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Journal of Survey in Fisheries Sciences 2(2)1-15 2016

A short overview about and its focused on humans, bioindicators and model organisms

Strungaru S.A.1; Plavan G.1*; Nicoara M.1

Received: December 2014 Accepted: March 2015

Abstract According to Paracelsus (1493-1541) everything from this planet is , only the dose makes the poison to be harmless. Even the essential elements for life support are toxic for all organisms in high amounts. Mercury, cadmium, arsenic and lead were responsible for and death of many humans and life forms from this planet for centuries. Cadmium forms different compounds that are used in industry for , pigments, stabilizers, Ni-Cd rechargeable batteries, semiconductors, solar cells. According to literature, human’s intake the highest amount of cadmium from cigarettes smoking and food. The level of cadmium in ’s bodies is important to analyze the environmental health. are very sensitive to environmental changes and pollutants. This short overview investigated the sources and pathways of cadmium within environment, its toxicity, symptoms and diseases focused on humans and other organisms. Some possible cure for humans’ acute and chronic exposure to cadmium was searched in different studies.

Keywords: Cadmium, Human exposure, Sources, Pathways, Toxicity

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1-Laboratory of Aquatic Ecology and Ecotoxicology, Faculty of Biology, “Alexandru Ioan Cuza” University of Iasi, B-dul Carol I, no. 20A, 700505 Iasi, Romania *Corresponding author's email: [email protected]

2 Strungaru et al., A short overview about cadmium and its toxicity focused on …

Introduction Sources of cadmium in environment Cadmium is a element with the Cadmium is extremely toxic for all life atomic number 48 and symbol Cd. It forms from this planet. It was has 64 neutrons, 48 protons/electrons, discovered by F. Stromeyer, a German the melting point is 320.9ºC (594.05K, chemist in 1817 (Nordberg et al., 609.62ºF) and the boiling point is 765ºC 2009).Cadmium forms different (1038.05K, 1409.62ºF). Its crystal compounds that are used in industry for structure is hexagonal, color silvery and electroplating, pigments, plastic oxidation states 21(Nordberg et al., stabilizers, Ni-Cd rechargeable 2009). According to Paracelsus (1493- batteries, semiconductors, solar cells 1541) everything from this planet is (Hooser et al., 2012). It naturally occurs poison, only the dose makes the poison in environment together with lead, to be harmless. Even the elements copper and at low levels; all types essential for life support are toxic for all of rocks and soils contain some organisms when in high doses. cadmium. Anthropogenic activities are Mercury, cadmium, metalloid arsenic the main sources of cadmium pollution: and lead were responsible for poisoning coal combustion, zinc and and death of many humans and life refining, mine wastes, the use of rock forms from this planet for centuries. and sludge in agriculture, Studies revealed that the need for the iron and steel production (Hooser et al., at global scale started with the 2012), waste disposal and cars traffic. It Industrial Revolution and the is absorbed from these sources by the technological development (Goldberg organisms and, afterwards, can be et al., 1977; Kähkönen et al., 1998). concentrated along the food webs. These phenomena released important quantities of high toxic compounds in Human exposure, toxicity and disease air, water and land, with no possibility Cadmium has a biological half-life of to defense against them. Cadmium is 10-30 years (Nordberg et al., 1996; one of these with devastating Satarug et al., 2006; Satarug et al., effects for human health and other life 2012) higher than lead 5-20 years forms. (Chen et al., 2014). The chronic This short overview investigated the exposure with cadmium it is pollution sources and pathways of responsible for the Itai-itai disease. cadmium within environment, its Inaba et al., 2005 described this disease Downloaded from sifisheriessciences.com at 3:55 +0330 on Saturday September 25th 2021 [ DOI: 10.18331/SFS2016.2.2.1 ] toxicity, symptoms and diseases in which is caused by the chronic humans and other organisms. A poisoning with cadmium and the literature research was performed in damages for the human body are: order to find some possible cure for and glomerular dysfunctions, acute and chronic exposure to cadmium bones damage associated with in humans. and . The first symptoms are femoral bone pain Journal of Survey in Fisheries Sciences 2(2) 2016 3

