Pig-to-monkey Ebola: is there something in the air?

Ebola has long been known to be a zoonotic virus–one which jumps between species. Though it took several decades to find evidence of Ebola virus in bats, these animals had previously been associated with human index cases of Ebola disease have worked in bat-infested warehouses or traveled to caves where bats roost. Non-human primates have also become infected with the virus, sometimes transmitting the virus to humans when killed primates are butchered for food. Ebola has also been suggested to infect dogs and other wild animals. However, livestock are a newer angle to Ebola virus ecology.

Ebola was first found in pigs in 2008 in the Philippines. This was the Reston virus, named after its discovery in imported Filipino monkeys in a facility in Reston, Virginia, in 1989. Though this virus spread among the captive monkeys, no humans came down with symptoms. However, follow-up studies showed that some humans did develop an immune response to the Reston virus–suggesting they had been infected, even if they didn’t realize it. At the time, there was suggestion that perhaps Reston might be spread via aerosol, as the virus appeared to spread amongst monkeys in two different rooms who did not come into physical contact with one another. However, this was not proven at the time and alternative explanations were possible.

When Reston resurfaced in swine and swine farmers in 2008, a similar phenomenon was observed. Though it was not known how the pigs initially became infected with the virus, they did appear to be able to spread it to humans working amongst them, even if those farmers didn’t have contact with blood or other secretions (the most efficient way to transmit Ebola viruses). Suggestive of possible transmission from pigs to people via air, but far from conclusive. Since then, two experimental studies have examined airborne transmission of Ebola via pigs.

The first study examined transmission of the Zaire strain of Ebola–the nastiest one, which can kill up to 90% of those infected–within laboratory pigs. Pigs were inoculated with the Zaire virus and housed with uninfected pigs, who were later tested and found to have acquired the virus. Interestingly, when the pigs got sick with Ebola Zaire, the symptoms were mainly respiratory and the virus replicated in the lungs. This was quite unlike what Zaire does in humans and our other primate cousins, where it’s a systemic disease and we can find virus in the blood. This suggests that pigs could be infected with even nasty types of Ebola, and we wouldn’t realize it.

Last week, Ed Yong reported on a new paper examining transmission of Zaire virus from experimentally-infected pigs to co-housed macaques. Like the previous paper, they observed that Ebola in pigs was a respiratory disease, and that it could spread to other animals (in this case, non-human primates). The macaques they tested developed the symptoms of Ebola that were expected–a systemic disease, with virus isolated from the blood. In this study, they also added in an air sampling component, and were able to detect evidence of virus (via PCR) in the air. However, the authors do note that this could have been aerosolized in other manners than directly from the exhaling pigs (such as during the floor-cleaning process). Finally, even if it does become aerosolized and spread in this manner, as noted in Ed’s article, Ebola is not “suddenly an airborne virus, like influenza.” Certainly more efficient transmission takes place via close contact with infected secretions during hospital procedures and funeral rites.

Interestingly, the authors note that other experimental studies that have looked specifically at airborne, primate-to-primate transmission of Ebola have come up negative, and that swine are known to generate “infectious short range large aerosol droplets more efficiently then other species.” Is there something specific about pig physiology that may make them better respiratory virus shedders? We know that pigs can be intermediate hosts for other viral pathogens as well, such as Nipah virus and of course influenza.  Are pigs playing any role in Ebola ecology, either in Asia or Africa? Might Ebola have more airborne potential than we previously thought? According to Ed, the authors of the second study are currently working on field studies in Africa to examine the pig question outside of the laboratory. The timing may be good for them, as Uganda is currently experiencing another Ebola outbreak;–the country’s third Filovirus outbreak in five months.


Weingartl, H., Embury-Hyatt, C., Nfon, C., Leung, A., Smith, G., & Kobinger, G. (2012). Transmission of Ebola virus from pigs to non-human primates Scientific Reports, 2 DOI: 10.1038/srep00811

“Spillover” by David Quammen

Regular readers don’t need to be told that I’m a bit obsessed with zoonotic disease. It’s what I study, and it’s a big part of what I teach. I run a Center devoted to the investigation of emerging diseases, and the vast majority of all emerging diseases are zoonotic. I have an ongoing series of posts collecting my writings on emerging diseases, and far too many papers in electronic or paper format in my office to count. Why the fascination? Zoonotic diseases have been responsible for many of mankind’s great plagues–the Black Death, the 1918 “Spanish” flu pandemic, or more recently, HIV/AIDS. So you can imagine my delight when I read about Spillover, a new book by David Quammen on zoonotic diseases.

I’ve previously highlighted some of Quammen’s work on this site. That link goes to a 2007 story he wrote for National Geographic on “infectious animals,” which really serves as a preview to “Spillover,” introducing some of the concepts and stories that Quammen elaborates on in the book.

“Spillover” is wide-ranging, tackling a number of different infectious agents, including viruses like Nipah, Hendra, and Ebola; bacteria including Coxiella burnetii and Chlamydia psittaci; and parasites such as Plasmodium knowlesi, a zoonotic cause of malaria. HIV is a big part of the story; Quammen devotes the last quarter or so of the book to tracing the discovery and transmission of HIV from primates to humans, and from 1900 to present-day. He even takes the time to explain the basic reproductive number–something that’s not always a page-turner, but Quammen manages to do it well and without being too tangential to the rest of the story; much more of a Kate-Winslet-in-Contagion than Ben-Stein-in-Ferris Bueller delivery.

Indeed, “Spillover” is somewhat unique in that it doesn’t read quite like your typical pop science book. It’s really part basic infectious disease, part history, part travelogue. Quammen has spent a number of years as a correspondent for National Geographic, and it shows. The book is filled with not only well-documented research findings and interviews with scientists, but also with Quammen’s own experience in the field, which gives the book a bit of an Indiana Jones quality. In one chapter, he details his adventure tagging along with a research team to capture bats in China, entering a cave that “felt a little like being swallowed through the multiple stomachs of a cow.” This was after an earlier dinner in which he describes his encounters with the an appetizer of the “world’s stinkiest fruit” (I’ll keep the description of the smell to myself) with congealed pig’s blood for a main dish (bringing to mind the scooping out of monkey’s brains in “Temple of Doom”–and the various zoonotic diseases that could be associated with those, come to think of it).

