Chemical Hazards in Products of Animal Origin in Cambodia from 2000 to 2023: A Systematic Review and Meta-Analysis
Abstract
1. Introduction
2. Materials and Methods
2.1. Protocol Development and Registration
2.2. Eligibility Criteria
2.2.1. Inclusion Criteria
2.2.2. Exclusion Criteria
2.3. Databases and Search Strategy
2.4. Screening and Study Selection
2.5. Quality Assessment Criteria
- Is the method of study scientifically sound and clear?
- Is the laboratory testing method used for chemical contaminants in food appropriate?
- Are the descriptions of data analysis for key outputs (sampling, test methods, and concentration) accurate and precise?
- Are the outcomes and conclusions of the selected studies clearly written?
2.6. Data Extraction
2.7. Data Analysis
2.7.1. Meta-Analysis of Arsenic and Mercury Concentration in Fish [28,29,30]
2.7.2. Descriptive and Basic Statistical Analysis
2.8. Health Risk Assessment of Chemical Toxins in Fishery Products
- C = concentration of the contaminant (μg/kg);
- F = weekly food consumption per person (kg);
- W = mean body weight (60 kg).
2.9. Calculation of DALY/Population of Cambodia
3. Results
3.1. Type of Study Initiatives
3.2. Number of Reviewed Studies and Geographical Coverage
3.3. Number of Publications and Reports from 2000 to 2023
3.4. Number of Studies for Different Groups of Chemical Contaminants
3.5. Summary of Evidence of Chemical Contaminants in POAO
3.5.1. Findings from Meta-Analysis of Arsenic (Meta-Regression)
3.5.2. Findings from Meta-Analysis of Mercury (Pooled Concentration)
3.5.3. Descriptive and Basic Statistical Analysis of the Results
3.6. Evidence of Elemental Contaminants Detected in POAO
3.6.1. Arsenic
3.6.2. Cadmium
3.6.3. Lead
3.6.4. Mercury
3.7. Evidence of POPs Reported in POAO in Cambodia from 2000 to 2023
3.7.1. Polycyclic Aromatic Hydrocarbons (PAH)
Benzo[a]pyrene (BaP)
Sum of Polycyclic Aromatic Hydrocarbon 4 (ƩPAH4)
Sum of Polycyclic Aromatic Hydrocarbon 12 (ƩPAH12)
3.7.2. Other Persistent Organic Pollutants (POPs)
Evidence of Butyl Tin in Fishery Products
Evidence of POPs (PBDE and Organochlorine Pesticides) in POAO
3.8. Evidence of Residues of Veterinary Medicines in Farmed Fish
3.9. Evidence of Other Chemical Contaminants in POAO
3.10. Health Risk Assessment of Exposure to Cadmium and Mercury in POAO
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
ADI | Acceptable daily intake |
AFRO | Africa Regional Office |
AMRO | America Regional Office |
AOAC | Association of Official Agricultural Chemists |
BaP | Benzo[a]pyrene |
BW | Body weight |
C | Concentration of the contaminant |
CAC | Codex Alimentarius Commission |
CCS | Cambodian Chemical Society |
CHLs | Heptachlor, trans-chlordane, cis-chlordane, trans-nonachlor, and cis-nonachlor |
CKD | Chronic kidney disease |
CTTF | Chemicals and Toxins Task Force |
DAD | Department of Aquaculture Department |
DALYs | Disability Adjusted Life Years |
DDT | dichloro-diphenyl-trichloroethane |
DG SANTE | Directorate-General for Health and Food Safety |
DL | DerSimonian–Laird method |
DRINs | Aldrin, dieldrin, and endrin |
EDI | Estimated daily intake |
EFSA | European Food Safety Authority |
EMRO | Eastern Mediterranean Regional Office |
ETAAS | Electrothermal atomic absorption spectrometry |
EU | The European Union |
EURO | European Regional Office |
EWI | Estimated weekly intake |
F | Weekly food consumption per person |
FAO | Food and Agriculture Organization of the United Nations |
