Medically important ants: a systematic review of the global distribution and clinical consequences of their bites and stings

Medically important ants: a systematic review of the global distribution and clinical consequences of their bites and stings

Hormigas de importancia médica: revisión sistemática de su distribución global y consecuencias clínicas de sus mordeduras y picaduras

About the authors:
  • 0000-0002-6885-6353 Olivera, Mario Javier 1 *
  • 0000-0003-1861-4601 Porras Villamil, Julián Felipe 2
  • 1  Instituto Nacional de Salud. Bogotá DC, Colombia.
  • 2  Universidad Nacional de Colombia, Facultad de Medicina. Bogotá DC, Colombia.
Authors notes:
Corresponding author: moliverajr@gmail.com

No conflict of interest exists.

Mario Javier Olivera: Conceptualization, formal analysis, methodology and writing original draft.

Julián Felipe Porras-Villamil: Conceptualization, formal analysis, methodology and writing original draft.

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ABSTRACT
Introduction:

From the medical point of view, only some ants are of special interest. Due to the diversity of ants and the growing contact with humans, it is necessary to have a better understanding of the factors and problems, which lead to adverse clinical outcomes.

Objective:

The aim of this study was to conduct a systematic review of published studies on ants and their impact on the medical field to synthesize fragmented knowledge and to inform the current state of this problem.

Methods:

A systematic literature review was conducted in Medline, EMBASE, SciELO and Google Scholar, with no time threshold. The search strategy was limited to articles published in Portuguese, English and Spanish. Eligible studies were case reports and case series that reported outcomes in humans caused by ant stings. Patient-level and study-level information was extracted.

Results:

The literature search yielded 1909 studies; of which 30 case reports and 16 case series reporting a total of 95 cases were included. Of these 48 patients were women (50.5%), and the median age was 36.1 ± 25.5 years old. The most frequently reported complications were severe pain, anaphylaxis and acute respiratory distress syndrome. The death of eighteen patients was documented (18.9%). Ants from the genera Solenopsis spp., Myrmecia sp., Paraponera clavata, Pachycondyla sennaarensis, Myrmecia rubra caused most of the accidents

Conclusions:

Severe allergic reactions caused by ants are a rare event, however, mortality can be high. An increase of ant related accidents is expected, a quick diagnosis and treatment is necessary to avoid fatalities.

RESUMEN
Introducción:

Desde el punto de vista médico, solo algunas hormigas son de especial interés. Debido a la diversidad de hormigas y al creciente contacto con humanos, es necesario comprender mejor los factores y problemas que conducen a resultados clínicos adversos.

Objetivo:

Realizar una revisión sistemática de estudios publicados sobre las hormigas y su impacto en el campo médico para sintetizar conocimientos fragmentados e informar sobre el estado actual del problema.

Métodos:

Se realizó una revisión bibliográfica sistemática en Medline, EMBASE, SciELO y Google Scholar, sin límite de tiempo. La estrategia de búsqueda se limitó a artículos publicados en portugués, inglés y español. Se seleccionaron informes y series de casos sobre consecuencias de las picaduras de hormigas en humanos. Se extrajo información a nivel de paciente y a nivel de estudio.

Resultados:

La búsqueda bibliográfica obtuvo 1 909 estudios, de los cuales se seleccionaron 30 informes y 16 series sobre un total de 95 casos. De estos, 48 pacientes eran mujeres (50,5 %) y la media de edad era 36,1 ± 25,5 años. Las complicaciones más frecuentes fueron dolor intenso, anafilaxia y síndrome de dificultad respiratoria aguda. Se documentó la muerte de 18 pacientes (18,9 %). Hormigas de los géneros Solenopsis spp., Myrmecia sp., Paraponera clavata, Pachycondyla sennaarensis y Myrmecia rubra causaron la mayoría de los accidentes.

Conclusiones:

Las reacciones alérgicas graves provocadas por hormigas son un evento raro; sin embargo, la mortalidad puede ser alta. Se espera un incremento de los accidentes relacionados con las hormigas. Se requiere un diagnóstico y tratamiento rápidos para evitar muertes.

Keywords:
    • ants;
    • Formicidae;
    • humans;
    • allergy;
    • bites and stings.
Palabras clave:
    • hormigas;
    • Formicidae;
    • humanos;
    • alergias;
    • mordeduras y picaduras.

