Evaluation of baseline cleanliness of food contact surfaces in Basrah Governorate restaurants using ATP-bioluminescence to assess the effectiveness of HACCP application in Iraq

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Ammar B. Altemimi
Nawfal Alhelfi
Athmar A. Ali
Antonella Pasqualone
Hafize Fidan
Tarek Gamal Abedelmaksoud
Angelo Maria Giuffrè
Salam A. Ibrahim


ATP-bioluminescence, bacteria, contamination, food safety, HACCP


The Hazard Analysis and Critical Control Points (HACCP) system prevents and manages physical, chemical and biological risks at places where foods and beverages are processed, packaged, distributed and consumed. The present study (1) assessed the level of microbial contamination of food contact surfaces using adenosine triphosphate (ATP)-bioluminescence in Iraq restaurants; (2) investigated the level of microbial contamination of food contact surfaces; and (3) evaluated the efficiency of sanitizers in removing biological hazards from food contact surfaces. The ATP-bioluminescence discovered the presence of Escherichia coli and Staphylococcus aureus on surfaces and tools. Results also showed that the HACCP application was very effective in the amelioration of food quality.

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Ali A.A., Altemimi A.B., Alhelfi N. and Ibrahim S.A. 2020. Application of biosensors for detection of pathogenic food bacteria: a review. Biosensors (Basel). 10(6): 58. 10.3390/bios10060058

Andrews W. 1992. Manual of food quality control. 4. Rev. 1. microbiological analysis. Food and Drug Administration. FAO Food Nutr Pap. 14(4 Revis 1): 1–338. PMid: 1426189

American Public Health Association (APHA). 1998. Standard Methods for the Examination of Water and Waste Water. Washington, DC: APHA.

Barbosa J., Albano H., Silva C.P. and Teixeira P. 2019. Microbiological contamination of reusable plastic bags for food transportation. Food Control. 99: 158–163. 10.1016/j.foodcont.2018.12.041

Batani G., Bayer K., Böge J., Hentschel U. and Thomas T. 2019. Fluorescence in situ hybridization (FISH) and cell sorting of living bacteria. Sci Rep. 9: 1–13. 10.1038/s41598-019-55049-2

Chae W., Kim P., Hwang B.J. and Seong B.L. 2019. Universal monoclonal antibody-based influenza hemagglutinin quantitative enzyme-linked immunosorbent assay. Vaccine. 37: 1457–1466. 10.1016/j.vaccine.2019.01.068

Champiat D., Matas N., Monfort B. and Fraass H. 2001. Applications of biochemiluminescence to HACCP. Lumin J Bio Chem Lumin. 16: 193–198. 10.1002/bio.647

Chatterjee A. and Abraham J. 2018. Microbial contamination, prevention, and early detection in food industry. In: Microbial Contamination and Food Degradation. London: Academic Press, pp. 21–47.

Chlebicz A. and Śliżewska K. 2018. Campylobacteriosis, salmonellosis, yersiniosis, and listeriosis as zoonotic foodborne diseases: a review. Int J Environ Res Public Health. 15(5): 863. 10.3390/ijerph15050863

Chollet R. and Ribault S. 2012. Use of ATP-bioluminescence for rapid detection and enumeration of contaminants: the milliflex rapid microbiology detection and enumeration system. In: Bioluminescence-Recent Advances in Oceanic Measurements and Laboratory Applications. London: IntechOpen, pp. 99–118.

Duffy G.F. and Moore E.J. 2017. Electrochemical immunosensors for food analysis: a review of recent developments. Anal Lett. 50: 1–32. 10.1080/00032719.2016.1167900

Etheridge J.R., Randolph M. and Humphrey C. 2019. Real-time estimates of Escherichia coli concentrations using ultraviolet--visible spectrometers. J Environ Qual. 48: 531–536. 10.2134/jeq2018.08.0294

Etter A.J., Hammons S.R., Roof S., Simmons C., Wu T., Cook P.W. and Oliver H.F. 2017. Enhanced sanitation standard operating procedures have limited impact on Listeria monocytogenes prevalence in retail delis. J Food Prot (JFP). 80: 1903–1912. 10.4315/0362-028X.JFP-17-112

Forsythe S.J. 2020. The Microbiology of Safe Food. Hoboken, NJ: John Wiley, 608 p.

