be decreased by parasitic infections (Gicik et al., 2003;Wang et al., 2004). It has been well documented that geese can be infected with a number of helminths, and many of them are not host-specific and can easily be transmitted to other species of poultry (Gicik et al., 2003;Olsen, 2009). For seldom causing mass mortality, infection of geese with intestinal helminths is often ignored in breeding management, but the limited published reports in China and other countries have revealed high prevalence rate, such as Shandong province (26.4%), Guizhou province (more than 50%), Kars District, Turkey (78.9%), Texas, USA (nearly 100%), so more studies on the epidemiology of helminthosis in geese are needed for developing

Study site
Qingyuan city is situated in the north central part of Guangdong province, China, between north latitudes of 23°31′ to 25°12′ and east longitudes of 111°55′ to 113°55′. It has an area of approximately 19,000 km 2 , and has approximately 4 million inhabitants (National Population Census data, 2008). This city has a subtropical climate, with an average annual temperature of 20.7°C. The average annual rainfall is approximately 1900 mm.

Sampling of geese
The survey took place between October 2010 and March 2011. Regardless of gender, a total of 330 intestine samples of adult geese were collected randomly from representative local markets in Qingyuan City. 150 of these geese were from modern commercial farms and the rest from small family-type farms ( Table 1). The small intestines, large intestines and the caeca were separated, opened and rinsed with water, and macroscopic examinations of the washings and organs were performed.

Identification of parasite species and infection rates
Worm counts were performed on all washings or a proportion of the total washings depending on the total number of worms present and the site of occurrence was noted. Nematode specimens were fixed in 70% (v/v) warm ethanol and stored in 70% ethanol containing 5% glycerol before being cleared by lactophenol and identified to species according to existing descriptions and keys (Li, 2004). Tapeworm specimens were fixed in 70% ethanol, stained with carmine, differentiated in acid alcohol, dehydrated in serial Table 2. Species, organs of predilection, prevalence and intensity of infection of helminths found in geese in Qingyuan City, Guangdong province, China.

Helminth species Organs of predilection Prevalence (%) Intensity of infection Heterakis gallinae
Caecum 2.42 1 -10 Hymenolepis coronula Small intestine 13.03 1 ->100 Drepanidotaenia lanceolata Small intestine 2.42 1 -10 concentrations of ethanol, cleared in xylene, mounted in Canada balsam, and then identified morphologically to species according to existing descriptions and keys (Yamaguti, 1958(Yamaguti, , 1959Schmidt, 1986). A goose was recorded as infected with a certain helminth species if at least one worm was found in that animal. The mean prevalence rate was calculated by dividing the number of infected geese with the total number of geese examined, and was expressed as percentage of all animals sampled.

RESULTS
No gross lesions were observed in the intestines of 330 geese examined in the present investigation, and 50 of which harboured helminths. The helminths included one nematode and two cestode species, which represented two phyla, two classes, two families and three genera. Heterakis gallinae (2.42%) was the only nematode species found. Two cestodes, namely Hymenolepis coronula (13.03%) and Drepanidotaenia lanceolata (2.42%) were detected. The mean prevalence was 15.15%, and the examination revealed that helminth infection was more severe in small family-type farms (25.55%) than in modern commercial farms (6%). The most abundant parasite is H. coronula which was found in the small intestine of geese. One or two helminth species were found in the intestine of a single goose, and the number of helminth ranged between 1 and over 100. The species of worms found and their predilection sites, prevalence and intensities of infection (ranges) are presented in Tables 1 and 2.

DISCUSSION
The goose industry is well-developed in Qingyuan city as compared with some other areas of China. The mean prevalence of helminths in the present survey was 15.15%, which was less than some previous studies such as Shandong province (26.4%) and Qindongnan, Guizhou province (more than 50%), suggesting that better management and animal health and welfare standard are available in Qingyuan city, Guangdong province (Wang et al., 2004;. As expected, the helminth prevalence in geese in modern commercial farms (6%), which have better management and animal welfare standards, was significantly lower than those that came from small family-type farms (25.55%) in Qingyuan city. Only one nematode (H. gallinae) and two cestodes (H. coronula and D. lanceolata) were found in this study, which were much fewer than in Qindongnan, Guizhou province (7 nematodes, 11 trematodes and 9 cestodes), and Jianjing, Chongqing city (5 trematodes and 1 cestodes). The dominant helminth in geese in Qingyuan city was H. coronula, but was mainly D. lanceolata and Echinostoma revolutum in other areas of China, possibly due to different ecological and geographical conditions (Jing et al., 2002;Ruan et al., 2003;Wang et al., 2005). This is the first survey of intestinal helminth infection in geese in Qingyuan City, Guangdong province, China. In the geese examined in this study, the high prevalence of cestodes mainly may be caused by their living habits in water, which increase their exposure and infection with intermediate hosts. Although only three species of parasites were found, the results of the present survey indicate that helminth infections are highly prevalent in geese in Qingyuan city. The results of our study provide a foundation for developing and monitoring improved control strategies against intestinal parasites of geese in this region and elsewhere.