125 Annales Universitatis Paedagogicae Cracoviensis Studia Naturae, 3: 125–134, 2018, ISSN 2543-8832 DOI: 10.24917/25438832.3.9 Iwona Ałtyn, Magdalena Twarużek* Department of Physiology and Toxicology, Institute of Experimental Biology, Faculty of Natural Sciences, Kazimierz Wielki University, Chodkiewicza 30 St., 85-064 Bydgoszcz, Poland, *twarmag@ukw.edu.pl; https://orcid.org/0000-0002-8655-0067, https://orcid.org/0000-0002-2568-1178 Heavy metal and mould contamination of herbal medicinal products – an overview The medicinal plant consists of many active chemicals, such as mucilage, polyphe- nols, polysaccharides, etc., which may modify the effects of the active principles. Therefore, it is believed that some natural remedies may have toxic effects on the body or act as an agonist or antagonist of the active substance (Dar, 2013). That is why toxicity tests for the pre-assessment of the efficacy of plant extracts are so impor- tant (Hewawasam, 2016). Herbal plants are exposed to different types of pollution, from chemical to microbiological, which, as mentioned above, can have a negative impact on the human body. There are numerous causes of chemical and microbiological pollution. One of them may be associated with the usage of human excreta, animal manures, and sewage as fertilisers. The World Health Organization’s (WHO) guidelines of Good Agricultural and Collection Practices (GACP) for medicinal plants prohibit the use of human manure as fertiliser. Moreover, they insist that animal manure should be thoroughly composted (WHO, 2003). Another cause of chemical pollution may be found in composted sewage, as well as in chemicals used in households and industrial chemicals, as the vast majority of them are found in analysed herbs and herbal mate- rials. The listed potential sources of herbal contamination may lead to the appearance of unwanted chemicals, not just during the preparation process, but also in its final product. According to the World Health Organization’s research, the level of pollution present in medicinal plants may change in different stages of its manufacture, such as post-harvest processing (e.g., drying), herbal preparation – extraction process, as well as in the finished herbal products (WHO, 2007). Therefore, the manufacture process of herbal preparation or its final pharmaceutical product should be controlled at each stage of production by GACP for medical plants and by Good Manufacturing Practic- es (GMP) for herbal medicines. Iw on a A łty n, M ag da le na T w ar uż ek 126 The purpose of this review is to show the mycological and chemical contamination of medicinal plants, as well as to indicate several important challenges related to the effective monitornig of their safety. Contamination by heavy metals The rapid growth of industry and agriculture in recent times has caused a serious problem of contamination of air, soil, and water with heavy metals (Orisakwe et al., 2012). Heavy metals are generally defined as a collection of metalloids with anatom- ic density greater than 6 g/cm3. Moreover, some of them (cadmium Cd, chromium Cr, copper Cu, mercury Hg, nickel Ni, lead Pb and zinc Zn) possess toxic properties (Awodele et al., 2013). In the sciences of biology and medicine, heavy metals are de- fined as elements used in the industry and simultaneously characterised by the toxici- ty to humans or the environment. The widespread environmental dispersion of heavy metals enter into the food chains through the epidemic pollution of air, water, and soil during cultivation (Husain et al., 1995). The use of herbal plant contaminated by heavy metals for the production of herbal medicines can trigger chronic accumulation of metals in the human organs (Ajasa et al., 2004; Ang et al., 2006; Arzani et al., 2007). Bioaccumulation of heavy metals in the body can cause both short-term and long-term health damages. It can cause abdom- inal