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Chinese “Herbal” Cigarettes are as Carcinogenic and Addictive as
Regular Cigarettes
Quan Gan, PhD1, Jie Yang, PhD MD MPH2, Gonghuan Yang, MD2, Maciej Goniewicz,
PhD1,3, Neal L. Benowitz, MD1,3,4, and Stanton A. Glantz, PhD1,4
1Center for Tobacco Control Research and Education, University of California, San Francisco
2China Center for Disease Control and Prevention, University of California, San Francisco
3Division of Clinical Pharmacology and Experimental Therapeutics, Departments of Medicine and
Biopharmaceutical Sciences, University of California, San Francisco
4Department of Medicine and Cardiovascular Research Institute, UCSF Helen Diller Family
Comprehensive Cancer Center, University of California, San Francisco
Abstract
Objective—To examine the Chinese tobacco industry's claim that herbal cigarettes are less harmful
than regular cigarettes.
Design—Cross-sectional study.
Participants—135 herbal cigarette smokers and 143 regular smokers from one city in China
completed a questionnaire on smoking behavior and provided a urine sample.
Main Outcome Measures—Cotinine and trans-3′-hydroxycotinine in all samples and polycyclic
aromatic hydrocarbon metabolites (PAHs) (1-hydroxypyrene, naphthols, hydroxyfluorenes and
hydroxyphnanthrenes) and the tobacco specific nitrosamine 4-(methylnitrosamino)-1-(3-pyridyl)-
butanol (NNAL) and NNAL-glucuronide in randomly selected 98 samples (47 from the herbal
smokers' group and 51 from the regular smokers' group). Values were normalized by creatinine to
correct for possible variability introduced by dilution or concentration of the urine.
Results—Health concern was among the main reasons that smokers switched to herbal cigarettes
from regular cigarettes. Smokers reported increased consumption after switching to herbal cigarettes
from regular cigarettes. For all the four markers analyzed (cotinine, trans-3′-hydroxycotinine, total
NNAL, total PAHs), we observed no significant difference in the levels (p=0.169, p=0.146, p=0.171,
p=0.554) between smokers of herbal cigarettes and smokers of regular cigarettes. Both total NNAL
and total PAHs were significantly correlated with cotinine and trans-3′-hydroxycotinine (p<0.001
for all four correlations).
Conclusions—Our findings showed that herbal cigarettes did not deliver less carcinogens than
regular cigarettes. The public needs to be aware of this fact and the Chinese tobacco industry should
avoid misleading the public when promoting herbal cigarettes as safer products.
Correspondence to: Stanton A. Glantz, PhD, 530 Parnassus Avenue, Suite 366, University of California, San Francisco, San Francisco,
CA 94143-1390, 415-476-3893, glantz@medicine.ucsf.edu.
Conflicts of Interest Statement: Dr. Benowitz has served as a paid expert witness in litigation against tobacco companies on issues
related to addiction and light cigarettes. The other authors have no conflict of interest.
NIH Public Access
Author Manuscript
Cancer Epidemiol Biomarkers Prev. Author manuscript; available in PMC 2010 December 1.
Published in final edited form as:
Cancer Epidemiol Biomarkers Prev. 2009 December ; 18(12): 3497–3501. doi:
10.1158/1055-9965.EPI-09-0620.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
Introduction
In Western countries, the term “herbal cigarettes” often refers to cigarettes that are made of a
mixture of different herbs and that contain no tobacco or nicotine. In China, the China National
Tobacco Corporation (CNTC) began in the late 1970s to develop tobacco cigarettes that also
contain Chinese medicinal herbs, which it also calls “herbal cigarettes” (1). In the manufacture
of these herbal cigarettes, extracts of Chinese medicinal herbs are mixed with or sprayed on
leaf tobacco (2) A host of Chinese herbs have been used as cigarette additives, from the
commonly known Ginseng to much less known ones such as Jiaogulan (2,3). Most of these
herbs are common ingredients in traditional Chinese medicine and are used for therapeutic
purposes or as dietary supplements. Since the first herbal cigarette brand in China, Changle,
was marketed by the Beijing Cigarette Factory (affiliated with the CNTC) in 1979 (2), many
herbal cigarette brands have been developed and marketed in China. In the 1990s herbal
cigarettes began to gain popularity in China. The two brands that have achieved the most sales
success in China were Jinsheng and Wuyeshen, which sold over 20 billion cigarettes in 2008,
accounting for more than 1% of all the cigarettes produced in China(4-6). (For comparison,
Lucky Strike had a 1.1% share of the US market in 1965(7), Virginia Slims had 2.6% in 2000
(8).) Most herbal brands in China, including Jinsheng and Wuyeshen, have the same machine-
determined yield of tar as regular cigarettes (15mg).