FERG | Foodborne Disease Burden Epidemiology Reference Group |
FiA | Fisheries Administration |
FLD | Fluorescence detector |
GAqP | Good aquaculture practices |
GC | Gas chromatography |
GDAHP | General Directorate of Animal Health and Production |
HCB | Hexachlorobenzene |
HCH | Hexachlorocyclohexane |
HI | Hazard index |
HPLC | High-performance liquid chromatography |
ICP-MS | Inductively coupled plasma mass spectrometry |
ICP-OES | Inductively coupled plasma optical emission spectroscopy |
ID | Intellectual disability |
ILRI | International Livestock Research Institute |
JECFA | The Joint FAO/WHO Expert Committee on Food Additives |
kg | kilogram |
LC-MS | Liquid chromatography-mass spectrometry |
LOD | Limit of detection |
LOQ | Limit of quantification |
MAFF | Ministry of Agriculture, Forestry and Fisheries |
Mirex | Organochlorine insecticide |
MS | Mass spectrometry |
NFCS | National Food Control System |
NRMP | National residue monitoring plan |
NIP | National implementation plan |
OCP | Organochlorine pesticide |
PAH | Polycyclic aromatic hydrocarbon |
PBDE | Polybrominated Diphenyl Ethers |
PCB | Polychlorinated biphenyls |
PFOS | Perfluorooctane sulfonate |
POAO | Products of animal origin |
POPs | Persistent organic pollutants |
PRISMA | Preferred Reporting Items for Systematic Review and Meta-analysis |
PROSPERO | International database for registering systematic review protocols |
QuEChERS | Quick, Easy, Cheap, Effective, Rugged, and Safe |
REML | Restricted Maximum Likelihood |
SEARO | Southeast Asia Regional Office |
SLR | Systematic literature review |
TWI | Total weekly intake |
UNEP | United Nations Environment Programme |
UNIDO | United Nations Industrial Development Organization |
USAID | United States Agency for International Development |
USEPA | United States Environmental Protection Agency |
VMP | Veterinary medical products |
W | Mean body weight |
WHO | World Health Organization |
WPR B | Western Pacific Region B |
WPRO | Western Pacific Regional Office |
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Name of Carcinogenic Chemical Hazard | Food Source (Products of Animal Origin) | High Risk Group | Reference |
---|---|---|---|
Heavy metals | |||
Arsenic (As)—Inorganic form | Fish, shellfish (especially near industrial zones) | YOPI group (Young, Old, Pregnant, Immunocompromised) | [11] |
Cadmium (Cd) | Liver, kidney (offal), shellfish (mussels, oysters) | YOPI, especially fetuses and young children | [12] |
Lead (Pb) | Meat (game hunted with lead bullets), canned fish | YOPI, especially young children | [13] |
Methyl mercury (MeHg) | Fish | YOPI, especially pregnant women and young children | [14] |
Persistent organic pollutants (POPs) | |||
Dioxins | Fish, meat, and dairy products | Especially young children and infants | [15] |
Polychlorinated Biphenyls (PCBs) | Fish, meat, dairy products | Young children and individuals with high consumption of fatty POAO | [16] |
DDT & Metabolites | Fish and meat | YOPI | [17] |
Polycyclic aromatic hydrocarbons (PAHs) | |||
Benzo[a]pyrene (BaP) | Grilled and smoked fish and meat | YOPI | [18] |
Dibenzo[a,h]anthracene | Processed meat and smoked cheese | YOPI | [18] |
Benz[a]anthracene | Grilled and smoked fish and meat | YOPI | [18] |
Quality Criteria | Good | Medium | Poor |
---|---|---|---|