followed by spine and ribs pain. manufactured by the local artisans from Patients that suffer the advanced level Cameroon. Also Romanians have many of the disease cannot walk because of traditional dishes cooked in handmade the intensive bones pain and they are aluminum cookware. It is possible that forced to remain in bed. The fractures in Romania to be the same situation like are common in this disease. in the study made in Cameroon or The first mass poisoning with this worse. Cookware are made from metal was known after World War II in recycled aluminum parts from old cars Toyama, Japan, when the Jinzu River and from scrap yards which are melted was contaminated with cadmium together without a properly purification released from mining activities (Inaba of other extremely toxic metals. In the et al., 2005). aluminum parts could be found Humans intake the highest amount cadmium which very easily of cadmium (Fig. 1) from cigarettes contaminates the food. In the above smoking and food (Andujar et al., 2010; mentioned study, the authors presented Faramawi et al., 2012; Menai et al., the importance of the food pH that is 2012; Rahimi et al., 2013; Santos et cooked in these pots. Food with an al., 2013; Rahbar et al., 2014; pH close to 4 can dissolve and release Rambousková et al., 2014; Sebastian et cadmium from the pots very fast. They al., 2014). Cadmium is present in large made an experiment with these pots to amounts in cigarettes (1-2 µg in a see how much cadmium is released in standard cigarette). A smoker 24h (ambient temperature) and 2h absorbs10-30% of this by inhalation (boiling) for a solution that simulated because tobacco intensively extracts the food with an acid pH close to 4. The cadmium from soil and accumulates it results were different for each pot in the leaves (Andujar et al., 2010). because of the cadmium concentration Approximately 80% of cadmium in the cookware, the source of absorbed in the human body is from aluminum parts is very important. The food resources (Järup et al., 2009). The cadmium range solution for 24h at element was found in high ambient temperature was 0.4-97.6 concentrations in: , potatoes, µg L-1 and for 2h boiling was 0.4-58.3 leafy vegetables, grains and cereals. µg L-1. Particles from the pots easily Uncontaminated food could be easily can contaminate the food. The level of poisoned with cadmium from contamination has many variables like: Downloaded from sifisheriessciences.com at 3:55 +0330 on Saturday September 25th 2021 [ DOI: 10.18331/SFS2016.2.2.1 ] cookware. Weidenhamer et al., 2014 aluminum source and purification, explained in their study how toxic are cooking time, food’s pH and mixing the aluminum cookware and utensils tools. 4 Strungaru et al., A short overview about cadmium and its toxicity focused on …

Figure 1: The sources with the highest risk of cadmium intake in the human body and the damages.

Many studies were focused on food conditioner is good for filtering the air contamination with cadmium and other from outside to inside the flat, but it toxic metals all around the world. Most consumes energy and it might be not of the samples were collected from healthy for the lungs. The windows species which are important in with mosquito nets may stop some dust. economical trade and their consumption It is recommended periodic cleaning of has a direct influence upon consumer’s the dust from the living rooms and health (Clemens et al., 2013; Adams et cleaning the shoes before step in the al., 2014). The contaminated food has house because they carry dust from no value and cannot be consumed. The outside to inside. healthy ecosystems will always provide quality food with the condition to have The effects on child development a balanced budget of nutrients. The cadmium level in cigarette The dust particles from the cities are smoker’s blood is 3-4 time higher than a source of cadmium exposure for for a non-smoker (Sun et al., 2014). human health. In a city with industry Sun et al., 2014 conducted a study on Downloaded from sifisheriessciences.com at 3:55 +0330 on Saturday September 25th 2021 [ DOI: 10.18331/SFS2016.2.2.1 ] and intensive cars traffic, cadmium 209 pregnant women living in Eastern particles are carried by air into the flats. China. They analyzed the lead, The most exposed flats are those near cadmium and from umbilical the boulevards. The vegetation area cord blood, maternal urine and blood. between the streets and flats is very They explained that the passive important because it may work as a smoking might increase the biofilter for dust particles. The air concentration of cadmium in urine, but Journal of Survey in Fisheries Sciences 2(2) 2016 5