Although the market share of herbal cigarettes is still relatively small in China, herbal brands
are quickly expanding their market there and into the global market. Jinsheng's export markets
in 2008 included the Philippines, Singapore, Indonesia, Malaysia, Cambodia, Myanmar,
Canada and Taiwan (9). In 2003 Jinsheng was so successful in the Philippines that it accounted
for 90% of imported cigarettes in Manila (10). Zhongnanhai, the first herbal brand with a low
tar rating (at 1, 3, 5, 6, 8 mg) has achieved considerable success in Japan and can also be found
in the markets of the United States, Singapore, Malaysia, Taiwan, Hong Kong and Macao
(11).
Many claims of health benefits for smokers of herbal cigarettes were made by the Chinese
tobacco industry. For example, Jinsheng claims a host of benefits, including less coughing and
sputum, nourishment of the kidneys and the lungs, boosting of sexual drive (12). The health
claims Jinsheng made can also be conveniently found in a card inserted in some cigarette
packages (12). Wuyeshen claims over 60% reduction in cancer-causing nitrosamines, including
tobacco specific nitrosamines, and the inhibition of benzo(a)pyrene's carcinogenicity (13).
Several studies have attempted to evaluate the health benefits of smoking herbal cigarettes by
either measuring the yields of tobacco-specific nitrosamines in mainstream tobacco smoke
with smoking machine or cellular response to tobacco smoke in in vitro experiments (14-17).
No studies have directly measured the levels of carcinogens from herbal cigarettes in smokers'
bodies. The present study examines, for the first time, the level of metabolites of several key
tobacco constituents in herbal cigarette smokers' urine. In contrast to the claims made by the
Chinese tobacco companies that herbal cigarettes are safer than regular cigarettes, we find no
difference in the levels of nicotine or carcinogens in smokers' bodies between these two types
of cigarettes.
Methods
Sampling protocol
All subjects were smokers smoking cigarettes of Chinese brands living in one city in China.
180 herbal cigarette smokers and 180 regular cigarette smokers were recruited through three
district community centers. (Since all herbal brands are still very localized in China currently
and all of the herbal smokers in our study smoked the same brand that was produced locally,
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we chose not to disclose the name of brand to protect our local collaborators from the retaliation
by the local tobacco company.) Regular cigarette smokers smoked cigarettes with 14 or 15 mg
machine-measured tar yields per cigarette. Herbal cigarette smokers were smokers of a local
popular herbal brand with 15mg of machine-measured tar yield. Several inclusion criteria were
applied: (1) subjects had to be male smokers (because few women smoke in China); (2) subjects
had to be between the ages of 18 and 65, with no diagnosis of cancer, heart disease or major
respiratory diseases; (3) subjects had to smoke on average at least 5 cigarettes per day; and
(4) subjects had to have been smoking the current brand for at least three months; (5) when
brand-mixing was present, smokers had to smoke either regular or herbal brands at least 90%
of the time.
Each subject signed a consent form and completed a questionnaire. At the end of the
questionnaire, a 25 ml urine sample was collected.
The protocol was approved by the University of California San Francisco Committee on
Human Research and the China Center for Disease Control and Prevention Committee on
Human Subjects.