Scientific method | -Clarity of study, including subject, setting, and sampling points in detail -Clear description of appropriate sampling method | -Detailed description of study subject, setting, and sampling points, but somewhat unclear. -Sampling methods were not clearly described but contained enough information for data extraction | -The key part of study setting for example sampling points are not described at all. -Unclear/invalid sampling methods |
Testing method | -Standard laboratory testing methods were used (use of relevant ISO method or equivalent), and accuracy of equipment meets the needs of the national/EU/Codex | -The laboratory testing methods were acceptable or valid (use of the AOAC method or equivalent), and accuracy of equipment meets the needs of the national/EU/Codex | -The laboratory testing method was not acceptable or was invalid (use of rapid test kit). Use of equipment did not guarantee the accuracy of results |
Information for use of equipment | -Detailed information available for use of equipment | -Sufficient information for use of equipment | -Insufficient or unclear information for use of equipment |
Results accuracy for data extraction | -Detailed and accurate results | -Sufficient results for data extraction | -Insufficient or incomplete results presentation |
Name of Hazard | Name of Food/Source | Sampling Location | Sampling Point | Total Number of Samples | Test Methods | Equipment Used | Ref. Paper No. (See S1) |
---|---|---|---|---|---|---|---|
Arsenic (Inorganic arsenic and total arsenic) | Snails, clams, fish, meat, viscera | Kampong Cham, Kandal, Kratie, Tonle Sap | Aquaculture site and nature (lakes, ponds, rivers) | 331 | Acid digestion, internal procedures | HPLC-ICP-MS, ICP-MS, ICP-OES, ETAAS | 1, 2, 10, 14, 15, 16, 18 |
Benzo[a]pyrene | Processed fishery products | Battambang, Kampong Cham, Kampong Chhnang, Kandal, Siem Reap | Processing sites and markets | 105 | Accelerated solvent extraction, modified QuECheRS | GC/MS, HPLC-FLD | 5, 11, 13 |
Cadmium | Fish and fishery products | Tonle Sap, Phnom Penh | Coastal water | 208 | Acid digestion method | ICP-MS, ETAAS | 9, 10, 14, 18 |
Chloramphenicol | Freshwater farmed fish | Kandal, Prey Veng, Takeo, Kampong Cham, Kampong Chhnang, Pursat, Battambang, Kampong Thom, Siem Reap, and Banteay Meanchey | Freshwater fish farms | 129 | LC/MS/MS | LC-MS/MS | FiA report 1, 2, 3, 4 |
Hexachlorobenzene (HCB) | Fish, mussels, meat, viscera | Kampong Cham, Kratie, Kandal, Sihanoukville | Coastal water and markets | 184 | USEPA 3620B and 3640A, lipid extraction | GC-MSD, GC-ECD | 3 (46 samples were collected not only from various locations in Cambodia but from China, Hong Kong, India, Indonesia, Japan, Malaysia, the Philippines, and Vietnam), 17 |
hexachlorocyclohexane isomers (HCHs) | Fish, meat, viscera | Kampong Cham, Kratie, Kandal | Coastal water | 46 | Lipid extraction | GC-ECD | 3 |
Lead | Fish | Coastal areas, Phnom Penh, Tonle Sap, Kandal, Prey Veng, Takeo, Kampong Cham, Kampong Chhnang, Pursat, Battambang, Kampong Thom, Siem Reap, and Banteay Meanchey | Coastal water, lake and freshwater fish farms | 249 | Acid digestion | ICP-MS | 9, 10, 14, 18, and FiA report 1, 2 & 3 |
Mercury | Fish, meat, viscera, egg | Kandal, Prey Veng, Takeo, Kampong Cham, Kampong Chhnang, Pursat, Battambang, Kampong Thom, Siem Reap, and Banteay Meanchey Phnom Penh, Tonle Sap | Coastal water, farms, and markets | 495 | Acid digestion, USEPA 7473, standard addition method, | AAS, Direct mercury analyser, ICP-MS | 7, 9, 10, 12, 19, and FiA report 1, 2,3,4 |
