Introduction
Clonorchis sinensis and
Opisthorchis species are important liver flukes of oriental or Chinese origin [
1‐
4]. Clonorchiasis whose symptoms are indistinguishable from opisthorchiasis is one of the most neglected tropical diseases which blight the lives of millions of people worldwide and threaten the health of several others [
5,
6]. A report by the World Health Organization in 2012 estimates a disease burden of at least 56 million people with one or more foodborne trematode infections which include clonorchiasis, opisthorchiasis, fascioliasis and paragonimiasis [
7]. It is important to mention that clonorchiasis alone is estimated to infect 35 million people globally with a greater percentage of the cases occurring in China, Korea, Japan and Vietnam with approximately 15 million cases in China alone [
8,
9]. Persistent or chronic infection by these trematodes frequently leads to hepatobiliary diseases such as cholangitis, cholelithiasis, cholecystitis, pancreatitis, hepatic fibrosis, cholangiocarcinoma and liver cancer [
10‐
12].
Clonorchis sinensis and
Opisthorchis species are flat, leaf-shaped hermaphroditic trematodes that belong to the opisthorchiid liver flukes group. The lifecycle of these flukes requires water snails of the genus
Melanoides, Bithynia or
Parafossarulus as the first intermediate hosts and freshwater fish and shrimps as their second intermediate host. Infection with these flukes occurs upon consumption of a raw or undercooked fish which contains encysted metacercariae in its muscles. The metacercariae then excyst and migrate to the bile duct where they mature. The incidence of human infection is high in areas where the people consume raw fish. However, its incidence in non-endemic areas has been associated with importation by immigrants from endemic areas [
13‐
15]. The emergence of
Clonorchis or
Opisthorchis in non-endemic areas has been linked to an increase in the consumption of raw or undercooked fish, expansion of water snail habitats due to rapidly growing aquacultures and increase in raw food distribution network [
1,
2,
5,
7,
11].
Currently, there is no documentation on cases of clonorchiasis/ opisthorchiasis in Ghana; the detection of opisthorchiid eggs in patients infected with malaria in Ghana calls for immediate strategies aimed at considering these liver flukes during diagnosis of patients presenting with malaria-like symptoms accompanied by abdominal pains.
Discussion
Clonorchiasis and opisthorchiasis have huge morbidity and mortality implications for the world populace. They pose a significant threat to human health since they infect key organs such as the liver and biliary system [
18]. Although most people with the infection are asymptomatic, about 5% to 10% of people with heavy fluke infections may exhibit nonspecific symptoms such as right upper quadrant abdominal pain, flatulence, and fatigue [
1,
3,
4,
10,
19]. These nonspecific symptoms in infected individuals imply that several cases may go undetected.
In Ghana, this is the first report of a possible case of Clonorchis sinensis/Opisthorchis species infection in two patients with malaria-like symptoms. Although they were diagnosed with malaria, opisthorchiid eggs were also detected in their stool samples. We acknowledge, however, that further sensitive and more reliable tests should have been performed to confirm the presence of Clonorchis sinensis or Opisthorchis species in the examined stools as well as identification of the worms in these patients. This was not possible because the patients did not report back to the hospital probably because their condition improved.
Previously reported infections of
Clonorchis or
Opisthorchis in the USA, Canada and Malaysia were suggested to have been imported from China [
13‐
15]. By contrast, these two patients with malaria and opisthorchiid eggs in their stools were Ghanaians who had not travelled outside Ghana. They indicated that they had not consumed raw fresh fish ever in their lives. Of interest, the occurrence of the intermediate host snails such as
Melanoides, Bithynia and
Parafossarulus species which are required to complete the fluke lifecycle have not been described in Ghana. However, the opisthorchiid eggs detected in patients in Ghana might have come from consumption of raw fish infested with metacercariae imported from China into Ghana. Furthermore, poor sanitary conditions in the country such as discharge of untreated faecal waste directly into water bodies and consumption of poorly cooked food could serve as sources of the opisthorchiid eggs detected in these patients in Ghana [
20,
21].
Microscopy continues to be the widely used method for identification and differentiation of the eggs of opisthorchiid and heterophyid species. Since the eggs of these organisms are very similar in shape, form, operculum and operculum knobs, several measurements of the parameters of eggs have been adopted to differentiate opisthorchiid and heterophyid organisms at the species level. These parameters include the nature of the operculum, shoulder rim, operculum knob, the shape, the form, length and width of the eggs as well as length-to-width ratio (LWR) and Faust-Meleney index (FMI) [
22]. Currently, more specific and sensitive serological and molecular methods such as polymerase chain reaction are available for identification and differentiation [
1,
23] but these methods are expensive and require specialized skills.
The Giemsa and Ziehl–Neelsen staining techniques were employed to investigate possible intestinal coccidian infection after direct smear and formalin-ether concentration techniques could not detect any of the commonly known intestinal worms or eggs in the stool samples. Although some studies have reported low sensitivity of direct smear, formalin-ether concentration and Kato-Katz techniques in cases of extremely light
Clonorchis sinensis infection have shown some improvement in egg recovery [
24,
25]. Since we could not recover any opisthorchiid eggs in both direct smear and the formalin-ether concentration, it is important to mention that the staining techniques used for this study could increase the efficiency of egg recovery of extremely light infections of these small ovoid and operculated eggs. However, Giemsa and Ziehl–Neelsen staining techniques do not offer any advantage to morphological differentiation between opisthorchiid and/or heterophyid eggs. In these two cases, we relied on the general features and egg parameter measurements such as the length, width, FMI (7160μm
3) and LWR (1.76) averages to predict the possibility of
Clonorchis sinensis/Opisthorchis species.
Identification of these two possible cases of Clonorchis sinensis/Opisthorchis species in patients infected with malaria in Ghana should create awareness for prompt response and treatment since prolonged infection may result in cholangiocarcinoma. Although this is the first documented report on Clonorchis/Opisthorchis in Ghana, it should be regarded as one of the emerging infections in the country. Moreover, due to the uncommon nature of clonorchiasis/opisthorchiasis and the lack of specific symptoms, the infection should be considered a possible diagnosis for all undiagnosed abdominal pain since the infection has propensity to cause hepatic fibrosis, liver cancer and cholangiocarcinoma.
Acknowledgement
This work was supported by Department of Human Biology, University of Cape Coast. We are grateful to the laboratory and the medical staff of St. Francis Xavier Hospital and Elmina Urban Health Centre, especially, Mr Mends, the District director of health services KEEA district for their support.
Competing interests
The authors declare that they have no competing interests.
Authors’ contributions
KKA, JNB, RA, EOA, GK-N and NBQ collected the data, analysed, interpreted and were involved in the drafting of the manuscript. AKT and KPT were involved in the diagnosis of the infection, interpretation and final manuscript preparation. All authors read and approved the final manuscript.