Вы находитесь на странице: 1из 6

670 M. Yoshinaga et al.

/ Chemosphere 201 (2018) 667e675

Fig. 2. Effects of sole exposure to Cr(VI) and Cr(III) on survival of HaCaT keratinocytes. (A) Ratios (mean ± s.d.; n ¼ 3) of surviving HaCaT keratinocytes cultured for the indicated
days in the presence (0.1e3 mM) or absence of Cr(VI) are presented. (B) Ratios (mean ± s.d.; n ¼ 3) of surviving HaCaT keratinocytes cultured for the indicated days in the presence
(10-1700 mM) or absence of Cr(III) are presented. The results are shown as ratio to the value of nil control on day 7 (Ctrl, open square). *, **Significantly different from the control as
(*p < 0.05, **p < 0.01) analyzed by Dunnett's test on each day.

Fig. 3. Effects of exposure to either Cr(VI) or Cr(III) on transforming activity in HaCaT keratinocytes. (A, B) Graphs (mean ± s.d.; n ¼ 4) showing the ratios of colony number per
well (A) and photographs of colonies (B) of HaCaT keratinocytes in the presence (0.001e0.1 mM) or absence of Cr(VI) are presented. (C, D) Graphs (mean ± s.d.; n ¼ 4) showing the
ratios of colony number per well (C) and photographs of colonies (D) of HaCaT keratinocytes in the presence (0.1e10 mM) or absence of Cr(III) are presented. The results (closed bars)
are shown as ratio to the value of nil control (Ctrl, open bar) (A, C). **Significantly different from the control (**p < 0.01) as analyzed by Dunnett's test.
M. Yoshinaga et al. / Chemosphere 201 (2018) 667e675 671

3. Results Then Cr pollution was focused on because the level of Cr was

252-fold and 2211-fold higher than the levels of Ba and As,
3.1. Levels of Cr, As and Ba in water of Buriganga River and canals at respectively, in canal water at Hazaribagh. Our analysis of chemical
Hazaribagh species showed the mean concentration of Cr(VI) [6.7 mg/L (0.1 mM)]
and mean total concentration of Cr [14284.7 mg/L (274.7 mM)] in
Sampling (Fig. 1A) was performed in the upstream region (a) canal water at Hazaribagh (Fig. 1E). The maximum concentrations
and proximal (d) and distal (e) downstream regions of Buriganga of Cr(VI) and Cr(III) were 38.1 mg/L (0.7 mM) and 88697.3 mg/L
River after defining the confluence (c) of Buriganga River and canals (1705.7 mM), respectively.
from tanneries at Hazaribagh (b) as a base point. Concentrations
(mg/L) of soluble forms of Cr (Fig. 1B), As (Fig. 1C) and Ba (Fig. 1D) in 3.2. Effects of exposure to either Cr(VI) or Cr(III) on anchorage-
water from 5 sections are shown. Mean levels of Cr in canal water at independent growth
Hazaribagh and in Buriganga River water from the confluence and
proximal and distal downstream regions were about 5160-fold, 5- A previous study showed that canal water at Hazaribagh
fold, 4-fold and 1-fold higher than the mean level of Cr in Bur- (UNICEF (The United Nations Children's Fund), 2010; Watch, 2012)
iganga River water from the upstream region, respectively (Fig. 1B). in addition to Buriganga River water (Rahman and Al Bakri, 2010)
However, mean levels of As and Ba in canal water at Hazaribagh and was used for washing and bathing by the residents. To examine the
Buriganga River water from the upstream, confluence, and prox- potential health risk of sole exposure to Cr(VI) and Cr(III), a colony
imal and distal downstream regions were comparable (Fig. 1C and formation assay was performed following a cell survival assay by
D). using human non-tumorigenic HaCaT keratinocytes (Figs. 2 and 3).

