General health aspects of hookah smoking

Health effects of hookah smoking have been regularly reviewed, updated and summarised over the last decade [3, 27]. CO levels are generally high, as early established by Sajid et al in 1993 [28]. However, the diverse types of charcoal, tobacco-based mixtures, the size of the device and, above all, the degree of ventilation (indoors, outdoors), play an important role in variations [3, 28]. Expired mean CO levels in smokers may thus reach values as low as 14.2 ppm in Jordan [29] and as high as 38.5 ppm at the end of a session (with quick-lighting charcoal) in a Lebanese café where patrons smoked cigarettes and hookah [30]. Levels are even more elevated in some ill-ventilated hookah lounges in France [3]. A study by Al-Kubati et al. on heart rate in hookah smokers, cited in a recent Cochrane review, did not assume that carbon monoxide levels might, perhaps, also account for observed differences with cigarettes, rather than the nicotine itself only [31, 32]. Besides, only 5 grams of the smoking product was used for a whole 45 minute session when the common value retained in most reliable studies of the Middle East are 20 grams [29, 30]. In these hard experimental conditions, the smoking mixture may char rapidly with a consequent overproduction of CO, carbonaceous material and tar [33, 34]. A recent study involving machine smoking shows that hookah mainstream smoke CO concentration is up to 13 times inferior than in cigarettes: 1.79 mg for a 1000 ml hookah (machine) puff and 1.06 mg for a 45 ml cigarette puff [35]. Another area of public health concern in the context of the global epidemic of hookah smoking is ETS (Environmental Tobacco Smoke). There has been a serious debate over statistics about cigarette ETS and their interpretation [36]. However, and in striking contrast with cigarettes, hookah does generate almost no side-stream smoke because of its peculiarities (charcoal topping the bowl and less elevated temperatures). So, the only smoke that should be taken into account is the one rejected by the smoker, i.e. the one filtered by the hookah at the level of the bowl, inside the water, along the hose and then by the smoker's lungs themselves. Consequently, the resulting smoke is expected to be less toxic for non-smokers than cigarette side-stream smoke. Notably, a great proportion of irritants, mainly aldehydes and phenols, are removed [19]. A team led by Guillerm in France early found that when passed through water (50 cm3), the combustion gases of cigarette smoke have no inhibitory effect on the respiratory epithelium cilia. The researchers concluded that narghile users can, "without apparent disorders, smoke dramatically greater quantities of tobacco than ours in our countries" [37]. Wynder et al have established that water filtered cigarette smoke is less toxic to clam gill tissue and that "a flask containing 200 ml of water dramatically can reduce the dose of ciliatoxic agents delivered to the ciliated epithelium" [38]. Weiss also reported that the effect of bubbling tobacco smoke through 15 ml of water was "equivalent to the effect of the better charcoal filters" [39]. Zaga and Gattavecchia have shown that the water in the vase of a hookah acts as an antioxydant against some short half-life free radicals [40]. Other substances are supposed to be affected by the water obstacle because of their solubility or the low temperatures: e.g. HCN, nitric oxides, etc. As for particles in the mainstream smoke, and particularly ultra fine ones (0.02 to 1 μm), a recent study shows that hookah smoke is up to 3 times less concentrated than cigarette smoke: 74.4 109 for a 1000 ml hookah (machine) puff and 9.24 109 for a 45 ml cigarette "puff" [35]. Similarly to ETS, there is a serious debate on the so-called "nicotine addiction" as this alkaloid is not seen as the central substance involved in the dependence phenomenon [41, 42]. Also, it is not the most dangerous one. Hookah dependence is very specific and research on it will help reconsider the "nicotine addiction" hypothesis. Recently, a Lebanese team has found that more than 90% of so-called "mild smokers" (3 pipes or less per week) and about 50% of the so-called "moderate" ones (3 to 6 pipes per week) are considered as non dependent [43]. A certain confusion is also a direct result of the misuse of smoking machines [33, 34]. A team in Kuwait has established with a rigorous methodology that the nicotine intake is not as high as in cigarettes [44]. Some of the smokers in our study, particularly the "heavy" ones, were obviously dependent. Further research is needed in this field and it is certainly too early to suggest the use of Nicotine "Replacement" Therapies and products to "hookah addicts", bupropion [32] or even Varenicline produced by Pfizer laboratories and marketed as Chantix and Champix.