Introduction

Ants are insects that belong to the Order Hymenoptera (with over 150 000 species)1 which include wasps, hornets and bees; ants are one of the most common insect families,2 they belong to the superfamily Formicoidea with currently more than 12 500 species in 290 genera being described.3 This insects are characterized by having a wide distribution, and an incredible species richness and abundance,4 and are one of the best adapted organisms to urban life and hostile environmental conditions5,6 and can cause a wide array of clinical conditions.7 Subfamilies Ponerinae, Dorylinae and Myrmiciinae are important to medical and veterinary dermatology.8 Due to their inherent diversity the members of this superfamily generate a diverse assemble of injuries from mechanical damage to envenomation to systemic manifestations.9

The ants that can cause systemic reactions have been found around the world, for example Fire Ants, have been found in Asia, Australia and throughout the American continent;10 showing the importance of this types of ants in the medical field.11 Being this the case, physicians must be aware of the management of the different medical conditions that can be produce after a bite or sting, which in severe allergic reactions, includes the use of intramuscular epinephrine in the lateral aspect of the thigh (Vastus lateralis),12 as well as the use of antihistamines and corticosteroids.13 One important aspect is that approximately 1% of children and 3% of adults are allergic to Hymenoptera stings, many without history of a sting reaction.14

On the other hand, ants can serve as mechanical vectors carrying potentially serious pathogens, possibly having an impact on hospital infections,15 circumstance that is increasingly important16 as more ants are being identified as carriers.17 On the other hand, ants appear to have beneficial properties. For example there is evidence that ant venom has anti-cancer properties,18 are important in the control of pests in certain settings19 and are able to distinguish between Diabetes Mellitus and Diabetes insipidus (ants are attracted to the urine of the former).20 Also, the use of mandibles of giant ants, such as Eciton burchellii, Eciton hamatum in America and Dorylus sp. in Africa, as a suture method has been documented. 21,22)

Finally, as greenhouse gases accumulate, new areas could be colonized, allowing invasive species to cross the environmental barriers that are being erased by climate change, making contact with such insects more probable and more clinically important.23 Especially in remote locations and rural areas,24 which can be a call to use mobile health teams and field epidemiologists to manage an attend these medical problems,25 which can be a good strategy. Due to the increasing importance of ants in the medical and veterinary field, due to the climatic changes that humanity will face head on in the following decades and the wide array of clinical conditions and species responsible of such, this study aimed to assess the impact on human health of ant bites/stings, through a systematic review

Methods

Search strategies

Systematic literature searches following the PRISMA strategy were conducted in the following databases: Medline, EMBASE, SciELO and Google scholar. The search strategy combined five search terms related to the impact of ant bites on human health: 1) Ants, 2) Formicidae, 3) Disease, 4) humans and 5) mortality. The search included all publications until July 31, 2018, with no specific start date.

Study selection and data extraction

The studies were eligible for inclusion if they reported cases or series of cases of ant bites and included at least one patient. We defined studies as a case report if they described a single case and as a series of cases if they described more than one patient. Studies that were not published in English, Spanish or Portuguese were excluded. Two reviewers independently screened the search results for inclusion and then extracted all data using a standardized data extraction form. The discrepancies were resolved through discussion until consensus was reached. Information was extracted about the first author, country, year of publication, genus and species of ant, number of patients, age, sex, clinical manifestations and the outcome of death or complete remission.

Statistical analysis

The data extracted were summarized as means with standard deviation for quantitative variables and as number and percentage for qualitative variables, as appropriate. Comparisons between groups were performed using the chi-square test or Fisher's exact test, depending on the case. All analyses were performed using the statistical package Stata, version 13.0 (Stata Corp LP, College Station, TX, USA).

Results

Description of included studies and data obtained

The systematic literature searches yielded 1909 studies (Fig. 1). Among these, 1453 duplicates were excluded. On screening titles and abstracts for relevance, 220 studies were excluded, giving a total of 236 full texts that were assessed. Of these, 46 studies met the inclusion criteria.

PRISMA strategy and results.