Fig. 4. Effects of coexposure to Cr(VI) and Cr(III) on transforming activity in HaCaT keratinocytes. Graphs (mean ± s.d.; n ¼ 4) showing the ratios of colony number per well (A,
C) and photographs of colonies (B, D) of HaCaT keratinocytes in the presence or absence of 0.001 mM Cr(VI) and/or 10 mM Cr(III) (A, B) or 0.003 mM Cr(VI) and/or 1 mM Cr(III) (C, D)
are presented. The results (closed bars) are shown as ratio to the value of nil control (Ctrl, open bar) (A, C). *Significantly different from the control (*p < 0.05) as analyzed by
Dunnett's test.
672 M. Yoshinaga et al. / Chemosphere 201 (2018) 667e675

and in the nil control (Fig. 5). Phosphorylated levels of AKT in cells
coexposed to 0.001 mM Cr(VI) and 10 mM Cr(III) were also higher
than those in cells solely exposed 0.001 mM Cr(VI) and 10 mM Cr(III)
and in the nil control (Fig. 5).

3.5. Adsorption of Cr(VI) and Cr(III) by MF-HT

Adsorption of Cr(III) and Cr(VI) by MF-HT was examined by a

batch method previously described (Kato et al., 2016). After
investigating plural adsorption models including Freundlich and
Langmuir isotherms, the use of Langmuir isotherms was selected as
a suitable method for examining the equilibrium adsorption results
of Cr in MF-HT. Equilibrium data of Cr(VI) (Fig. 6A) and Cr(III)
(Fig. 6C) and Langmuir isotherms for Cr(VI) (R2 > 0.95; Fig. 6B) and
Cr(III) (R2 > 0.95; Fig. 6D) adsorption by MF-HT are shown.
Maximum adsorption capacities of MF-HT for Cr(VI) and Cr(III)
calculated from the Langmuir isotherms were 9.0 mg/g and
1041 mg/g, respectively, in theory.
An adsorption test for Cr by MF-HT was finally performed in
canal water containing wastewater from tanneries at Hazaribagh.
The mean concentration of Cr (1213 mg/L) in canal water samples
(n ¼ 10) treated with 1% weight of MF-HT for 1 min was decreased
to 142 mg/L (Fig. 6E and F).

