Introduction
The reemergence of Rocky Mountain spotted fever (RMSF) in western North America is life-threatening to hundreds of people annually.1,2 When the brown dog tick (Rhipicephalus sanguineus) inoculates Rickettsia rickettsii into human or canine hosts, RMSF can progress in a week to fatality unless early antibiotic treatment is initiated with a tetracycline-class antibiotic.2 Brown dog tick–transmitted RMSF impacts several tribal communities in Arizona and urban centers in northern Mexico, predominantly in impoverished areas with large numbers of free-roaming and stray dogs that host massive peridomestic populations of R sanguineus. Protecting public health from RMSF is challenged owing to the lack of awareness among medical professionals and the public and a mismatch between available and needed resources to control dogs, ticks, and disease. In this report, we summarize the status of RMSF in highly impacted northern Mexico and the US states of California and Arizona, synthesize its ecology, catalog management challenges, and report opportunities for intervention.
From Historically Sporadic Rural Cases to Community and Urban Epidemics
RMSF has been diagnosed since the early 1900s in 10 Mexican states2,3 and is responsible for more fatalities than any other tick-borne disease in North America.1 However, initial presentation resembles other milder infections, and delays in diagnosis are common.1 Despite modern medical care and antibiotics, case fatality rates are 5% to 7% in the US and > 30% in Mexico; risk of fatality increases 2- to 3-fold if treatment is delayed more than 5 days and increases 4-fold if delayed > 6 days.1,2
Typically in endemic states in the US, most cases of RMSF are associated with Dermacentor spp ticks,4 whereas cases in Mexico, California, and Arizona are transmitted by tropical and temperate lineages of brown dog ticks.3,5 This tick thrives in heat and aridity and feeds on dogs or occasionally humans, particularly when dogs are scarce and temperatures are elevated.6,7
We summarize RMSF prevalence; case fatality; reporting dates in northwestern Mexico, California, and Arizona; and other information in Supplementary Table S1. Early Mexican cases were sporadic and rural, with a possible hiatus during decades of intense DDT (dichlorodiphenyltrichloroethane) use.3 In contrast, modern RMSF is increasingly urban in all northern Mexican states2 (Figure 1). Sonora recorded at least 2,917 cases and 745 deaths between 2003 and 2022.8 Studies in Sonora indicate that risk factors are poverty, nearby canals, lack of home security, dirt floors, presence of nonfunctioning vehicles, and dogs with abundant ticks.2 These factors may reflect environmental attributes that provide harborage for ticks as well as confounding low socioeconomic status as contributors to risk.
Rocky Mountain spotted fever human cases in 4 northern Mexican states and Arizona between 2015 and 2021.
Citation: Journal of the American Veterinary Medical Association 262, 5; 10.2460/javma.23.07.0377
Rocky Mountain spotted fever human cases in 4 northern Mexican states and Arizona between 2015 and 2021.
Citation: Journal of the American Veterinary Medical Association 262, 5; 10.2460/javma.23.07.0377
Rocky Mountain spotted fever human cases in 4 northern Mexican states and Arizona between 2015 and 2021.
Citation: Journal of the American Veterinary Medical Association 262, 5; 10.2460/javma.23.07.0377
In Coahuila state, foci of cases extended from Comarca Lagunera and Ramos Arizpe in the north to Saltillo city. From 2012 to 2017 in Saltillo, there were 14 patients from 1.5 to 13 years of age9 and 43% with contact with dogs, and 57% died. There were 6 cases statewide in 2021,10 and as of 2022, case fatality had increased to more than 76%, mostly in Saltillo.11 Chihuahua documented 74 cases during 2021, mostly in Ciudad Juárez at the US border,10,12 and 1 group reported an R rickettsii PCR-positive tick in Juárez.13
The epidemic was first confirmed in Baja California by PCR and DNA sequencing of human blood from patients who had died in the impoverished Mexicali neighborhood of Los Santorales in 2009,14 and subsequent cases in Santorales have exceeded 854 through 2022.15 During a door-to-door investigation, the majority (80%) of people in Mexicali were cognizant of RMSF, but only 48% used acaricides in the home or on dogs.16 Case neighborhoods and those with high canine seroprevalence tended to be on the city periphery or in the adjacent agricultural valley, while neighborhoods with a human case tended to have dirt ground cover. After the initial outbreak, there were 50 cases and 24 deaths in Mexicali in 2022 and, by April of 2023, already 8 cases and 4 deaths.15 The epidemic also spread to the city of Tijuana, which (together with near-border cities) had 29 cases and 8 deaths in 2022 and 4 cases and 3 deaths in early 2023; to the more southerly coastal city of Ensenada (5 cases and 1 death in 2022, none in early 2023); and even farther south in the San Quintin area (6 cases and 4 deaths in 2022). The epidemic may have finally erupted after low-level transmission prior, given that a cross-sectional study17 6 years earlier in Ensenada showed a 4% seroprevalence of antibodies reactive to spotted fever group Rickettsia among 384 people ages 1 and up and not known to have reported symptoms of rickettsiosis.