it might not increase it in the maternal Are the men smokers more affected than and umbilical blood. They suggested women smokers? the possibility of crossing the placenta The answer at this question has many barrier, described in previous studies, variables in the equation. There are that plays an important role in heavy factors like: number of cigarettes day-1, metals accumulation (Ronco et al., type of cigarettes, life style, food type, 2005). The dietary intake was not age, working place, inhabiting analyzed in this study but the authors environment (city/country side) and so suggested its importance. It is possible one. There is no difference of cadmium that selenium to have a protective role presence in the blood for different age against cadmium. Menai et al. (2012) groups. There are studies that prove a studied the cadmium effect on 901 higher cadmium level in woman than pregnant women smokers and non- man blood, but there also are others smokers from Western and Eastern with no significantly difference France. Both studies had almost same (Rambousková et al., 2014). There are baseline characteristics (e.g.: body mass significantly differences between weight index, baby birth weight, baby smokers and non-smokers like 1.29 birth height). The median of cadmium µg L-1 and 0.53 µg L-1(Rambousková et concentration from maternal blood and al., 2014). Lin et al., 2014 explained cord blood in Menai et al. (2012) study that the cadmium concentration in the were 0.8 µg L-1 and 0.5µg L-1; in Sun et blood samples from smokers (0.47-1.50 al., 2014 study were 0.48 µg L-1 and µg L-1) was 3 times higher than for a 0.15µg L-1. This made the cadmium non-smoker (0.13-0.35 µg L-1).The from blood (according to Menai et al., population from a large city is more 2012) to be a biomarker for smoking exposed to cadmium than the toxicity in child development, knowing population from a smaller city that the birth weight in the high- (Rambousková et al., 2014). This exposed to cadmium group was reduced depends very much on the by 204 g compared to the low-exposed anthropogenic activities, population, to cadmium group. economic factors and industrial Cadmium exposure was also studied development. to see if it is responsible for ADHD (attention deficit hyperactivity disorder) Damage of , kidneys and in children. The partial conclusions did osteoporosis Downloaded from sifisheriessciences.com at 3:55 +0330 on Saturday September 25th 2021 [ DOI: 10.18331/SFS2016.2.2.1 ] not find it responsible for this, but Cadmium has been classified as a future studies are necessary to prove the human by IARC toxicity in children (Kim et al., 2013). (International Agency for Research on Cadmium from sea food and blood ) and US National were not associated with Autism in Program (Filipič et al., 2012). It is Jamaica (Rahbar et al., 2014). rapidly transported by the blood to 6 Strungaru et al., A short overview about cadmium and its toxicity focused on …

several organs in the body. This quickly sphingosine kinases), LPA occurs after its absorption. It (lysophosphatidic acid), knowing that irreversibly accumulates in the kidneys, chronic exposure induces renal failure liver and lungs (Chang et al., 2012). to fibrosis. On the other hand, cadmium The kidneys have the central role in induced injuries could not be directly cadmium elimination from the body applied to humans. and they represent the first target of Chen et al. (2014) run a study on cadmium toxicity (Lin et al., 2014). In 321 individuals from China (202 Lin et al. (2014), cadmium from women and 119 men). They suggested was correlated with that a higher level of cadmium in blood the risk of eGFR (estimated glomerular is associated with a lower bone filtration rate) decreasing and density in women. The smoker’s albuminuria in the U.S. population aged percentage in this study was below 5% 20 or older. The lower level of serum and the study was limited because there zinc was associated with the risk of were several variables that influence the reducing GFR. Zinc has an important bone mineral density, like diet. Kim et protective role in cadmium toxicity. Its al., 2014 conducted their study on 1086 toxicity was associated with a high risk (456 males and 630 females) living level of diabetes and diabetic residents near a cooper refinery plant in nephropathy (Lin et al., 2014). Most of Korea. The reported Cd2+ levels in urine the studies on neurotoxicity, were higher in female subjects hepatotoxicity and nephrotoxicity are (reported as µg g-1creatinine) than in conducted on models organism. Yuan et male subjects. Their results suggested al. (2014) experimented on rats. Their that an increased Cd2+ body burden in aim was to study the oral acute men directly decreased the bone exposure of rats to different mineral density which on contrary

