Ecology of Zoonotic Diseases Figuring out the What, Where and When of Disease Outbreaks

The Ecological Society of America Ecology of Zoonotic Diseases Figuring out the What, Where and When of Disease Outbreaks Bob Parmenter, Director, Scientific Services Division, USDA Valles Caldera National Preserve, New Mexico bparmenter@vallescaldera.gov, 505-428-7727 Gregory Glass, Professor, Johns Hopkins School of Public Health, Maryland, and Director, Global Biological Threat Reduction Program, Southern Research Institute, Alabama; glass@sri.org Lyme vector: black-legged tick A West Nile Virus host: American Robin Sampling rodents for Hantavirus & plague

Zoonotic Infectious Diseases: Diseases from pathogens contracted from animals (ticks, mosquitoes, rodents, etc.) Pathogens include viruses, bacteria, and parasites. Lyme vector: black-legged tick A West Nile Virus host: American Robin Sampling rodents for Hantavirus & plague

Distribution of human deaths by cause (world-wide, males and females) Disease outbreaks

Ecology of zoonotic diseases: Routes of infection. Direct pathogen transmission from animal to human (rabies/mammals, hantavirus/rodents, influenza/swine or fowl, Schistosomiasis/snails) Rabies Hantavirus Influenza Schistosomiasis Pathogen transmission via a vector (Lyme disease/tick, malaria/mosquito, plague/fleas, Leishmaniasis/sand flies) Lyme disease Malaria, West Nile Plague Leishmaniasis

Zoonotic disease outbreaks influenced by the ecology of hosts, pathogens and humans during interactions with the environment. General categories of national significance: 1. Climate dynamics (short-term) and long-term directional climate change 2. Land-use changes (anthropogenic and natural) 3. Global connectivity from travel and commerce 4. Emerging diseases from new discovery or pathogen evolution 5. Biowarfare/terrorism

Understanding the ecology of infectious diseases: National Science Foundation (NSF) Ecology and Evolution of Infectious Diseases Program (EEID). Ecological research on a diversity of diseases Echinococcus Schistosomiasis Malaria Chagas Trematodes Hantavirus Rabies Encephalitis Dengue West Nile P.Craig Herpesvirus Canine distemper Prion disease Tuberculosis Mycoplasma Leptospirosis E. coli Plague Cholera Chitrid fungi C. Kosoy

Scientific monitoring, testing and research on outbreaks of zoonotic diseases: CDC Special Pathogens Branch: National and international response collaborative teams for sudden outbreaks and newly emerging diseases.

Examples: How ecological dynamics influence host-pathogen disease outbreaks The 1993 Hantavirus epidemic in the Southwest

Radiographic Progression of HPS in the Lungs May 27, 1993 May 30, 1993 Source: Dr. L. Ketai May 31, 1993

After the first human cases in May, CDC scientists identified the virus as a Hantavirus in early June. Biologists began field surveys of rodents, and found the host was the deer mouse, Peromyscus maniculatus. Hantavirus host: Rodents Transmission pathway: Direct inhalation of virus in aerosolized urine and feces Exposure: Peridomestic, recreational, occupational. Mortality rate: 38% Vaccine or cure: None

Transmission of Hantaviruses Chronically infected rodent Horizontal transmission of infection by mouse-to-mouse aggressive behavior Virus is present in aerosolized excreta, particularly urine Virus also present in throat swab and feces Secondary aerosols, mucous membrane contact, and skin breaches are also sources of infection

Ecological Drivers of Rodent-Borne Disease Outbreaks: Trophic Cascades and Dispersal Waves

University of New Mexico field crew sampling rodents for hantavirus in the Sandia Mountains near Albuquerque, NM. Pulling blood sample from a deer mouse (Peromyscus maniculatus) Mobile field laboratory vehicle

Forest/woodland to grassland transitions Sevilleta NWR Valles Caldera National Preserve

Distance (km) of SNV HPS patient s home from nearest refugium 0 30 60 90 120 150 Time (days) since start of epidemic Time of Onset of Human SNV HPS Cases Related to Linear Distance from Refugia; 1993 HPS epidemic, Southwest USA 24 16 8 0

With El Niño bringing a wet winter, rodent populations have ballooned to levels approaching those in 1993, when Hantavirus was first identified in New Mexico

The 1993 hantavirus outbreak led to fears of biowarfare and terrorism. Congress held hearings into the causes of the epidemic. (article from Scientific American, November, 1993)