In the US, prior to 2003, existing dogma was that Dermacentor spp ticks were the vector of RMSF. However, only brown dog ticks were found, and abundantly, on examination of 17 impacted houses yielding more than 6,000 total ticks, during the abrupt onset of an outbreak of RMSF on tribal lands in the US state of Arizona in 2003.18 During the first investigations after identification of an index case in 2003, surveillance done by the CDC found 13 additional cases over the next 2 years.19 Multiple studies18–22 highlighted an abundance of dogs, particularly free-roaming or stray dogs, as a critical factor in the epidemic. For example, evaluation of early cases found many free-roaming dogs near case patients’ homes. At these tribal sites, 4 out of 4 patients’ dogs that were tested had serological titers > 1:16,000, an R rickettsii PCR-positive tick was recovered from a dog, and R rickettsii PCR positivity was detected in 3% of questing ticks from the environment.20 An aggressive intervention campaign reduced human case numbers.22 From 2012 to 2014, all dogs in a 600-home community were given long-acting tick collars, and environments were treated with acaricide monthly. Canine spay and neuter and restraint to the homesite were promoted, yielding a reduction in infestation rates on dogs of 1% (compared to 64% in a nearby community with no intervention) and no detectable ticks in the environment.
A recent 40-year review4 of confirmed and probable cases in California showed a significant near doubling in incidence as well as a shift from case patients being largely residents in the northern part of the state and likely associated with Dermacentor spp tick exposure to southern California (and with Mexican travel) and brown dog ticks; further, the review showed an increase in cases in Hispanic/Latino people. In this California review, in the last 20 years, 30 of 53 (57%) of reported cases were hospitalized, and 3 of 53 (6%) died.
Among 4 fatal human cases in California and Arizona from 2013 to 2016 associated with travel to Mexico, there was travel history to Hermosillo and Nogales (in the Sonora state epidemic) and Mexicali.23 The fourth case, in Calexico, California, had no travel history, although friends and family often traveled with their pets to and from Mexico and an R rickettsii PCR-positive tick was found near her home. Over the last 5 years, at least 6 people in California with RMSF reported recent travel to Mexico,24 but of 3 cases in 2022, only 1 had travel history to Tijuana, while the others may have acquired infection locally (in San Diego and in Los Angeles County). In late 2023, a health alert was issued by the CDC concerning the identification of severe and fatal RMSF in individuals with exposure in Tecate, Mexico, a newly emerging location of RMSF.
Veterinary Perspectives and Animal Reservoirs
Due to close interactions with humans and susceptibility to vector-borne zoonoses, dogs make useful sentinels of human disease risk. Dogs can become ill or die with RMSF, are the preferred host for brown dog ticks, and serve as a reservoir of infection for people.25 Canine RMSF disease and death is often a sentinel event that precedes identification of disease in humans.26,27 Infected dogs can develop fever and thrombocytopenia, similar to other tick-borne diseases of dogs such as canine ehrlichiosis and anaplasmosis. Progressive disease manifestations include petechiae, lethargy, limb or facial edema, and death.25 Epidemiological tracking of canine RMSF is difficult, and such data generally are not available. However, seroprevalence studies in dogs can highlight regions where R rickettsii is circulating and may represent risk to people. Even if a dog is not seropositive against a rickettsial organism and ticks are not seen, we can infer brown dog tick exposure and therefore possible risk of RMSF based on canine serology surveys for other brown dog tick–transmitted pathogens. These include the canine and rarely zoonotic Anaplasma platys and Ehrlichia canis and the emerging pathogen Rickettsia massiliae, which has a broad host range and has been found in Arizona, southern California, and Mexico.28
RMSF outbreaks in Arizona tribal lands are associated with high site-specific canine rickettsial seroprevalence19,20 (Supplementary Table S1). This contrasts starkly with the retrospective canine seroprevalence of 5% among 329 dogs evaluated 7 years before the initial outbreak recognition in 2003. However, even among tribal communities reporting no human cases, canine spotted fever group serology was 61% during 2005 to 2007, possibly suggesting a regional but sometimes undetected epidemic or cross-reacting rickettsiae given that serologic tests do not differentiate among related rickettsiae.29 Before the epidemic in Mexicali, owned dogs at veterinary clinics and stray dogs had a similar but high seroprevalence of about 60%,30 increasing to 85% in a pilot of symptomatic dogs in the high-risk Los Santorales neighborhood during the epidemic.31 Epidemiological evaluation did not find any significant difference between dogs in neighborhoods of human cases and randomly chosen controls, but seropositive dogs were significantly more likely to have poor body condition and to have a body mass of < 10 kg.16 Heavy tick loads occurred more on dogs that were underconditioned, those that were seropositive, those near canals, and those in homes with abundant yard litter.