pain, disease of the foetus, which may lead to abortion and/or preterm labour, as well as mental retardation to children, while adults may suffer from hypertension, fatigue, as well as impaired kidney and brain damage (Hifsa et al., 2009). Prolonged consumption of products contaminated with heavy metals may also lead to skin erup- tions, intestinal ulcers, and different types of cancer (Shad et al., 2008). Due to the high health risks, the WHO has developed limit guidelines for the maximum values of these compounds in herbal medicine. According to the WHO, remedies should be checked for the presence of different contaminants such as heavy/toxic metals, fungi, and microorganisms (WHO, 1998; 2007). Several studies have tested herbal medicine preparations for heavy metal con- tamination. Filipiak-Szok et al. (2015) determined the highest concentration of lead Pb (9.27 µg), cadmium Cd (0.36 µg) and arsenic As (1.25 µg/g), in dietary supple- ments. For Ni 0.16–14.21 µg/g dry mass (d.m.), while for Ba 0.49–11.45 µg/tablet and 11.64 µg/g d.m. The lowest concentration of all analysed heavy metals was found for antimony Sb. For plants it was at the level of 0.003 µg/g d.m. and 0.10 µg/g d.m. for dietary supplements. Chuang et al. (2000) and Singh and Garg (1997), analysed the Chinese root of Panax ginseng C.A. Meyer. The results showed the level of Pb as – 0.16 ± 0.11 µg/g, Cd as – 0.06 ± 0.04 µg/g and As as – 0.05 ± 0.03 µg/g; 4.62µg/g bari- um Ba and 223 µg/g Sb. H eavy m etal and m ould contam ination of herbal m edicinal products – an overview 127 Olowoyo et al. (2012) showed that the maximum concentration of zinc Zn in the roots of Datura stramonium L. was recorded at value of 90.65 ± 1.22 μg/g. The concen- tration of Cu from both plant parts ranged from 3.84 ± 0.33 μg/g – 14.05 ± 0.02 μg/g. Contamination by nickel Ni from the plant parts were in the range from 4.36 ± 0.25 μg/g to 15.78 ± 0.14 μg/g. Pb concentration in all the plant parts ranged from 0.51 ± 0.01 μg/g to 2.13 ± 0.02 μg/g, while Cr levels ranged from 5.65 ± 0.05 μg/g to 18.31 ± 0.01 μg/g. Başgel et al. (2006) determined the high concentration of calcium Ca from 965 mg/kg (Rosae caninae fructus) to 17.740 mg/kg (Tilia × vulgaris H. and Urtica di- oica L.). Magnesium Mg in the seven herbs and their infusions was in the range of 1643–3778 mg/kg and 610–2078 mg/kg, respectively. The iron Fe content of the herbs and their infusions was in the range of 224–502.7 mg/kg and 4.90–107.4 mg/kg, re- spectively. The content of Al in the herbs varied between 87 mg/kg (T. × vulgaris) and 596 mg/kg (U. dioica). Manganese Mn in the herbs varied in a wide range of 23–244 mg/kg (R. c. fructus); whereas, its concentration in the infusions varied be- tween 4.30 mg/kg (Foeniculum vulgare Mill.) and 49.1 mg/kg (R. c. fructus). The high- est concentration of Cu was in the Matricaria chammomilla L. infusion as 6.75 mg/ kg and the lowest value was determined in the Cassia anqustifolia Vahl infusion as 2.45 mg/kg. Sr in the herbs was found between the range of 17.5 mg/kg (Salvia of- ficinalis L.) and 174 mg/kg (U. dioica); whereas, in the infusions, it varied between 2.45 mg/kg (S. officinalis) and 43 mg/kg (U. dioica). Caldas (2004) showed that none of the 38 analysed samples of Cynara cardunculus var. scolymus (L.) Fiori, Solanum melongena L. or Paullinia cupana Kunth contained detectable levels of cadmium Cd (< 0.2 mg/g), mercury Hg (< 0.01 mg/g), or lead Pb (< 2.0 mg/g). Cadmium concentrations varied from < 0.20 to 0.74 mg/g. Centella asi- atica (L.) Urban. The levels of Hg varied from < 0.01 to 0.09 mg/g with Ginkgo biloba L. The levels of lead in the samples varied from < 2.0 to 1480 mg/g with Aesculus hip- pocastanum L. having the highest concentrations. Ting et al. (2013) research on Chinese herbal medicine showed that out of the 6 metals (Mn, Pb, Cu, Cd, Fe, Zn), the highest concentration which reached the level of 