One of the significant goals in the United Nations Agenda 2030 is food security, which is a multi-dimensional goal for Sustainable Development goals (SDGs); since its related to many SDGs such as zero hunger (2nd goal) and good health and wellbeing (3rd goal)38. Food ingestion is the typical pathway of exposure to many health risks in humans, such as metal exposure. In low- and middle-income nations, malnutrition is a substantial challenge.
Fish play a significant role in enhancing food and nutrition security through addressing these global challenges. Since fish is a rich source of many fundamental nutrients for human including high-quality proteins, omega-3 fatty acids, minerals, and vitamins39. Beyond its nutritional benefits, fish contribute in a significant way to food availability by providing a sustainable and affordable source of animal protein, especially in low-income countries. In Egypt, fish is an essential constituent in the Egyptians’ regime owing to its availability and affordability.
This study was conducted to establish a relationship between tissue HM concentrations of M. cephalus and fish size. The present study revealed a size-specific patterns of HM accumulation in M. cephalus from Manzala Lake. The results indicate that most statistically significant cases demonstrate strong relationships between fish sizes and HM load in M. cephalus muscles. These findings are in agreement with a previous study by Al-Yousuf et al.40 who stated a positive correlation between the bioaccumulations of Cu and Cd in fish and both fish length and weight.
HM accumulation in M. cephalus
HM accumulation in the organs of aquatic animals can also be affected by environmental supplies, size, sex, and maturation processes26. Additionally, Widianarko et al.41 investigated the relationship between HM concentrations and the size of fish, reporting a substantial decline in Pb concentrations with increasing size, while Cu and Zn concentrations persisted unaffected by body weight. Other studies have also identified negative relationships between fish size and HM concentrations42.
Despite these outcomes, there is no definitive or established relationship between HM concentration and fish size. It has been observed that HM accumulation in fish reaches a steady state after a certain age43. This steady state suggests that concentrations of Cu and Zn essential for fish metabolism are regulated and maintained at specific levels. However, the dilution of tissue HM concentrations typically associated with growth and lower metabolic activity in older individuals26 may not be evident if environmental HM concentrations exceed the regulatory capacity of these individuals.
Furthermore, older fish possess more advanced enzymatic systems and enhanced elimination pathways such as excretion or reproduction compared to younger fish. It is also important to note that changes in diet as fish grow larger can contribute to decreased contaminant concentrations since the accumulation of contaminants is influenced by the dietary formula44. Consequently, adult fish that consume prey with lower HM contamination levels will be exposed to lower HM contaminant. In such cases, continued HM accumulation can occur, leading to positive relationships between fish size and metal concentrations in tissues1.
In heavily polluted waters, the HM content of fish tissues may be higher by several folds than the permissible levels45. Therefore, consuming polluted fish at high rates can persuade many health problems for humans, particularly for most coastal residents who consider fish as the main dietary source of animal protein46.
Risk assessment associated with consuming different sizes of M. cephalus
The present findings of risk assessment indexes underscore the importance of monitoring HM contamination in fish, particularly for populations that consume fish frequently47. Our data suggests a clear size-related pattern in HM accumulation and associated health risks, with smaller fish generally posing higher risks due to their higher concentrations of HM. The non-carcinogenic risk in the present study was expressed through the THQ, which is a significant risk assessment input associated to HM-polluted food ingestion. Consequently, the documented THQ values were > 1.0 for each HM independently, which suggests that fish are harmless for both habitual and normal human ingestion patterns. Meanwhile the THQ studies each HM individually, the THQ cannot be considered as a direct assessment of hazard34.
Although the present study reported a negligible and/or low carcinogenic risk, we documented non-carcinogenic risks for habitual consumers of all M. cephalus sizes from northern east area of Lake Manzala. While individual THQs were < 1, habitual consumers faced cumulative risks (HI > 1), warranting advisories for frequent consumption of small fish. Highlighting the potential health impacts of long-term exposure to HM contaminants through diet.
Occurrence of Myxobolus parasite and histopathological lesions in M. cephalus
Myxobolus is a genus of myxosporean parasites that can infect various fish species, including M. cephalus. Fish parasites can produce proteolytic enzymes responsible for tissue deterioration and potentially parasite encystation. The activation of melanomacrophage centers plays a crucial role in developing an immune response to the parasite, facilitating the deposition of resistant pathogens like parasitic spores and antigen processing in immune responses. Water pollution, especially with HM, can severely impact aquatic ecosystems and the organisms within them. Heavy metals such as Pb, Hg, Cd, among others, are known to be toxic to aquatic organisms, including fish48.
Fish under stressful conditions require additional energy sourced from stored nutrients like proteins, fats, and carbohydrates to adapt. Certain metals (e.g., As, Cd, Cr, Cu, Fe, Hg, Ni, Pb, Zn) can generate reactive oxygen species (ROS) due to their redox potential, which play a role in maintaining fish physiology. However, an excess of ROS can lead to oxidative stress, damaging proteins, lipids, DNA, and affecting cellular function. These pollutants enter the marine environment through industrial discharges, agricultural runoff, and other human activities49. Anuprasanna et al.50 suggested that scientific literature supports the use of fish parasites as indicators of environmental contamination, indicating a connection between fish parasites and various contaminants, including toxic metals and sewage pollutants. Moreover, the statement proposes that fish parasites can aid their hosts in surviving in heavily metal-polluted environments. Beyond HMs, parasitic infections like Myxobolus spp. further compromise fish health, with potential synergies from HM-induced immunosuppression. Radwan et al.51 implied that this assertion is backed by scientific research, suggesting that fish parasites may accumulate larger quantities of heavy metals, acting as “metal sinks”. While larger fish hosted more parasites52, their lower HM levels suggest parasites may sequester metals53, though this requires further isotopic tracing to confirm. Székely and Molnár54 reported similar findings in the gills of sea bream infected with four Myxobolus species (M. macrocapsularis, M. impressus, M. bramae, and M. hungaricus), infecting the capillary network of the gill lamellae and respiratory plate. Dias et al.55 stated alterations in the capillary network, hyperplasia of gill epithelium, and structural disorganization of secondary lamellae in fish infested by parasite. Moreover, Chavda et al.56 reported hemorrhagic and necrotic changes in epithelia and connective tissues of the gills of major aquaculture carp (Catla catla) infested by myxozoan parasites.