Laboratory analysis of tobacco smoke compounds in smokers' urine
The urine samples were frozen and shipped to San Francisco General Hospital for analysis in
the Tobacco Biomarker Core Facility of the UCSF Helen Diller Family Comprehensive Cancer
Center. Cotinine and trans-3′-hydroxycotinine, both metabolites of nicotine, 4-
(methylnitrosamino)-1-(3-pyridyl)-butanol (NNAL) and NNAL-glucuronide, metabolites of
NNK, a tobacco specific nitrosamine and one of the most potent carcinogens in tobacco smoke
(18), and metabolites of polycyclic aromatic hydrocarbons (PAHs), which represent a class of
combustion products that include a number of carcinogens, were measured. All analytes, were
measured using liquid chromatography by methods described previously: Cotinine and
trans-3′-hydroxycotinine (19),. NNAL and NNAL-glucuronide reported as total NNAL.(20),
metabolites of the PAHs including 1-hydroxypyrene, naphthols, hydroxyfluorenes and
hydroxyphenanthrenes and reported as total PAHs (21). Concentrations of cotinine, trans-3′-
hydroxycotinine, total PAHs and total NNALs were normalized by urine creatinine to correct
for variations due to dilution or concentration of urine. Per cigarette level of normalized total
PAHs, total NNAL, cotinine and trans-3′-hydroxycotinine were estimated by dividing the
concentrations by the number of cigarettes the subject reported smoking per day.
Every sample was analyzed for the levels of cotinine and trans-3′-hydroxycotinine (for a total
of 360 samples). A random sample of 60 samples from each group of smokers (for a total of
120 samples) was analyzed for PAHs and NNAL. Nine subjects were dropped because of
incomplete demographic information in the questionnaire. Three samples were excluded from
the results due to abnormally low levels of creatinine. Twenty-seven subjects who claimed to
smoke herbal cigarettes and 19 who claimed to smoker regular cigarettes were dropped from
the study because their urine samples indicated cotinine levels (< 50 μg/liter (22)) of a typical
non-smoker. Seven smokers of regular cigarettes were dropped from the study because the
main brand they smoked had a tar level of light cigarettes (< 14mg). In sum, the results reported
in this paper are based on 278 samples for cotinine and trans-3′-hydroxycotinine, 93 samples
for PAHs and NNAL.
Statistical Analysis
Survey questions were analyzed using chi-square. Levels of biomarkers were analyzed using
a Mann-Whitney rank sum test. Calculations were done with Stata 10.1.
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Results
Demographic information for the subjects is presented in Table 1. Herbal cigarette smokers
and regular cigarette smokers did not differ in age, number of cigarettes smoked per day,
educational level, employment status or income.
Urine levels of cotinine, trans-3′-hydroxycotinine total PAHs and total NNAL
Adjusted for creatinine, neither the levels of cotinine (p=0.169) nor trans-3′-hydroxycotinine
(p=0.146) were significantly different between herbal smokers and regular smokers (Table 1
and Figure 1). (Unadjusted cotinine and trans-3′-hydroxycotinine (ng/ml) were lower in herbal
cigarette smokers, p=0.047 and p=0.058, respectively.) The levels of total PAHs (p=0.554)
and total NNAL were not statistically different between the two groups (p=0.171) (Table 1 and
Figure 2). Results per cigarette showed the same patterns (details not shown). Both NNAL and
PAHs significantly correlated with cotinine (NNAL: rs=0.535, p<0.001; PAHs: rs=0.668,
p<0.001) and trans-3′-hydroxycotinine (NNAL: rs=0.539, p<0.001; PAHs: rs=0.674, p<0.001)
(scatter plots of cotinine vs NNAL and PAHs shown in Figure 3). Using a multiple regression
model (results not shown), the relationships did not depend on the type of cigarettes the subjects
smoked.
Cigarette switching
There was no significant difference in daily cigarette consumption between regular and herbal
smokers (Table 1). 106/135 (86%) of the herbal smokers had switched from regular cigarettes
a median of 6.25 years earlier (IQR: 4-10 years). Smokers reported increased numbers of
cigarettes smoked per day after switching to herbal cigarettes from regular cigarettes (Table
1). The most often cited reason for switching to herbal cigarettes was “better taste” compared
to regular cigarettes (47%). Health concern was the second most popular reason reported for
switching (24%) (Table 2). “Convenience of purchase” and “support for a local product and
business” accounted for 21% and 15% of the responses, respectively. There are two opposite
concerns about the price: some smokers switched because the current brand was more
affordable, while others switched because the current brand was more expensive and “good
for face” when offering cigarette to others, which is a common social etiquette in China.