Gehring K.B. and Kirkpatrick R. 2020. Hazard analysis and critical control points (HACCP). In: Food Safety Engineering. Cham, Switzerland: Springer, pp. 191–204.

Gursoy D. 2019. Foodborne illnesses: an overview of hospitality operations liability. J Hosp. 1(1): 41–49. http://htmjournals.com/jh/index.php/jh/article/view/6

Harper M., Amodio E., Cannova L., Villafrate M.R., Merendino A.M., Aprea L. and Calamusa G. 2014. Comparison of ATP-bioluminescence and aerobic bacterial count for evaluating surface cleanliness in an Italian hospital. J Occup Environ Hyg. 11: D23–D27. 10.1080/15459624.2013.852281

Hassan F., Lakshmanan P.T., Geethalakshmi V. and Mukundan M.K. 2013. Evaluation of stabilised hydrogen peroxide as sanitiser in seafood processing industry. Indian J Fish. 60(2): 145–149. http://krishi.icar.gov.in/jspui/handle/123456789/15377

Jayan H., Pu H. and Sun D.W. 2020. Recent development in rapid detection techniques for microorganism activities in food matrices using bio-recognition: a review. Trends Food Sci Tech. 95: 233–246. 10.1016/j.tifs.2019.11.007

Joint FAO/WHO Expert Committee on Food Additives (JECFA). 2004. Available at: https://inchem.org/documents/jecfa/jeceval/jec_1068.htm

Khairallah A. 2014. Quality and Safety of Food Processing. Khartoum North, Sudan: Industrial Research and Consultancy Center (IRCC). ISBN: 978-99942-3-423-3.

Liu, Y, Cao Y., Wang T., Dong Q., Li J., and Niu C. 2019. Detection of 12 common food-borne bacterial pathogens by TaqMan real-time PCR using a single set of reaction conditions. Front Microbiol. 10: 222. 10.3389/fmicb.2019.00222

McDonnell G. 2009. The use of hydrogen peroxide for disinfection and sterilization applications. In: Patai's Chemistry of Functional Groups, New York, United States, pp. 1–34.

Mishra G.K., Barfidokht A., Tehrani F. and Mishra R.K. 2018. Food safety analysis using electrochemical biosensors. Foods. 7: 141. 10.3390/foods7090141

Nakao J.H., Talkington D., Bopp C.A., Besser J., Sanchez M.L., Guarisco J. and Xavier K. 2018. Unusually high illness severity and short incubation periods in two foodborne outbreaks of Salmonella Heidelberg infections with potential coincident Staphylococcus aureus intoxication. Epidemiol Inf. 146: 19–27. 10.1017/S0950268817002655

Nemati M., Hamidi A., Dizaj S.M., Javaherzadeh V. and Lotfipour F. 2016. An overview on novel microbial determination methods in pharmaceutical and food quality control. Adv Pharm Bull. 6: 301–308. 10.15171/apb.2016.042

Osimani A., Garofalo C., Clementi F., Tavoletti S. and Aquilanti L. 2014. Bioluminescence ATP-monitoring for the routine assessment of food contact surface cleanliness in a university canteen. Int J Env Res Public Health 11: 10824–10837. 10.3390/ijerph111010824

Patel P.D. 2020. Biosensors for measurement of analytes implicated in food safety: a review. Trends Anal Chem. 21: 96–115. 10.1016/S0165-9936(01)00136-4

Poghossian A., Geissler H. and Schöning M.J. 2019. Rapid methods and sensors for milk quality monitoring and spoilage detection. Biosens Bioelec. 140: 111272. 10.1016/j.bios.2019.04.040.