Rattus norvegicus Microtus pennsylvanicus Peromyscus maniculatus (grass) Peromyscus maniculatus (forest) Peromyscus leucopus (NE) Peromyscus leucopus (NW) Peromyscus leucopus (SW) Reithrodontomys megalotis Reithrodontomys mexicanus Sigmodon hispidus texensis Sigmodon hispidus Sigmodon alstoni Oryzomys palustris Oligoryzomys flavescens Oligoryzomys chacoensis Oligoryzomys longicaudatus (N) Oligoryzomys longicaudatus (S) Oligoryzomys microtis Calomys laucha Akodon azarae Bolomys obscurus Seoul Prospect Hill Sin Nombre Monongahela New York Blue River (IN) Blue River (OK) El Moro Canyon Rio Segundo Muleshoe Black Creek Canal Caño Delgadito Bayou Lechiguanas Bermejo Oran Andes Rio Mamore Laguna Negra Pergamino Maciel

Colonization of North America by rodents. ASIA 20 Million years ago Copemys (16 Mya) Abelmoschomys (9 Mya) Oryzomys?, Sigmodon? 7-9 Million years ago Auliscomys (4.5 Mya)

Sin Nombre Peromyscus maniculatus Muleshoe Sigmodon hispidus Isla Vista Microtus californicus El Moro Canyon Reithrodontomys megalotis Calabazo Zygodontomys brevicauda Choclo Oligoryzomys fulvescens Caño Delgadito Sigmodon alstoni Rio Mamore Oligoryzomys microtis Orán Oligoryzomys longicaudatus Bermejo Oligoryzomys chacoensis Andes Oligoryzomys longicaudatus New World Hantaviruses New York Peromyscus leucopus Prospect Hill Microtus pennsylvanicus Bloodland Lake Microtus ochrogaster Bayou Oryzomys palustris Black Creek Canal Sigmodon hispidus Juquitiba Unknown Host Rio Segundo Reithrodontomys mexicanus Laguna Negra Calomys laucha Maciel Necromys benefactus Hu39694 Unknown Host Lechiguanas Oligoryzomys flavescens Pergamino Akodon azarae

Human Hantavirus cases in U.S., 1993-2012. Histograms: Number of cases nation-wide Black line: Percentage fatalities

Yosemite National Park, 2012 Hantavirus outbreak among visitors; 10 cases, 3 fatalities.

Double-walled tent-cabins provided perfect nest-site habitat for deer mice

Ecology Example #2: Plague: The Black Death How do ecological factors affect plague occurrence and distributions?

Direct contact Plague Cycle Wild Rodent Cycle Wild Rodent Direct contact Secondary plague pneumonia Infective Flea contaminated soil Infective Flea Direct contact Bubonic or Septicemic plague Primary pneumonic plague cases Infective Flea Wild Rodent Domestic Rodent Pathways usual occasional rare or theoretical Infective Flea Domestic Cycle Domestic Rodent

Bubonic Plague: Bubo locations Bacteria proliferate in regional lymph nodes Locations* Inguinal/femoral: 55-70% Axillary: 20% Cervical: 10% Most often solitary, but can occur in multiple locations (10-20%) *Politzer R. Plague. World Health Organization Monograph Series. 1954. CDC. Unpublished data. Photos courtesy of CDC.

Septicemic plague infects entire Photos courtesy of CDC, Public Health Image Library. bloodstream, affects extremities first.

Pneumonic Plague into the lungs Short incubation period (1-4 days) Death in 3-6 days if not treated early Primary pneumonic plague more easily spread person to person

The Nippon Maru, docked in San Francisco, 1899. Photo: Bancroft Library, U. C. Berkeley

Bob lives here

New Mexico: Land of the Flea, Home of the Plague

Status of Plague in North America Plague Line at about the 100 th Meridian

Plague in the Southwest Almost 80% of U.S. cases Over 80% of cases exposed in peridomestic environments Poor rodent sanitation increases plague risks Rock squirrel fleas are primary source of exposure Prairie dog flea bites and handling infected prairie dogs, cats, rabbits, etc. are also sources of exposure (Eisen et al. 2007) Areas at risk for peridomestic plague

Hypothetical Pathways for Plague Outbreaks: 1. Trophic Cascade from increased PPT, raising numbers of mammal hosts; 2. PPT increases soil moisture and enhances survival and reproduction of fleas. 3. Increased hosts and fleas raise probability of plague events.

Impact of Late Winter Precipitation and Threshold Temperatures on Human Plague in the Four Corners Region (Enscore et al. 2002) Modified Trophic Cascade Model Increased rodent food sources Effects of Increased Precipitation Feb. March (Major effect) Rodent numbers increase above critical threshold (Davis et al. 2004 Predictive thresholds paper) Increased rodent survival and reproduction High rodent densities favor epizootic spread July Aug (Minor effect) Feb. March (Minor effect) Cool summer (15 18 months after first wet winter) (Major effect) Widespread epizootics Increased flea survival and reproduction Cool temperatures favor survival of infected fleas Enscore et al. 2002 Increased human plague risks Supportive results observed for plague in prairie dogs (Collinge et al. 2005) and in comparison of plague and hantavirus risks in Southwest (Eisen et al. 2007)

PLAGUE PREVENTION Fuge cito, vade longe, rede tarde Flee quickly, go far, return slowly