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Bull Environ Contam Toxicol (2013) 90:742–749

DOI 10.1007/s00128-013-0998-3

Outline of Occupational Chromium Poisoning in China


Yuan Yang • Hong Liu • Xian-hong Xiang •

Fu-you Liu

Received: 3 September 2012 / Accepted: 12 April 2013 / Published online: 20 April 2013
Ó Springer Science+Business Media New York 2013

Abstract The present study analyzed the feature of Keywords Occupational chromium poisoning 
occupational chromium poisoning in China since the Epidemiological characteristics  China
1980s. The collected data were acquired from 18 previous
surveys of chromium poisoning in 14 cities of China. The
method of risk assessment was applied to calculate the The heavy metal chromium (Cr) exists widely in the
relative risk and 95 % CI, p \ 0.05 was considered as a environment in the hexavalent form (chromate) and can be
significant risk. The results showed that nasal disease was refined through the process of industrial melting. Hexava-
the most common sign of occupational chromium poison- lent chromium [Cr (VI)] is frequently used in making
ing, and the prevalence rate of nasal disease was 17.83 % stainless steel, leather tanning, pigment production, elec-
in total population of 6,998. Further, the risk analysis troplating and in other applications. Therefore, in the pro-
showed that occupational chromium poisoning led to an cess of Cr (VI) production or use, workers can suffer from
increased risk of lung or liver cancer in male workers due extensive damage to the respiratory system, digestive
to the definite carcinogenicity of hexavalent chromium. system and skin as result of constant exposure to chromium
Significantly, an increased risk of spontaneous or threa- through the respiratory tract, alimentary canal and skin.
tened abortion was also found in female workers. In con- The presence of these conditions can indicate the occur-
clusion, these studies suggest that early detection of rence of occupational chromium poisoning (OCP). At
impaired reproductive function or impaired lung or liver present, nasal disease, dermatitis, hepatomegaly, damage to
function in female or male workers is essential for con- reproductive functions and cancers of the lung, liver or
trolling occupational chromium poisoning in China. breast are considered as common clinical features of OCP
(Cohen et al. 1993; IARC 1990; Costa 1997).
Occupational chromium poisoning is widespread in
industrialized countries worldwide. Therefore, some epi-
demiological studies of the association between lung or
gastrointestinal tract cancers and OCP were conducted in
Y. Yang  H. Liu  F. Liu (&)
the United States (Gatto et al. 2010; Pastides et al. 1994;
Post-doctoral Research Stations, Nephrology Institute,
The Second Xiangya Hospital, Central South University, Sheffet et al. 1982). For China, the OCP is really no single
Changsha Hunan 410011, China case report in many cities. Many epidemiological studies
e-mail: fuyoul213@163.com; LFY410@yahoo.com.cn had revealed that OCP was prevalent to varying degrees in
Cr (VI)-exposed workers in many big cities since the
Y. Yang
Department of Clinical Laboratory, Huaihua Medical College, 1980s. Despite this, there has never been a comprehensive
Huaihua Hunan 418000, China and systematic analysis of all the epidemiological studies
of OCP in China in the last three decades. Therefore, the
X. Xiang
present study synthesized the survey results of OCP from
Department of interventional Radiology, The First Affiliated
Hospital, Sun Yat-sen University, Guangzhou GuangDong 510080, the last 30 years and analyzed the epidemiological features
China of nasal disease, dermatitis, hepatomegaly, reproductive

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Bull Environ Contam Toxicol (2013) 90:742–749 743