Additionally, “no fake cigarettes” was reported by 4% of the respondents as the reason for
switching to herbal cigarettes.
Discussion
The present study is the first that examines the level of tobacco toxins in the bodies of smokers
of Chinese herbal cigarettes. We examined the major metabolites of nicotine and two groups
of tobacco carcinogens among smokers of herbal cigarettes. There was no detectable difference
in levels of nicotine or total NNAL, the metabolite of the main tobacco specific carcinogen
NNK, or PAHs between herbal cigarette smokers and regular cigarette smokers.
Smokers of herbal cigarettes had lower concentrations of unadjusted cotinine and trans-3′-
hydroxycotinine in the urine, but not after normalizing for creatinine. This result may suggest
slightly lower intake of nicotine from their cigarettes, or more concentrated urine among herbal
cigarette smokers. The reason for lower nicotine is unclear, as we did not measure the nicotine
content of the various types of cigarettes. The primary toxicity of nicotine is sustaining
addiction, and it is doubtful that very small differences in nicotine exposure, as were seen in
our study, would have any meaningful effect on the addiction potential of the cigarettes. In any
event, measures for tobacco smoke carcinogen biomarkers demonstrate no evidence
whatsoever of lower exposure in herbal cigarette smokers, suggesting no less cancer risk.
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While our results show that herbal cigarette smokers have similar levels of carcinogens in their
bodies as regular cigarette smokers, we could not test the industry claim that the herbal additives
inhibit the toxicity of these carcinogens. We could not locate any published studies that
examined or supported such claims.
We found significant correlations between total NNAL/total PAHs and the metabolites of
nicotine (cotinine and trans-3′-hydroxycotinine). The correlations persisted after stratifying for
the type of cigarette smoked. Our findings support previous research that NNAL and cotinine
are significantly correlated among smokers (23,24). This result suggests that cotinine and
trans-3′-hydroxycotinine in smokers' urine are indicative of the levels of total NNAL and total
PAHs in Chinese herbal and regular smokers due to smoking.
Herbal smokers who switched to herbal cigarettes from regular cigarettes reported increased
cigarette consumption after switching. Because of the cross-sectional design, the current study
was not able to examine the effect of this increased consumption on the nicotine and carcinogen
intake from tobacco smoke. It would be of interest for future studies, especially with short or
long-term switching experimental designs, to examine whether it was the health messages and/
or the herbal additives that triggered this increased consumption.
Many of the herbal constituents in herbal cigarettes present therapeutic benefits if used alone
(generally taken orally, rather than burned and smoked). When burned with processed tobacco
and inhaled, these herbal constituents are likely to undergo complex physical and chemical
changes. Of the three main herbal brands in China, Wuyeshen, Jinsheng and Zhongnanhai, we
did not find any literature evaluating the health benefits of Jinsheng and Zhongnanhai. Three
studies examined the safety claims of Wuyeshen (15-17). One study found reduction of tobacco-
specific nitrosamines in mainstream smoke compared to regular cigarettes (17). The other two
studies found lower toxicological effects from test animals smoking Wuyenshen and reduced
deaths in mouse embryonic cells and human endothelial cells in in vitro experiments (14-16).
None of these studies were conducted by independent researchers: one was by a researcher
from the tobacco company that manufactured Wuyeshen (17) and the others by researchers
with close ties with the tobacco industry (15,16). A full independent evaluation of the final
products, which is yet to be undertaken, would be necessary before any conclusion can be
reached to support claims of therapeutic effects of herbal cigarettes.
The marketing of herbal cigarettes as safer products by the Chinese tobacco industry, though
unfounded, has been effective; we found health concern to be the second most reported reason
for smokers to switch to herbal cigarettes (Table 2).
In 2001, Jinsheng and Zhongnanhai were among 36 most prestigious brands selected by CNTC
out of hundreds of brands in China (25). With a strong foothold in several provinces in China,
several herbal brands are being exported to Japan, Korea, countries in Southeast Asia and North
America (1,9,11). Because of the health benefits the marketing implies and the fact that smokers
in many of these countries are more health conscious, herbal cigarettes is, albeit slowly, gaining
popularity in these countries. Local regulatory agencies should be aware of the unsubstantiated
health claims and take measures to restrict the marketing of herbal cigarettes.