Specific aspects of hookah smoking in Pakistan

Tobacco smoking generally elevates CEA concentrations as reflected in the work by Fukuda et al [12], Alexander et al [11], Naghilbahossaini et al [16], summarised in Table 4. In our study, the subjects were divided into 3 groups according to the number of preparations; the number of sessions and the total daily smoking time: Light (1; 1; ≤ 20 minutes); Medium (1–3; 1–3; >20 min to ≤ 2 hrs) and Heavy smokers (2–4; 3–8; >2 hrs to ≤ 6 hrs). CEA mean level in light smokers (1.06 ± 0.492 ng/ml; n = 5) was significantly low when compared with values in non-smokers (2.35+0.71 ng/ml; n = 36). The low mean level of light smokers relative to the non-smokers does not necessarily indicate that low-level hookah smokers are free from any health risk. Instead of drawing definitive conclusions about these apparently low values relative to non-smokers, we think that the effect of low assay (analytical) sensitivity at lower concentration region, small size of data and some cross interferences in the reaction mixture, should also be taken into consideration. The increased CV in the reproducibility data at (and below of course) 1.6 ng CEA/ml could also be one of the reasons. The mean CEA level in medium smokers (2.52 ± 1.15 ng/ml; n = 28) was not significantly different from the levels in non-smokers. The overall CEA levels (3.58 ± 2.61 ng/ml; n = 59) are thus not affected by the levels in light and medium smokers. However, CEA mean level in heavy smokers (5.11 ± 3.08 ng/ml; n = 26) was significantly raised relative to non-smokers. These values are low compared to those reported in cigarette smokers (9.19 ± 14.9 ng/ml; n = 122) and mixed cigarette/hookah smokers (7.16 ± 10.38 ng/ml; n = 14) in our previous study [19]. This shows that the daily rate of smoking and its duration effects CEA levels. Also, noteworthy is the fact that the quantities of the tobacco mixture involved in hookah smoking in Pakistan are high if compared with cigarettes: up to 120 times (60 times by taking into account the molasses element [19].

Table 4 Tobacco smoking and elevation of CEA concentrations Full size table

The range of "normal" values provided by the manufacturer of our kits (DPC, USA) were: 2.1–6.2 ng/ml for male smokers (153 individuals study) and 1.3–4.9 ng/ml for female smokers (81 individuals study). The overall range of values (males+females) in these individuals was 1.3–6.2 ng/ml. The range was 1.1–3.2 ng/ml and 0.8–2.5 ng/ml for male (226 persons study) and female non-smokers respectively (262 persons study). The overall range (males+females) of values in non-smokers was 0.8 – 3.2.

In our last study we observed a mean CEA level of: 9.19 ng/ml (± 14.9) in 122 cigarette smokers; 7.16 ± 10.38 in mixed hookah smokers; and 2.35 ng/ml (± 0.71) in non-smokers [19]. Regarding levels in cigarette smokers, the chemiluminescent immunoassay, more sensitive and specific than the technique (Hansen-Z-gel) used by Alexander et al [11], may account for the differences. However, the origin and quality of tobacco and the environment should also be taken into consideration.

In our last study, CEA levels increased with the number of cigarettes smoked per day and the highest levels were reached by users who smoked more than 31 cigarettes per day [19]. Doll and Peto had established that the annual lung cancer incidence is: 0.273 × 10-12. (cigarettes/day+6)2.(age-22.5)4.5 [45]. However, some decades ago, people used to smoke at a later age than today. The formula was revisited by Hill who insisted that the most relevant parameter for the assessment of tobacco consumption is duration and not dose (expressed in pack-years) [46]. If consumption is doubled, the risk is multiplied by 2. In striking contrast, if the duration is increased twofold, the risk is multiplied by 23 (24.5 exactly). Therefore, the exposure duration to tobacco smoke is much more important than the daily number of cigarettes. One conclusion is that quitting as early as possible remains the most powerful factor. Although critical, Lebeau also considers that there is no treshhold dose for risk [47].

In the case of the world fashionable tobacco-molasses smoking mixture called moassel (tobamel), users feel the smoke is very mild (because of the actual water trapping of notorious irritants such as aldehydes) and one direct consequence is that they often inhale considerable amounts of the smoke: randomly varying between 100 ml at least (but less sometimes) and up to 500 ml and sometimes more. These quantities of smoke go directly into their lungs with no previous dilution and stocking inside the mouth (as in the case of cigarettes)[3]. However, in the case of the Desi Punjab tobacco-molasses mixture smoked in Pakistan, and probably because of the different composition (no glycerol, more nicotine) and the higher temperatures, the smoke is not inhaled directly into the lungs and therefore it is diluted. Zahran stated that 15 minutes of its smoking "would provide approximately the same amount of tobacco smoke as one cigarette"[20].

A careful data analysis of our samples shows that CEA values are not normally distributed among the individuals of the various groups (Figures 6, 7, 8, 9, 10). We have therefore applied Wilconson's test to compare CEA values among the different groups. The p-values we obtained this way lead us to almost the same conclusions as those we get to with the t-test except for the comparison between overall CEA levels and non-smokers, where we get a non-significant result in Wilcoxon's test in contrast to a significant one in t-test. This may be due to the high sensitivity of Wilcoxon test over t-test. We are not getting a bimodal pattern in the distribution curve for our smokers, so the grouping according to such a pattern cannot be strictly followed. Therefore, the grouping on the basis of smoking level remains the good criterion for the grouping of our subjects.

