|Year : 2018 | Volume
| Issue : 1 | Page : 13-19
Smoked cooked meat as a risk factor for Nasopharyngeal Carcinoma: A case control study among Saudi populations
Khalid Hakami1, N Prepageran2, Talal Al Thubaity1, Eidah Al Juaid1, Nawaf Al Solami3
1 Department of Otolaryngology, Head and Neck Surgery, Alhada Armed Forces Hospital, Taif, Saudi Arabia
2 Department of Otorhinolaryngology, Faculty of Medicine, University of Malaya, 50603 Kuala Lumpur, Malaysia
3 Department of Otolaryngology, King Fahad Armed Forces Hospital, Jeddah, Saudi Arabia
|Date of Web Publication||23-Dec-2019|
Department of Otolaryngology, Head and Neck Surgery, Alhada Armed Forces Hospital, Taif; P.O.Box 6667, Taif 21944
Source of Support: None, Conflict of Interest: None
Background: Head and neck cancers constitute about 6% of malignancies diagnosed annually in the Kingdom of Saudi Arabia and represent 33% of these are of nasopharyngeal origin.
The epidemiological studies of nasopharyngeal carcinoma (NPC) suggested that factors like viral agents, dietary factors and genetic susceptibility have a major role to play in the disease etiology. Objective: To investigate the possible roles of smoked cooked meat (like Mandi which is traditional dish in Saudi Arabia) in the development of NPC.
Subjects and Methods: A case-control study included 43 incident cases of NPC and 84 control subjects was carried out at Otorhino laryngology, Head and Neck Surgery department at Al-Hada Armed Forces Hospital, Saudi Arabia, throughout the period 2014-2015. All information on dietary, environmental, social, and demographic factors was collected. Univariate and multivariate logistic regression analysis using maximum likelihood method was used to analyze data.
Results: The study included 43 cases with confirmed nasopharyngeal carcinoma and 84 age and sex matched control subjects. Most of cases 29 (67.4%) were presented with neck mass whereas the remaining 14 (32.6%) presented with otitis media. Multivariate logistic regression analysis revealed that smokers were at almost 3-fold risk to develop nasopharyngeal carcinoma compared to non-smokers (Adjusted “AOR”=3.05; 95% confidence intervals: 1.37-6.79) and consumption of smoked meat as participants consumed it on weekly or monthly bases were at highly significant risk to develop NPC compared to those who never consumed it (AOR=9.32; 95% CI: 1.12—77.39 and 14.44; 95% CI: 1.71-121.81. respectively) [Table 2].However, consumption of Canned Fava beans and Arabic Coffee were not found to be associated with NPC.
Conclusion: The rate of consumption of meats was increased in the last tow decades among Saudi population. The N-nitrosamines (NA) is a large group of compounds of which many are carcinogenic. In many studies, the nitrosamines were detected as high level in smoked meat. The results from this study suggested that consumption of smoked cooked meat and cigarette smoking is independent risk factors for NPC in Saudi Arabia.
Keywords: Smoked meat; nasopharyngeal carcinoma; Mandi; Saudi Arabia
|How to cite this article:|
Hakami K, Prepageran N, Al Thubaity T, Al Juaid E, Al Solami N. Smoked cooked meat as a risk factor for Nasopharyngeal Carcinoma: A case control study among Saudi populations. Saudi J Otorhinolaryngol Head Neck Surg 2018;20:13-9
|How to cite this URL:|
Hakami K, Prepageran N, Al Thubaity T, Al Juaid E, Al Solami N. Smoked cooked meat as a risk factor for Nasopharyngeal Carcinoma: A case control study among Saudi populations. Saudi J Otorhinolaryngol Head Neck Surg [serial online] 2018 [cited 2023 Jan 27];20:13-9. Available from: https://www.sjohns.org/text.asp?2018/20/1/13/273914
| Introduction|| |
Head and neck cancers constitute about 6% of all malignancies diagnosed annually in the Kingdom of Saudi Arabia and represent 33% of these are of nasopharyngeal origin, with an annual age-standardized incidence rate of 2.5 and 0.8 per 100 000 for males and females respectively as demonstrated in the cancer incidence report in Saudi Arabia 1999-2000 .