1.394–18.545 mg/L belonged to Mn. Cd had the lowest level which was identified as 0.105–0.314 mg/L. Other metals were all < 3 mg/L. Naga Raju et al. (2006) showed that Ocimum sanctum L. were contaminated by Ni (24.1 ± 4.7 µg/g). The same high level of Ni 33.7 ± 50 µg/g was shown in the results of a study conducted by Gowrish- ankar et al. (2010). The O. sanctum was an object of research conducted by Professor Kumar and his team. In their work, the results showed very high concentration of Al at the 8249 µg/g (Devi et al., 2008). Harris et al. (2011) study showed that all samples of Chinese herbal medicine were contained by at least one heavy metal. 34.4% of samples had detectable levels of all five metals. The highest concentration of Cr and Ar, were Iw on a A łty n, M ag da le na T w ar uż ek 128 21 ppm and 20 ppm, respectively (Egan et al., 2007; Lendinez et al., 2001; Saper et al., 2004; USDA, 2009; US FDA, 2007; US GAO, 2010). Fungal contamination Moulds comprise a large group of around 100 thousand species, and they are widely distributed in nature. Moreover, they are one of the most widespread environmental pollutants. The reason for this phenomenon is connected with their high ability to multiply on various raw materials, under favourable conditions (Ahmad et al., 2014). Therefore, it is estimated that approx. 25% of them have moulds (Hussein et al., 2001). Contamination by such fungi as Aspergillus spp., Penicillium spp., Fusarium spp. and Alternaria spp. is especially dangerous due to the production of toxic secondary me- tabolites – mycotoxins, which can cause both acute and chronic toxicities or even death (FAO, 2001). Herbal medicinal products preparations have been analysed for fungal contamina- tion in a number of studies. Efuntoye (1996) showed that samples were contaminated by the colony of Aspergillus spp., Pencillium spp., Fusarium spp., and Rhizopus spp. Moreover, Mucor spp., Aspergillus spp. was isolated in all the samples of studied herbs, while the species Aspergillus niger Tiegh and A. flavus Link were the most prevalent. The genus Fusarium spp. was found in six of the plants studies. Colonies of Tricho- derma viride Pers. were isolated from Azadirachta indica A. Juss., Plumbago zeylanica L. and Jatropha curcas L., while colonies of Cladosporium bantianum (Sacc.) Borelli and Alternaria humieola Oudem. were found in Xylopia aethiopica (Dunal) A.Rich. and Mangifera indica L., respectively. Penicillium spp. were found in samples, with frequency at a level of 87.5% and makes up 18.5% of the total fungi. Tournas et al. (2006) showed that 100% of the Siberian, 56% of the Chinese and 48% of the American ginseng root samples were contaminated with fungi. The high- est contamination level (4.3×105 cfu/g) was observed in the locally grown American ginseng root, while the lowest (< 100 cfu/g) in ginseng extract. Alternaria alternata (Fr.) Keissl. was found at levels as high as 4.0×104 cfu/g, while Aspergillus spp. and Cladosporium spp. were found at levels ranging between < 100 and 1.0×104 cfu/g. Eu- rotium chevalieri L. was present in 11%, whereas Penicillium spp., Rhizopus spp. and yeasts were found in 33% of the tested samples. Penicillium spp. levels were between < 100 and 1.0×103 cfu/g. The lowest level (< 100 – 4.0×102 cfu/g) of Aspergillus niger was present in 22% of the samples. Additionally, Raman et al. (2004) also examined the dietary supplements including ginseng and the results showed that samples were contaminated with fungi, but the study did not quantify the fungal contaminants. Zhang and Zhang (2002) also isolated moulds from American ginseng seeds. Accord- ing to the results of their work, researched samples were contaminated by high levels H eavy m etal and m ould contam ination of herbal m edicinal products – an overview 129 of Fusarium spp., Alternaria spp., Penicillium spp., Rhizopus spp. and low levels of Aspergillus