Quammen’s book is an excellent, and entertaining, overview of the issues of zoonotic disease–why do they emerge? Where have they come from? How do they spread? The only thing that’s missing is more of a cohesive discussion about what to do about them. However, that’s rather understandable, as we certainly have less of a grasp of this question than we do about the others (and even with some of those, our knowledge is spotty at best). I hope “Spillover” will inspire another generation of future germ-chasers, as “The Coming Plague” did almost 20 years ago.

Going out with a Bangs: Control of Human Brucellosis by means of an Animal Vaccine

This is the thirteenth of 16 student posts, guest-authored by Jessica Ludvik. 

One Disease, Many Species

Brucellosis, more commonly known as undulant fever in humans or bangs disease in cattle, is one of the oldest bacterial scourges of livestock-producing nations, especially those in which the animals live in close proximity with the human population.  The disease is caused by bacteria of the genus Brucella.  Within this category are many species of bacteria, each almost exclusive to a particular animal species.  A few of the most common seen in veterinary and human medicine today are listed in Table 1.  Of these, all but B. ovis has been shown to be transmissible to humans [1].

Why Should I care about Brucellosis?

            The presence of Brucellosis in a region is catastrophic to the economy and animal and human health.  In many livestock species, the bacteria elicits its major effects on the reproductive system, leading to late term abortions and stillbirths in females, weak newborns leading to death soon after birth, and inflammation of the testicles and testicular abscesses in males [2].  Abortion storms of 30-80% have been documented in cattle herds infected by B. abortus [2].  B. abortus and B. melitensis are the most common of the strains associated with human infection, and the World Health Organization (WHO) estimates that 500,000 new cases of human cases of human Brucellosis occur annually, making it the most common zoonotic disease in the world [3].  Its importance has earned it a spot on the Center for Disease Control’s (CDC) 2012 list of Nationally Notifiable Conditions.  To view this list visit the CDC’s website at http://www.cdc.gov/osels/ph_surveillance/nndss/phs/infdis.htm.

Symptoms include fever, profuse sweating, headache, fatigue, depression, loss of appetite, irritability, cough, chest pain, and upset stomach [1].  It can also affect bones and joints causing arthritis [1].  If untreated, symptoms may recur after a latent period of many years [1].  For the official case definition, click http://www.cdc.gov/osels/ph_surveillance/nndss/casedef/brucellosis_current.htm. 

What’s the Risk?

            Most human cases of Brucellosis are a result of occupational exposure to the bacteria [2].  It can penetrate mucus membranes of the digestive or respiratory tract, or can enter through skin wounds or abrasion after contact with reproductive fluids, aborted fetus or placenta, or aerosolized particles from the aforementioned [2].  Brucellosis can also be contracted by people via accidental injection with the cattle vaccine or by ingestion of unpasteurized dairy products of infected animals [2].

Most people diagnosed with Brucellosis recover fully with treatment, which usually consists of a six to eight week antibiotic regimen [4].  Less than 2% of untreated individuals die, however chronic complications such as endocarditis and meningitis may occur [2].

On the Global Scale….

Figure 1: Worldwide incidence of human Brucellosis [5] Click to enlarge.

As the major mode of human infection is through direct contact with infected animals otr through the consumption of products from those animals, the most logical means of disease prevention in the human population has been through the prevention of the disease in animals.  Many developed regions such as North America, Australia, and Northern Europe have dramatically reduced the prevalence of brucellosis in livestock through widespread vaccination efforts [5].  The United States Department of Agriculture (USDA) implemented an eradication program in 1934, which involved the testing and identification of diseased animals, slaughter of infected animals, and trace back and investigation of their herds of origin [2].  In 1951, Animal Plant Health Inspection Services (APHIS) made compliance of all states mandatory [2].   Currently, RB51 vaccine is the standard in cattle and Rev-1 vaccine in goats.  Both of these are attenuated live vaccines, which are strains of bacteria that cause a similar but less severe infection in the vaccinated individual, so the animal’s immune system will respond to and eliminate the agent.  Immune cells then remember the bacteria, so that if the animal is exposed to the wild type strain of bacteria, it will destroy it before it becoming infected.  One of the advantages of the RB51 vaccine that has helped to make testing for the disease effective is that the vaccine strain lacks a specific surface molecule that the wild type strain of bacteria possesses, so tests can distinguish between diseased cattle and those vaccinated with RB51 [1].  The Program has decreased the number of infected herds in the US from 124,000 in 1957, to 2 as of December 2003 [2].  These vaccines are not approved for human use, and as mentioned before may actually cause clinical illness if accidently injected into the handler [1].

In February of 2008, all States in the US were classified as disease-free [6].  In September of that year however, the states of the Greater Yellowstone Area (GYA), Montana, Wyoming, and Idaho lost their disease-free status [6].  For more information on this, see APHIS’s website at http://www.aphis.usda.gov/newsroom/content/2009/10/printable/brucellosis_concept_paper.pdf.  What was the source of the infections that triggered this revocation?  Brucellosis is endemic in the herds of elk and bison in the area.  8-60% of elk herds and 11-75% of bison herds were positive for B. abortus by serologic tests [7].  Studies of mapping the molecular profiles of the isolates from this area show that cattle are more likely to be infected by elk than bison, and indicate that there may be a possibility of transmission between cattle and feral pigs, though it is unclear of the direction [7].  These wild reservoirs pose another significant barrier to the complete eradication of the disease in the US.

In the Future

The issue of wildlife reservoirs for Brucellosis will need to be addressed to prevent transmission of the disease to people, especially those at particularly high risk of infection by this route, such as hunters, hikers, and campers.  Some proposed strategies include the daunting tasks of selectively culling bison herds and vaccinating elk and bison [7].

Control of human Brucellosis through vaccination of livestock has been successful thus far because it virtually eliminates our exposure to the infectious agent, so it is a sort of indirect prevention. But how will we prevent disease outbreak should we be exposed by a different means?  There is no human vaccine for Brucellosis, it can be aerosolized, and it only takes 10-100 organisms to cause disease in humans [1].  All these characteristics make it a possible agent of bioterrorism [1].  Although the mortality rate is low, the morbidity rate is high, so an outbreak would cause a tremendous consumption of money and resources to treat the affected, and a dramatic decrease in workforce and morale. Control of human Brucellosis is another area in which we must not allow ourselves to fall victims to our own success.  We must continue to support the vigilant monitoring and livestock vaccination efforts and encourage efforts in the development of a vaccine that is safe and effective for use in humans.


