PHILIPPINE FOODBORNE-DISEASE OUTBREAKS (19952004)

MA. PATRICIA V. AZANZA1

Department of Food Science and Nutrition

College of Home Economics
University of the Philippines 1101
Diliman, Quezon City, Philippines

Accepted for Publication September, 2004

ABSTRACT

The study presented details about 60 reported Philippines foodborne

outbreaks for the period of 19952004. It was established that meat-
containing dishes were the more common causes of the outbreaks evaluated,
with spaghetti as the leading food vehicle. Common risk settings for the
outbreaks were the food services of schools and workplaces. Salmonella and
Vibrio spp. were cited as the primary causes of infections, while human
intoxications involved staphylococcal enterotoxins, paralytic shellfish poison-
ing (PSP) toxins and histamine.

INTRODUCTION

The continued and increased awareness of the significance of food safety

worldwide further emphasized the need for the systematic monitoring of
foodborne-disease outbreaks (Archer 2002). Collected data from these out-
breaks should allow the evaluation of outbreak trends based on etiologic
agents, food vehicles and venues. Food regulatory agencies involved in the
implementation of food-hygiene systems must rely heavily on these surveil-
lance data for the appropriate formulation of the prevention and control
measures for food safety. Unfortunately, an effective and working national
food-safety program for the Philippines is yet to be realized. The recent
upsurge in the number of foodborne-disease outbreaks in the country attest to
this situation. For the period of March to April 2005 alone, at least 7 major
outbreaks were reported involving more than 200 morbidities and 27 mortali-
ties. Epidemiologic information from past outbreaks could well serve the
country in coming up with a more comprehensive approach to a food-safety

1
Corresponding author. TEL: (632) 920-5473; FAX: (632) 928-6512; EMAIL: ma_patricia.azanza@
up.edu.ph

Journal of Food Safety 26 (2006) 92102. All Rights Reserved.

92 2006, The Author(s)
Journal compilation 2006, Blackwell Publishing
 FOODBORNE DISEASES 93

system. The objective of this article was to present trends in the foodborne-
disease outbreaks for the period of 19952004.

MATERIALS AND METHODS

Data from 60 foodborne outbreaks in 19952004 from the Field Epide-

miology Training Program, Department of Health (DOH) of the Philippines
and the health advisories released at the DOH website were reviewed and used
as compilation sources. The information were categorized and evaluated in
terms of associated food vehicles, etiologic agents, venues of outbreaks and
morbidity and mortality cases. Relative percentages were calculated for the
compiled statistics.

RESULTS AND DISCUSSION

Food Vehicles of Outbreaks

Table 1 presents the various food types that were implicated in the 1999
2004 Philippine foodborne-disease outbreaks evaluated in the study. Meat-
containing dishes and processed meat products were found to be the more
common causes of the outbreaks. Interestingly, spaghetti with meat sauce was
shown to be the leading food vehicle causing the local outbreaks during the
period evaluated. At least two new reported disease outbreaks again implicated
the consumption of spaghetti with meat sauce in the first half of 2005, thus
establishing more than 80 morbidities per outbreak (DOH 2005; Manila Times
2005). The use of low-cost and inferior quality minced meat as ingredient,
quantity preparation with extended hold-on at ambient temperatures of final
product, multiple handling during portioning of the dish and inadequate
reheating are specific conditions that are typically used in the preparation and
handling of spaghetti with meat sauce in many food-service establishments,
and households were also previously cited to increase the safety risks of the
dish (Azanza and Ortega 2000).
The inadequate cooking of some meat dishes by flash heating will result in
the immediate oxidation or burning of outer portions of meat cuts like those that
are roasted or fried at high temperatures, and may help explain in part the
involvement of such types of dishes in the evaluated outbreaks. Immediate
burning of the outer portions of meat before the inner sections are fully cooked
may possibly cause the subsequent impaired heat transfer in the flash-heated
meat. Two recent outbreaks of local food poisoning involved whole roasted pig
with a recorded 52 and 28 morbidities which occurred at Calinan, Mindanao and
94 MA. P.V. AZANZA

TABLE 1.
FOODBORNE-DISEASE OUTBREAKS IN THE PHILIPPINES CLASSIFIED BY
INCRIMINATED FOOD TYPES FROM 1995 TO 2004 (N = 60)