spp. Rajeshwari and Raveesha (2016) revealed that 6 of the herbal drugs’ raw materials were highly contaminated: Withania somnifera (L.) Dunal (100%) followed by Curcu- ma angustifolia Roxb. (92%), Centella asiatica (L.) Urban (88.6%), Acorus calamus L. (88%), Tinospora cordifloia (Willd.) Hook. f. & Thomson (86%), and Myristica fragrans Houtt. (82%). Therefore, researchers were able to identify and isolate 41 fungal species belonging to 16 genera. The most predominant were Aspergillus spp. and Penicillum spp., while the A. niger was the most frequently occurring fungi. Roy and Chourasia (1990) analysed traditional herbal drugs from India. The results showed that Asper- gillus spp., Fusarium spp., Penicillium spp. and Trichoderma spp. were the common moulds isolated from most of the samples. Aspergillus spp. were isolated from almost all samples with a frequency at 66.2% on Strychnos nux-vomica L. seeds. The Fusar- ium spp. was at the level of 11.6 ± 6.5 in the 3 samples of Ichnocarpus frutescens (L.) W.T.Aiton. Hitokoto et al. (1978), while analysing herbal drugs’ samples, discovered that the most predominant fungi were Aspergillus spp. and Penicillium spp. Mucor spp., Rhiz- opus spp., Cladosporium spp., and Aureobasidium spp. were found in a few samples. The species of Penicillium spp. predominated from powdered Japanese peony roots – Paeoniae Radix Pulverata (2.579 colonies/g) and powdered coptis – Coptidis Rhizoma Pulveratum (9.500 colonies/g). Aspergillus spp. with the highest frequency was found in powdered coptis (3.438/g), powdered scutellaria roots – Scutellariae Radix Pulver- ata (2.241/g), powdered Japanese peony roots (1.523/g), and powdered cininidium – Cinidii Rhizoma Pulveratum (1.133/g). The species A. niger was the most frequently encountered group in the drugs, accounting for 24.6% of the total isolates. The Asper- gillus glaucus (L.) Link and A. flavus Link were the next most prevalent species with 9.3% and 7.8% of the total isolates, respectively. On the other hand, Udagawa et al. (1976) showed that A. niger, A. glaucus and A. flavus were the most prevalent species in herbal drugs. Matsushima et al. (1958) showed that Aspergillus awamori Nakaz., A. glaucus, A. mangini Thom & Raper, A. niger, A. ochraceus Wihelm, Penicillium frequentans West., P. variabile Sopp., O.J., and Rhizopus spp. were predominant. Chourasia (1995) examined the herbal drugs from the Indian Pharmacopoeia. The maximum level of fungi was found in the fruits of Piper longum L., P. nigrum L. and Elettaria cardamo- mum (L.) Maton. The most frequently isolated fungi were Aspergillus spp. and Fusar- ium spp., while the lowest frequently isolated ones were Alternaria spp., Emericella spp., Mucor spp., Penicillium spp., and Chaetomium spp. Rizzo et al. (2004) conducted a study to assess the presence of fungi in dried me- dicinal herbs. 27% of all samples were contaminated with Aspergillus flavi section, Iw on a A łty n, M ag da le na T w ar uż ek 130 25% Circumdati section (Aspergillus alliaceus Thom & Church, A. ochraceus and A. sclerotiorum G.A. Huber) and 16% with Fusarium spp. The most frequent contam- inants were A. nigri. Ahmad et al. (2014) studies showed that 90% of medicinal plant samples were con- taminated with moulds and 70% of them exceeded the permissible limits determined by the United States Pharmacopeia (2005). Mould contamination in Withania coag- ulans (Stocks) Dunal (3.4×1011 CFU g-1), Papaver somniferum L. (6.1×1012 CFU g-1), Olea europaea L. (1.08×105 CFU g-1), Stevia rebaudiana (Bertoni) Bertoni (7.1×105 CFU g-1), Ocimum basilicum L. (2.4×105 CFU g-1), Aloe vera (L.) Burm. f. (3.5×103 CFU g-1), Opuntia monacantha Haw. (5.8×104), Glycyrrhiza gabra L. (2.2×105 CFU g-1), and Cymbopogon citratus (DC.) Stapf (4.6×103 CFU g-1) were observed less often but still in a significant quantity. The most frequently isolated species were Aspergil- lus