[1]         Ficht, TA, and LG Adams. Brucellosis. Vaccines for Biodefense and Emerging and Neglected Disease. Elsevier Inc. 2009. Ch 42.

[2]         http://www.cfsph.iastate.edu/DiseaseInfo/disease.php?name=brucella-abortus&lang=en. Accessed 9 June, 2012.

[3]         Atluri, VL, MN Xavier, MF de Jong, AB den Hartigh, RM Tsolis. Interactions of the Human Pathogenic Brucella Species in Their Hosts. Annual Review of Microbiology. 2011. 65:523-41.

[4]         Solis Garcia del Pozo, J, J Solera. Systematic Review and Meta-Analysis of Randomized Clinical Trials in the Treatment of Human Brucellosis. PloS One. 2012. 7(2):e32090.

[5]         Pappas, G, P Papadimitriou, N Akritidis, L Christou, EV Tsianos. The New Global Map of Human Brucellosis. Lancet Infectious Disease. 2006. 6:91-99.

[6]        http://www.aphis.usda.gov/newsroom/content/2009/10/printable/brucellosis_concept_paper.pdf. Accessed 9 June, 2012.

[7]         Higgins, J, T Stuber, C Quance, WH Edwards, RV Tiller, T Linfield, J Rhyan, A Berte, B Harris. Molecular Epidemiology of Brucella abortus Isolates from Cattle, Elk, and Bison in the United States, 1998 to 2011. Applied Environmental Microbiology. 2012. 78(10):3674-84.

Coexisting with Coyotes

This is the twelfth of 16 student posts, guest-authored by Stanley Corbin.

Disease in wildlife is an important concern to the health and safety of humans and domestic animals. The expanding growth of our nation and resultant land use changes with urbanization has resulted in a shrinking habitat and fragmentation for all animals, including humans. The effects of ecological disruption are universally recognized and adversely effects wildlife through multiple mechanisms.

Hand it to the coyote (Canis latrans) for its ability to exist with humans. The resilience of this animal can be attributed to its natural instincts, remarkable intelligence and survivability. Opportunistic is another word that can be used to define them. Once an animal roaming the mid-west prairies, their territory has expanded throughout the North American continent and beyond. Coyotes demonstrate their wily nature by meeting the challenges of the American landscape.  

Progression of coyote range expansion throughout North America and Mexico. (7) Click to enlarge. 

Precise population estimates of coyotes in the United States are not available and unclear at best. However, to put it in perspective, the California Department of Fish and Game estimates a population range of  250,000  to 750,000 animals.(1)  The greater metropolitan area of Chicago estimates home to between 200-2000 coyotes. (3) The coyote population in New York during the summer is approximately 20,000-30,000. (2)  In March 2010, a lone coyote led a police chase through lower Manhattan, deep in New York City.

Coyotes can thrive in suburban settings and even some urban ones creating a concern for public health. A study by wildlife ecologists at Ohio State University yielded some surprising findings in this regard. Researchers studied coyote populations in Chicago over a seven-year period (2000–2007), proposing that coyotes have adapted well to living in densely populated urban environments while avoiding contact with humans. They found, among other things, that urban coyotes tend to live longer than their rural counterparts. (3)

As with most all wild animals, the coyote population represents a reservoir for diseases. Zoonotic (animal to human) diseases in particular are on the rise, comprising 75% of emerging infectious diseases. Viruses, bacteria, fungi, internal and external parasites, and other pestilence are only the headings for what’s out there.

Fortunately, the rabies virus is rather uncommon in coyotes as reported. The only exception was the 1974-1998 rabies epizootic (epidemic in animals) in south Texas. The world’s largest wildlife oral rabies vaccine (ORV) drop, 11.6 million doses covering over 189.6 square miles, was performed beginning in 1995 and led to the total elimination of the domestic dog-coyote (DDC) variant by 2006. (4) A study performed by the USDA, APHIS, Wildlife Services, National Wildlife Research Center concluded; “In Texas, the use of the ORV stopped the northward spread and led to the progressive elimination of the DDC variant of rabies in coyotes”. (5) This campaign was a win for our tax dollars as well. The economic evaluation study yielded “total estimated benefits of the program approximately ranged from $89 million to $346 million, with total program costs of $26,358,221 for the study period”. This represents benefit-cost ratios that ranged from 3.38 to 13.12. (5)

Coyote rabies surveillance reported by the Center for Disease Control (CDC) for 2010 declared 10 confirmed cases. None of these cases were DDC variant, which remains non-detected from the populations. The raccoon variant and skunk variant represented 8 (AL, GA, NC, NJ, NY, NYC) and 2 (CA, CO) cases respectively. (6)These coyote rabies cases were diagnosed from New York City (1) on the east coast to California (1) in the west, confirming the widespread distribution of this terrestrial carnivore. An interesting fact that comes from this data is that the coyote is not a player in the zoonotic rabies front. From a public health concern, a human has a significantly greater chance of contracting the disease from the backyard domestic cat.

Canine Distemper Virus is an enzootic disease (prevalent in an animal population) in the coyote. The neurological form is rightfully confused with a rabies infection as the two appear similar clinically. Humans are not susceptible to the disease, however it is highly contagious to dogs. Greater Yellowstone Park has a dynamic management study to assist with the surveillance of the disease enzootic in the parks coyote population.

The parasitic disease Sarcoptic mange is what gives the animal the “mangy” look. Caused by the mite Sarcoptes scabei, the disease in humans is called Scabies. Severely affected coyotes are unsightly and are perceived as threatening by their appearance. The compromised condition may explain the increased frequency of nesting and scavenging in suburban areas, especially in daylight hours. Coyotes with extensive mange infections are not considered aggressive as concluded by The Cook County, Illinois, Coyote Project.(7) Human infections from animal sources are short-lived and self-limiting due the highly host species-specific nature of the bug.