The CEA test, although widely used for diagnosis and monitoring the therapy of cancer is not 100% specific for this disease [48]. So when someone's CEA level is high, it does not necessarily mean that the patient has cancer. Similarly, if someone's CEA level is low or close to lower normal limit, it does not mean that the individual is protected from cancer. In the light of these facts, we decided not to merge the light and medium groups of smokers.

Hookah smoking and Cancer

53 years ago, the British Medical Journal tried to answer the following question: "Does the custom of filtering tobacco smoke through water as in the Eastern hookah remove the noxious elements? Carcinoma of the lung is very rare, in my experience, in hookah-smoking Indians" [49]. A review of what research says about hookah smoking and cancer is therefore necessary to understand the possible influence of the type of exclusive hookah smoking ("light" and "medium" vs. "heavy") on CEA levels, supposed to reflect cancer risks. About half a century ago, Rakower and Fatal investigated this issue further to their analysis of rare available epidemiological statistics on narghile smoking [50]. However, the pioneer in this field is Angel Roffo in 1939 [51]. A recent review of his work was recently published although his very study on narghile was not included for some reason [52]. Roffo was the first to design a machine for the analysis of narghile smoke chemistry. He examined the fluorescence and spectrography of the tar filtered by both a water (narghile) and cotton filter. He was surprised by the filtration rate of the water itself: about 30%. However, he concluded that water and cotton filters could not be used as a means of "absolute prevention" for the prophylaxis of cancer. Lesions on animals appeared more lately than when the tar was directly applied on them. In the researcher's view, this represents a way to reduce the harm of tobacco use ("un medio de aminorar la accion del tabaquismo")[51]. Rakower and Fatal used a more sophisticated smoking machine and speculated on the reasons for which lung cancer would be less prevalent among narghile users: particularly the lower temperatures in relation to the formation of PAH (polynuclear aromatic hydrocarbons)[50]. This study has been sometimes cited in the available literature to support the statement that narghile smoking causes lung cancer [53], i.e. the opposite finding reached by its authors. This has resulted in a wide confusion [54]. More recently, a renowned Syrian lung specialist who has extensively studied narghile smokers, concluded that the low temperatures and filtration of part of the tar may account for the low rates of cancer observed in her country [55].

The hazards of tar, and particularly its carcinogenicity are directly related to the working temperatures whereby not only combustion and pyrolysis are involved, as a WHO report states, but also distillation, as emphasised by Baker et al [21, 56]. This is particularly true in the case of shisha smoking where the temperatures of the tobacco-molasses mixture in the bowl does not go in excess of 150°C, allowing a chemical reaction of the Maillard type [27]. Even when using a smoking machine and despite the bias these methods entail, the temperature hardly reaches 200°C [34, 35]. The more the temperature is elevated, the more carcinogenic the smoke is. In these conditions, hookah tar is qualitatively very different from that produced by cigarettes. Furthermore, in the case of the fashionable shisha (using flavoured molasses tobacco with glycerol), a great portion of the calculated "tar" is expected to be made up of glycerol which has proved not "adversely alter the smoke chemistry or biological effects normally associated with exposure to mainstream cigarette smoke" [57] as in the harm reduction Eclipse cigarette (about 40%). In any case, what might be really hazardous for tobacco smokers are, apart from PAH, nitrosamines the weight of which does not reach, in certain brands of cigarettes, the 10,000th part of the tar figures printed on the packets. Gray et al, in a study on Polish products, showed that cigarettes containing more nitrosamines were not those with a higher tar content [58]. Consequently, the rating of tar, particularly produced by smoking machines, makes no sense and may deceive tobacco users. Sound and deep research is needed in this field, all the more that a recent study by Sepetdjian et al, based on a smoking machine, has found great amounts of carcinogenic PAH [59]. The underlying methods, including the smoking topography, have been criticised for considerably reducing a highly complex human and social situation [34]. For example, the FTC (Federal Trade Commission) and ISO norms suggest the use of a 1 minute machine smoking interval between 2 puffs in the case of cigarettes for which the duration of a session barely exceeds 5 minutes. However, and by a striking contrast, the hookah smoking device used in the laboratory was based on steady puffs every 17 seconds. This implies that about 1 out of every 4 puffs is supposed to be a human breath for a whole one-hour session (171 regular puffs were drawn this way). Also, contrary to common practice in the real life, the charcoal was left in the same position over the bowl during all this period. In these conditions, the nature and yields of toxicants in the smoke are questionable. Furthermore, the low temperatures involved, as highlighted several times in our study [27, 33–35, 50, 55], do not theoretically allow for the abundant formation of hazardous PAHs. Sepetdjian et al suggest that one source for the PAHs might be the charcoal and that different types of the latter might induce different yields. As in the case of CO, Sajid et al had early established in 1993 that concentrations of this gas depend on the nature of charcoal (natural vs. commercial)[28]. In any case, assays on human subjects (urinary carcinogens, chemical or biological markers) would be more appropriate as in our previous study and the present one [19].