function damage and cancer of the lung or liver associated Results


with occupational chromium exposure.
Distribution of Occupational Chromium Poisoning
in Large Chinese Cities
Materials and Methods
There are about forty big cities in China. As shown in
The data were acquired from 18 previous epidemiological Fig. 1, OCP in China is mostly concentrated in fourteen
studies of occupational chromium poisoning in 14 cities in cities: Tianjin, Taiyuan, Jinzhou, Jinan, Qingdao,
China, which was retrieved openly and available online. Zhengzhou, Chongqing, Changsha, Shenzhen, Nanjing,
The study was permissive for using the data from all authors Suzhou, Wuxi, Changzhou and Shanghai. Based on the
of these surveys. The areas of survey consisted of 14 cities studies we have used, OCP is most concentrated in five
of more than one million people, or 6 provinces and 3 coastal cities of Shanghai and Jiangsu provinces. In central
municipalities. The studies were conducted between 1983 China, OCP is found in Zhengzhou, Changsha and Taiyuan,
and 2010 involved in 18 retrospective surveys of occupa- and Chongqing is a representative city with high OCP
tional chromium poisoning in China. The linked web sites prevalence located in the western inland area.
for 18 surveys were shown as Table 1. In these epidemio-
logical studies, workers with Cr (VI) exposure in production Rank of Occupational Chromium-Induced Diseases
workshops were considered as the exposed group, while Prevalence
coworkers with no Cr (VI) exposure were designated as
controls. For occupational chromium-induced nasal disease, As shown in Table 2, nasal disease was the most frequently
the diagnostic criteria of (GBZ12-2002) and clinical occurring disease associated with occupational chromium
examination were used to make medical diagnoses. Stan- exposure. In addition to nasal disease, occupational chro-
dard Mortality Ratio (SMR) analysis was performed mium exposure can also cause occurrences of dermatitis,
according to age-specific mortality references for Chinese hepatomegaly, reproductive system lesions and malignant
cities from 1975 to 1978 (Health ministry office of cancer tumors. In Fig. 2, these diseases are arranged by prevalence
prevention and control research in China 1987). For the rate from highest to lowest: nasal disease (17.83 %), der-
statistical analysis, the method of risk assessment was matitis (12.94 %), spontaneous abortion (11.10 %), threa-
applied to calculate the relative risk (RR) and 95 % CI tened abortion (6.33 %), hepatomegaly (5.70 %), and
(95 % CI), p \ 0.05 was considered as a significant risk. maliganant tumors (3.93 %).

Table 1 The linked web sites for 18 surveys of occupational chromium poisoning in China
No References The linked web sites

1 Wen-bin et al. (2010) http://www.cnki.com.cn/Article/CJFDTotal-ZYJK201014003.htm


2 Jun-qi et al. (2006) http://wuxizazhi.cnki.net/Search/ZYJK200621002.html
3 Wen-bin et al. (2004) http://www.cnki.com.cn/Article/CJFDTotal-ZYJK200412017.htm
4 Guo-jin (2004) http://www.cnki.com.cn/Article/CJFDTotal-SOLE200401026.htm
5 Mei-li and Shen-xi (2004) http://www.cnki.com.cn/Article/CJFDTotal-ZYJK200404016.htm
6 Yong-ling et al. (2001) http://www.cnki.com.cn/Article/CJFDTotal-ZYJK200102001.htm
7 Deng-jiu et al. (2001) http://mall.cnki.net/magazine/Article/LDBK200103015.htm
8 Chun-lian and Ling-ping (1994) http://www.cnki.com.cn/Article/CJFDTotal-GYWZ404.019.htm
9 Guang-zhi et al. (1992) http://www.cnki.com.cn/Article/CJFDTotal-XYYX199205008.htm
10 Jian-yu et al. (1991) http://lib.cqvip.com/qk/97285X/199101/657570.html
11 Zheng-ping (1988) http://www.cnki.com.cn/Article/CJFDTotal-XYYX198803004.htm
12 Shou-kang et al. (1988) http://www.cnki.com.cn/Article/CJFDTotal-XYYX198802004.htm
13 Hui-ren et al. (1987) http://www.cnki.com.cn/Article/CJFDTotal-LDYX198704018.htm
14 Zheng and Chun-ling (2003) http://www.cnki.com.cn/Article/CJFDTotal-SAFE200303010.htm
15 Rui-mei et al. (2003) http://www.cnki.com.cn/Article/CJFDTotal-GGWS200301054.htm
16 Qiong-yu et al. (1997) http://www.cnki.com.cn/Article/CJFDTotal-GYWZ199703026.htm
17 Shi-xiong and Mei-yuan (1994) http://wuxizazhi.cnki.net/Search/SOLE406.000.html
18 Shi-xiong et al. (1986) http://www.cnki.com.cn/Article/CJFDTotal-ZHLD198604007.htm

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Fig. 1 Geographic distribution


map of occupational Cr (VI)
exposure in China. Red and
green colors are indicative of
cities and regions in which
occupational Cr (VI) exposure
occurs (Color figure online)

Table 2 Prevalence rate of


OCAD Time Average age Examination number/ Occurred Prevalence
nasal disease, dermatitis,
(year) (A) times frequency ( %)
hepatomegaly, abortion and
malignant tumors Nasal disease 1983–2010 33.88 6,998 1,248 17.83
Dermatitis 1983–2010 32.7 3,716 481 12.94
Hepatomegaly 1983–2004 35.6 3,316 189 5.70
Spontaneous 1997–2002 34.0 216 24 11.10
abortion
Threatened 2002 32.5 158 10 6.33
OCAD occupational chromium abortion
exposure-associated diseases, Maliganant 1958–1989 m 2,545 100 3.93
m is indicative of missing data tumors
in literatures