4. Discussion

Our environmental monitoring in wide areas of Buriganga River

and canals at Hazaribagh provided more direct evidence of
Fig. 5. Effects of coexposure to Cr(VI) and Cr(III) on MEK/ERK and AKT signaling in Hazaribagh-dependent pollution with Cr and Hazaribagh-
HaCaT keratinocytes. Results of immunoblot analysis in HaCaT keratinocytes with nil
independent pollution with As and Ba in Buriganga River. Since
control (lane 1; Ctrl), sole exposure to 0.001 mM Cr(VI) (lane 2) and 10 mM of Cr(III)
(lane 3) and co-exposure to 0.001 mM of Cr(VI) and 10 mM of Cr(III) (lane 4) are pre- the level of Cr is > 2000-fold and >200-fold higher than the levels
sented. Photographs show levels of phosphorylation of MEK (pMEK), ERK (pERK) and of As and Ba, respectively, in canal water at Hazaribagh, we focused
AKT (pAKT) and expression of MEK (MEK), ERK (ERK), AKT (AKT) and TUBLIN (TUBLIN). on Cr pollution. There has been no study showing the biological
effects of coexposure to Cr(VI) and Cr(III). Therefore, the biological
effects of coexposure to the range of molar ratios of Cr(VI) and
After confirming that 0.3 mM Cr(VI) (Fig. 2A) and 30 mM Cr(III) Cr(III) in canal water at Hazaribagh were examined using human
(Fig. 2B) had no effect on the survival of HaCaT keratinocytes in our non-tumorigenic skin keratinocytes. Our colony formation assay
cell survival assay for 7 days, colony formation assays of 0.1 mM demonstrated for the first time that coexposure to Cr(VI) and Cr(III)
Cr(VI) (Fig. 3A) and 10 mM Cr(III) (Fig. 3B) were performed. Levels synergistically promoted transforming activity of HaCaT keratino-
of anchorage-independent growth were 2.3-fold and 2.2-fold cytes. MEK/ERK and AKT, which regulate transforming activity
increased by sole exposure to 0.03 mM and 0.1 mM Cr(VI), respec- (Thang et al., 2015a; Yajima et al., 2015), were synergistically acti-
tively (Fig. 3A). On the other hand, levels of anchorage-independent vated by coexposure to Cr(VI) and Cr(III). Synergistic promotion of
growth of cells solely exposed to 0.1 mM, 1 mM and 10 mM Cr(III) transforming activity by coexposure to 0.001 mM Cr(VI) and 1 mM
were comparable with that of the nil control. Cr(III), which are in the range of ratios in the water of Dhaka City,
was also shown in our colony formation assay using human non-
3.3. Effects of coexposure to Cr(VI) and Cr(III) on anchorage- tumorigenic lung epithelial Beas-2B cells (see Supplementary
independent growth Fig. S1 online). Our results using plural human cells provided
more solid evidence of the synergistic promotion of transforming
Our results of environmental monitoring in Dhaka City indi- activity by coexposure to Cr(VI) and Cr(III). Our results also partially
cated that the skin of residents was possibly exposed to molar ratios revealed the molecular mechanism of the synergistic promotion.
of Cr(VI):Cr(III) ranging from 1:29 to 1:32782. Therefore, the effect Since our results showed a synergistic effect when low-toxicity
of coexposure to Cr(VI) and Cr(III) in that range of ratios on Cr(III) was present in conjunction with high-toxicity Cr(VI), both
anchorage-independent growth of HaCaT keratinocytes was Cr(VI) and Cr(III) must be effectively removed. Our analysis of
examined. Unexpectedly, levels of anchorage-independent growth environmental engineering by using Langmuir isotherms showed
were 2.5-fold and 2.3-fold increased by coexposure to 0.001 mM that our original MF-HT could maximally adsorb 9.0 mg/g Cr(VI)
Cr(VI) and 10 mM Cr(III) (Fig. 4A) and coexposure to 0.003 mM Cr(VI) and 1041 mg/g Cr(III) in theory. To our knowledge, the Cr(III)
and 1 mM Cr(III) (Fig. 4B), respectively, compared to that of the nil removal ability of MF-HT is greater than that of any other previ-
control. ously reported depuratives evaluated by the Langmuir isotherm
(see Supplementary Table S1 online). Since the cost of MF-HT was
3.4. Effects of coexposure to Cr(VI) and Cr(III) on MEK/ERK and AKT calculated to be 0.7 cents per kg from previous reports (Gillman,
signaling in HaCaT keratinocytes 2006; Kato et al., 2016), MF-HT, a depurative of low cost and high
efficacy, could be a strong tool for countermeasures for environ-
Phosphorylated levels of MEK/ERK in HaCaT keratinocytes mental pollution and health risks caused by wastewater from
coexposed to 0.001 mM Cr(VI) and 10 mM Cr(III) were higher than tanneries. Since Cr-polluted canal water at Hazaribagh could
those in cells solely exposed to 0.001 mM Cr(VI) and 10 mM Cr(III) actually be remediated by MF-HT, we propose that MF-HT be
M. Yoshinaga et al. / Chemosphere 201 (2018) 667e675 673

Fig. 6. Capability of MF-HT for chromium adsorption. (AeD) Equilibrium data (A, C) and Langmuir isotherms (B, D) for MF-HT-mediated adsorption of Cr(VI) (A, B) and Cr(III) (C,
D) are presented. Ce and qe are the concentration of chromium in solution at equilibrium and the amount of chromium absorbed by MF-HT at equilibrium, respectively. (E, F)
Chromium levels of each sample (E) and mean ± s.d. (n ¼ 10) (F) in canal water at Hazaribagh with (lane 2 in E and F) or without (lane 1 in E and F) treatment with 1% weight of MF-
HT for 1-min incubation. **Significantly different from the control (**p < 0.01) as analyzed by the Mann-Whitney U test (F).

installed at the sources of chromium pollution (tanneries, in this Cr(VI) is increased in the presence of Cr(III), suggesting the
case). We anticipate that MF-HT will be applied after the tanning importance of removal of Cr(III) in addition to Cr(VI) from water.
process in tanneries in the near future. Moreover, it was shown in Our study of environmental engineering finally showed that MF-
our previous studies that MF-HT could remove pentavalent and HT, a low-cost and high-efficacy depurative, can be used for
trivalent As, Ba, iron (Fe) and uranium (U) from well water in rural removal of both Cr(VI) and Cr(III). Thus, our comprehensive study
areas of Bangladesh, Vietnam and Afghanistan (Kato et al., 2016, has provided a realizable countermeasure for Cr pollution in canal
2013; Kumasaka et al., 2013). Thus, MF-HT can be used for removal and river water in Dhaka City, Bangladesh. More importantly, our
of toxic elements in various countries as well as rural and urban study suggests an efficient solution to address the worldwide
areas of Bangladesh. environmental Cr pollution caused by tannery wastes.

