In Egypt, HCV is still the most important public health problem, its prevalence in 2008 reached about 15% among Egyptians (1). The virus prevalence was the highest in Menoufia province (2). 
On the other hand, schistosomiasis is an epidemic disease in Egypt (3). Schistosoma mansoni, which resulted in intestinal schistosomiasis, was among the main causes of chronic liver disease in Egypt (4). Clinical studies showed that HCV co-existence with schistosomiasis caused more severe liver disease complications than infection with HCV alone (5, 6).
Amebiasis is food or water-borne disease caused by acquiring the cyst form of the parasite Entamoeba histolytica, which is the cause of amebic colitis, and can migrate to the liver and result in liver abscesses (7). Mølle et al (2001) concluded that liver cirrhosis is the main risk factor for pyogenic liver abscesses (8). E. histolytica infection could result in liver injury and increase the production of the liver enzymes in the sera compared to parasite non-infected subjects (9, 10).
Besides the association of Toxoplasma gondii with abortion or neonatal mortalities, it can invade the liver and cause liver damage (11-13). Chronic HCV patients with related cirrhosis expressed a higher prevalence of T. gondii seropositivity (14).
All of these parasitic diseases schistosomiasis, toxoplasmosis, or amebiasis, were frequent among Egyptian citizens (3, 15-18). Co-infection of HCV and any of these parasites are possible and this can affect the liver status in various ways. Therefore, this study was conducted to investigate the incidence of Entamoeba histolytica, Toxoplasma gondii, or Schistosoma infection among HCV patients from Menoufia province.
 

The examined parasitic infections among HCV Egyptian patients were summarized in Table 1. The overall incidence of T. gondii IgG and IgM was 65% and 3.89%, respectively. Moreover, the incidence of E. histolytica and Schistosoma using (serology and fecal examination) was (50% and 21.67) and (42.22% and 1.67%), respectively.

 
Table 1. Incidence of Toxoplasma gondii, Entamoeba histolytica and Schistosoma infection among HCV infected patients

Data are expressed as: number (% among study population).
 

Regarding age, the higher incidence was recorded in older HCV patients infected with T. gondii, E. histolytica, or Schistosoma using serological tools than in younger patients (Tables 2-4). Similar results were obtained on the level of multiple parasitic infections (Table 5). Significant differences (P > 0.05) were observed among the HCV older patients during the infection with Schistosoma, or the multiple infections with (E. histolytica and Schistosoma), (T. gondii and E. histolytica, and Schistosoma) when compared to younger patients. Without any significant changes, E. histolytica cyst detection in feces showed higher incidence in older HCV patients than in younger patients.
Gender-wise, a significant percentage increase (P > 0.05) was observed among the HCV female patients during the acute infection with T. gondii (IgM positive) when compared to male patients (Table 2).
No significant changes were recorded during the infection with E. histolytica (Table 3).  On the other hand, a significant increase (P > 0.05) was observed among the HCV male patients during the infection with Schistosoma, or the multiple infections with (T. gondii and Schistosoma), (T. gondii, E. histolytica, and Schistosoma) when compared to female patients (Tables 4 & 5).
 
Table 2. Socio-demographic characteristics and incidence of T. gondii infection among HCV infected patients

Data are expressed as: number (% among study population). * P<0.05 indicate significant difference.
 
Table 3. Socio-demographic characteristics and incidence of E. histolytica infection among HCV infected patients using ELISA and fecal examination

Data are expressed as: number (% among study population). * P<0.05 indicate significant difference.
 
Table 4. Socio-demographic characteristics and incidence of S. mansoni infection among HCV infected patients using indirect haemagglutination test and fecal examination

Data are expressed as: number (% among study population). * P<0.05 indicate significant difference.
 
Table 5. Socio-demographic characteristics and incidence of mixed parasitic infections among HCV infected patients

Data are expressed as: number (% among study population). * P<0.05 indicate significant difference. Toxo: Toxoplasma gondii, Enta: Entamoeba histolytica, and Schi: Schistosoma.
 