Furthermore, fish exhibited severe congestion of submucosal blood vessels and perivascular hemorrhage. The histopathological analysis of gills infected with Myxosporean sp. revealed the accumulation of fibrinous exudates mixed with leukocytes and myxospores45. Similar hepatic alterations were recorded by Novoa et al.57 who stated inflammations, erythrocytes’ accumulation outside the blood vessels forming a red lump of blood, and fibrosis progressing to cirrhosis represents an irreversible process accompanied by subsequent mechanical effects, and neoplasia implications. MacKenzie et al.58 and Asad et al.59 postulated that this inflammatory response is to support the recovery process of tissue and suppress the causative agent of necrosis.
Moreover, parasite infections can lead to various cell alterations, including hepatic coccidiosis, which is characterized by the enlargement of oocysts and the formation of granulomas from connective tissue or fibrotic capsules, partially replacing the host liver parenchyma60, similar findings were observed in our results. Similarly, fish exposed to HM recorded hepatic lesions in the form of hemorrhage, necrosis, hepatocyte vacuolization, nuclear degeneration, and presence of macrophages61. Fatima and Usamani8 also reported hepatic histopathological alterations including vacuolization, nuclear pyknosis, blood vessel rupture, and bleeding in fish exposed to HM.
The present kidney histopathological findings are consistent with previous studies62,63,64, which demonstrated that asynchronous spore development leads to the compression and degeneration of tubular cells, resulting in changes in lumen size. Furthermore, the degree of pathogenicity can vary, with additional observations such as hyaline degeneration, glomerular congestion, cellular edema, and the formation of a connective capsule around the spores, as seen in kidney infections in the pacu species P. mesopotamicus65. Additionally, Oreochromis niloticus infected with myxosporidian parasites exhibited degenerative and necrotic changes in the lining epithelium of renal tubules, along with numerous extra-sporogenic and sporogenic stages of myxosporidian parasites, associated with the activation of melanomacrophage66.
The degenerative changes in the liver and kidneys of fish can lead to hypoxia, osmoregulatory failure, and death of the host. The degree of pathogenicity is influenced by various factors, including the Myxosporean species, its life cycle, biology, host species, age, nutritional status, and host resistance21. Pathogenicity can result in the rupture of cysts, leading to hemorrhages, blood loss, and granulomas67. In the present study, the liver exhibited a higher degree of pathogenicity due to the presence of spores: severe focal areas of congestion in small fish, focal areas of granulomas in medium-sized fish, and dilated veins with congestion surrounded by hyaline substances in large fish. Similarly, in kidney sections, medium-sized M. cephalus showed spores alongside large cysts containing numerous myxobolus at different stages, leading to a higher degree of pathogenicity compared to small and large sizes, which only showed a large number of spores.
Salaah and El-Gaar68 indicated that exposure to HM is related to negative health effects that can suppress immunity in fish, making them more susceptible to infections and parasitic diseases. Myxobolus infections have been reported in various fish species, with their prevalence and severity potentially influenced by environmental factors, including water quality and pollutants51. On the other hand, Mahmoud et al.69 concluded that while the precise mechanisms linking HM pollution and Myxobolus infection in M. cephalus fish may vary, several potential pathways exist. HM can induce physiological stress and compromise the fish’s immune system, thereby increasing susceptibility to infections. Moreover, HM might directly influence the life cycle and reproductive capabilities of Myxobolus parasites, potentially increasing infection rates in fish populations70. Based on the finding of Radwan et al.51, parasites might actually aid their hosts in surviving by sequestering these harmful metals in HM-polluted environments.
According to Bagge et al.52, the larger the fish, the more parasites they commonly harbor, while small host individual’s incapable of supporting relatively high parasite abundances71,72. Barber73, the most accurate predictor of parasite mass was the host’s growth rate, adjusted for body size. This suggests that the larger fish tended to develop the largest parasites. Therefore, larger-growing hosts seem to provide more favorable environments for parasite growth.
Moreover, Brázová53 there is a notable relationship between HM accumulation and parasitic infections in fish. Their research found that parasites can accumulate higher levels of HM compared to their host fish. Our findings align with these findings, as we recorded lower HM accumulation in medium – and large -sized fish compared to small-sized fish, as well as a higher presence of parasites in larger fish. This relationship suggests that while larger fish show lower levels of HM accumulation and health risks, they recorded higher parasitic infections. Such findings highlight the complex interactions between HM-parasite infection exposure in fish. Our findings directly inform SDG 2 (Zero Hunger) and 3 (Good Health) by identifying size-based consumption risks in a key Egyptian fishery.