5. Conclusions

Our environmental monitoring showed 38 mg/L Cr(VI) and

88697 mg/L Cr(III) in water of Buriganga River and canals con- Conflicts of interest
taining wastewater from tanneries in Dhaka City, Bangladesh. Our
study of molecular biology then showed that the carcinogenicity of The authors declare that they have no conflict of interest.
674 M. Yoshinaga et al. / Chemosphere 201 (2018) 667e675

Acknowledgements using hydrotalcite. Sci. Total Environ. 366, 926e931. https://doi.org/10.1016/

Hara, N., Saito, H., Takahashi, K., Takeda, M., 2013. Lower urinary tract symptoms in
This study was supported in part by Grants-in-Aid for Scientific patients with Niigata Minamata disease: a case-control study 50 years after
Research (A) (15H01743 and 15H02588), (B) (17KT0033) and (C) methyl mercury pollution. Int. J. Urol. 20, 610e615. https://doi.org/10.1111/
(16K11177, 16K08440, 16K08343 and 17K09156), Grant-in-Aid for iju.12001.
IARC, (International Agency for Rsesarch on Cancer), 2016. Agents Classified by the
Challenging Exploratory Research (26670525), Grant-in-Aid for IARC Monographs, vols. 1e117 [WWW Document]. http://monographs.iarc.fr/
Scientific Research on Innovative Areas (16H01639 and 24108002) ENG/Classification/index.php.
and Grant-in-Aid for Research Activity Start-up (15H06274) from Kato, M., Azimi, M.D., Fayaz, S.H., Shah, M.D., Hoque, M.Z., Hamajima, N.,
Ohnuma, S., Ohtsuka, T., Maeda, M., Yoshinaga, M., 2016. Uranium in well
the Ministry of Education, Culture, Sports, Science and Technology, drinking water of Kabul, Afghanistan and its effective, low-cost depuration
the Mitsui & Co., Ltd. Environment Fund (R13-0014), Foundation using Mg-Fe based hydrotalcite-like compounds. Chemosphere 165, 27e32.
from Center for Advanced Medical and Clinical Research of Nagoya https://doi.org/10.1016/j.chemosphere.2016.08.124.
Kato, M., Kozue, T., Kawamoto, Y., Tsuzuki, T., Hossain, K., Tamakoshi, A.,
University Hospital, The Mitsubishi Foundation (27310), Ichihara Kunisada, T., Kambayashi, Y., Ogino, K., Suzuki, H., Takahashi, M., Nakashima, I.,
International Scholarship Foundation (196), KENKO-KAGAKU Zai- 2004. c-Kit-targeting immunotherapy for hereditary melanoma in a mouse
dan (Health Sciences Foundation), Aichi Health Promotion Foun- model. Canc. Res. 64, 801e806. https://doi.org/10.1158/0008-5472.CAN-03-
dation, AEON Environmental Foundation, Nagono Medical Kato, M., Kumasaka, M.Y., Ohnuma, S., Furuta, A., Kato, Y., Shekhar, H.U., Kojima, M.,
Foundation, Grant for Environmental Research Projects from the Koike, Y., Thang, N.D., Ohgami, N., Ly, T.B., Jia, X., Yetti, H., Naito, H., Ichihara, G.,
Sumitomo Foundation (163119) and The Salt Science Research Yajima, I., 2013. Comparison of barium and arsenic concentrations in well
drinking water and in human body samples and a novel remediation system for
these elements in well drinking water. PLoS One 8, e66681. https://doi.org/
Appendix A. Supplementary data Kumasaka, M.Y., Yamanoshita, O., Shimizu, S., Ohnuma, S., Furuta, A., Yajima, I.,
Nizam, S., Khalequzzaman, M., Shekhar, H.U., Nakajima, T., Kato, M., 2013.
Enhanced carcinogenicity by coexposure to arsenic and iron and a novel
Supplementary data related to this article can be found at remediation system for the elements in well drinking water. Arch. Toxicol. 87,
https://doi.org/10.1016/j.chemosphere.2018.03.026. 439e447. https://doi.org/10.1007/s00204-012-0964-6.
Li, X., Ohgami, N., Omata, Y., Yajima, I., Iida, M., Oshino, R., Ohnuma, S., Ahsan, N.,
Akhand, A.A., Kato, M., 2017. Oral exposure to arsenic causes hearing loss in
