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. 2013 Sep 30;21(4):387–390. doi: 10.1016/j.sjbs.2013.09.010

The intestinal cestode Hymenolepis diminuta as a lead sink for its rat host in the industrial areas of Riyadh, Saudi Arabia

Saleh Al-Quraishy a,⁎, Mohamed M Gewik a, Abdel-Azeem S Abdel-Baki a,b
PMCID: PMC4150222  PMID: 25183950

Abstract

The present study sought to assess the potential of the cestode Hymenolepis diminuta as a bioindicator for lead accumulation in two industrial areas of the city of Riyadh, Saudi Arabia. Rats (Meriones libycus) were collected from two sites (industrial area II and Salbukh) in Riyadh. In the industrial area II, the mean levels of lead concentrations were found to be 1.96, 1.92, 1.4 and 30.72 μg/g in the rats’ liver, kidney and intestine, and in H. diminuta, respectively. In Salbukh, meanwhile, the lead concentrations were 1.63, 1.52, 1.20 and 21.31 μg/g in the rats’ liver, kidney, and intestine, and in H. diminuta, respectively. In addition, in industrial area II, compared with the liver, kidney and intestine of their host, the bioconcentration factors of lead were found to be, respectively, 15.6, 16 and 21.9 times higher in H. diminuta, and were 7.5, 8, and 10.2 times higher in the same organs compared to H. diminuta in Salbukh. The present study, therefore, proved that H. diminuta could be used as a bioindicator for heavy metal contamination in the industrial areas of the city of Riyadh.

Keywords: Lead, Helminthes, Bioindicator, Saudi Arabia

1. Introduction

In recent years, considerable scholarly attention has been devoted to the use of intestinal parasites as indicators for environmental quality (Sures, 2001, 2003; Morsy et al., 2012). The accumulation of heavy metals in parasitic helminthes has been extensively studied in fish (Sures et al., 1997, 1999, 2000a; Dural and Bickici, 2010; Khaleghzadeh-Ahangar et al., 2011; Morsy et al., 2012; Jankovská et al., 2011; Jankovská et al., 2012) but, comparatively, there have been few studies on the accumulation of metals in the mammalian helminthes (Sures et al., 1998, 2000b, 2002). Several studies, however, have showed that acanthocephalans parasitising rats have an exceptional heavy metal accumulation capacity (Scheef et al., 2000; Sures et al., 2000b), while adult cestodes from the intestine of mammals appear to be even more useful indicators for heavy metals than acanthocephalans (Sures et al., 2002; Sures, 2003; Eira et al., 2005; Torres et al., 2006). The aim of the present study, therefore, was to detect the potential of the intestinal parasitic cestode Hymenolepis diminuta within the host rat system as a bioindicator for lead accumulation.

2. Materials and methods

2.1. Sampling

Between April and May 2012 twenty adult Meriones libycus rats (140 ± 30 g) were collected from industrial area II (12 km South of the city of Riyadh) and a further twenty rats (135 ± 33 g) from Salbukh (40 km North of the city), using traps placed over the exits of rat burrows. Soil samples were collected on several occasions during the sampling period and subsequent metal analysis of these was used to indicate differences in the levels of lead pollution at the two chosen sites. The captured rats, meanwhile, were transferred to the laboratory, killed immediately, weighed and dissected. Samples of liver, kidney and intestine as well as the parasites (adults of H. diminuta) from the intestine were excised out and frozen at −20 °C until processing for metal analysis.

2.2. Analytical procedure

Rat tissue samples (liver, kidney and intestine) and helminthes (H. diminuta) of about 200 mg (wet weight) were digested by adding 1.8 ml of conic nitric acid and 6 ml of hydrochloric acid followed by destruction in a microwave oven. After digestion was completed, the sample was washed in a 25 ml flask. Analysis of the metals was made using an inductively coupled plasma mass spectrometer (ICP-OES method).

The collected soil samples, meanwhile, were air-dried for 24 h, ground, homogenised and sieved through a 0.4 μm-mesh. After sieving they were digested according to the method described by Kouadia and Trefry (1987). 35 ml of conic nitric acid was used to digest about 2.0 g of soil in a 250 ml conical flask. This flask was then put in a shaker and shaken vigorously for 16 h. The sample was then centrifuged at high speed (3000 rpm for 10 min) before the supernatant was removed with a pipette and the filtered solution was stored in a scintillation bottle until analysis.

Data were analysed using a statistical package for social science (SPSS, USA, version 10). The bioconcentration factor as the ratio of the metal concentration in the parasite and the host tissue (C[parasite]/C[host tissue]) was determined according to Sures et al. (1999).