The epidemiological studies of nasopharyngeal carcinoma (NPC) suggested that factors like viral agents, dietary factors and genetic susceptibility have a major role to play in the disease etiology ,. The disease is an endemic in certain areas such as Hong Kong, Southern China, Singapore, and North Africa as they have high incidence rates of NPC ,. These areas are characterized by high consumption of salted fish, preserved or fermented foods, including meats, and the use of Chinese medicinal herbs, hence association with nitrosamines . However, the socioeconomic changes over the last 50 years have impacted on the meat consumption habits among Saudi population. The worldwide consumer demand for meat and meat products has been growing unabated due to both economic and social changes over the last two decades. The dietary habits of Saudis have changed drastically due to improved socioeconomic conditions and an increasingly urban lifestyle .
Poultry meat consumption in Saudi Arabia is among the highest in the world, with per capita consumption last year is currently estimated at 48 kg per year (USDA Foreign Agricultural Service, Saudi Arabia Poultry and Products Annual, 2015.)  [Figure 1].
|Figure1:United States Department of Agriculture, Saudi Arabia Beef and Veal Meat Domestic Consumption by Year .|
Click here to view
A major focus of the present study to investigate the possible roles of smoked cooked meat (like Mandi which is traditional dish in Saudi Arabia) in the development of NPC. Mandi is a traditional dish in Saudi Arabia usually made from rice, meat, and a mixture of spices where meat is cooked in the tandoor, which is a special kind of oven. Tandoor is usually a hole dug in the ground and covered inside by clay. To cook Mandi, dry wood is placed in the tandoor and burned to generate a lot of heat turning into charcoal. The meat is then suspended inside the tandoor without touching the charcoal. After that, the whole tandoor is closed without letting any of the smoke out [Figure 2].
Subjects and Methods
A case-control study included 43 incident cases of NPC and 84 control subjects was carried out at Otorhinolaryngology, Head and Neck Surgery department, Al-Hada Armed Forces Hospital, Saudi Arabia throughout the period 2014-2015. Cases were included provided that they were histological confirmed as NPC and permanently residing in Saudi Arabia. Neighborhood age and sex matched controls were recruited. We excluded none-Saudi patients, those diagnosed before 2005 and those who were not histological confirmed diagnosis. A standard predesigned form was used to collect information about demography, social factors and other risk factors from cases as well as controls. The research proposal has been approved by Regional Research and Ethics committee at Al-Hada Armed Forces Hospital, Taif, Saudi Arabia. In addition, written consent forms were obtained from both cases and controls prior to study conduction. All patients’ information was kept confidential.
| Results|| |
The study included 43 cases with confirmed nasopharyngeal carcinoma and 84 age and sex matched control subjects. All cases and control subjects are Saudi and diagnosed after Jan 2005. 110 subjects were males, 36 cases (32.7%) and 74 (67.3%) were controls whereas 37 subjects were females 11 cases (29.7%) and 26 (70.3%) were controls. [Figure 3] illustrates that most of cases 29 (67.4%) were presented with neck mass whereas the remaining 14 (32.6%) presented with otitis media.
In bivariate analysis, the significant risk factors were occupation as military workers were at almost 3-fold risk to develop nasopharyngeal carcinoma compared to civilian workers (crude odds ratio “COR”=3.55; 95% confidence intervals: 1.37-9.15), smoking history as smokers were more likely to develop nasopharyngeal carcinoma compared to non-smokers (COR=2.61; 95% confidence intervals: 1.22-5.60) and consumption of smoked meat as participants consumed it on monthly basis were at highly significant risk to develop NPC compared to those who never consumed it (COR=25.38; 95% confidence intervals: 2.99-215.16). However, the reset of the variables (consumption of Canned Fava Beans and Arabic Coffee) were not found to be associated with NPC [Table 1].