References young people aged 12e29 years and in young mice. Sci. Rep. 7, 6844. https://
Akhand, A.A., Kato, M., Suzuki, H., Liu, W., Du, J., Hamaguchi, M., Miyata, T., Maruzeni, S., Nishijo, M., Nakamura, K., Morikawa, Y., Sakurai, M., Nakashima, M.,
Kurokawa, K., Nakashima, I., 1999. Carbonyl compounds cross-link cellular Kido, T., Okamoto, R., Nogawa, K., Suwazono, Y., Nakagawa, H., 2014. Mortality
proteins and activate protein-tyrosine kinase p60c-Src. J. Cell. Biochem. 72, 1e7. and causes of deaths of inhabitants with renal dysfunction induced by cadmium
https://doi.org/10.1002/(SICI)1097-4644(19990101)72:1<1::AID- exposure of the polluted Jinzu River basin, Toyama, Japan; A 26-year follow-up.
JCB1>3.0.CO;2-Y. Environ. Health 13, 18. https://doi.org/10.1186/1476-069X-13-18.
Anawar, H.M., Safiullah, S., Yoshioka, T., 2000. Environmental exposure assessment Mishra, S., Bharagava, R.N., 2016. Toxic and genotoxic effects of hexavalent chro-
of chromium and other tannery pollutants at Hazaribagh area, Dhaka, mium in environment and its bioremediation strategies. J. Environ. Sci. Health
Bangladesh, and Health Risk. J. Environ. Chem. 10, 549e556. https://doi.org/ Part C 34, 1e32. https://doi.org/10.1080/10590501.2015.1096883.
10.5985/jec.10.549. Ohgami, N., Hori, S., Ohgami, K., Tamura, H., Tsuzuki, T., Ohnuma, S., Kato, M., 2012.
Azom, M.R., Mahmud, K., Yahya, S.M., Sontu, A., Himon, S.B., 2012. Environmental Exposure to low-dose barium by drinking water causes hearing loss in mice.
impact assessment of tanneries: a case study of Hazaribag in Bangladesh. Int. J. Neurotoxicology 33, 1276e1283. https://doi.org/10.1016/j.neuro.2012.07.008.
Environ. Sustain Dev. 3, 152e156. https://doi.org/10.7763/IJESD.2012.V3.206. Ohgami, N., Mitsumatsu, Y., Ahsan, N., Akhand, A.A., Li, X., Iida, M., Yajima, I.,
Belay, A.A., 2010. Impacts of chromium from tannery effluent and evaluation of Naito, M., Wakai, K., Ohnuma, S., Kato, M., 2016. Epidemiological analysis of the
alternative treatment options. J. Environ. Protect. 1, 53e58. https://doi.org/ association between hearing and barium in humans. J. Expo. Sci. Environ.
10.4236/jep.2010.11007. Epidemiol. 26, 488e493. https://doi.org/10.1038/jes.2015.62.
Bharagava, R.N., Mishra, S., 2018. Hexavalent chromium reduction potential of Perry, H.M., Kopp, S.J., Perry, E.F., Erlanger, M.W., 1989. Hypertension and associated
Cellulosimicrobium sp. isolated from common effluent treatment plant of tan- cardiovascular abnormalities induced by chronic barium feeding. J. Toxicol.
nery industries. Ecotoxicol. Environ. Saf. 147, 102e109. https://doi.org/10.1016/ Environ. Health 28, 373e388. https://doi.org/10.1080/15287398909531356.
j.ecoenv.2017.08.040. Putila, J.J., Guo, N.L., 2011. Association of arsenic exposure with lung cancer inci-
Biedermann, K.A., Landolph, J.R., 1990. Role of valence state and solubility of dence rates in the United States. PLoS One 6, e25886. https://doi.org/10.1371/
chromium compounds on induction of cytotoxicity, mutagenesis, and journal.pone.0025886.
anchorage independence in diploid human fibroblasts. Canc. Res. 50, Rahman, M.A., Al Bakri, D., 2010. A study on selected water quality parameters
7835e7842. along the River Buriganga, Bangladesh. Iran. J. Energy Environ. 1, 81e92.
Boukamp, P., Petrussevska, R.T., Breitkreutz, D., Hornung, J., Markham, A., Sampson, M.L., Bostick, B., Chiew, H., Hagan, J.M., Shantz, A., 2008. Arsenicosis in
Fusenig, N.E., 1988. Normal keratinization in a spontaneously immortalized Cambodia: case studies and policy response. Appl. Geochem. 23, 2976e2985.