A recent hot epidemiological study conducted in Santa Clara County, California, identified coyotes as a wildlife reservoir for a disease caused by Bartonella vinsonii subsp. Berkhoffii .(8) The disease in humans is characterized by endocarditis, an inflammation of the interior lining of the heart. The study was prompted by the coyote bite of a child who developed symptoms compatible with Bartonella infection. Among 109 coyotes sampled, 31 animals (28%) were found to be bacteremic and 83 animals (76%) had Bartonella vinsonii seropositve antibodies. The disease is thought to be transmitted by insect vectors (ticks, biting flies, fleas), however further studies are necessary to elucidate additional modes of transmission to humans.(8) Bartonellosis in domestic cats is commonly called “cat scratch fever”, caused by a different species variant of Bartonella. The role coyotes play in this emerging infectious zoonose and public health concern are yet to be resolved.

Additional diseases exist in the coyote populations warranting public health attention. Anyone concerned with coyote interaction and communicable diseases will need to seek information relative to their geographical location. The ubiquitous nature of this animal and the corresponding diseases posing risks to humans and domestic animals respectively are regionally specific.

Coyotes are here to stay. Most every state (excluding Hawaii) has a control program in effect to manage the public health risks and deprivation to human welfare. The Humane Society of the US has issued techniques to resolve coyote conflict and how to discourage coyotes.  Project Coyote champions innovative solutions to live in peace with the coyote despite differences, especially in terms of human policy. (9) A collaborated and integrated management approach is required to maintain a balance of needs for this specie of animal and humans. Wildlife specialist Jeffery Green summarizes; “regardless of the means used to stop damage, the focus should be on damage prevention and control rather than elimination of coyotes”. (10)

Pet owners need to adapt to coyote presence and take precautionary measures in securing their animal’s health and safety. Routine core vaccinations and other preventative health care are effective in stopping the transmission of nearly all the important diseases from the coyote to a pet animal.

Coyote attacks on humans are rare; the coyote human avoidance factor is responsible for the low incidence. In the cases of human attacks, approximately 30% were reported as humans feeding coyotes. (8) Additionally, greater than 50% of the human attack cases were in California, (8) where coyotes have a longer history of habituation with humans.

A person who sees a coyote should feel lucky since they avoid humans and are mostly invisible.

The most important advice to prevent human exposure is: do NOT feed coyotes and ensure your environment is NOT coyote friendly. Any attempt to domesticate or habituate the coyote will surely be a kiss of death for its existence. Survival of coyotes is dependent on living side by side but not together with humans.

The “tricksters still run wild and provoke all sorts of all-too-human difficulties, pitting the spirit of the wild against the sturdy values of our American farmers and their need to protect livestock. Somehow we need both”. (11)

Our Canadian neighbors at The Royal Canadian Geographical Society  conclude; “the more we cut down habitat and build, the happier the scavenging and opportunistic coyote”. (12)

As they say in Texas, “when the human population fails, cockroaches and coyotes will survive”. (13)


  1. L.A. County Department of Animal Care and Control website. Accessed June 15, 2012. Available at: http://animalcare.lacounty.gov/coyote.asp
  2. New York State Department of Environmental Conservation website. Accesses June 15, 2012. Available at: http://www.dec.ny.gov/animals/9359.html
  3. World Science website: Thriving under our noses, stealthily: coyotes.  Accessed June 13, 2012. Available at:  http://www.world-science.net/othernews/060105_coyotefrm.htm
  4. Texas Department of State Health Service website. Accessed June 12, 2012. Available at: http://www.dshs.state.tx.us/idcu/disease/rabies/orvp/statistics/
  5. Stephanie A. Shwiff, PhD; Katy N. Kirkpatrick, BS; Ray T. Sterner, PhD. Economic evaluation of an oral rabies vaccination program for the control of a domestic dog-coyote rabies epizootic: 1995-2006. JAVMA, Vol.233, No.11, Dec.1, 2008. Available at http://www.avma.org/avmacollections/rabies/javma_233_11_1736.pdf
  6. Jesse D. Blanton, MPH; Dustyn Palmer, BA; Jessie Dyer, MSPH; Charles E. Rupprecht, VMD,PhD. Rabies surveillance in the United States during 2010. Vet Med Today: Public Veterinary Medicine. JAVMA, Vol. 239, No. 6, September 15, 2011. Available at: http://avmajournals.avma.org/doi/pdf/10.2460/javma.239.6.773
  7. The Cook County, Illinois, Coyote Project website. Accessed June 13, 2012. Available at: http://urbancoyoteresearch.com/Coyote_Project.htm
  8. Chang CC, Kasten RW, Chomel BB, Simpson DC, Hew CM, Kordick DL, Heller R, Piedmont Y, Breitschwerdt EB. Coyotes (Canis latrans) as the reservoir for a human pathogenic Bartonella sp.: molecular epidemiology of Bartonella vinsonii subsp. Berkhoffii infection in coyotes from central coastal California. J Clin Microbiol. 2000 Nov; 38 (11): 4193-200. Available at: http://www.ncbi.nlm.nih.gov/pubmed/11060089
  9. Project Coyote website. Accessed June 15. 2012. Available at: http://www.projectcoyote.org/programs.html
  10. Jefferey S. Green, Urban Coyotes: Some Summary Thoughts. Proceedings of the 12th Wildlife Damage Management Conference (D.L. Nolte, W.M. Arjo, D.H. Stalman, Eds. 2007
  11. Shake-Spear’s Bible.com website; Coyote: An Instant Classic. Post by Roger Strirtmatter, October 25, 2011. Accessed June 13, 2012. Available at: http://shake-speares-bible.com/2011/10/25/coyote-an-instant-classic/
  12. The Royal Canadian Geographical Society website. Accessed June 13, 2012. Available at: http://www.canadiangeographic.ca/wildlife-nature/?path=english/species/coyote/2
  13. Personal correspondence; James Wright; Tyler Texas. Retired Texas Department of State Health Service official.

Aw Schucks: When the world is NOT your oyster!

This is the eleventh of 16 student posts, guest-authored by Ilze Berzins. 

When one hears the words “food-borne illness”, what comes to mind?  For me, I think of a medium rare, pink, juicy hamburger, or something like potato salad that may be made with mayonnaise containing raw eggs, or maybe a fresh green garden salad sprinkled with sprouts.   I am sure we have all heard about outbreaks or recalls surrounding these familiar dishes.  And the usual suspects contaminating these food stuffs are often bacteria with familiar names such as E.coli or Salmonella.   The fear of getting “food poisoning” from these products may encourage us to buy fresh seafood from the grocery store, or order the shrimp or salmon when out at a restaurant instead of steak, thinking seafood might be a safer bet.  And of course, aren’t health benefits from seafood supposed to be an added bonus?  But not so fast!    Believe it or not, one can also become ill when eating, or even just handling, seafood.  Gives the phrase “fresh catch of the day” a whole new meaning!