Food type Occurrence Relative percentage (%)

Meat-based dishes and processed meat products

Spaghetti with meat sauce 9
Pork dishes (stewed, roasted) 4
Fried processed meats (hotdog, sausage, deli meat) 3
Water-buffalo meat dish 2
Fried chicken 1
Subtotal 19 32
Fish and other seafood dishes
Fish dishes (albacore, mackerel, round scad, milkfish) 7
Shellfish dishes (oyster, green mussel) 2
Shrimp salad 1
Fried fishball 1
Fried calamari 1
Subtotal 12 20
Bakery and confectionery products
Cakes and pies (rice cake, egg pie, custard roulade) 4
Egg sandwich 2
Chocolate mousse 1
Bread roll with custard filling 1
Cream puff 1
Sweet bread with salted egg and cheese 1
Subtotal 10 17
Toxin-containing or unedible materials
Wild mushrooms (Amanita sp., Psilocyb sp. and 3
Chlorphyllum molybdite)
Big purge nut (Jatropha curcas) 2
Puffer fish 2
Wild yam (Dioscorea hispida) 1
Subtotal 8 13
Other dishes
Stir-fried noodles (rice and egg noodles) 3
Rice congee 1
Fried spring roll with sauted coconut pith 1
Gravy 1
Subtotal 6 10
Beverages
Juice (strawberry, soursop) 2
Distilled fermented coconut toddy 2
Tapioca pearl, agar-agar light syrup 1
Subtotal 5 8

Total 60 100
 FOODBORNE DISEASES 95

Danao City, Cebu in the Philippines, respectively (ABS-CBN News 2005;

Villaflor 2005). Another recent family outbreak implicating a meat dish is a stew
prepared from pork meat, innards and blood, popularly called dinuguan, which
was reported last January 2005 with 1 mortality and 7 morbidities (Balnig
2005).
Fish and other seafood dishes, bakery and confectionery food items
ranked second while local beverages and a mixed group of food items ranked
last as food vehicles of the outbreaks evaluated. It is not unexpected to have
fishery products and dishes to be among the food vehicles of foodborne-
disease outbreaks in the Philippines because it is an archipelagic country and
therefore has a rich supply of seafood. A recent reported outbreak because of
the consumption of spoiled mackerel scad involved the death of an 8-year-old
boy and the hospitalization of 23 others in Negros Occidental (Balita 2005).
It is significant to note that among the bakery and confectionery products
implicated in the outbreaks, those containing egg as a major ingredient such as
egg sandwiches and custard-filled pies were identified in the evaluated out-
breaks. Eggs are established as a major vehicle of foodborne-disease outbreaks
worldwide particularly in those implicating pathogenic Salmonella spp. (Gast
and Holt 2000).
Involvement of nontraditional foods that need special preparation proce-
dures to render it safe for consumption and other materials which are actually
not edible were interestingly also identified as causative agents in the out-
breaks evaluated. Tubers of the wild yam (Dioscorea hispida), which contains
the toxic alkaloid dioscorine, have also been reported to cause death in the
country (Roces et al. 2000). The tubers of this wild yam can be rendered edible
only after repeated washing, soaking in water or brine, boiling and drying. The
wild mushrooms in the evaluated foodborne outbreaks that caused human
intoxications belonged to the Psilocyb and Amanita genera. Poisonings
because of these wild mushrooms were linked to cardiac toxicity and liver
damage (Parish and Doering 1986; McPartland et al. 1997). Just recently, five
residents of a village in Kidapawan City, Sultan Kudarat, were rushed to a
hospital for wild mushroom poisoning (Tupas 2005).
Puffer fishes, which are known to contain the neurotoxin tetradotoxin in
its skin, liver, blood and gonads, also require expert preparation to render it
safe for consumption (PCHRD 2005). Recently, a 45-year-old mother died
while her two children and a son-in-law were hospitalized after eating puffer
fish for dinner (Masqueda 2005).