∑Organochlorine pesticides (∑Organochlorine pesticides included the summation of DDT, HCH, CHL, DRINs, Mirex, and HCB) | Mussels, fish, meat, viscera | Kampong Cham, Kandal, Kratie | Markets | 138 | USEPA 3620B and 3640A | GC-MSD | 17 |
Phthalate esters | Fish, meat, viscera | Kampong Cham, Kandal, Kratie | Farms and markets | 42 | USEPA 3540C and 3620B | GC-MS | 6 |
Polycyclic aromatic hydrocarbon (PAH4) | Smoked freshwater fish | Battambang, Kampong Cham, Kampong Chhanag, Kampong Thom, Kandal, Siem Reap | Market, processing sites | 105 | In-house method, Accelerated solvent extraction, modified QuECheRS | HPLC-FLD, GC-MS | 5,11,13 |
Polycyclic aromatic hydrocarbon (PAH12) | Mussels, smoked freshwater fish | Battambang, Kampong Cham, Kampong Chhnang, Kandal, Koh Kong | Jetty, wharf wall, buoys, and rocks, processing sites | >87 (>30 + 57) | In-house extraction method, modified QuECheRS | GC-MS | 8 (Paper 8 did not specify the exact number of samples; instead, it stated that more than 30 samples were collected), 11 |
polybrominated diphenyl ethers (PBDEs) | Green mussels and blue mussels | Koh Kong, Koh Preab, Sihanoukville | Coastal water | 46 | Lipid extraction | GC-ECD | 3 |
Total bytyltin | Green mussels | Koh Kong, Sihanoukville | Fisheries sites and international and commercial harbors | 419 | Modified lipid extraction | GC-FPD | 4 |
Tri butyltin | Green mussels | Koh Kong, Sihanoukville | Fisheries sites and international and commercial harbors | 419 | Modified lipid extraction | GC-FPD | 4 |
Chemical Contaminant | Product | Minimum Concentration in mg/kg | Maximum Concentration in mg/kg | Average Concentration in mg/kg | % Exceeded National MRL (Mostly Based on Codex’s MRL) | % Exceeded the EU’s MRL/Action Level |
---|---|---|---|---|---|---|
Arsenic | Beef | 0.004 | 0.1 | 0.056 | NA | NA |
Arsenic | Beef viscera | 0.002 | 0.03 | 0.01 | NA | NA |
Arsenic | Egg | 0.02 | 0.06 | 0.04 | NA | NA |
Arsenic | Pork | 0.01 | 0.02 | 0.015 | NA | NA |
Benzo[a]pyrene | Fishery products | 0.005 | 0.9 | 0.13 | 94.29 | 100 |
Cadmium | Fish | 0.0003 | 0.28 | 0.035 | 9.09 | 9.09 |
Chloramphenicol | Freshwater fish | 0.03 | 1.18 | 0.255 | 100 | 100 |
Lead | Freshwater fish | <LOD | 0.31 | 0.05 | 5.88 | 5.88 |
Mercury | Beef | 0.004 | 0.02 | 0.01 | NA | NA |
Mercury | Beef viscera | 0.001 | 0.01 | 0.004 | NA | NA |
Mercury | Egg | 0.001 | 0.024 | 0.02 | NA | NA |
Mercury | Pork | 0.002 | 0.02 | 0.01 | NA | NA |
∑Organochlorine pesticides | Beef | 0.01 | 0.04 | 0.025 | 100 | 100 |
∑Organochlorine pesticides | Beef viscera | 0.007 | 0.19 | 0.05 | 100 | 100 |
∑Organochlorine pesticides | Egg | 0.009 | 0.028 | 0.018 | 100 | 100 |
∑Organochlorine pesticides | Fishery products | 0.008 | 0.04 | 0.019 | 100 | 100 |
∑Organochlorine pesticides | Pork | 0.009 | 0.14 | 0.01 | 100 | 100 |
Phthalate esters | Beef | 0.88 | 2.65 | 1.73 | NA | NA |
Phthalate esters | Beef viscera | 0.99 | 2.28 | 1.87 | NA | NA |
Phthalate esters | Fishery products | 0.92 | 2.26 | 1.59 | NA | NA |
Phthalate esters | Pork | 0.92 | 1.24 | 1.08 | NA | NA |
Polycyclic aromatic hydrocarbon (PAH 4) | Processed fishery products | 0.034 | 17.2 | 1.92 | NA | 100 |
Polycyclic aromatic hydrocarbon (PAH 12) | Mussels, processed fishery products | 0.021 | 17.2 | 4.05 | NA | NA |
Tributyltin (Wet weight) | Marine fish | 0.0024 | 0.088 | 0.015 | NA | NA |
Total butyl tin (wet weight) | Marine fish | 0.0024 | 0.15 | 0.027 | NA | NA |