From: Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 6(7): e1000097. doi.10.1371/journal.pmed.1000097

Of the 46 included studies, 30 case reports and 16 case series reported a total of 95 cases. The 95 cases included in this review had an average age of 36.1±25.5 years old and 48 were women (50.5%). Tables 1 shows some sociodemographic characteristics of the cases included in this study, as well as the outcome of the case and the involved ant species in a regional basis. Table 2 shows the signs and symptoms registered in the different reports.

Case Reports, Sociodemographic characteristics, Country and Ant Species involved from the different regions of the World

Regarding clinical manifestations, it was found that the most frequently reported complications were Severe pain, Anaphylaxis and Acute Respiratory Distress Syndrome. The death of eighteen patients was documented (18.9%), all of these reported fatalities originated from the United States of America, although deaths secondary to ant attacks must have occurred elsewhere. Ants from the genera Solenopsis spp, Myrmecia pilosula, Paraponera clavata, Pachycondyla sennaarensis, Brachyponera chinensis, Myrmecia rubra, Pseudomyrmex spp. caused most of the accidents.

Results found in this review by region were the following:

  • Asia: In this region of the included cases 64.2% were Male. 14 cases were included. The countries of origin were Iran, Korea, Taiwan, Sri Lanka, India and Thailand. The average age of the cases was 25.6±13.4. Pachyncondyla sp., Polyrachis sp., Solenopsis sp., Oecophylla sp., Barchyponera sp., Pheidole sp. and Monomorium sp.

  • Africa: Just one report, a 40 years old Male from Uganda, with a case produce by Dorylus sp.

  • Europe: 3 reports, one from Spain the others from Italy, with a mean age of 15±11.5, 66% female. Involved genus: Solenopsis sp., Crematogaster sp. and Pheidole sp.

  • North America: A total of 19 reports (18 from the United States of America, 1 from Canada), 47.3% were women, Mean age of 36.4±28.5 years-old. Solenopsis sp, Formica sp. and Pogonomyrmex sp.

  • South America: 6 cases, 4 Males 2 females, mean age of 42.1±20 years. Genus involved: Solenopsis sp., Pseudomyrmex sp., Pachycondyla sp., Odontomachus sp. and Dinoponera sp.

  • Oceania: 3 reports from Australia, 2 males 1 Female, mean age 18±25. Genus involved: Myrmecia sp. Rhytidoponera sp. and Solenopsis sp.

Signs and symptoms registered in the case reports included in this review

Additionally, in this systematic review it was found that 40% of the reports originated from the United States of America, followed by Iran (8.6%), Australia (6.5%) and Brazil (6.5%), the majority of reports (76%) were published posterior to the year 2000, 21 from 2000 to 2009 and 14 from 2010 to 2018. At last, in an study published by from Klotz et al.,72 cases were registered from Europe (Formica rufa), Australia (Myrmecia pilosula, Myrmecia forficate, Myrmercia pyriforimis), Tasmania, Korea (Brachyponera chinensis, Pachycondyla (Ectonomyrmex) sp.), Japan (Brachyponera chinensis), Venezuela (Odontomachus bauri) and the United States (Hypoponera punctatissima, Solenopsis aurea, Solenopsis xyloni, Solenopsis geminate, Tetramorium sp, Pogonomyrmex maricopa, Pogonomyrmex barbatus, Pseudomyrmex ejectus) some of those from different species than those found in this review.

Global distribution of medically important ants according to the Systematic Literature Review

Table 3 shows a summary of the medically important ants divided by the regions in which reports have been written based on the findings of the systematic research of literature.

Distribution of ant species and medical Importance based on the Information found in this Review

Africa

In this continent, Safari ants (Dorylus spp.), also known as Siafu, Army or Driver ants, are characterized by having colonies with millions of individuals capable of causing ulcers secondary to biting26 and anaphylaxis by injecting venom in multiple stings.41 Allergic reactions can also be caused by Cataglyphis sp.73 and Pachyncodyla sennaarensis,39 the latter with severe anaphylactic reactions.74

South America

In this region of the world systemic reactions are cause in general by ants of the genera Solenopsis sp. (Fire Ants, “Hormiga Colorada”), Pseudomyrmex sp. (Novice ants) and Paraponera sp. (Tocandira or Bullet Ants).9 A clinical condition, first diagnosed in 1968,75 called West Indian Punctate Keratopathy76 is in reality caused by Wasmannia auropunctata77 which can cause leukomas.78 Fire Ants, as well, can cause damage to the cornea.79 Other important ants are: Pseudomyrmex spp.,64Odontomachus bauri65 and Pachycondyla goeldii.67 On the other hand, Dinoponera gigantea 80) can cause mechanical damage.