US and Mexican residents commonly travel with pets across the border.32 In a border seroprevalence study with the Imperial County (California) Public Health Department, Rickettsia spp–seropositive dogs were statistically closer to a California-Mexico border crossing station than seronegative dogs, with other positive risk factors including owners seeing ticks on the dog, travel to Mexico, and living in a rural area. However, as there were some seropositive dogs without travel to Mexico, it is possible that rickettsial infection was acquired locally.
Sheltered and roaming dogs can be an important reservoir of zoonotic pathogens, and the movement and rehoming of sheltered dogs is a documented risk factor for vector and pathogen spread.33 For example, in 1994, there was no evidence of E canis in shelter dogs in southern California,34 but since 2012, data from private commercial laboratories show a marked increase in seroprevalence for Anaplasma and Ehrlichia antibodies in dogs from San Diego and Imperial County.35 In 2009, a third of shelter dogs in Imperial County were infested with brown dog ticks.36 In a recent study37 of dogs in shelters on both sides of the US-Mexico border, 2 dogs in Tijuana were actively infected with R rickettsii, rickettsial seropositivity ranged from 15% to 80%, and extensive exposure and active infection with E canis and A platys were also detected. Crucially, detection of R rickettsii in blood samples from multiple dogs in Tijuana suggests that the infection prevalence was likely very high, given that rickettsemia in dogs is transient, lasting only 3 to 14 days.25
Rickettsia rickettsii Herd Immunity and Persistence in Metapopulations
Emergent, hyperendemic RMSF at the southwestern US-Mexico border is best approached at the scale of neighborhoods, tribal communities, and communals. These small patches may be linked in metapopulations, which are dynamically interacting local patches, each subject to extinction and recolonization from nearby patches. A metapopulation in northern Mexico may comprise cities in Sonora, Mexicali, Tijuana, and other towns in Baja California and possibly into the US. Each patch has its own RMSF force of infection (rate at which susceptible individuals become infected) determined by dog numbers, transmission rate from ticks to dogs, and infected tick numbers. Dog numbers and local environmental conditions impact tick numbers and are important determinants of local force of infection. Herd immunity arises as dogs survive RMSF but also from dogs recovering from infection with cross-immunizing rickettsiae, including R massiliae or Rickettsia rhipicephali.38 Turnover in the canine population due to birth of puppies and high death rates impedes herd immunity and fuels an epidemic. For example, high-risk areas in Mexicali had higher proportions of younger dogs and higher female dog fecundity compared with lower-risk sites.39
Because of transovarial R rickettsii transmission in ticks, local infection could be maintained without canine infection, although transovarial transmission may incur fitness costs to the female tick and is less efficient than tick-dog-tick transmission.40 In the absence of high host turnover, RMSF tends toward local extinction due to herd immunity, loss of infection in ticks, and demographic stochasticity (as infected ticks became less numerous, there is a random chance that infection may not be transmitted).
Natural declines in rates of RMSF could be misattributed to interventions by public health workers. However, regardless of why a local epidemic declines, interconnection of patches in a metapopulation can account for regional disease persistence. Key to persistence of a pathogen in a metapopulation is a balance between extinction and colonization: excessive colonization contributes to herd immunity and collapse of the metapopulation. RMSF could colonize new patches through human-assisted transport of dogs and less plausibly (given the distances) through movement of roaming dogs and movement of ticks on wildlife. Roaming dogs are an unlikely source for R rickettsii colonization among distant patches because dogs move over only relatively short distances such as 450 m in Mexicali.39 This highlights that human transport of owned and sheltered dogs is a serious risk if not subject to well-implemented surveillance.