Morbidity and Mortality Records

Table 2 presents the various locations where the evaluated foodborne-
disease outbreaks occurred. The reported morbidity cases were shown to be
96 MA. P.V. AZANZA

TABLE 2.
OUTBREAK LOCATION FOR PHILIPPINE FOODBORNE
DISEASE FROM 1995 TO 2004 (N = 60)

Percentage (%)

Occurrence Morbidity Mortality

Home 43 18 96
Workplaces 20 39 4
Schools 15 24 0
Restaurants 12 8 0
Unknown 10 11 0

TABLE 3.
RANKING OF CAUSATIVE AGENTS OF FOODBORNE POISONING IN THE PHILIPPINES
BASED ON RECORDED MORBIDITY CASES IN 19952004 (N = 3313 CASES OUT OF
60 OUTBREAKS)

Type of food poisoning Cases Percentage (%)

Microbiological Chemical/Toxin

Salmonella spp. 985 30

Staphylococcal enterotoxin 767 23
480* 15
Vibrio parahaemolyticus 336 10
Paralytic shellfish poisoning toxin 144 4
Vibrio cholerae 144 4
Histamine 124 4
Aeromonas spp. 73 2
Escherichia coli 70 2
Psylocibin/Psilocin 39 1
Ciguatoxin 38 1
Jatropha curcas toxin 25 1
Nitrite 25 1
Tetradotoxin 21 1
Amatoxin 17 1

* Unclassified.

mainly outbreaks occurring outside the home, particularly in workplaces and

schools. However, it has been cited that caution should be practiced in inter-
preting the results of the locations of outbreaks, because incidences in com-
mercial food-service settings are likely to receive more publicity and scrutiny
than those that occurred in households (Sumner et al. 2000).
Table 3 presents in detail the etiologic agents that caused the recorded
morbidity cases under study. Salmonella and Vibrio spp. were established as
 FOODBORNE DISEASES 97

the primary causes of infections, while human intoxications were attributed

mainly to staphylococcal enterotoxins, paralytic shellfish poisoning (PSP)
toxins and histamine. Salmonella human infections are among the more sig-
nificant causes of worldwide morbidity and mortality. The infections may
cause life-threatening illnesses like typhoid fever and various forms of food-
borne salmonellosis, which are caused by Salmonella enterica typhi and
Salmonella enteriditis or Salmonella typhymirium, respectively (Glynn and
Bradley 1992; Xiao-Li et al. 2003). Salmonella infections generally cause
nausea, vomiting, abdominal pain, diarrhea, fever and headache with the
symptoms appearing only after about 2 days of incubation (Jay et al. 1997).
Virulent vibrios include several pathogens, which can elicit a spectrum of
clinical illnesses like acute diarrheal cholera and the self-limiting diarrheal
form caused by Vibrio cholerae and Vibrio parahaemolyticus, respectively.
Human cholera infection, with a relatively short incubation period of 24 to
48 h, is characterized by profuse watery stool, vomiting and leg cramps
(Yamamoto et al. 1983). The rapid loss of body fluids and electrolytes may
lead to dehydration and shock. The major clinical manifestations of human
V. parahaemolyticus infection include diarrhea which can be bloody
abdominal pain, nausea and vomiting following a short incubation of 4 to 30 h
(Sakazaki and Shimada 1986). Staphyloenterotoxicosis is a type of food
intoxication characterized by profuse vomiting and diarrhea occurring about
2 to 8 h after consumption of food containing staphylococcal enterotoxin
(Mossel et al. 1995). The clinical manifestation of the illness is rarely fatal but
can cause in a short duration complete incapacitation of the victim (Bergdoll
1989).
PSP outbreaks in the Philippines are associated mainly with seafoods like
mussels, oysters and scallops as food vehicles (Sidharta et al. 1999). The PSP
outbreaks involve the gastrointestinal, neural and respiratory systems with
symptoms that include numbness, general body malaise, dizziness, vomiting
and abdominal pain (Pastor et al. 1989). The reported cases ranged from mild
to severe and sometimes led to death mainly because of respiratory failure
(Pastor and Corrales 1989).
Histamine poisoning is also known as scombroid-fish poisoning because
of the usual involvement of the fish species belonging to the Scombridae and
Scomberesocidae families (e.g., tuna, bonito, mackerel) (Taylor et al. 1979).
The symptoms of histamine poisoning generally include: nausea, vomiting,
diarrhea, an oral-burning sensation or peppery taste, hives, itching, red rashes
and hypertension appearing a few hours up to 24 h after ingestion of the
implicated food (Taylor et al. 1989).
Recorded mortalities were attributed primarily to PSP, methanol and
tetradotoxin as the causative agents (Table 4). Several previous mortalities
because of the consumption of edible shellfishes and other filter-feeding
98 MA. P.V. AZANZA