Multivariate logistic regression analysis revealed that smokers were at almost 3-fold risk to develop nasopharyngeal carcinoma compared to non-smokers (Adjusted “AOR”=3.05; 95% confidence intervals: 1.376.79) and consumption of smoked meat as participants consumed it on weekly or monthly bases were at highly significant risk to develop NPC compared to those who never consumed it (AOR=9.32; 95% CI: 1.12—77.39 and 14.44; 95% CI: 1.71-121.81. respectively) [Table 2].
| Discussion|| |
This is a case-control study undertaken to determine the possible risk factors of NPC in Saudi Arabia, in particularly the dietary factors. Among dietary factors, consumption of N-nitrosamines (NA) are produced in nitrite preserved meat products. The NA is a large group of compounds of which many are carcinogenic (IARC, 1998) . N-nitrosamines (NA) occur in sodium nitrite preserved meat products as bacon, sausages, ham and several types of luncheon meats. Several of these NA are carcinogenic and high intake of processed meat products has been associated with increased risk of cancer and other adverse health effects in some epidemiological studies . Ciemniak A., et al, in his study the comparison of N-nitrosodimethylamine (NDMA) contents in selected meat products found that The level of NDMA was varied from 0.049 mg/kg to 16.47 mg/kg. The highest level of NDMA was found in smoked sausage .
Laboratory findings also suggest an etiological role for smoked meat in the oncogenesis of NPC. Earlier Indian studies demonstrated mutagenicity in the extracts of smoked meat samples using the sperm head abnormality test and Ames test using Salmonella More Details typhimurium TA- 98 strain .
Besides, analyses of the smoked meat samples have also demonstrated the presence of nitro-sodimethylamine (NDMA), nitrosodiethylamine (NDEA) and nitrosopyrrolidine (NPYR) .
In Taiwan, a case-control study concluded that Guangdong salted fish consumption during childhood (more than or equal once /week) was significantly associated with elevated NPC risk .
Epidemiologic studies investigating the association between cigarette smoking and the risk of NPC have been inconsistent as some studies suggested cigarette smoking to be a risk factor for NPC ,,,, others failed to observe this association ,,. in the present study, smoking history, regardless its duration was significantly associated with NPC even after controlling for confounders in multivariate analysis.
The observation that military people in the bivariate analysis in present study were at higher risk for NPC compared to civilians is not surprising. This could be attributed to the fact that they are more smoker than civilians and this is confirmed by the study conducted recently by Al-Khashan, et al  who reported that smoking is prevalent among military personnel in Saudi Arabia than other categories with a rate of 38%. In Multivariate analysis, military occupation was not significant whereas smoking and consumption of smoked meat were predictors of NPC.
| In conclusion,|| |
The rate of consumption of meats was increased in the last two decades among Saudi population. The N-nitrosamines (NA) is a large group of compounds of which many are carcinogenic. In many studies, the nitrosamines were detected as high level in smoked meat. The results from this study suggested that consumption of smoked meat even at small frequency and smoking history are independent NPC risk factors in Saudi Arabia. Further investigation included larger sample of patients from different areas of the Saudi Arabia with determination of total nitrosamines compounds in smoked cooked meat like (Mandi) is highly recommended.
| References|| |
Cancer incidence report: Saudi Arabia 1999–2000. Riyadh, Saudi Arabia, National Cancer Registry Authority, 2004.
Henderson B.E., Louie E., Jing JSH, Bwell P., Gardener M. Risk factor associated with Nasopharyngeal Carcinoma. N Engl J Med.
1976; 295: 1101-1106.
Janse van Rensburg, E., Van Heerden W.F., Robson B.A., Swart T.J., Engelbrecht S. Epstein-Barr virus strain characterization in South African patients with nasopharyngeal carcinomas. Anticancer Res.
2000; 20: 1953-1957.
Whelan S.L., Parkin D.M., Masuyer E., editors. Pattern of cancer in five continents. Vol. V. No. 102. World Health Organization International Agency for Research On Cancer. Lyon (FR): IARC Scientific Publications; 1990. p. 116-117.
Higginson J., Muir C.S., Munoz N., editors. Human cancer: epidemiology and environmental causes. Cambridge Monograph on Cancer Research. Nasopharynx. Cambridge (UK): Cambridge University Press;
1992. p. 256-260.
Yu M.C., Ho J.H.C., Lai SH, Henderson B.E. Cantonese-style salted fish as a cause of Nasopharyngeal carcinoma: report of a case control study in Hong Kong. Cancer.
1986; 46: 956-961.
Selvanathan S., Selvanathan E.A., Albalawi S., Hossain M. Meat and fish consumption patterns in Saudi Arabia. Applied Economics.