Distribution of Nasal Disease Prevalence and Its


Association With Chromium Exposure

As shown in Table 3, between 1983 and 2010, 15 surveys


of nasal disease were performed in factories of ten cities.
There were 6,998 workers with occupational chromium
exposure in these studies between the ages of 17 and
59 years. The time of working ranged from 0.1 to 32 years.
The ratio of male to female workers ranged from 1.01 to
3.13. In this population, 1,248 cases of nasal disease were
diagnosed. Among these, there were 333 cases of nasal
septum ulcers or perforations, 26.68 % of the total. As
Fig. 2 Prevalence of diseases related to occupational chromium shown in Figs. 3a, b, the regional distribution of occupa-
poisoning in China tional chromium-associated nasal disease suggested the

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Table 3 Characteristics of occupational chromium-induced nasal disease in China


City Time n Average age (A) WY Ratio (M:F) Nasal disease ( %)
Erosion ulcer/hole Total

Changzhou 2010 248 29.0 8.0 3.13 6 6 12 (4.84)


Suzhou 2005 1,228 32.0 7.0 1.15 13 8 21 (1.7)
Changzhou 2004 357 32.5 10.2 1.11 113 22 135 (37.82)
Wuxi 2004 472 35.6 6.7 3.03 0 41 41 (8.69)
Tianjin 2004 121 34.0 [1.0 1.16 28 2 30 (24.8)
Changsha 2001 233 33.0 12.8 1.77 23 1 24 (10.33)
Jinan 2001 363 35.0 7.5 2.86 60 47 107 (29.48)
Taiyuan 1994 333 36.2 0.5–21 1.64 47 39 86 (25.8)
Shanghai 1992 656 35.8 0.2–12 1.01 143 70 213 (32.5)
Chongqing 1989 247 33.5 0.1–23 1.6 67 4 71 (28.74)
Chongqing 1988 251 34.5 0.1–22 2.22 118 4 122 (48.61)
Nanjing 1988 1,941 32.8 0.3–9.0 1.02 204 26 230 (11.85)
Shanghai 1987 151 33.3 0.8–12 1.40 0 25 25 (16.7)
Chongqing 1985 198 35.0 0.4–32 1.87 93 9 102 (51.5)
Wuxi 1983 199 36.0 0.8–10 1.42 0 29 29 (14.6)
Total 6,998 33.88 915 333 1,248 (17.83)
WY is represented as working years for chromium exposure; M male, F female

A (29.93 %) from 1989 to 1994. However, there was an


Suzhou 1.7
obvious decrease for the nasal disease prevalence (2.24 %)
Changsha 10.33
from 2005 to 2010. Furthermore, the result of correlation
Wuxi 10.43
analysis suggested a significant association between chro-
Changzhou 24.3 mium concentration in working place and nasal disease
Tianjin 24.8 prevalence, more details were shown in and Table 4.
Taiyuan 25.8
Jinan 29.48 Risk Analysis of Nasal Disease Due to Occupational
Shanghai 29.49 Chromium Exposure
Chongqing 42.39

0 5 10 15 20 25 30 35 40 45
As shown in Table 5 and Fig. 4, compared with polishing
Prevalence (%) workers, the incidence rate of nasal disease among elec-
troplaters increased obviously, and the risk of nasal disease
B 35
in electroplaters increased by 4.27 times compared to
29.93
30 polishing workers. In factory workshops where the con-
Prevalence (%)

25
21.8 centration of chromium exceeds hygienic standards, the
20 18.54 incidence of nasal disease increased obviously, and the risk
15 of nasal disease increased by 2.91 times compared to fac-
10 tory workshops where the concentration of chromium met
5 2.24
hygienic standards. However, the difference of incidence
0 rates and risk of nasal disease were not statistically sig-
1983-1988 1989-1994 1999-2004 2005-
nificant between groups working less than 10 years and
Temporal distribution of occupational
chromium-induced nasal disease those working longer.