Seafood is a broad term…and no…it is not the game you played as a child that while eating you asked people if they wanted seafood and you opened your mouth (get it?  SEE food?).   Seafood refers to all species of fish and shellfish, coming from both fresh and saltwater sources.  Salmon, snapper, trout, tuna, perch, tilapia are just a few of the fish that come to mind.  But what is shellfish?  Shellfish consists of a mixed group of mollusks and crustaceans that have a shell or shell-like body covering known as an exoskeleton.  For the mollusks, this would include oysters, clams, mussels, abalone, and scallops.  And although they don’t have an obvious shell (it is very small or absent), squid and octopus are also in this group.  Crustaceans that are edible shellfish include lobsters, shrimp, crabs, and crayfish.  Yum.

What can make you sick from eating seafood?  There are several main categories including infectious pathogens (parasites, viruses, and bacteria – oh, my!), contaminants (heavy metals such as mercury in the form of methymercury), and drug and chemical residues.  These can be synthetic compounds but can also come from natural bio-toxins.  One such compound is found in the tissues of small aquatic organisms in overgrowth situations or “blooms” such as in red tide events.

Eating raw or undercooked seafood definitely increases the risk of a food-borne illness, but even just handling or processing seafood can cause problems for humans (7, 10).  Topically acquired or contact zoonoses can be acquired through stings, bites, or spine/pincer puncture wounds.  Zoonoses are illnesses transmitted from animals to humans.  Some groups at risk include commercial fishermen, fish farmers (aquaculture), hobbyists, aquarists working in public display facilities, fish food processors, chefs, and even you when you are preparing dinner!  Bacteria are the primary causative agents for zoonotic infections through a contact route. Viruses, fungi, and parasites contact infections have rarely been reported (7, 8).   However, I am not quite sure how to classify a recent case report on a “parasite-like” infection by the squid Todarodes pacificus (5).   A 63-yr-old Korean woman was reported to have experienced severe pain in her oral cavity immediately after eating a portion of parboiled squid along with its internal organs. She did not swallow the portion, but spat it out immediately. She complained of a pricking and foreign-body sensation in the oral cavity.   Twelve small, white spindle-shaped, bug-like organisms stuck in the mucous membrane of the tongue, cheek, and gingival were completely removed. On the basis of their morphology and the presence of sperm, the foreign bodies were identified as squid spermatophores!!  Not sure if I would call that “parasite-like”?!   I digress!  Let’s focus!

There are lots of species of seafood and many reports of associated food-borne illnesses (1,2).  Where should we start?  In this blog, I will focus on a group within the mollusks, the bivalves.  Bivalves are mollusks with two shells including oysters, clams, and mussels.   I want to focus on this group because given the propensity of humans to eat raw oysters, eating them raw elevates the risk of acquiring a viral or bacterial food-borne illness.   In subsequent blogs, I will review other members of the mollusks, then on to crustaceans, and of course, fish, so stay tuned!

Safety issues for bivalves center around two categories; first, the quality of water in which these animals are grown in, and second, the conditions under which they are harvested, processed, and distributed (1,2,8).  In 1925, the Bureau of Chemistry (now the United States Food and Drug Administration) met to establish guidelines for the oyster industry.  Attendees resolved to control “the beds on which shellfish are grown” and “the plants in which the shellfish are shucked” (shucking refers to removing the animal from its shell)(11).  In the late 1800s and early 1900s, most outbreaks of seafood food-borne illness resulted from sewage contamination in the areas where shellfish were grown (11).  From the late 1970s through today, there has been an increased incidence of disease associated with naturally occurring shellfish pathogens (11).  There are some that think this trend is suggestive of emerging environmental problems such as increasing water temperatures associated climate change.  While the species of pathogen isolated in bivalves may vary with salinity of the water the oysters or clams grow in, it is noted that all of these pathogens increase in numbers with an increase in water temperature (11).

How often do we see illness? In a 10 year study on mollusk shellfish food-borne illness, a total of 2795 cases, with 96 deaths, were documented (11).  Oysters accounted for the highest proportion of cases (49%) and death (97%).  Shellfish from the East and Gulf costs were equally likely to cause disease.  Most from the East Coast were viral contaminated clams, where as on the Gulf Coast, most cases were oysters infected with non-cholera bacteria in the family Vibronaceae.

The naturally occurring bacterial pathogens of concern include Vibrio vulnificus, V. parahaemolyticus, V. mimicus, V. hollisae, and V. furnissi.   When eating raw oysters, one might become exposed to V. vulnificus.  Incubation can take 1-5 days, though the median time is around 28 hours (3).  Symptoms include high fever, chills, nausea, vomiting, diarrhea, and abdominal pain.  The ill person can become rapidly dehydrated, and the infection can become systemic (body wide) if bacteria enter the blood.  V. vulnificus in some cases can multiply so rapidly that blood vessels may become infected (known as vasculitis), and blood clots can develop which may lead to digit or limb amputation, or even death (3)!

How about from contaminated sources? Viral and bacterial enteric pathogens of public health concern are caused by fecal contamination of the waters from which molluscan shellfish are harvested and of the environment in which they are processed.  Pathogens of concern that have been associated with disease include human enteric viruses; hepatitis A, non-A, non-B enteral hepatitis (hepatitis E), unclassified viruses; and such bacteria as Salmonella, Shigella, Campylobacter jejuni, and pathogenic Escherichia coli (11). The group of unclassified viruses includes the Norwalk and Norwalk-like viruses.

Do we stop eating seafood?  NO!!!  But measures to increase the safety of raw shellfish could be, and are being implemented (11).  These measures might include policies on when and where to collect (season, time/temperature), requiring harvest areas near sewage treatment facility outflows to be more closely evaluated (9), and continuing to improvement the technology of sewage treatment.  Some aquaculture techniques have included lowering temperatures and controlled purification which involves disinfecting (or purifying) the water in which the bivalves are grown. This may reduce gut bacterial levels but it does not entirely remove them.   When processing shellfish, facilities can employ techniques such as rapid chilling and cold storage to reduce overgrowth and contamination.  Irradiation of the harvested product has been suggested but has yet to be approved. Laboratory tests to detect contamination are moving beyond traditional culture techniques and include identifying pathogens based on their individual DNA using molecular methods (6).   Focusing on identifying groups at risk such as those individuals who are immunocompromised (young, old, ill) and concentrating on the more common agents could help resources go further.