3. Results

The results of the present study showed that 40% (8/20) of the rats caught at industrial area II and 50% (10/20) of those collected from Salbukh were infected with H. diminuta. Furthermore, the soil lead concentration was 10.45 μg/gm in industrial area II and 5.62 μg/gm in Salbukh. The mean levels of lead concentration in the animals collected from industrial area II were 1.96, 1.92 and 1.4 in the liver, kidney and intestine, respectively, but 30.72 μg/g in H. diminuta (Table 1). In Salbukh, the lead concentrations were 1.63, 1.52 and 1.20 in the liver, kidney and intestine, respectively, and 21.31 μg/g in H. diminuta (Table 1). The lead concentration in H. diminuta was therefore significantly higher than in any of the organs. Among the organs, however, the liver showed the highest lead concentration, but there was little difference between the concentrations in the kidney and intestine. Subsequent determination of the bioconcentration factor revealed that for those animals collected at industrial area II it was 15.6, 16 and 21.9 times higher for lead in H. diminuta compared with the liver, kidney and intestine of their host, respectively. In Salbukh, meanwhile, it was 7.5, 8, and 10.2 times higher for lead in H. diminuta compared with the same organs of their host.

Table 1.

Percent of infection and mean values of lead concentrations in soil and rat organs (liver, kidney and intestine), and its parasite (H. diminuta) collected from two sites in Riyadh city.

Sites of sampling Rat
 Mean lead concentration (μg/g) wet weight
Number examined Number infected Percent of infection Rat organs
 Soil Parasite (H. diminuta)
Liver Kidney Intestine
Industrial area II 20 8 40 1.96 1.92 1.40 10.45 30.72
Salbukh 20 10 50 1.63 1.52 1.20 5.62 12.31
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4. Discussion

The accumulation of heavy metals in terrestrial habitats has become a problem of great interest worldwide. Metals may accumulate to highly toxic levels to the extent that, although there may be no visible indication, they may have a severe impact on living organisms (Gupta et al., 2009). Consequently, the regulation, handling and bioremediation of hazardous materials require an assessment of the risk they pose to living species other than human beings (Adham et al., 2011). In this regard, the use of small mammals such as sentinel or biomonitor, species can provide data with which one can monitor the quality of the environment of their biological habits (Sánchez-Chardi et al., 2007; Adham et al., 2011). Rat intestinal parasites have attracted great interest as indicators for environmental quality since they can bioconcentrate several heavy metals to significantly higher concentrations than the tissue of their hosts (Sures et al., 2000a,b). In the present study we therefore investigated the suitability of the cestode H. diminuta for use as a bioindicator for lead. The study revealed that the livers and kidneys of rats have a high concentration of lead. This is in accordance with the literature since the liver and kidney are known to be the main accumulation organs for lead in mammals (Merian, 1991; Sures et al., 2000a; Adham et al., 2011). The intestine, however, showed the lowest lead concentration, which makes it an unsuitable organ for use as a bioindicator (Al-Quraishy, 2008).

While it is well known that the kidney has a greater ability to concentrate lead than the liver (Sures et al., 2000a) in the present study we found that the lead level in the liver was slightly higher than that in the kidney. A similar result was reported by Sures et al. (2000a); they found that infection with H. diminuta reduced the accumulation of lead in the kidneys of rats. It has also been found that intestinal parasites of fish significantly reduce the lead concentration in fish organs (Sures and Taraschewski, 1995; Sures and Siddall, 1999; Abdel-Monem, 2003).

The present study revealed that H. diminuta exhibited a higher lead content compared to their host tissue lead levels, with a bioconcentration factor that reached a maximum of 21.9 times. This bioconcentration factor was similar to those reported by Sures et al. (2002) for the same parasite, while Al-Quraishy (2008) found that the bioconcentration factor reached a maximum of 38 times for the same parasite in the same host in Riyadh city. The difference between the bioconcentration factor found in our study and that found in Al-Quraishy (2008) may be due to the different sampling sites; the season of sampling and the method of lead determination.

It has been found that the liver fluke Fasciola hepatica contained 172, 53 and 115 times more lead than the muscle, kidney and liver, respectively, of its bovine host (Sures et al., 2000a). It is also known that in mammals lead is excreted from the liver into the intestine via bile (Lehnert and Szadkowski, 1983) and since F. hepatica lives in the bile ducts surrounded by bile liquid, lead could be absorbed across the tegument of the flukes in a lipophilic form after complexing with bile acids (Sures et al., 2000a). In contrast, H. diminuta takes up lead from the intestinal lumen of the rats, as Sures et al., 2000a, 2002) showed by comparing the amounts of lead excreted with the host’s faeces.

Conclusively, rats are widely distributed all over the kingdom of Saudi Arabia and they are used as the final host for many cestodes including H. diminuta which have a great ability to bioaccumulate metals. Therefore rats and their helminthes could be a very useful and promising tool for environmental monitoring in Saudi Arabia.

Acknowledgement

The authors extend their appreciation to the Deanship of Scientific Research at King Saud University for funding the work through the research group project number RGP-VPP-004.

Footnotes

Peer review under responsibility of King Saud University.

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