Fig. 3 a Distribution of occupational chromium-induced nasal dis- Risk of Abortion Occurring in Female Workers
ease in cities of China. b Temporal distribution of occupational
chromium-induced nasal disease in China of Occupational Chromium Exposure

highest prevalence occurred in Chongqing (42.39 %), the As shown in Table 6 and Fig. 5, an increased risk of
lowest in Suzhou (1.7 %). The time distribution of nasal spontaneous abortion or threatened abortion was observed in
disease suggested that there was a higher prevalence female workers, compared to the control of non-occupational

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Table 4 Correlation between chromium exposure dose in working place and nasal disease
Data source Sample sizeb Overproof rates (%) Cr exposure (mg/m3)c Workers (n) Prevalence ( %) Correlation
coefficient

Changzhou (2010) 147 12.93 0.026 248 4.84 0.619*


Changzhou (2004) 111 19.82 0.156 357 37.82
Wuxi (2004) 116 16.28 0.154 472 31.99
Tianjin (2004) 121 100.00 0.296 121 24.88
Changsha (2001) 15 60.00 0.183 233 10.30
Jinan (2001) 141 78.70 0.287 363 29.48
Taiyuan (1994) 60 70.00 0.578 220 33.60
Chongqing (1991)a 64 98.44 3.090 696 45.69
Shanghai (1988) 72 18.10 0.074 151 16.75
a
Chongqing (1991) is represented as the result of Chongqing (1985, 1988, 1989), referred in Jian-yu et al. 1991
b
The collection place of air sample is limited in operation site of chromium exposure, which is not involved in workshop office, worker’s lobby,
employee’s dinning room
c
Cr exposure is represented as average chromium concentration in workshop, according to GBZ2.1-2007, the occupational exposure limits for
chromium is 0.05 mg/m3
* Pearson correlation test between average chromium concentration and nasal disease prevalence indicates the p value is 0.076, p \ 0.10

Table 5 Risk analysis of occupational chromium-induced nasal disease in China


Districts Groups Cases group Controls group AR (%) OR (95 % CI)

Nanjing Factory (?) 129 630 10.42 2.91* (2.11–3.99)


Factory (-) 63 894
Changsha, Taiyuan Working year 0- 54 289 2.07 0.86 (0.57–1.29)
Working year 10- 57 263
Taiyuan Electroplater 74 146 23.02 4.27* (2.20–8.26)
Polisher 12 101
Factory (?) is indicative of factory exceeding chromium standard; Factory (-) is indicative of factory meeting chromium standard; Exceeding
the standard indicates Cr2O3 concentration in the workshop exceeds the maximum allowable concentration of Hygienic Standards for the Design
of Industrial Enterprises (TJ36—79)- ([0.05 mg per cubic meter or [0.05 mg/m3)
* p \ 0.05, the value of OR was significant following analysis with the Chi squared test

9
6.00 %, respectively. So the risk of spontaneous abortion
8
OR value of nasal disease

or threatened abortion increased by 2.31 or 20.47 times,


7
respectively, compared to unexposed controls.
6
5
4.27 Risk Analysis of Malignant Tumors in Workers
4
2.91 Exposed to Chromium
3
2
1
1.00 1.00 As shown in Table 7 and Fig. 6, cancers of the lung or liver
0 in male workers were closely associated with occupational
electroplater polisher Factory(+) Factory(-) chromium exposure compared with unexposed controls.
Taiyuan Nanjing The risk of lung or liver cancer incidence in occupationally
exposed workers increased by 3.53 and 2.03 times,
Fig. 4 Risk analysis of occupational chromium-induced nasal dis-
ease. The upper limit of 95 % CI was labelled on the top of the respectively. Similarly, the death risk of cancer of the lung
diagram or liver also increased by 2.27 (average value of 1.97 and
2.57) and 1.29 times (average value of 1.28 and 1.30),
chromium exposure. For female workers with occupational respectively, compared to mortality of the general popu-
chromium exposure, the incidence rate of spontaneous lation. For breast cancer in female workers, the incidence
abortion or threatened abortion increased by 5.58 % or rate was slightly higher than those who were unexposed to

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Table 6 Risk analysis of abortion occurring in female workers exposed to chromium in China
Reproductive toxicity Groups Number of pregnancies Abortion Non-abortion AR (%) OR (95 % CI)

Spontaneous abortion Exposure 232 24 208 5.58 2.31* (1.25–4.27)


Non-exposure 420 20 400
Threatened abortion Exposure 158 10 148 6.00 20.47* (2.60–161.44)
Non-exposure 304 1 303
* p \ 0.05, the value of OR was significant following analysis with the Chi squared test

12 role in the regulation of blood glucose (Valko et al. 2006;