Rajapaksha P., Elbourne A., Gangadoo S., Brown R., Cozzolino D. and Chapman J. 2019. A review of methods for the detection of pathogenic microorganisms. Anal J. 144: 396–411. 10.1039/c8an01488d

Randhawa M.A., Asghar A., Nadeem M. and Ahmad N. 2018. Food safety: benefits of contamination control on consumers health. In: Food Safety and Preservation. Academic Press, Cambridge, Massachusetts, United States, pp. 13–38.

Sankarankutty K.M. 2014. Biosensors and their applications for ensuring food safety. Global J Pathol Microbiol. 2: 15–21. 10.14205/2310-8703.2014.02.01.3

Shama G. and Malik D.J. 2013. The uses and abuses of rapid bioluminescence-based ATP assays. Int J Hyg Environ Health. 216: 115–125. 10.1016/j.ijheh.2012.03.009

Shen M. and Singh R.K. 2022. Detoxifying aflatoxin contaminated peanuts by high concentration of H2O2 at moderate temperature and catalase inactivation. Food Control. 142: 109218. 10.1016/j.foodcont.2022.109218

Simmons C., Stasiewicz M.J., Wright E., Warchocki S., Roof S., Kause J.R. and Oliver H.F. 2014. Listeria monocytogenes and Listeria spp. contamination patterns in retail delicatessen establishments in three US states. J Food Prot (JFP). 77: 1929–1939. 10.4315/0362-028X.JFP-14-183

Singh M.R. and Gupta A. 2016. Water Pollution-Sources, Effects and Control. Nagaland, India: Centre for Biodiversity, Department of Botany, Nagaland University.

Tabata S., Kamimura H., Ibe A., Hashimoto H. and Tamura Y. 1994. Degradation of aflatoxins by food additives. J Food Prot. 57: 42–47. 10.4315/0362-028X-57.1.42

Tesson V., Federighi M., Cummins E., de Oliveira Mota J., Guillou S. and Boué G. 2020. A systematic review of beef meat quantitative microbial risk assessment models. Int J Environ Res Public Health. 17: 688. 10.3390/ijerph17030688

Ukuku D.O., Pilizota V. and Sapers G.M. 2001. Bioluminescence ATP assay for estimating total plate counts of surface microflora of whole cantaloupe and determining efficacy of washing treatments. J Food Prot. 64: 813–819. 10.4315/0362-028x-64.6.813

US Food and Drug Administration (FDA). 2022. Subpart B – Listing of specific substances affirmed as GRAS. Available at: https://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfcfr/CFRSearch.cfm?fr184.1366&SearchTermhydrogenperoxide. Accessed on June 22, 2022.

Van Arkel A., Willemsen I. and Kluytmans J. 2021. The correlation between ATP measurement and microbial contamination of inanimate surfaces. Antimicrob Resist Infect Control. 10: 116. 10.1186/s13756-021-00981-0

Wang W., Wang Y., Lin L., Song Y. and Yang C.J. 2019. A tridecaptin-based fluorescent probe for differential staining of Gram-negative bacteria. Anal Bioanal Chem. 411: 4017–4023. 10.1007/s00216-018-1465-0

Yousif E.I., Ashoush L.S., Donia A.A. and Goma K.H. 2013. Critical control points for preparing chicken meals in a hospital kitchen. Ann Agric Sci. 58: 203–211.

Zambrano A.A., Jones A., Otero P., Ajenjo M.C. and Labarca J.A. 2014. Assessment of hospital daily cleaning practices using ATP-bioluminescence in a developing country. Braz J Inf Dis. 18: 675–677. 10.1016/j.bjid.2014.06.008

Zhang K., Pan R., Zhang T., Xu J., Zhou X. and Yang Y. 2019. A novel method: using an adenosine triphosphate (ATP) luminescence-based assay to rapidly assess the biological stability of drinking water. App Microbiol Biotechnol. 103(11): 4269–4277. 10.1007/s00253-019-09774-3