TABLE 4.
RANKING OF CAUSATIVE AGENTS OF FOODBORNE
POISONING IN THE PHILIPPINES BASED ON RECORDED
MORTALITY CASES IN 19952004 (N = 25 CASES OUT OF
60 OUTBREAKS)

Causative agent Percentage (%)

Paralytic shellfish poisoning toxin 34

Tetradotoxin 19
Methanol 19
Dioscorine 8
Arsenic 8
Unclassified 8
Nitrite 4

animals were established to be contaminated with the toxic dinoflagellate

Pyrodinium bahamense var. compressum that produce the neurotoxin saxitoxin
(Sidharta et al. 1999). Puffer fish poisoning is likewise sporadically identified as
the causative agent of foodborne outbreaks because it also contains the neuro-
toxin tetradotoxin (PCHRD 2005). The anomalous adulteration of local dis-
tilled spirits from fermented coconut toddy has been the major cause of the
rather peculiar methanol poisoning in the country. Methanol poisoning can
cause extremely hazardous intoxication with the onset of metabolic acidosis
followed by optical symptoms progressing to visual impairment (McKellar
et al. 1997). Prognosis for the intoxication is positive if early treatment protocol
is used, which involves: the administration of alkali for the acidosis, use of
ethanol as an antimetabolite and hemodialysis to remove the alcohols and its
toxic metabolite from circulation (Jacobsen and McMartin 1986).

RECOMMENDATIONS

Although the data presented in the study may be a severe understatement

of the actual number of outbreaks that did occur for the period 19952004 in
the Philippines, some significant information was established that can be used
as the basis for sound, local public health actions. Considering that meat-
containing dishes were found to be the leading food vehicles in the outbreaks
evaluated, it would be pertinent for food-regulatory agencies in the country to
disseminate the appropriate information to correct the faulty food preparation
and handling practices for these types of foods in both foodservice institutions
and local households. The Philippine National Meat Inspection Services,
Department of Agriculture in coordination with the local Bureau of Food and
 FOODBORNE DISEASES 99

Drug (DOH) must include in their community-education extension efforts

activities that address issues related to the safe handling, processing, storage
and preservation of meat and meat products. The sanitarians of the various
health units of the Department of Interior and Local Government (DILG) must
also consider the results of the evaluation of foodborne outbreaks in the
country as presented in this article in the hygiene courses that they provide to
food handlers of commercial foodservice institutions in their introductory or
annual refresher courses on food safety.
Review of current regulatory food audits for food-service establishments
must be undertaken specifically for those in schools and workplaces, as these
were identified as the crucial risk settings for foodborne outbreaks in recent
years. The existing system of the food-safety audits conducted by food-
hygiene inspectors of the DILG units for commercial food services like
schools and work places in the country are still entirely based on a walk-
through assessment of good manufacturing procedure (GMP) implementation.
Unfortunately, most of the sanitarians doing the audit are even ill-prepared to
do a basic GMP audit. The concept of a hazard analysis critical control point
(HACCP) system is yet to be introduced to this group of food-hygiene audi-
tors. The updating of the level of competency of the sanitarians on food-safety
audits for commercial establishments must be immediately be implemented to
prevent further involvement of commercial food services with foodborne-
disease outbreaks.
Public health authorities must also study and promote education based on
the unique involvement of nontraditional foods that need special preparation
procedures to render it safe for consumption and other materials that were not
even edible. Food-safety education of mothers may perhaps be one of the more
effective strategies in minimizing the problems from nontraditional and ined-
ible foods. The health care centers in the various townships in the country may
sponsor seminars for mothers and other food handlers to help identify risky
foods and explain the hazards that may befall their families because of the
consumption of nontraditional foods and most specifically, the inedible mate-
rials. Likewise, parallel teaching of health-education teachers of schools who
can subsequently inform their students about it to further prevent consumption
of these risky materials.
Overall, public food-safety education must be strongly advocated and
implemented to help avert the various causes of foodborne-disease outbreak in
the country. The recommended steps presented in this article are geared toward
increased education of those concerned including: industry stake-players, the
general public and food-regulatory agencies. Well-educated food-regulatory
personnel are expected to be in a better position to provide effective services,
while the recipients of these services who are also well informed are likely to
follow appropriately the guidelines provided to them.
100 MA. P.V. AZANZA