10.34 Singh et al. 1998a, b). While Cr (VI) exhibits strong oxi-
Incidence of abortion (%)

10
dation activity, and its toxicity is 100 times greater than
8 that of Cr (III) (Valko et al. 2005). Cr (VI) can readily enter
6.33
6 cells through the nonspecific anion channel of the cyto-
4.76 membrane. Activated redox reactions in cells can generate
4
a variety of reactive oxygen species (ROS), lead to oxi-
2 dative stress and form Cr-DNA adducts, and DNA–protein
0.33 or DNA-Cr-DNA crosslinks. Further, activation of DNA-
0
Exposure Non-exposure Exposure Non-exposure dependent protein kinases (DNA-PK) and the P53 gene
Spontaneous abortion Threatened abortion induces subsequent cell apoptosis (Hamilton et al. 1998;
Blankenship et al. 1994; Manning et al. 1994; Singh et al.
Fig. 5 Risk analysis of spontaneous or threatened abortion in female
workers
1998a, b). Apoptosis is an important factor influencing the
malignant transformation of cells, involving the activation
chromium, but the between-group difference was not sig- of specific oncogenes and consequent carcinogenesis. Due
nificant (p [ 0.05). to the occupational Cr (VI) exposure is an inevitable risk
Besides the above characteristics of chromate poisoning, factor in industries using Cr (VI), so some epidemiological
hepatomegaly can also be found in workers of chromate studies have shown that occupational Cr (VI) exposure
production workshops (referred in Zheng and Chun-ling leads to an increased risk of lung or breast cancer in the
2003; Deng-jiu et al. 2001). The survey disclosed that the United States, Britain and other countries, and some
incidence rate of hepatomegaly increased by 9.04 %, and research also found a close association between an
the incidence risk increased by 2.97 times compared to increased cancer risk and Cr (VI) exposure in drinking
other local workers without chromium exposure. water (Dayan and Paine 2001; Kilic et al. 2004; Goldbohm
et al. 2006; Scientific American 2009; Allan et al. 2009;
Beaumont et al. 2008).
Discussion For China, the present study collected 18 epidemiolog-
ical surveys studying occupational chromium poisoning
Chrome is a heavy metal element, the common forms of from 1983 to 2010 and analyzed them for incidence or
chemical valence are Cr (III) and Cr (VI). Cr (III) is an relative risk of occupational Cr (VI) nasal disease, chrome
essential trace element for humans, playing a significant dermatitis, hepatomegaly, abortion, and malignant tumor.

Table 7 Risk analyses of malignant tumors in occupational workers exposed to chromium


Sex Groups Cancer Cases Controls AR (%) OR (95 % CI) SMR

Male Exposure Lung cancer 31 1,810 1.2 3.53* (1.97–6.32) 1.971 2.572
Non-exposure 18 3,709
Exposure Liver cancer 17 1,824 0.47 2.03* (1.04–3.99) 1.283 1.304
Non-exposure 17 3,710
Female Exposure Breast cancer 4 700 0.43 4.19 (0.77–22.95) m
Non-exposure 2 1,468
* p \ 0.05, the value of OR was significant following analysis by the Chi square test; according to the results of surveys conducted from 1975 to
1978, age-specific mortality of lung or liver cancer in large1, 3 and medium-sized2, 4 cities was considered for each as the standard calculation of
standard mortality ratio-SMR (Health ministry office of cancer prevention and control research in China 1987); m is indicative of missing data in
literatures

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748 Bull Environ Contam Toxicol (2013) 90:742–749

7 examination of reproductive function in female workers or


6 functions of lung and liver in male workers is significant to
Risk of malignant tumors

improve the life quality of workers in occupational chro-


5
mium exposure. On the other hand, we can also take some
4 3.53 other measures, such as improving production processes,
3 reducing the chrome concentration in workshops,
2.27 2.03
2
strengthening personal protection and health education.
1.29 These measures would reduce the occurrence of occupa-
1
tional chromium poisoning as much as possible. With
0 economic development in China and improvement of liv-
OR SMR OR SMR
Lung cancer Liver cancer
ing standards, prevention and control of occupational
chromium poisoning is receiving more attention from
Fig. 6 Risk analyses of lung or liver cancer in workers exposed to government departments and the people.
chromium. The upper limit of 95 % CT was labelled on the top of the
diagram Acknowledgments This study was sponsored by the Postdoctoral
Science Foundation of Central South University, China (2013–2015).
We sincerely thanks for the contribution of authors in 18 surveys of
Our goals were to produce an overview of Chinese occupa- occupational chromium poisoning in China. YY performed the col-
tional chromium poisoning and help guide the future work on lection, clearance, analysis of epidemiological data and drafted the
prevention and control. The present study involved 14 big manuscript, and XXH proposed many valuable advices on the man-
uscript. LFY and LH checked and revised the manuscript. All authors
cities in China and investigated about 9,701 workers in 270 declare that they have no competing interests.
factories producing chromate salts, performing electroplat-
ing, or engaging in other uses of chromium. There were 7,096
workers without Cr (VI) exposure who were also studied and References
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