Lessons Learned from Xuanwei, China: A Case Study in Indoor Air Pollution and Lung Cancer

Outline

About half of the world’s population, approximately 3 billion people, almost all living in developing countries such as China, are exposed daily to high levels of domestic fuel combustion products.[1] Indeed, indoor air pollution from solid fuel use is estimated to be the eighth largest risk factor for global disease (expressed as disability-adjusted life years lost, or DALYs) and is a major public health problem in developing countries.[2,3]

Coal is used extensively in China for heating and cooking and is being increasingly utilized to generate electricity in many countries, including the United States. The excess in lung cancer and widespread use of coal for heating and cooking, often without ventilation, in Xuanwei, China has provided a unique opportunity to study the association of lung cancer with exposure to in-home coal smoke. For the past 25 years, ecological, toxicological, and epidemiological studies in Xuanwei have researched the human health risks of domestic coal combustion, and the health benefits of reducing coal smoke exposure. In 2006 the International Agency for Research on Cancer (IARC) convened a Working Group for preparation of IARC Monograph Volume 95, Carcinogenicity of household solid fuel combustion and of high-temperature frying. The Xuanwei studies formed an important basis of the Working Group’s conclusion that indoor emissions from household combustion of coal are carcinogenic to humans (Group 1). [4]

1. A Unique Scientific Opportunity

Xuanwei is a coal-rich semi-mountainous county on a high plateau in northeastern Yunnan Province, China. Xuanwei covers an area of 6257 square kilometers and consists predominantly of Han Chinese. Ninety percent of its residents are farmers with minimal industrial and automotive air pollution exposure. [5]

Homes in Xuanwei are primarily two-story mud-brick or wooden houses. Cinder-block houses are also quite common. The ground floor typically has a sitting room and a cooking area with a coal stove. The bedrooms are located to the rear of the house, along with shelter for animals.

In Xuanwei, nearly all women and few men cook, while most men and nearly no women smoke tobacco.[6] Women spend many hours in the home each day attending to cooking and caring for children and elderly relatives. On average, women spend about 7 hours per day near the household stove, according to a survey of 64 Xuanwei residents.[7] The survey also concluded that men spent on average 9.6 hours per day working outdoors.

There are three different types of fuels for domestic cooking and heating in Xuanwei: “smoky coal” (bituminous), “smokeless coal” (anthracite), and wood. The majority of residents of Xuanwei burn
smoky coal for cooking and heating in unvented homes. Xuanwei smoky coal has relatively low sulfur content, and, as its name implies, smokes heavily on combustion. Smokeless coal, on the other hand, has high sulfur and ash content and does not produce significant smoke levels. Traditionally, fuel burning for cooking and heating takes place in a simple, unvented firepit in the floor of the family room. Such burning exposes Xuanwei residents to exceptionally high levels of indoor air pollution from conception through adulthood.[5] This exposure, coupled with low automotive and industrial air pollution exposures, provides a unique opportunity to study risks of lung cancer and other diseases of indoor air pollution from household coal burning.

Figure 18.1 County-Specific Female Lung Cancer Mortality Rates (per 100,000) in China, 1973-1975

2. Ecological and Toxicological Studies

Ecological studies in Xuanwei have documented very high lung cancer rates. As shown in Figures 1 and 2 and in Table 1, 1973-75 annualized age-adjusted lung cancer mortality rates in Xuanwei were 27.7 per 100,000 in men (among China’ s highest) and 25.3 per 100,000 in women (China’s highest).[6] The similarity of rates in men and women is of considerable interest, because almost all women are non-smokers. [5;8;9] Further, the population-attributable risk proportion of coal burning for lung cancer in Xuanwei is over 90 percent.[10]

Early ecological and toxicological studies in Xuanwei suggested that risk of lung cancer attributed to coal exposure
might be driven by exposures to polycyclic aromatic hydrocarbons (PAHs). Exposure assessments of the indoor air pollution generated from the burning of smoky coal in firepits found elevated levels of airborne particulate matter (sometimes exceeding 20 mg/m³), benzo[a]pyrene (BaP), benz[a]anthracene (BA), 5-methylchrysene (SMC), indeno[1,2,3-c,d]pyrene (IDP), benzofluranthene (BFT), dibenzo[a,e]pyrene (DBP), and other organic compounds. [5;11] BaP, a strong indicator of the presence of PAHs, was observed to be as high as levels found among coke oven workers, in the mg/m³ range. [5] An ecological study of eleven Xuanwei communes from 1973-1979 found a close relationship between in-home BaP concentration and lung cancer mortality (Table 2). [12] In-home BaP concentration was positively and statistically significantly correlated with lung cancer mortality (p < 0.01).