niger, A. flavus, A. parasiticus, Speare, A. terreus Thorn, Penicillium verrucosum Dierckx, P. citrinum Thom. C, Fusarium sp., Rhizopus sp., and Alternaria alternata. Among them, Aspergillus niger were found in 50% of the samples, followed by A. fla- vus reaching 43%. Those results are in agreement with findings of Abou-Arab et al. (1999) and Abou Donia (2008), which showed that A. niger and A. flavus were the most dominant moulds in the collected samples of medicinal herbs in Egypt. Bugno et al. (2006) results showed that, in Cymbopogon citratus (DC. ex Nees) Stapf, the level of fungal pollution was of 3.98×105 cfu/g-1. Additionally, research conducted by Jahani et al. (2013) on the subject of fungal contamination in barberry showed high levels of Aspergillus spp. and Penicillium spp. Filipiak-Szok et al. (2016) examination of plants and dietary supplements showed that the sum of moulds and yeast were lower than 69 cfu/g-1, with the most frequently species Cladosporium spp. Rawat et al. (2014) examined 40 samples of 8 different medicinal plants: Saraca indica L., Terminalia arjuna (Roxb.) Wight & Arn., Withania somnifera (L.) Dunal, Bacopa monnieri (L.) Wettst., Evolvulus alsinoides (Linn.) Linn., Zingiber officinale Roscoe. 92.5% of all analysed samples were found to be contaminated by more than one fungal species. Those findings revealed that the highest frequency of contamination in sam- ples belongs to Aspergillus niger (38.56%) then Mucor spp. (32.05%), Rihzopus spp. (12.82%), A. flavus (12.82%), A. nidulans (2.56%) and Myceliophthora spp. (1.28%). Conclusions Nowadays, due to the stressful working mode and lack of time for healthy meals, con- sumers are increasingly relying on medicinal plants as medications for health and ail- ments, or even dietary supplements. The presented results of multiple research studies indicate that plants for medical use should be carefully stored and evaluated for their possible contamination. Long-term studies on heavy metal and fungal contaminants H eavy m etal and m ould contam ination of herbal m edicinal products – an overview 131 show how important monitoring is in determining the safe levels of pollutant con- centration in medicinal plants and their products. Each level of contamination that humans are exposed to by the intake of medicinal plants needs to be considered in- dividually for every type of medicinal plant. Therefore, to protect consumers against the contaminant health hazards, storage conditions of medicinal plants should be improved. Moreover, good agricultural practice should be implemented to lower the presence of moulds on the medicinal plants. Due to the wide range of different factors threatening a plant’s health, it is very important to continuously exert regular myco- logical evaluations. 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Jednakże w dzisiejszych czasach mogą one nie spełniać wymagań dotyczących jakości, bezpieczeństwa i  skuteczności. Większość produktów ziołowych nie jest testowana, a ich efekty działania są słabo monitorowane. Konsekwencją tego jest niewystarczająca wiedza na temat przebiegu ich działania, skutków ubocznych, przeciwwskazań oraz interakcji z występują- cymi na rynku produktami farmaceutycznymi oraz żywnością. Przyczyną negatywnego wpływu surowców ziołowych na organizm może być ich zanieczyszczenie przez różne grzyby pleśniowe, powstające podczas zbioru, przetwarzania, przechowywania, a także dystrybucji. Zanieczyszczenie surowców zielarskich może być również spowodowane przez różnorodne metale ciężkie, które występują w wielu aspektach współcze- snego życia. Celem niniejszej pracy jest przegląd informacji na temat stanu mykologicznego i chemicznego roślin leczniczych, a także wskazanie kilku ważnych wyzwań związanych z efektywnym monitorowaniem ich bezpieczeństwa. Key words: contamination, heavy metals, medicinal plants, mould Received: [2018.02.23] Accepted: [2018.10.16]