Consumer education is also very important. Prevention strategies should focus on preparation and consumption.  Cooking oysters to an internal temperature of 85-90°C will destroy both viruses and bacteria of public health concern. But what if you want to eat them raw?  Maybe think about cooking oysters during periods of warm weather and go for raw during colder times of the year!  An excellent, comprehensive web site about food safety issues is www.foodsafety.gov .  It addresses a variety of audiences including consumers, food professionals and industry workers, and provides the latest news, safety alerts, recalls, and health warnings.   The site also allows for individuals to report cases, and it has information for physicians on how to diagnose and manage food-borne illnesses.  Other useful sites include www.foodsafetywatch.com and www.fda.gov.

With any food product, it is probably wise to stop and ask “To Eat or Not To Eat?”(4). Stay safe!


  1. Butt, A.A., Aldridge, K.E., and Sanders, C.V.  2004.  Infections Related to the Ingestion of Seafood Part I: Viral and Bacterial Infections.  Lancet Infect. Dis. 4: 201-212.
  2. Butt, A.A., Aldridge, K.E., and Sanders, C.V.  2004.  Infections Related to the Ingestion of Seafood Part II: Parasitic Infections and Food Safety.   Lancet 4: 294-300.
  3. Daniels, N.A.  2011.  Vibrio vulnificus Oysters: Pearls and Perils.  Clin. Infect. Dis. 52 (6):788-792.
  4. Galson, S.K.  2009.  To Eat or Not to Eat:  Food Safety in the United States: Practical Applications from the Surgeon General.   J. Am. Dietetic Assc. 5(20): 1142.
  5. Park, G.M., Kim, J.Y., Kim, J.H., Huh, J.K.  2012.  Penetration of the Oral Mucosa by Parasite-Like Sperm Bags of Squid: A Case Report in a Korean Woman.  J. Parasit. 98 (1): 222-223.
  6. http://www.rapidmicrobiology.com/test-methods/Vibrios.php
  7. Huss, H. H., Reilly, A., and Ben-Embarek, P.K.  2000.  Prevention and control of hazards in seafood. Food Control 11:149-156.
  8. Iwamoto, M., Ayers, T., Mahon, B.E., and Swerdlow, D.L. 2010. Epidemiology of Seafood-Associated Infections in the United States.  Clin. Microbiol. Reviews 23 (2): 399-411.
  9. Rabinowitz, P.M., Gordon, Z., Holmes, R., Taylor, B., Wilcox, M., Chudnov, D., Nadkarni, P. and Dein, F.J. 2005. Animals as Sentinels of Human Environmental Health Hazards: An Evidence-Based Analysis. EcoHealth 2: 26-37.
  10. Vinh, D.C., Mubareka, S., Fatoye, B., Plourde, P., and Orr, P.  2006.  Vibrio vulnificus Septicemia after Handling Tilapia sp. Fish: A Canadian Case Report and Review.  Can. J. Infect. Dis. Med. Microbiol. 17(2): 129-132.
  11. Wittman, R.J. and Flick, G.J.  1995.  Microbial Contamination of Shellfish: Prevalence, Risk to Human Health, and Control Strategies.  Annu. Rev. Public Health 16: 123-40.


A Query about Q fever –Answers to the Questions you should ask

This is the tenth of 16 student posts, guest-authored by Jean DeNapoli. 

I own a small back yard flock of sheep and lambing season is the most exciting and rewarding time of the year.  Nothing is more enjoyable than watching a lamb who takes a few wobbly steps and nurses for the first time as her mother nickers encouragement.  Within a day, the lamb will be playing, bucking, running, and exploring her world.

Despite the pastoral wonders of the season, lambing is also inherently stressful.  I must constantly check the barn to monitor for birthing problems and help out when necessary.   This help might include repositioning a lambs stuck in the birthing canal, pulling a lamb when the ewe is unable to push it out herself, and cleaning the face and airway of a newborn when its mother is too exhausted to follow through on her own.  Shepherds all over the world share the same experiences that I do.  But what many of them don’t know is that they are probably being exposed to Q fever.

When the disease was first recognized it was given the temporary name Query fever (since very little was understood about it).  We now know it is caused by a bacteria called Coxiella burnetii.  It is found word wide and it is estimated that 15-20% of all cattle, sheep and goats have been exposed to it.  The livestock rarely show signs of illness, but it can contribute to reproductive problems such as abortions.

In an infected animal, the organism can be found in milk, urine, and feces.  But the greatest concentration of bacteria is in the amniotic fluid and placenta.  Ticks can spread the disease, but much more frequently, it is passed directly to other animals at the time of birth.  It can develop into a long lasting spore-like form and can then contaminate dust and be carried by the wind.  Q fever is very easily spread and it takes only one organism to cause disease!

Q fever is zoonotic; it can be passed from animals to people.  When people become infected, they may have fevers, headache and weakness.  Fortunately, the fatality rate is low (<2%).  But some people, especially pregnant women and those with heart disease or who are immune deficient, end up with a more chronic and severe disease.  Q fever may also cause pre-term delivery or miscarriage if women become infected while pregnant.

I am not only a shepherd, but I am a veterinarian and it surprises me that few shepherds (at least the hobby farmers I know) discuss Q fever or take the recommended precautions.  In research facilities, Q fever is a biosafety 3 organism (on a scale of 1-4), requiring special laboratory containment precautions. To put this in perspective, other level 3 organisms include tuberculosis, anthrax, SARS, and yellow fever.  Yet many farmers routinely assist in births without any thought to their own health.

Q fever is fairly common and can be difficult to detect in healthy animals, so experts recommend treating all sheep as if they are infected.  Pregnant women or women who may become pregnant should avoid working with sheep at lambing time.  Other people at increased risk (people with impaired immune systems and heart valve abnormalities) should also stay away from the barn at lambing time.