concentrations Pb (NO3)2-CdCl2 for 14 knowing that the female women are days and sub-chronic oral toxicity for more exposed than man. The increased ninety days. Their results explained that Cd2+ body burden in females firstly the rat female were more sensitive than induced the renal microtubular damage male to higher concentrations and the and leads to osteoporosis. In Shin et al., toxic effects were targeted on blood, 2011 a total of 804 residents were kidneys, liver and testicles. The number surveyed from an industrial complex of red cells from the blood was area in Korea. The aim of their study Downloaded from sifisheriessciences.com at 3:55 +0330 on Saturday September 25th 2021 [ DOI: 10.18331/SFS2016.2.2.1 ] significantly decreased and the liver was to investigate the relationship functions were reduced. Tsutsumi et al. between the bone mineral density and (2013) run a study to observe if the rats the urinary cadmium in different age exposure to Cd2+ modifies the plasma groups for males and females. The levels of S1P (produced by authors concluded that females had a phosphorylation of sphingosineby higher risk to osteopenia and Journal of Survey in Fisheries Sciences 2(2) 2016 7

osteoporosis than males based on the authors concluded that the soybeans relation urinary Cd2+ and bone mineral diet may provide benefits as an density. Osteopenia was associated with antioxidant in prevention of arterial high concentration of urinary Cd2+ for injuries caused by cadmium exposure in females and males. The mineral density experimental conditions. It is possible for children and adolescents (Age < 19) to protect the aorta against the cadmium groups was not correlated with urinary toxicity. Cd2+ and gender; the risk was not Caffeic acid phenethyl ester– present at this age. Only the adult group Kobroob et al. (2012) studied on Wistar had a significant correlation between rats the role of this compound in kidney these parameters, suggesting that the mitochondria protection. This is an exposure period and age have the most active component of the propolis from important role (Shin et al., 2012). honeybee. In the first part of their study the authors showed that cadmium was Is there any cure against cadmium responsible for kidney mitochondrial exposure? dysfunction by producing the oxidative Tetraethylammonium salt of monesic stress in isolated mitochondria groups acid – Ivanova et al. (2012) suggested incubated with 10, 20, 30 and 40 µM

that this compound can be used as CdCl2. The results presented the treatment of subacute cadmium antioxidant potential of caffeic acid intoxication because phenethyl ester in kidney mitochondrial tetraethylammonium salt of monesic protection against the renal toxicity acid is a good chelating agent. The caused by cadmium. general with chelating agents is Litchi chinensis Sonn.(litchi) flower used for the treatment of acute and extract – Hwang et al. (2013), observed

chronic metal intoxication. This on rat liver cells treated with CdCl2 that compound was tested on mice. The litchi flower extract had an active cadmium level from kidneys and liver antioxidant effect against cadmium decreased with 50% comparative with toxicity in liver by decreasing the the control group consequent to the oxidative damage and the TGF-β1in treatment. The testing group was treated HSCs activation. during the 15th day of the 28 experiment Allium cepa L.(common onion) days with 16 mg/body weight. extract–Ige and Akhigbe (2013) run an Soybeans diet– Díaz Matías et al. experiment on male Wistar ratsto Downloaded from sifisheriessciences.com at 3:55 +0330 on Saturday September 25th 2021 [ DOI: 10.18331/SFS2016.2.2.1 ] (2013) used male Wistar rats in an analyze if the common onion extract is experiment with tape water a possible remedy for cadmium 2+ contaminated with CdCl2 (15 and 100 exposure. The rats that were under Cd ppm Cd2+). Two types of diet were exposure received contaminated

analyzed in this experiment: one with drinking water with CdSO4 (1.5ml/kg -1 casein and one with soybeans. The body weight from 0.3mg ml CdSO4). 8 Strungaru et al., A short overview about cadmium and its toxicity focused on …