aneuploid human keratinocyte cell line. J. Cell Biol. 106, 761e771. https:// https://doi.org/10.1016/j.apgeochem.2008.06.022.
doi.org/10.1083/jcb.106.3.761. Saxena, G., Chandra, R., Bharagava, R.N., 2016. Environmental pollution, toxicity
Calay, D., Vind-Kezunovic, D., Frankart, A., Lambert, S., Poumay, Y., Gniadecki, R., profile and treatment approaches for tannery wastewater and its chemical
2010. Inhibition of Akt signaling by exclusion from lipid rafts in normal and pollutants. In: de Voogt, P. (Ed.), Reviews of Environmental Contamination and
transformed epidermal keratinocytes. J. Invest. Dermatol. 130, 1136e1145. Toxicology, vol. 240. Springer, Cham, pp. 31e69. https://doi.org/10.1007/398_
https://doi.org/10.1038/jid.2009.415. 2015_5009.
Chen, Y.-C., Su, H.-J.J., Guo, Y.-L.L., Hsueh, Y.-M., Smith, T.J., Ryan, L.M., Lee, M.-S., Thang, N.D., Yajima, I., Kumasaka, M.Y., Iida, M., Suzuki, T., Kato, M., 2015a. Deltex-3-
Christiani, D.C., 2003. Arsenic methylation and bladder cancer risk in Taiwan. like (DTX3L) stimulates metastasis of melanoma through FAK/PI3K/AKT but not
Canc. Causes Contr. 14, 303e310. https://doi.org/10.1023/A:1023905900171. MEK/ERK pathway. Oncotarget 6, 14290e14299. https://doi.org/10.18632/
Dietz, D.D., Elwell, M.R., Davis Jr., W.E., Meirhenry, E.F., 1992. Subchronic toxicity of oncotarget.3742.
barium Chloride dihydrate administered to rats and mice in the drinking water. Thang, N.D., Yajima, I., Kumasaka, M.Y., Ohnuma, S., Yanagishita, T., Hayashi, R.,
Fund. Appl. Toxicol. 19, 527e537. https://doi.org/10.1016/0272-0590(92)90091- Shekhar, H.U., Watanabe, D., Kato, M., 2011. Barium promotes anchorage-
U. independent growth and invasion of human HaCaT keratinocytes via activa-
Drobna , Z., Del Razo, L.M., García-Vargas, G.G., S anchez-Pen~ a, L.C., Barrera- tion of c-SRC kinase. PLoS One 6, e25636. https://doi.org/10.1371/
Herna ndez, A., Stýblo, M., Loomis, D., 2013. Environmental exposure to arsenic, journal.pone.0025636.
AS3MT polymorphism and prevalence of diabetes in Mexico. J. Expo. Sci. En- Thang, N.D., Yajima, I., Ohnuma, S., Ohgami, N., Kumasaka, M.Y., Ichihara, G.,
viron. Epidemiol. 23, 151e155. https://doi.org/10.1038/jes.2012.103. Kato, M., 2015b. Enhanced constitutive invasion activity in human non-
Fan, W.-T., Zhao, X.-N., Cheng, J., Liu, Y.-H., Liu, J.-Z., 2015. Oxidative stress and tumorigenic keratinocytes exposed to a low level of barium for a long time.
hepatocellular injury induced by oral administration of Cr3þ in chicken. Environ. Toxicol. 30, 161e167. https://doi.org/10.1002/tox.21881.
J. Biochem. Mol. Toxicol. 29, 280e287. https://doi.org/10.1002/jbt.21697. Tinni, S.H., Islam, M.A., Fatima, K., Ali, M.A., 2014. Impact of tanneries waste disposal
Farenzena, M., Ferreira, L.D.S., Trierweiler, J.O., De Aquim, P.M., 2005. Tanneries: on environment in some selected areas of Dhaka City Corporation. J. Environ.
from waste to sustainability. Braz. Arch. Biol. Technol. 48, 281e289. https:// Sci. Nat. Resour. 7, 149e156. https://doi.org/10.3329/jesnr.v7i1.22164.
doi.org/10.1590/S1516-89132005000400035. UNICEF, (The United Nations Children’s Fund), 2010. Living in the Urban Jungle
Field, R.W., Withers, B.L., 2012. Occupational and environmental causes of lung [WWW Document]. https://www.unicef.org/bangladesh/Living_in_the_urban_
cancer. Clin. Chest Med. 33, 681e703. https://doi.org/10.1016/j.ccm.2012.07.001. jungle.pdf.
Gillman, G.P., 2006. A simple technology for arsenic removal from drinking water Wang, M., Xu, Y., Pan, S., Zhang, J., Zhong, A., Song, H., Ling, W., 2011. Long-term
M. Yoshinaga et al. / Chemosphere 201 (2018) 667e675 675