Figure 18.2 County-specific female lung cancer mortality rates (per 100,000) in Yunnan Province, 1973-75 (note: Xuanwei County in red, Fu Yuan County is adjacent in orange).

Table 18.1 Annual Lung Cancer Mortality Rates in China and the United States. [9]

Place	Time Period	Lung Cancer Mortality Rate, per 100,000
		Unadjusted		Age-Adjusted to 1964 China Population		Age-Adjusted to 1970 US Population
		Males	Females	Males	Females	Males	Females
China	1973-1975	5.0^*		6.80	3.2	12.3	5.7
US	1970	53.7	12.0	30.0	6.3	53.7	12.0
Yunnan Province	1973-1975	2.8^*		4.3	1.5	6.9	2.5
Xuanwei County	1973-1979	27.0	24.5	27.7	25.3	43.2	38.7
communes of highest lung cancer mortality	1973-1979	114.4	120.6	118.0	125.6	186.8	193.4
55-59 yr age group in high-mortality communes	1973-1979	849.4	904.0
communes of low lung cancer mortality	1973-1979	4.0	2.8	4.3	3.1	5.8	4.3
55-59 yr age group in low-mortality communes	1973-1979	17.1	18.1
^*Unadjusted rate for both sexes combined

Beyond the initial ecological studies, analyses of biological samples also supported the hypothesis that lung cancer attributed to coal exposure might be driven by PAH exposure. For example, mutations in the p53 gene in tumor samples from nonsmoking women in Xuanwei were consistent with those of PAHs and different from those of lung cancer tumors from smokers.[14] Also, exposure to smoky coal was associated with increased levels of PAHs bound directly to human DNA, or PAH-DNA adducts, in placentas and umbilical cord white blood cells.[15]

Table 18.2 Percentage of households burning fuel before 1958, BaP concentration in indoor air, and 1973-79 age-adjusted lung cancer mortality rates, Xuanwei communes. [13]

Commune	Smoky coal (%)	Wood (%)	Smokeless Coal (%)	BaP (ug/100m³)	Mortality (1/100,000)
Chengguan	100.0	0.0	0.0	108.56	174.21
Laibin	89.7	8.7	1.6	67.97	128.31
Rongcheng	81.9	18.1	0.0	248.50	104.09
Longtan	78.0	22.0	0.0	55.98	22.96
Longchang	76.1	17.9	6.0	107.99	39.46
Banqiao	34.0	16.4	49.6	39.95	19.03
Baoshan	87.1	12.9	0.0	46.37	9.18
Haidai	49.7	22.5	27.8	53.94	13.48
Puli	35.2	52.0	12.8	28.62	7.49
Luoshui	2.7	39.0	58.3	43.76	9.55
Reshui	0.0	66.6	33.4	35.60	2.08

In 1985, the first case-control study was undertaken to characterize the effect of in-home coal use and smoking on lung cancer in Xuanwei. [16;17] The questionnaire collected information on smoking history, family and personal medical history, domestic fuel use history, cooking history, and demographic characteristics. As expected, the results suggested that smoking may play a role in lung cancer among males (Table 3). [18] However, the effect of smoking was an order of magnitude lower than that of smoky coal use, suggesting that the lung cancer etiology in Xuanwei is not primarily driven by tobacco smoking. In support of this hypothesis, cooking, but not passive smoking, appeared to be the major risk factor for lung cancer in females (Table 4). [19]

Table 18.3 Unadjusted odds ratios (OR) and 95% confidence intervals (CI) for lung cancer in males, Xuanwei, China. [20]

		Cases (n)	Controls (n)	OR (95%CI)	p-trend
Ever smoked
	No	4	19	1.00 (reference)
	Yes	52	205	1.20 (0.39-3.69)
Age started to smoke
	Never	4	19	1.00 (reference)
	≥20	20	80	1.19 (0.36-3.88)
	< 20	32	125	1.22 (0.39-3.82)	>0.05
Years of smoking
	None	4	19	1.00 (reference)
	< 35	30	146	0.98 (0.31-3.07)
	≥ 35	22	59	1.77 (0.55-5.73)	>0.05
Amount of smoking, kg/month
	None	4	19	1.00 (reference)
	< 1.2	45	190	1.12 (0.36-3.47)
	≥ 1.2	7	15	2.22 (0.55-8.86)	>0.05
Smoking index^*
	< 0.1	4	34	1.00 (reference)
	0.1 – 2.2	44	179	2.09 (0.72-6.07)
	> 2.2	8	11	6.18 (1.69-22.57)	<0.01
Often cooks food
	No	44	200	1.00 (reference)
	Yes	12	24	2.27 (0.98-5.24)
^*Smoking index = years of smoking x amount of smoking / age started to smoke