Discussion

In the current study, T. gondii, E. histolytica, and Schistosoma incidence in 180 HCV infected patients from Menoufia Province was detected. T. gondii IgG and IgM incidence were 65% and 3.89%, respectively. Moreover, E. histolytica and Schistosoma incidence using serological tools was 50% and 42.22%, their incidence using fecal examination was 21.67and 1.67%, respectively. Multiple parasitic infections were determined among HCV patient’s sera from Menoufia Province. Each parasite T. gondii, E. histolytica, or Schistosoma co-existence with HCV have been detected previously (6, 14, 20). El-Nahas et al. (2014), detected high T. gondii seropositivity 92.6% and 13.6% for IgG and IgM antibodies, respectively, among HCV cirrhotic patients and 76.9% and 12.8% for IgG and IgM antibodies, respectively, among HCV non-cirrhotic patients, who attended Mansoura University Hospital, Egypt (21). Moreover, using real-time quantitative PCR, T. gondii parasitemia was positive in 31.4% of HCV-infected patients from Cairo, Egypt (14). Likewise, a high prevalence of 40.2% and 27.3% of both HCV and schistosomiasis were detected among Egyptian subjects (22, 23). Seventy-two cases out of 96 (75%) high positive anti-HCV antibodies Egyptian patients were anti- Schistosoma mansoni IgG positive (24). Previous studies reported high HCV antibody positivity among Schistosoma mansoni infected Egyptian patients (25, 26). A case study performed by Matsuo et al (1998), detected that E. histolytica subclinical infection in HCV female Japanese patient subjected to IFN therapy was developed into an amoebic liver abscess (20). While Abd-Alla and Ravdin (2002) demonstrated E. histolytica antigens in 43% using ELISA in Egyptian patients suffering from acute diarrhea from Cairo (27), Abozahra et al. (2020) detected E. histolytica in 14.7% of fecal samples using PCR in patients with gastrointestinal diseases in Behira, Egypt (18). According to our knowledge, this is the first report to detect multiple parasitic infections among HCV patients from Egypt. 
In the current study, the sero-detection of T. gondii, E. histolytica, and Schistosoma mono-parasitic infection or multiple parasitic infections were increased among older HCV-infected patients. Similar patterns were obtained previously on the level of mono-parasitic infection among older HCV-infected patients (18, 24). Schistosome infection could happen at any age, by coming into contact with cercariae-containing freshwater (28). Al-Areeqi et al. (2017) reported that the age group of 18 to 40 years was considered among the major risk groups of amebiasis in Yemen (29). Moreover, T. gondii positivity was significantly observed more in older pregnant women than in the younger ones (17). Previous reports demonstrated the increase in Toxoplasma positivity with human age (30, 31).
In the present study, the incidence of the acute infection of T. gondii was increased among HCV female patients when compared to males. A previous report observed that Malaysian females from Pangkor Island in Peninsular were mostly infected with Toxoplasma compared to males (32). On the contrary, in the current study, the incidence of the acute infection of Schistosoma mono-parasitic or multiple parasitic infections was increased among HCV male patients when compared to females. Similar results were recorded among male HCV-infected patients infected with Schistosoma (24). A previous meta-analysis of thirty-two studies revealed that males were more often re-infected with different Schistosoma spp. (six and twelve months) after treatment with praziquantel than females (33).
Despite, several studies reported the high prevalence of E. histolytica in rural areas (18, 34), the current study demonstrated a significantly higher incidence among urban area residents, which suggest poor sanitation and unhygienic practices, especially in fast food shops/restaurants. In the present study, the incidence of Schistosoma and (T. gondii and Schistosoma) was higher among rural area residents. In these rural areas many activities such as crossing the contaminated water with bare feet, swimming in contaminated water streams, washing utensils and clothes using contaminated stream water, and fishing were among the major risk factors. In previous studies, similar findings have been demonstrated among rural residents (3, 35).

 

Conclusion

T. gondii, E. histolytica, and Schistosoma infections are frequent among HCV Egyptian patients from Menoufia Province. Obtained results provide important data regarding the co-existence of HCV and T. gondii, E. histolytica, and/or Schistosoma in Egyptian patients and shed the light on the importance of screening of these parasites among HCV patients.

 

Acknowledgements

None.

 

Funding

 This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

 

Conflicts of Interest

The authors declare that they have no conflicts of interest.