REFERENCES

ABS-CBN NEWS. 2005. Food poisoning downs 56 people. http://www.abs-

cbnnews.com/storypage (accessed May 3, 2005).
ARCHER, D.L. 2002. Global foodborne disease surveillance system faces
hurdles. Food Technol. 56(2), 24.
AZANZA, M.P.V. and ORTEGA, M.P. 2000. Terminal report: Application of
HACCP to small scale fastfood establishments. Office of Research Coor-
dination (ORC)-Project No. 001. University of the Philippines, Diliman,
Quezon City, Philippines.
BALITA. 2005. Seven downed by galunggong in Silay City. http://
news.balita.ph/html/public (accessed May 12, 2005).
BALNIG, J.D. 2005. Toddler dies: 7 confined due to food poisoning.
http://www.sunstar.com.ph/static/ilo/2005/01/07/news/toddler.dies.7.
confined.due.food.poisoning.html/externallink (accessed May 12,
2005).
BERGDOLL, M.S. 1989. Staphylococcus aureus. In Foodborne Bacterial
Pathogens (M.P. Doyle, ed.) pp. 463523, Marcel Dekker, New York,
NY.
DEPARTMENT OF HEALTH (DOH). 2005. Spaghetti downs 84 persons in
Tarlac. Press release by the Office of the Secretary, Department of Health,
Philippines (Media Relations Unit). http://www.news.balita.ph/html/
public_html/article.php?story=20050317193530002 (accessed March
17, 2005.
GAST, R.K. and HOLT, P.S. 2000. Influence of the level and location of
contamination in the multiplication of Salmonella enteritidis at different
storage temperatures in experimentally inoculated eggs. Poult. Sci. 79,
559563.
GLYNN, J.R. and BRADLEY, D.J. 1992. The relationship between infecting
dose and severity of disease in reported outbreaks of Salmonella infec-
tions. Epidemiol. Infect. 109, 371388.
JACOBSEN, D. and MCMARTIN, K.E. 1986. Methanol and ethylene glycol
poisonings: Mechanism of toxicity, clinical course, diagnosis and treat-
ment. Med. Toxicol. 5, 309334.
JAY, L.S., GRAU, F.H., SMITH, K., LIGHTFOOT, D., MURRAY, C. and
DAVEY, G.R. 1997. Salmonella. In Foodborne Microorganisms of
Public Health Significance, 5th Ed. (A.D. Hocking, G. Arnold, I. Jenson,
K. Newton and P. Sutherland, eds.) pp. 169230, Australian Institute of
Food Science and Technology, Inc., New South Wales, Australia.
MANILA TIMES. 2005. Spoiled spaghetti downs 83 in Manaoag. http://
www.manilatimes.net (accessed April 26, 2005).
 FOODBORNE DISEASES 101