Shepherds should wear disposable gloves when assisting lambing or handling newborn lambs.  Masks should also be worn, especially in dusty conditions.   Farmers should not eat or drink in the barn and should clean their footwear and wash their hands when leaving the barn.

Clothes have also been shown to carry the organism and they are capable of causing infection in people handling the laundry.  Therefore, high-risk people should not handle clothing that has been worn in the barn until it has been cleaned.

Farmers should use good sanitation when handling birthing materials and bury or compost the placentas.  Birthing areas should be cleaned frequently and in a way that will not cause excessive dust.  It is very important that farmers understand biosecurity precautions in general and specific Q fever prevention protocols to keep themselves, their families and their neighbors safe.

Shepherds should also work closely with their veterinarian to keep their flock as healthy as possible.   In the event of an abortion, the fetal material (placenta) should be submitted to the veterinary diagnostic laboratory for testing.

But what if you are not a farmer, do you need to be concerned?  Well, you should at least be aware of the disease.

Although usually associated with farm animals, dogs and cats may also transmit Q fever to people, most commonly at and around the time of birth.  Again, people who are most susceptible should avoid association with pets at those times.  Coxiella burnetii has been found in milk, so dairy products should be properly pasteurized before being consumed.

The organism is easily transmitted through the air (it is even considered a possible bioterrorism risk for this reason).  The Netherlands had a recent outbreak of Q fever in people living close to goat farms due to unintentional airborne transmission.  However, the people who generally are at the greatest risk are farmers, veterinary workers and researchers.  They are the people most likely to be near animals giving birth or handling the organism during the course of their daily work.

With education and reasonable safety precautions, a visit to the barn does not have to be a risky event.  Through the simple sharing of information, we can keep future generations of farmers safe, healthy, and productive.


Prevalence of Coxiella burnetii infection in domestic ruminants:  A critical review.  Raphael Guatteo, Henri Seegers, Ann-Freida Taurel, Alain Joly, Francois BeaudeauVeterinary Microbiology 149 (2011) 1-16

Q Fever:  Current State of Knowledge and Perspectives of Research of a Neglected Zoonosis.  Sarah Rebecca Porter, Guy Czaplicki, Jacques Mainil, Raphael Guatteo, and Claude Saegerman.  International Journal of Microbiology Volume 2011 (p 1-22)

Eurosurveillance, special issue on Q fever, vol. 17, 19 January 2012

New York Department of health Q fever facts sheet (2011) http://www.health.ny.gov/diseases/communicable/q_fever/fact_sheet.htm

World Organization for Animal Health (OIE) fact sheet on Q fever (2011) http://www.oie.int/fileadmin/Home/eng/Media_Center/docs/pdf/Disease_cards/Q-FEVER-EN.pdf

Center for Disease Control (CDC) Q fever information (2011) http://www.cdc.gov/qfever/index.html

Public Health Agency of Canada pathogen safety data sheet for Q fever (2010) http://www.phac-aspc.gc.ca/lab-bio/res/psds-ftss/coxiella-burnetii-eng.php

Health Protection Agency Q fever information for farmers (2010) http://www.hpa.org.uk/webc/HPAwebFile/HPAweb_C/1210834106356

University of Florida IFAS Extension, The Herd Health Handbook for Goat Producers:  Biosecurity at the Farm Level, Ray Mobley and Carmen Lyttle-N’guessan.  (2009) http://edis.ifas.ufl.edu/famu006

Wyoming State Veterinary Laboratory, Q fever fact sheet (2004) http://www.uwyo.edu/wyovet/disease-updates/2004/files/qfever.pdf

Institute for Biosecurity, Saint Louis University School of Public Health, Q fever fact sheet (2001) http://www.bioterrorism.slu.edu/bt/quick/qfever01.PDF

Eurosurveillance Q Fever in the Netherlands: an up date on the epidemiology and control measures, W van der Hoek, et al. (2010) http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19520

Photographs are courtesy of Laura Cowperthwaite and Triple J Farm.

Does bestiality increase your risk of penile cancer?

Aah, the things one learns when awake at 3AM on a Saturday night. Via a few different Tweeps, I ran across this article from Men’s Health magazine, titled “Urgent Warning: Sex with Animals Causes Cancer.”

I probably should have just stopped there.

But no, I read the magazine article, which states:

Brazilian researchers polled nearly 500 men from a dozen cities, and found that–we’re not joking around here–roughly 35 percent of the men had “made it” with an animal. That’s a problem, because screwing a horse, donkey, pig, or any other animal was found to up your likelihood of developing cancers of the penis by 42 percent.

Of course, this meant that now, I had to go dig up the actual journal manuscript. Though nothing is cited by Men’s Health, a quick PubMed search using the terms “sex with animals” and “Brazil” turned up Sex with Animals (SWA): Behavioral Characteristics and Possible Association with Penile Cancer. A Multicenter Study, published last month in The Journal of Sexual Medicine.

Though the MH write-up makes the research sound ridiculous, it’s not a bad paper overall. Starting out with the observation that penile cancer is common in impoverished regions in the world but relatively rare in developed areas, the authors wanted to examine one possible difference in this urban/rural divide: bestiality. So they enrolled 492 individuals who had spent their childhood in rural areas: 118 cases who had penile cancers and 374 controls who were seen at the same clinics for other issues, including check-ups and “cancer prevention” (though it’s not really defined what’s included in that catch-all). All participants were asked a variety of questions about their sexual history, including sex with animals and humans (frequency, number of partners, the usual drill), circumcision status, as well as other factors that might influence cancer outcomes, such as smoking status and history of sexually transmitted diseases and other health conditions.

The authors did find in the univariate analysis (basically, looking at one factor at a time) that there were several statistically significant differences between the cancer group and the control group. These included smoking, a history of sex with prostitutes, the presence of penile premalignant lesions (not surprising) and phimosis (NSFW), a condition where “the foreskin cannot be fully retracted over the glans penis.” As the title suggests, they also found that having sex with animals was significantly higher in the case than the control group (44.0 vs 31.6 percent, p<.008). When they combined risk factors into their multivariate analysis, a few factors still remained in the model. Phimosis was the big one, with an odds ratio of 10.41; SWA was down the list at 2.07 (95% CI: 1.21-3.52, p=0.007). Penile premalignant lesions and smoking also remained, with odds ratios in the middle of the other two. Finally, just because I know many of you out there are curious, they also break down those who have SWA by types of animals they, um, frequent:

The animal types most often cited were mares (N = 80), followed by donkeys (N = 73), mules (N = 57), goats (N = 54), chickens (N = 27), calves (N = 18), cows (N = 13), dogs (N = 10), sheep (N = 10), pigs (N = 6), and other species (N = 3).