USDA Foreign Agricultural Service. Global Agricultural Information Network, Saudi Arabia Poultry and Products Annual, GAIN Report Number SA1509,
Uan J.M., Wang X.L., Xiang Y.B., Gao Y.T., Ross R.K., Yu M.C. Preserved foods in relation to risk of nasopharyngeal carcinoma in Shanghai, China. Internat J Cancer.
Guo X., Johnson R.C., Deng H., Liao J., Guan L., Nelson G.W., et al. Evaluation of nonviral isk factors for nasopharyngeal carcinoma in a high-risk population of Southern China. Int J Cancer.
2009 Jun 15;124(12):2942-7.
Chelleng P.K., Narain K., Das H.K., Chetia M., Mahanta J. Risk factors for cancer nasopharynx: A case-control study from Nagaland, India. National Med J India.
Shuaib M.A. Ministry of Agriculture, Veterinari Diagnostic Labs, based Poultry Systems in the Kingdom of Saudi Arabia, FAO
Animal Production and Health Division, December 2007.
Herrmann S.S., L. Duedahl-Olesen L, K. Granby K. Occurrence of volatile and non- volatile N-nitrosamines in processed meat products and the role of heat treatment. Elsevier J Food Control.
2015; 48: 163-169.
Herrmann S.S. N-nitrosamines in processed meat products-analysis, occurrence, formation, mitigation and exposure, DTU Food, National Food Institute. Technical University of Denmark,
PhD Thesis, 2014.
Ciemniak A. A comparison of N-nitrosodimethylamine contents in selected meat products, Rocz Panstw Zakl Hig.
Kumar S., Zinyu R., Singh I.K.K., Medhi S.B., Baruah T., Das B., et at. Studies on nasopharyngeal carcinoma with reference to the north eastern region of India. Ann Natl Acad Med Sci (India).
Sarkar S., Nagabhushan M., Soman C.S., Tricker A.R., Bhide S.V. Mutagenicity and carcinogenicity of smoked meat from Nagaland, a region of India prone to high incidence of nasopharyngeal cancer. Carcinogenesis.
Yang X.R., Diehl S., Pfeiffer R., Chen C.J., Hsu W.L., Dosemeci M., et al. Evaluation of risk factors for nasopharyngeal carcinoma in high-risk nasopharyngeal carcinoma families in Taiwan. Cancer Epidemiol Biomarkers Prev.
Nam J.M., McLaughlin J.K., Blot W.J. Cigarette smoking, alcohol, and nasopharyngeal carcinoma: a case-control study among U.S. Whites. J Natl Cancer Inst.
Cheng Y.J., Hildesheim A., Hsu M.M., et al. Cigarette smoking, alcohol consumption and risk of nasopharyngeal carcinoma in Taiwan. Cancer Causes Control.
Chow W.H., McLaughlin J.K., Hrubec Z., Nam J.M. Blot W.J. Tobacco use and nasopharyngeal carcinoma in a cohort of US veterans. Int J Cancer.
Yuan J.M., Wang X.L., Xiang Y.B., GaoY.T., Ross R.K., Yu M.C. Non-dietary risk factors for nasopharyngeal carcinoma in Shanghai, China. Int J Cancer.
Henderson B.E., Louie E., SooHoo J.J., Buell P., Gardner M.B. Risk factors associated with nasopharyngeal carcinoma. N Engl J Med.
1976;295:1101 – 6.
Lee H.P., Gourley L., Duffy S.W., Esteve J., Lee J., Day N.E. Preserved foods and nasopharyngeal carcinoma: a case-control study among Singapore Chinese. Int J Cancer.
Zou J., Sun Q., Akiba S., et al. A case-control study of nasopharyngeal carcinoma in the high background radiation areas of Yangjiang, China. J Radiat Res (Tokyo). 2000;41 Suppl:53-62. 26. Al-Khashan H.I., Al Sabaan F.S., Al Nasser H.S., Al Buraidi A.A., Al Awad A.D., Horaib G.B., et al. The prevalence of smoking and its associated factors among military personnel in Kingdom of Saudi Arabia: A national study. J Family Community Med.
2014 Sep-Dec; 21(3): 147–153.
[Figure 1], [Figure 2], [Figure 3]