Product | Hazard | Location | Concentration in mg/kg | Reference (See S1) |
---|---|---|---|---|
Mussels | PBDEs (mono-hepta) | Sihanoukville | 0.0053 | Paper 3 |
Mussels | PBDEs (mono-hepta) | Sihanoukville | 0.0023 | |
Mussels | HCB | Sihanoukville | <0.001 | |
Mussels | HCB | Sihanoukville | <0.001 | |
Fish | HCB | Kampong Cham | 0.00009 | Paper 17 |
Fish | HCB | Kratie | 0.00025 | |
Fish | HCB | Kandal | 0.00107 | |
Fish | CHLs | Kampong Cham | 0.00035 | Paper 17 |
Fish | CHLs | Kratie | 0.00111 | |
Fish | CHLs | Kandal | 0.0032 | |
Fish | DRINs (DRINs is the combination of aldrin, dieldrin, and endrin) | Kampong Cham | 0.00051 | Paper 17 |
Fish | DRINs | Kratie | 0.00065 | |
Fish | DRINs | Kandal | 0.00294 | |
Fish | Mirex | Kampong Cham | 0.00045 | Paper 17 |
Fish | Mirex | Kratie | 0.00031 | |
Fish | Mirex | Kandal | 0.00035 | |
Mussels | DDTs | Sihanoukville | 0.12 | Paper 3 |
Mussels | DDTs | Sihanoukville | 0.12 | |
Fish | DDTs | Kampong Cham | 0.00547 | Paper 17 |
Fish | DDTs | Kratie | 0.00949 | |
Fish | DDTs | Kandal | 0.023 | |
Mussels | PCBs | Sihanoukville | 0.3 | Paper 3 |
Mussels | PCBs | Sihanoukville | 0.2 | |
Mussels | CHLs | Sihanoukville | 0.0041 | Paper 3 |
Mussels | CHLs | Sihanoukville | 0.0025 | |
Mussels | HCHs | Sihanoukville | 0.0055 | Paper 3 |
Mussels | HCHs | Sihanoukville | 0.0072 | |
Fish | HCHs | Kampong Cham | 0.00101 | Paper 17 |
Fish | HCHs | Kratie | 0.00186 | |
Fish | HCHs | Kandal | 0.00572 |
Hazard | Name of Product | HI (Minimum) | HI (Maximum) | HI (Average) |
---|---|---|---|---|
Cadmium | Freshwater fish | 0.002 | 0.28 | 0.22 |
Mercury | Beef | 0.002 | 0.008 | 0.004 |
Mercury | Beef viscera | 0.0004 | 0.004 | 0.002 |
Mercury | Egg | 0.0004 | 0.01 | 0.008 |
Mercury | Fish | 0.5 | 1.0 | 0.75 |
Mercury | Pork | 0.002 | 0.01 | 0.008 |
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San, S.P.; Nicolaides, L.; Grace, D.; Charaslertrangsi, T.; Chamnan, C.; Thombathu, S.S.; Thorng, R.; Kong, L.; Noeurn, S.; Fidero, K.; et al. Chemical Hazards in Products of Animal Origin in Cambodia from 2000 to 2023: A Systematic Review and Meta-Analysis. Int. J. Environ. Res. Public Health 2025, 22, 1299. https://doi.org/10.3390/ijerph22081299
San SP, Nicolaides L, Grace D, Charaslertrangsi T, Chamnan C, Thombathu SS, Thorng R, Kong L, Noeurn S, Fidero K, et al. Chemical Hazards in Products of Animal Origin in Cambodia from 2000 to 2023: A Systematic Review and Meta-Analysis. International Journal of Environmental Research and Public Health. 2025; 22(8):1299. https://doi.org/10.3390/ijerph22081299
Chicago/Turabian StyleSan, Shwe Phue, Linda Nicolaides, Delia Grace, Tumnoon Charaslertrangsi, Chhoun Chamnan, Shetty Seetharama Thombathu, Ra Thorng, Leab Kong, Sreymom Noeurn, Kuok Fidero, and et al. 2025. "Chemical Hazards in Products of Animal Origin in Cambodia from 2000 to 2023: A Systematic Review and Meta-Analysis" International Journal of Environmental Research and Public Health 22, no. 8: 1299. https://doi.org/10.3390/ijerph22081299
APA StyleSan, S. P., Nicolaides, L., Grace, D., Charaslertrangsi, T., Chamnan, C., Thombathu, S. S., Thorng, R., Kong, L., Noeurn, S., Fidero, K., Ratana, C., Zand, N., & Chea, R. (2025). Chemical Hazards in Products of Animal Origin in Cambodia from 2000 to 2023: A Systematic Review and Meta-Analysis. International Journal of Environmental Research and Public Health, 22(8), 1299. https://doi.org/10.3390/ijerph22081299