Yes, chickens for 27 of them. I don’t even want to know, but I’m sure if I did, I could find out somewhere on the Internets. Please, don’t educate me on that one. They also note that almost a third of the men reported “SWA with a group of men.” I’m leaving that one alone as well (especially as that one wasn’t any different between cases and controls, so it didn’t seem to be an important variable for penile cancer development).

So how do they explain these findings? Their discussion is a bit odd, in my opinion, and narrows in on the SWA finding to the exclusion of their other significant risk factors. Of course, coming from my background, my first thought regarding SWA and cancer jumps to infectious agents. They acknowledge in the introduction that the human papillomavirus (HPV) is associated with about half of penile cancers. Other species of animals can also be infected with papillomaviruses, such as the rabbit of jackalope mythology. A previous study identified five potentially novel papillomaviruses in Australia, just by doing skin swabbing. As such, it’s certainly safe to say that we know very little about the diversity of these viruses that exist in other animal species, much less their cancer-causing potential. It would be fascinating to look at tumor samples from the men in this group who were known to have sex with animals, and see if any novel viruses (papillomas or otherwise) could be identified.

However, they don’t limit their suggestion to only zoonotic infections. That’s when it gets a bit weird to me, as they say things like:

Speculation exists regarding cancer status as an infectious disease in humans [24,25], as studies have suggested that tumor cells can be transmitted from one mammal host to another within the same species [26,27]. PC is frequent in equines [28], but transmission of malignancies between animals and humans has not been reported.Virology does not consider possible viral movement from animals to humans except in cases of zoonosis, such as rabies or pandemic forms of bird or swine flu. However, the hypothesis that the HIV epidemic resulted from simian-human virus transmission has not been fully explored.

Um, huh? First, the citation they use for the HIV claim is from 1999–indeed, at that point there was still a lot that was unknown about cross-species HIV transmission, but that was 12 years ago! The field has moved on since then. I’m baffled as to what they mean by their first sentence–as far as I know, “Virology” doesn’t consider anything–“Virologists” do, and why would this not be a zoonosis? Though I think direct transmission of cancer cells (like in the case of the Tasmanian devil transmissible cancer) would be unlikely, transmission of microbes which could lead to cancer development is certainly plausible and well within the realm of virology/bacteriology/etc. In my opinion, it’s infinitely more likely than the idea they also suggest of more directly carcinogenic animal secretions.

There were also a number of limitations in the paper. Though they grouped frequency of sex with prostitutes into a “more/less than ten times” dichotomous variable, I don’t see any similar “dose” analysis for the frequency of SWA in their models, even though they did ask the men about this. They make one statement that “long-term SWA (>3 years) was reported by 64% of the PC patients and 46.6% of the controls (P = 0.044).” This difference was statistically significant at the usual cutoff (p< .05), but it doesn't appear that they studied this further--why not? If you have a typical dose-response relationship (the more times the men had sex with animals, the more likely they were to develop cancer in the future), that would strengthen their case for a connection between the two. They also didn't ask about sexual orientation or the nature of the self-reported past STDs. Are any of these participants HIV positive, for example? Anyway, with these limitations in mind, it does appear that Men's Health got it mostly right: don't have sex with animals if you value your penis. But it's unfortunate that they just go for the sensationalism and ignore the more important variables from a public health standpoint, like "don't smoke" and "if you have abnormal penile conditions, you may want to get those checked out, k?" References

Zequi SD, Guimarães GC, da Fonseca FP, Ferreira U, de Matheus WE, Reis LO, Aita GA, Glina S, Fanni VS, Perez MD, Guidoni LR, Ortiz V, Nogueira L, de Almeida Rocha LC, Cuck G, da Costa WH, Moniz RR, Dantas Jr JH, Soares FA, & Lopes A (2011). Sex with Animals (SWA): Behavioral Characteristics and Possible Association with Penile Cancer. A Multicenter Study. The journal of sexual medicine PMID: 22023719

Antonsson and McMillan, 2006. Papillomavirus in healthy skin of Australian animals.

When is MRSA not MRSA?

…when it contains a weird gene conferring methicillin resistance that many tests miss.

Methicillin-resistant Staphylococcus aureus (MRSA) has become a big issue in the past 15 years or so, as it turned up outside of its old haunts (typically hospitals and other medical facilities) and started causing infections–sometimes very serious–in people who haven’t been in a hospital before. Typically MRSA is diagnosed using basic old-school microbiology techniques: growing the bacteria on an agar plate, and then testing to see what antibiotics it’s resistant to. This can be done in a number of ways–sometimes you can put a little paper disc containing antibiotics right onto a plate where you’ve already spread out a bacterial solution and see which discs inhibit growth, or sometimes you can grow the bacteria in a plate with increasing concentrations of antibiotics, to see when the drugs are high enough to stop growth. Both look at the phenotype of these bacteria–the proteins they’re expressing which lead to the bacteria’s drug resistance.

However, these culture-based methods are slow–they can take days between when the patient first is seen by a doctor and the time the results come back from the clinical lab. For this reason, increasingly labs are moving to molecular methods, which are much quicker than the culture-based methods. Indeed, detection of the gene responsible for methicillin resistance, mecA, has been the gold standard for *really* identifying MRSA, even beyond phenotypic methods.

A new pair of papers demonstrate the limitations of this reliance. Like many science discoveries, this one started with a “huh, weird” moment. Investigators noticed that a number of their S. aureus samples were categorized as MRSA using the traditional phenotypic methods, but were negative when it came to the mecA DNA test. Genetic analysis showed that these isolates carried a different mecA gene, dubbed mecALGA251. The investigators searched their isolate collection in England, and also worked with collaborators in Scotland and Denmark to search through their banks for additional mecA-negative MRSA, and found almost 70 isolates, including one dating back to 1975. (A second paper by a different group examined two isolates in Ireland).

Now is when it starts to get really interesting. (Continued below)
Continue reading “When is MRSA not MRSA?”