Onion extract (1 ml/100 g body weight) 100 µM). The results explained the was administrated to the treatment protective effect of epigallocatechin-3- group. The authors firstly demonstrated gallate against metabolic dysfunction cadmium toxicity: damage in vascular and lipoperoxidationin brain function, hemorheology, dyslipidaemia mitochondria from rat brain caused by and . The onion extract Cd2+ neurotoxicity. This compound was a good protector against proved important antioxidant and atherosclerotic condition via a chelating properties in this experiment. mechanism depending on lipid The future of epigallocatechin-3-gallate peroxidation induced by cadmium. It as treatment against Cd2+ neurotoxicity was considered to have applications in is not far away, but there are required the treatment of atherosclerosis and morein vivo exams and hypertension induced by Cd2+. pharmacological studies. Procyanidin extract from grape Chlorpromazine and verapamil– the seed–Chen et al. (2013) tested on study was done by Xu et al. (2008) on Kunming mice the beneficial effect of Wistarrats in vivo experiment. The

procyanidin extract against renal authors intraperitoneally injected CdCl2 damage (oxidative damage, renal (7µM/kg body weight/day) and apoptosis related genes Bax and Bcl-2) different concentrations of produced by cadmium. The authors chlorpromazine and verapamil. They used for Cd2+ exposure the studied the toxicity of cadmium in concentration of 5mg/kg body weight kidneys. These two compounds reduced

CdCl2 for all groups, orally the kidneys damage caused by administrated. The groups were treated cadmium (oxidative damage; with procyanidin extract in different Ca2+intracellular disturbance of doses (50, 100 and 200mg/kg body homeostasis; abnormal activation of weight). The higher dose of procyanidin PKC, Na+-K+-ATPase and extract had a protective effect against Ca2+ATPase).Chlorpromazine and Cd2+ in renal oxidative damage and verapamil reduced the oxidative stress reduced the renal apoptosis by and stabilized calcium homeostasis. interfering with Bax and Bcl-2 Succimer – Cao et al. expression. (2013) studied the cadmium exposure Epigallocatechin-3-gallate from in children from US. They observed the green tea – Abib et al. (2011) analyzed succimer treatment against the Downloaded from sifisheriessciences.com at 3:55 +0330 on Saturday September 25th 2021 [ DOI: 10.18331/SFS2016.2.2.1 ] the protective role of epigallocatechin- cadmium poisoning because it was 3-gallate in brain mitochondria obtained approved for pediatric . from Wistar rats against neurotoxicity The studies run on animals provided of Cd2+. The samples were incubated positive effects in reduction of

with CdCl2 (100, 200 or 300 µM) and cadmium absorption and protection of epigallocatechin-3-gallate (10, 50 or the organism against it. According to Journal of Survey in Fisheries Sciences 2(2) 2016 9