North America

In the United States the most commonly involved ants are the Red Fire Ants (Solenopsis invicta) and the Black Fire Ants (Solenopsis richteri). These ants arrived in the first half of the XX century through the port of Mobile, Alabama. 81) The sting of this ant causes pustules with a clear clinic pathologic evolution.81 This ant has invaded at least 14 states82. Such attacks can be fatal.83 In infested areas the frequency of stings per month84 and annual attack rate are high85. In addition, cutaneous sporotrichosis caused secondary to stings of this kind of ants has been reported86. Several other species of ants of medical importance in this region have been reported.52,87 In Canada, the first reported case of Fire ant attack was documented in 2013. 88) The attacks of this ants have been documented in all age groups and in all places and settings.54,89

Asia

In Asia, medically important species belong to the genus: Pachycondyla sp.,27,90Polyrachis dives91 and Solenopsis geminate (30). Weaver Ants eggs have also been involved in allergic reactions.92 Other less common ants belong to the following genus: Tetraponera sp., Odontomachus sp.32 and Brachyponera sp.93 In the Middle East the Black Samsun Ant94 is one of the most important causes of allergies. Ants of the species Pheidole sp., which are believed to be lipophilic, can cause alopecia.34-36 Allergic reactions to Monomorium pharaonis have also been reported.95

Oceania

In Australia, Myrmecia pilosula (96), Rhytidoponera metallica (97) and Myrmecia pyriformis are considered dangerous (90). Solenopsis invicta has caused anaphylaxis cases (71) and deaths (98). Other ants to which patients have shown hypersensitivity belong to the genus Myrmecia sp. (99). Solenopsis geminata have caused allergic vasculitis in Indonesia.100

Europe

In Italy, the most frequent insects causing cutaneous allergies were ants of the species Solenopsis fugax and Monomorium destructor.101 Allergic reactions has been reported caused by Solenopsis invicta,102Crematogaster scutellaris42 and Formica rufa.103 In Italy a case of alopecia caused by ants of the species Pheidole pallidula (Barber ant) on an Italian adolescent when he acquired the infestation in Iran.43

Ants as Mechanical Vectors

These insects can be mechanical vectors of many pathogens104 and can be pests in hospitals.105 A study conducted in Brazil, found that at least 19 species of ants belonging to 5 subfamilies infested hospitals and nosocomial settings, including species of Acromyrmex sp., Labidus sp., and Solenopsis sp.,106 associated bacteria include Bacillus spp., Listeria spp., Arcanobacterium spp., Streptococcus spp., Pseudomonas aeruginosa among others.107 Also they can transport this nosocomial bacteria to the community.108

Ants in the Forensic Field

Formicidae are also important in the forensic field being active in several if not all the stages of the decomposition process. For example, if we consider that this process can be divided in 5 stages (Fresh carcass, Bloated, Active, Advanced and the final stage Remains),109 several genera of ants (Camponotus sp., Cephalotes sp., Solenopsis sp., amongst others) are the most prominent insect species in the first two stages. In this invasion ants influenced the time of decomposition of the carcasses and preyed on eggs and larvae of Diptera delaying colonization and decomposition.110 Additionally, ants are capable of producing post-mortem injuries specially in the early period111 that can cause post-mortem bleeding112 and injuries that can be confused of being done in an antemortem setting,113 obscuring the estimation of the postmortem interval.114 The invasion of dead bodies have been documented in other locations involving similar genera.115 On the other hand, ants can aid in the forensic investigation, the analysis of such insects, in this case the species Lasius fuliginous, led to the identification of the crime scene.116

Ants as Biomarkers of Environmental Degradation

Ants also can be used to determine the state of environmental health; in Brazil, for example a study in Mato Grosso found that species of Camponotus (Mymaphaenus) sp. and Forelius brasiliensis can be considered bioindicators of environmental degradation whereas Camponotus atriceps, Pachycondyla crassinoda and Paraponera clavata are associated to preserved environmental condition.117

Ants as Pests in Insectariums

It has been shown that ants can be detrimental and damaging to the species of arthropods contained in insectariums. One of such examples are the species Tapinoma melanocephalum which is capable of eating the eggs of different species of Mosquitos (for example Aedes aegypti) and Triatomine bugs (for example Triatoma flavida).118

An infographic summarizing the findings of these review can be found in figure 2.