heavy metal pollution and mortality in a Chinese population: an ecologic study. Yajima, I., Kumasaka, M.Y., Iida, M., Oshino, R., Tanihata, H., Al Hossain, A.,
Biol. Trace Elem. Res. 142, 362e379. https://doi.org/10.1007/s12011-010-8802- Ohgami, N., Kato, M., 2017. Arsenic-mediated hyperpigmentation in skin via NF-
2. kappa B/endothelin-1 signaling in an originally developed hairless mouse
Watch, H.R., 2012. Toxic Tanneries: the Health Repercussions of Bangladesh's model. Arch. Toxicol. 91, 3507e3516. https://doi.org/10.1007/s00204-017-1975-
Hazaribagh Lether [WWW Document]. https://www.hrw.org/sites/default/files/ 0.
reports/bangladesh1012webwcover.pdf. Yajima, I., Kumasaka, M.Y., Ohnuma, S., Ohgami, N., Naito, H., Shekhar, H.U.,
WHO, (World Health Organization), 2017. Guidelines for Drinking-water Quality, Omata, Y., Kato, M., 2015. Arsenite-mediated promotion of anchorage-
fourth ed. incorporating the first addendum. [WWW Document]. http://apps. independent growth of HaCaT cells through placental growth factor. J. Invest.
who.int/iris/bitstream/10665/254637/1/9789241549950-eng.pdf. Dermatol. 135, 1147e1156. https://doi.org/10.1038/jid.2014.514.
Yajima, I., Ahsan, N., Akhand, A.A., Al Hossain, M.A., Yoshinaga, M., Ohgami, N., Yajima, I., Uemura, N., Nizam, S., Khalequzzaman, M., Thang, N.D., Kumasaka, M.Y.,
Iida, M., Oshino, R., Naito, M., Wakai, K., Kato, M., 2018. Arsenic levels in cuta- Akhand, A.A., Shekhar, H.U., Nakajima, T., Kato, M., 2012. Barium inhibits
neous appendicular organs are correlated with digitally evaluated hyperpig- arsenic-mediated apoptotic cell death in human squamous cell carcinoma cells.
mented skin of the forehead but not the sole in Bangladesh residents. J. Expo. Arch. Toxicol. 86, 961e973. https://doi.org/10.1007/s00204-012-0848-9.
Sci. Environ. Epidemiol. 28, 64e68. https://doi.org/10.1038/jes.2016.70.