Progress Toward One Health
Because dogs are reservoirs for the pathogen and keystone hosts for the tick, canine-focused management is an efficient strategy to manage RMSF epidemics. Brown dog tick populations reach enormous densities in neighborhoods with abundant free-roaming or stray dogs,18,22,41 and the Mexicali survey documented elevations in tick numbers in homes with dogs.16 Aggressive intervention campaigns featuring education programs for physicians and the public, dog spay and neuter programs, treatment of houses with acaricide, and use of long-acting acaricidal collars on dogs saved lives in Mexicali, Sonora, and Arizona, albeit at considerable cost and with rebounds in tick abundance.22,41
Stabilization of dog populations can improve dogs’ quality of life, promote herd immunity, reduce other problems such as damage to vehicles that strike dogs and spread of other diseases such as rabies, and strengthen human-animal bonds. At present, stabilization of dog populations comprises reduction of the susceptible pool of dogs through spay-neuter campaigns and encouraging residents to keep fewer dogs as well as campaigns to restrain dogs to a home. On-dog acaricide treatment can help reduce tick numbers. Targeted interventions in Arizona and Sonora used long-lasting tick collars (10% imidacloprid, 4.5% flumethrin), marketed as controlling ticks for 8 months. Another effective acaricide against brown dog ticks is oral flurulaner, which is administered every 3 months.
Anti-tick or anti-Rickettsia vaccines for dogs would be an enormously beneficial strategy to reduce RMSF42 and could allow for reduced acaricide use, lower environmental contamination, reduced acaricide resistance, and protection against multiple tick species. Progress in vaccinating against ticks has been made, including for example BM86, which protects cattle from Boophilus ticks by allowing them to develop antibodies against key tick proteins, reducing fecundity or survival of the ticks exposed to the vaccinated host.43 A crude tick gut extract showed slight efficacy against brown dog ticks in dogs.44 Of note, however: while tick numbers would hopefully decline, a vaccinated dog might still be vulnerable to infection by any ticks that do bite. Therefore, anti-rickettsial vaccines are another important tool. Despite the benefits of such a vaccine, limited profits to vaccine makers would tend to slow progress due to relatively low numbers of cases and their limited geographical scope.
Knowing the force of infection and turnover rates in canine populations, it is possible to calculate the fraction of the canine population that must be vaccinated to achieve protection through herd immunity. This would superimpose upon naturally developing herd immunity in a stable population of dogs that survive infection. One report45 claimed persistent antibodies for at least 1 year following tick-induced infection with R rickettsii, suggesting that resistance to reinfection is likely to extend beyond a year. Importantly, control of RMSF must target an entire community rather than individual homes, in part because dogs often roam and carry their ticks with them, and people may be infected even if they do not own dogs.16
Challenges to One Health and Management of RMSF
Lack of resources, lack of knowledge, technology challenges, and policies contribute to an inability to contain RMSF epidemics. These challenges are summarized in Supplementary Table S2. A needed technological advance would be canine vaccines, as described above. Data would also be needed, potentially integrated into synthetic mathematical modeling, on canine population turnover rates of dogs dying and puppies being recruited, numbers of dogs per home, fractions of homes having dogs, and so forth. Evaluating vaccine efficacy is also predicated on knowing human and canine infection prevalence, which is challenged by low serosurvey specificity and low PCR prevalence. Where cases are common, risk assessment is informed by human case reports. More work is needed to identify early canine cases through advanced molecular and related approaches.
Poverty is an overarching risk factor for epidemic RMSF, contributing to low health literacy, lack of awareness of risk and measures to protect oneself, impeded access to medical care, and an inability to manage or protect dogs. Neighborhoods with high marginalization status often feature dirt, rock, and concrete substrate (as opposed to grass), proximity to agriculture canals, and trash on the property and are often on a hillside. Even where the public seems knowledgeable about RMSF and dog owners treat their dogs with an acaricide, this often includes ineffective products including garlic, some flea medications, herbs, and unmedicated shampoos. Fipronil is a cost-effective acaricide often used in Mexico (not including the methoprene packaged in proprietary combinations in the US), but is not recommended for brown dog tick eradication.46 Effective long-acting acaricides are cost-prohibitive in many areas. Also, area-specific acaricide resistance should be investigated, given reports of resistance to permethrin, fipronil, and deltamethrin in parts of the world.46
Brown dog ticks are notoriously difficult to eradicate,47,48 and infestation often reoccurs, possibly associated with inadequate penetration of the acaricide into building and landscape cracks or reinfestation. Better integrated pest management approaches to brown dog tick management in the environment should be developed.