Infographic of the Medical Importance of Ants.

Discussion

This comprehensive systematic review provides an overview of the ants of medical importance, their distribution and effects of the sting on human health, which can lead to death. Although not all ant stings lead to allergic reactions, some species have the capacity to generate an allergic response with a range of clinical presentations, which may include local reactions to serious systemic reactions such as anaphylactic shock. Although these events are rare, once they occur, mortality is high.

Our results show that there are different species of ants that can generate important consequences in human health. These ants are distributed worldwide and can affect people in any age range and sex. In this review no difference in the reports between sexes was found.

The contact of humans with this type of insects and other arthropods,119 is increasing, and in turn increases the number of accidents. This increase is the result of urban expansion, the accumulation of garbage that attracts insects, and the incredible capacity of the Formicidae superfamily to adapt to diverse environments, from humid forests to deserts.23

Despite their importance they are a little studied group, they have not received the due attention from the researchers; it is necessary to know much more about ants and the Order Hymenoptera. There is still controversial evidence about possible cross-reactions between different poisons of different species,120 the evolutionary relationship of such poisons across genera and the distribution of attacks around the world.121,122

The clinical effects caused by ant stings can range from localized reactions with clinical manifestations such as pain, papules, vesicles, pustules and ulcers to systemic reactions with blurred vision, dizziness, vomiting, diarrhea and anaphylaxis,9 also coma123 or alterations during pregnancy,124 reactions with varying degrees of severity,125 which can have fatal consequences.126 This systemic reactions, that can be immediate127 or not existent,128 are important in children,129 and are usually caused by allergens present in the venom of some genera of ants (for example Solenopsis sp., Pachycondyla sp., and Myrmecia sp.). These allergens are different between genera and are composed of biogenic amines, cytotoxic and neurotoxic peptides (melittin, apamin, mastoparan) as well as proteins (for example phospholipase A).130,131

The venom of Fire Ants (Solenopsis sp.), which are one of the most studied ants groups,81 because this species has invaded several countries around the world in the continents of America, Europe, Asia and Oceania. It is an aggressive genus that have displace the indigenous species and are responsible for vicious indoors and outdoors attacks and have proven to be a difficult to control ant, with over 70 years of foothold in the United States. Although its global importance has already been documented,10 have a venom with at least have at least four different groups of allergens, each with different functions, primarily enzymes and proteins.97 This venom have cross reactivity across species of the same genera132 and other members of the order,133 although cross reactivity with other genera of ants have controversial evidence.134 For the management of the allergic reactions there is an existent therapy to desensitize the patients,135 although there are designed patterns of administration,136,137 there is contradicting evidence of the effectivity of this therapy.138 At last, the epidemiology of attacks and its distribution in central and south America is all but unknown, although attempts to identify and clarify such aspects of their ecoepidemiology.139

Lastly, ants carry a several number of potentially serious pathogens,140 one of the first reports of this aspect of its biology was published in the seventies involving Pharaoh’s ants (Monomorium pharaonis) in the United Kingdom141 and Germany.142 Circumstance that is increasingly important 16) given that other ants have been identified as carriers of this poison and have been found in places considered clean, such as nurseries and food depots.(17)

The main limitations of this study include a possible publication bias because less significant findings are less likely to be published, and that may have inflated estimates of mortality. On the other hand, information on the clinical manifestations and comorbidities of the patients was limited, which have a strong impact on mortality. In addition, there were case reports, which are known to have low methodological quality and are not representative of the population.

In conclusion, the systematic review conducted in this study indicates that severe allergic reactions caused by the bite/sting of ants are a rare event, however, once they occur, mortality is high. It is expected to increase the number of accidents of ants of medical interest with humans, for which it is necessary to quickly diagnose and treat cases adequately and thus avoid a death. All the clinical manifestations that can be caused by the bite/sting of ants are unknown. It is important to mention that only a small percentage of the ant species are of medical interest and some species are of great importance in other fields of knowledge.

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History:
  • » Received: 18/02/2019
  • » Accepted: 19/12/2020
  • » Publicado : 01/04/2021

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