Acknowledgments
We express our deep appreciation to our local sampling collaborators in China, without whose help this project would
not have been possible. We are also grateful to Margaret Peng and Lisa Yu for performing the analytical chemistry,
and Drs Peyton Jacob III and Christopher Havel for supervised the laboratory analyses. This work was supported by
National Cancer Institute Training Grant CA-113710, the William Cahan Endowment and the UCSF Bland Lane
Center of Excellence on Secondhand Smoke funded by the Flight Attendants Medical Research Institute and the UCSF
Helen Diller Family Comprehensive Cancer Center, and the China CDC. The external funding agencies played no
role in the design of the project, collection and analysis of the data or preparation of the manuscript.
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Figure 1.
There is no significant difference in levels of cotinine and trans-3′-hydroxycotinine
(normalized by creatinine to account for differences in urine concentration) between herbal
smokers and regular smokers.
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Figure 2.
There is no significant difference in PAHs between herbal smokers and regular smokers.
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Figure 3.
There is no significant difference in NNAL between herbal smokers and regular smokers.
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Figure 4.
Scatterplots of cotinine vs total NNAL (rs=0.535, p<0.001) and total PAHs (rs=0.668, p<0.001)
show that higher levels of cotinine are associated with higher levels of carcinogens. (Crosses:
herbal smokers; dots: regular smokers.)
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Table 1
Demographic characteristics of the subjects.
Smokers of herbal cigarettes Smokers of regular cigarettesp-value
Sample size, N 135 143
Age (yrs), Median (IQR) 48 (38-56) 48 (39-54)p=0.567*
Cigarettes per day on average
Median (Interquartile range) 20 (15-20) 20 (15-20)p=0.962*
Education, N (%)
Junior high school and below 70 (52%) 77(54%)
Secondary technical school 41 (30%) 42 (29%)
Junior college 20 (15%) 18 (12%)
College and above 4 (3%) 6 (4%)p=0.621†
Employment status, N (%)
Employed 81 (60%) 94 (66%)
Unemployed 54 (40%) 49 (34%)p=0.979†
Monthly income, N(%)
<500 yuan 19 (14%) 30 (21%)
500-999 yuan 40 (30%) 41 (29%)
1000-1999 yuan 58 (43%) 52 (36%)
2000-4999 yuan 17 (12%) 18 (12%)
>=5000 yuan 1 (1%) 2 (1%)p=0.567†
Change in daily consumption after switching from regular cigarettes (14-15mg) to herbal cigarettes
Increased daily consumption 47% -
Decreased daily consumption 30% -
No change in daily consumption 23% -
Cotinine and trans-3′-hydroxycotinine (Median and Interquartile range)
Sample size 134 142
Cotinine (μg/mg creatinine) 12.8 (5.57-22.2) 14.3 (8.00-23.7)p=0.169*
Cotinine (ng/ml) 1142 (476-2175) 1538 (666-2463)p=0.047*
trans-3′-hydroxycotinine (μg/mg creatinine) 33.0 (9.88-61.4) 41.1 (15.6-65.7)p=0.146*
trans-3′-hydroxycotinine (ng/ml) 2799 (732-6346) 3732 (1518-7230)P=0.058*
Total PAHs and total NNAL (Median and Interquartile range)
Sample size 44 49
Total PAHs (pmol/mg creatinine) 172 (87.1-245) 159 (126-225)p=0.554*
Total NNAL (pmol/mg creatinine) 0.454 (0.256-0.862) 0.410 (0.291-0.649)p=0.171*
*Based on Mann-Whitney signed rank test;
†Based on chi-square test.
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Table 2
Reasons for herbal cigarette smokers to switch from regular cigarettes (14-15mg tar) to current herbal brands.*
Ranking of reasons Specific reasons Response (%)
1 Better taste 50 (47%)
2 Health concerns 26 (24%)
3 Convenience of purchase 22 (21%)
4 Support for local product & business 15 (15%)
5 Price 10(9%)
6 No fake cigarettes of current brand 4 (4%)
*106 out of 135 subjects who smoked herbal cigarettes answered this multiple-choice question. Percentages do not add to 100% because respondents were
allowed to report more than one reason.
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