Of great concern is the shift from isolated rural areas to large urban centers and from northern to southern California. In Mexicali and Tijuana, some of the hardest-hit neighborhoods have characteristics resembling some rural villages with dirt roads, temporary shelters for housing, minimal municipal facilities, and abundant roaming dogs. Although phylogeographic analysis clearly indicated that the origin of the epidemic in Arizona was not Mexico or Central America but rather the eastern US5 and that northern Mexican cases could have had Rocky Mountains origins,49 typically we do not know whether new hotspots represent new introductions or areas where sporadic cases had been overlooked. We also lack understanding of how much movement there is of dogs among neighborhoods and cities.
Wraparound intervention includes physician and public education, improved access to medical care and tetracycline, canine management, and environmental and on-dog tick treatment. However, not knowing the relative contribution of each component impedes future, less well-funded interventions where the most efficacious single approach must be prioritized.
There is no evidence that either brown dog ticks or the pathogen has evolved to spread disease more efficiently or to be more pathogenic, although isolates of R rickettsii from northern Mexico are not available for experimental work. In fact, were the tick or pathogen to have become more efficient, development of local herd immunity might be more rapid and lead to local extinction of the disease.
Policy constraints to RMSF management include anthropogenic climate change. Despite generalizations that the tropical lineage of the brown dog tick is restricted to tropics and subtropics zones,50 this lineage can be found sympatrically with the temperate lineage,51 suggesting that we do not know true environmental determinants for the species. Environmental warming could promote expansion of the tropical tick lineage52 and RMSF cases to cooler, coastal cities. However we do not know in detail how the 2 lineages differ in vectorial capacity (ie, the composite of the vector’s innate capacity for pathogen acquisition, propagation and transmission, and host and other environmental factors that influence pathogen dissemination from the vector). Because clinical index of suspicion and early treatment are essential for survival, changes in tick and disease distributions represent a serious challenge for management of RMSF.
Another policy concern relates to transport of infected dogs and ticks. People and dogs move all over the world, particularly at the Tijuana–San Diego border crossing. An outbreak in Yucatan state was speculated to have occurred due to movement of RMSF associated with global trade.53 To this point, moving dogs across international borders with very limited disease surveillance or regulatory oversight could represent a chronic risk of disease introduction and spread.
Because of differing case definitions for human infection and reporting guidelines between the US and Mexico and among Mexican states, it is difficult to compare epidemiology and progress in control. Intervention is under-resourced everywhere, but we advocate for increased data sharing and harmonization of methodology and reporting guidelines, which could also reduce redundant efforts across jurisdictions and preserve resources for RMSF management.
Conclusion
RMSF is a devastating tick-borne disease that disproportionately targets impoverished communities, marginalized neighborhoods, and tribal towns at the US-Mexico southwestern border. Dogs and people suffer this often fatal infection, and awareness of the risk, means to protect people and dogs, and treatment may be limited. Intervention campaigns protect lives but are extremely resource-intensive. Even with unlimited resources, more science is needed to understand strategic but effective use of resources. Additional veterinary capacity could enhance spay-neuter and canine control programs, together with education campaigns regarding benefits of canine management. Research innovations to bring vaccines into use and modeling to guide interventions are needed, as are sociopolitical changes such as dog restraint regulations and harmonized interstate and international reporting and communication. We encourage a One Health disease ecology framework to prevent and manage, and to guide interventions and assessments, because this very large problem requires efficient, creative, and evidence-based solutions.
Supplementary Materials
Supplementary materials are posted online at the journal website: avmajournals.avma.org.
Acknowledgments
None reported.
Disclosures
The findings and conclusions in this article are those of the authors and do not necessarily represent the official position of the CDC. The findings and conclusions in this article are those of the authors and do not necessarily represent the views or opinions of the California Department of Public Health or the California Health and Human Services Agency.
No AI-assisted technologies were used in the generation of this manuscript.
Funding
This research was funded through the Pacific Southwest Regional Center of Excellence for Vector-Borne Diseases, funded by the US CDC (Cooperative Agreement 1U01CK000516).
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