MASQUEDA, M., 2005. Puffer fish kills mother, downs 3 other. http://
www.mb.com.ph/issues/2004/09/16/Prov200409618619.html (accessed
May 12, 2005).
MCKELLAR, M.J., HIDAJAT, R.R. and ELDER, M.J. 1997. Acute ocular
methanol toxicity: Clinical and electrophysiological features. Aust. NZ.
J. Ophthalmol. 3, 225230.
MCPARTLAND, J.M., VILGALYS, R.J. and CUBETA, M.A. 1997. Mush-
room poisoning. Am. Fam. Physician 55, 17971800, 18051809.
MOSSEL, D.A., CORRY, J.E., STRUNK, C.B. and BAIRD, R. 1995. Essen-
tials of the Microbiology of Foods: A Textbook for Advanced Studies, pp.
147150, John Wiley and Sons Ltd, West Sussex, U.K.
PARISH, R.C. and DOERING, P.L. 1986. Treatment of Amanita mushroom
poisoning: A review. Vet. Hum. Toxicol. 28(4), 318322.
PASTOR, N.I. and CORRALES, R.A. 1989. Discussion on medical and
epidemiologic issues. In Biology, Epidemiology and Management of
Pyrodinium Red Tides, Proceedings of the Management and Training
Workshop, Bandar Seri Begawan, Brunei Darussalam (G.M. Hallegraff
and J.L. Maclean, eds.), Fisheries Department, Ministry of Development,
Bandar Seri Begawan, Brunei Darussalam and International Center for
Living Aquatic Resources Management, Metro Manila, Philippines, pp.
173178.
PASTOR, N.I., GOPEZ, I., QUIZON, M.C., BAUTISTA, N., WHITE, M. and
DAYRIT, M. 1989. Epidemics of paralytic shellfish poisoning in the
Philippines, 19881989. In Biology, Epidemiology and Management of
Pyrodinium Red Tides, Proceedings of the Management and Training
Workshop, Bandar Seri Begawan, Brunei Darussalam (G.M. Hallegraff
and J.L. Maclean, eds .), Fisheries Department, Ministry of Development,
Bandar Seri Begawan, Brunei Darussalam and International Center for
Living Aquatic Resources Management, Metro Manila, Philippines, pp.
165172.
PHILIPPINE COUNCIL FOR HEALTH RESEARCH AND DEVELOP-
MENT (PCHRD). 2005. Puffer fish poisoning. http://www.pchrd.dost.
gov.ph/PCHRD/ARCHIVES/healthissues/puffer-01.html (accessed May
12, 2005).
ROCES, M.C., ABAD-VIOLA, G., VILLANUEVA, N.L., GUZMAN, J.C.,
BUGTONG, J.Z. and LONGID, C. 2000. Nami kalot poisoning out-
break, Bakun, Benguet, November 1999: Internal report. Field Epidemi-
ology Training Program Scientific Papers 13(6), 97100.
SAKAZAKI, R. and SHIMADA, T. 1986. Vibrio species as agents of
food-borne infection. In Development in Food Microbiology, Vol 2
(R.K. Robinson, ed.) pp. 12315, Elsevier Applied Science, London,
U.K.
102 MA. P.V. AZANZA

SIDHARTA, B.R., AZANZA, R.V. and AZANZA, M.P.V. 1999. Studies on

associated bacteria of Pyrodinium bahamense var. compressum in
culture: Some preliminary results. Proceedings of the 9th JSPS Joint
Seminar on Marine and Fisheries Sciences, Lembaga Ilmu Pengetahuan
Indonesia, Jakarta, Indonesia, and Japan Society for the Promotion of
Science, Tokyo, Japan, pp. 6370.
SUMNER, J.L. ROSS, T. and MCMEEKIN, T.A. 2000. Food poisoning rate
in Australia: An alternative view. Food Aust. 52(7), 34, 274276.
TAYLOR, S.L., GUTHERTZ, L.S., LEATHERWOOD, M. and LIEBER, E.R.
1979. Histamine production by Kleibsiella pneumoniae and incident of
scombroid fish poisoning. Appl. Environ. Microb. 37, 274278.
TAYLOR, S.L., STRATTON, J.E. and NORDLEE, J.A. (1989) Histamine
poisoning (scombroid fish poisoning) and allergy-like intoxication. J.
Toxicol.-Clin. Toxic. 27(45), 225240.
TUPAS, J.M. 2005. Poisoning mushrooms down 5. Sun Star Network Online.
http://www.sunstar.com.ph/static/net/2005 (accessed May 7, 2005).
VILLAFLOR, M.M. 2005. Contaminated food, 52 suffer diarrhea after eating
at party. http://www.mindanaotimes.com.ph/news/story (accessed May
12, 2005).
XIAO-LI, S., ZHANG, Z., KIN, B. and LI, Y. 2003. Capillary Immunosensing
System for Rapid Detection of Salmonella typhimurium. ASABE
Technical Library. Paper No. 037061, ASAE Technical Meeting. http://
asae.flymulti.com/abstract.asp?aid=14182&t-2 (accessed September 19,
2005).
YAMAMOTO, K., TAKEDA, Y., MIWATANI, T. and CRAIG, J.P. 1983.
Evidence that non 01 Vibrio cholera produces enterotoxin similar but not
identical to cholera enterotoxin. Infect. Immun. 41, 896901.