this study results, after orally animals are not similar to those from administration of the treatment, the experimental conditions which are cadmium level from the children blood clearer (Burger et al., 2008). was slightly increased. The succimer Binkowski et al. (2013) analyzed did not reduce the cadmium level. liver and kidney samples from Anas Cadmium once entered in the cells, platyrhynchos L. (Mallard) and bounds to different compounds and is Fulicaatra L. (Coot). The birds were hard to eliminate it in cases of legally collected by hunters in 2006- Cd2+poisoning. 2008 during hunting seasons near Zator in Poland. The study was focused on Cadmium in birds lead and cadmium concentrations and The level of cadmium in birds is lesions from liver and kidneys. Most important to analyze the environmental exposed to lead and cadmium were the health. Birds are very sensitive to mature birds; they had more liver and environmental changes and pollutants. kidneys lesions than juveniles. Some The satellite monitoring system of specimens were more intoxicated with bird’s populations provided information lead than with cadmium. The about their routes, feeding and conclusions did not recommend reproduction places. The researcher can consumption of mallards and coots measure anthropogenic impact better from Zator area because the and better. The studies can be done in concentrations of these metals were laboratory conditions and by over the limit accepted by European observation in nature. Toxicological safety norms. Binkowski and Sawicka- studies conducted in laboratory Kapusta (2015) used same species to conditions provide fast and clear results study the cadmium distribution for about the toxicity of a compound, but mallards and coots collected from Zator they are limited: they cannot be and Milicz, Poland. The birds were replicated with all environmental and legally collected by hunters in 2006- food conditions. There are many 2009, during the hunting seasons. There possible interactions which are not were analyzed samples from: feathers, correlated and cannot be replicated bones, muscle, brain, spleen, liver, (Burger et al., 2008). Toxicological kidneys, blood, gizzard content and observations in nature and analyzes are excrements. Their results generally closer to reality but are extremely showed that cadmium concentration in Downloaded from sifisheriessciences.com at 3:55 +0330 on Saturday September 25th 2021 [ DOI: 10.18331/SFS2016.2.2.1 ] complicated and restricted by many kidneys>liver>spleen>brain>muscle>b interactions such as: environmental one>feather for both studied species. chemistry-organism, organism- The authors observed that the mallards organism, organism-biochemical and coots from Zator area were more processes inside the body. affected by Cd2+ than the ones from Toxicological results from free living Milicz. The in vivo biomarkers 10 Strungaru et al., A short overview about cadmium and its toxicity focused on …

(feathers, blood and excrements) had We presented in this study a few not significant results in order to problems caused by cadmium in conclude in their study. humans and other life forms with the Mallory et al. (2014) studied the answers based on the scientific work hepatic cadmium and zinc in Somateria made by researchers all around the mollissima L.(common eider) from world to whom we are grateful. There three Canadian colonies. They selected are many questions without an answer for the study females of common eider. about cadmium toxicity and possible The birds were euthanized by cervical diseases that may be caused in humans’ dislocation. This avoids any possible bodies and others life forms. This metal contamination. The samples collected in high concentrations has a negative in 2008 were analyzed and compared impact and it is a problem for now and with the results from 1992-1993 and in the future. Even if the pollution 2001-2002. This study was very sources are stopped; - what will it important for the cadmium monitoring happen with the cadmium entered in the in the Artic area. The concentrations of food webs? Should we be afraid of this cadmium in liver were: 8.23±3.03 µg g- element? The answers at this final 1in 1992-1993, 15.70±3.93 µg g-1in question will be different for each 2001-2002 and 44.67±18.82 µg g-1 in person, but it is necessary to know the 2008. This study represents a warning exposure risk and sources. message regarding the changes occurred in the arctic marine Acknowledgments ecosystems and the contamination of This study was supported by the the food webs with cadmium. strategic grant There were reported in vitro POSDRU/159/1.5/S/133391, Project experiments proving that cadmium and “Doctoral and Post-doctoral programs lead decreased the number of of excellence for highly qualified erythrocytes and induced the apoptosis human resources training for research of the blood cells from Anas in the field of Life sciences, platyrhynchos L. (Mallard) and Buteo Environment and Earth Science” buteo L. (Common buzzard) (Romero cofinanced by the European Social et al., 2009; Hernández-García et al., Fund within the Sectorial Operational 2014). In laboratory conditions, Program Human Resources Cadmium caused malformations of Development 2007 – 2013. Downloaded from sifisheriessciences.com at 3:55 +0330 on Saturday September 25th 2021 [ DOI: 10.18331/SFS2016.2.2.1 ] chicken at early stages of development and DNA methylation in hens (Zhang et References al., 2009; Yamamoto et al., 2012). Abib, R.T., Peres, K.C., Barbossa, A. Chicken embryos are model organisms M., Peres, T.V., Bernardes, A., in the study of cadmium genotoxicity Zimmermann, L.M., Quincozes- and different organs development. Santos, A., Fiedler, H.D., Leal, Journal of Survey in Fisheries Sciences 2(2) 2016 11

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