Review article Ant allergens and hypersensitivity reactions in response to ant stings Rutcharin Potiwat1 and Raweerat Sitcharungsi2 Summary Hypersensitivity reactions caused by ant stings are increasingly recognized as an important cause of death by anaphylaxis. Only some species of ants ( e.g. Solenopsis spp., Myrmecia spp., and Pachycondyla spp.) cause allergic reactions. Ant species are identified by evaluating the morphologic structures of worker ants or by molecular techniques. Ant venom contains substances, including acids and alkaloids, that cause toxic reactions, and those from Solenopsis invicta or the imported fire ant have been widely studied. Piperidine alkaloids and low protein contents can cause local reactions (sterile pustules) and systemic reactions (anaphylaxis). Imported fire ant venoms are cross-reactive; for example, the Sol i 1 allergen from S. invicta has crossreactivity with yellow jacket phospholipase. The Sol i 3 allergen is a member of the antigen 5 family that has amino acid sequence identity with vespid antigen 5. The clinical presentations of ant hypersensitivity are categorized into immediate and delayed reactions: immediate reactions, such as small local reactions, large local reactions, and systemic reactions, occur within 1–4 hours after the ant stings, whereas delayed reactions, such as serum sickness and vasculitis, usually occur more than 4 hours after the stings. Tools for the diagnosis of ant hypersensitivity are skin testing, serum specific IgE, and sting challenge tests. Management of ant hypersensitivity can be divided into immediate (epinephrine, corticosteroids), symptomatic (antihistamines, bronchodilators), supportive (fluid resuscitation, oxygen therapy), and preventive (re-sting avoidance and immunotherapy) treatments. (Asian Pac J Allergy Immunol 2015;33:267-75) From 1. Department of Medical Entomology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand 2. Department of Tropical Pediatrics, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand Corresponding author: Raweerat Sitcharungsi E-mail: [email protected] Submitted date: 11/12/2015 Keywords: Allergy, ant stings, hypersensitivity, immunotherapy, treatment Introduction Ants are insects and belong to the order Hymenoptera and the family Formicidae. There are currently more than 12,500 ant species known. Although some species of ants can bite and sting humans, only some ant genera, such as Solenopsis, especially S. invicta and S. ricteri (commonly known as imported fire ants), cause life-threatening allergic reactions. Ant hypersensitivity is one of the most important causes of severe systemic reactions or anaphylaxis with reports of fatalities from ant anaphylaxis occurring worldwide in both urban and rural areas. The diagnosis of ant hypersensitivity can be performed by allergic history and physical examination of the ant sting, or by in vivo and in vitro tests. The management of ant hypersensitivity can be divided into immediate treatment for anaphylaxis, and preventive treatment. However, knowledge of ant-induced allergic reactions in some parts of the world is limited. This article reviews ant diversity and distribution, the medical importance of ant stings, ant allergens, and their cross-reactivity, as well as the clinical presentations and management of ant hypersensitivity reactions. This information will enhance the basic knowledge of ants for scientists and provide an overview of therapeutic guidelines for physicians. Ant diversity and distribution Ants are social insects classified in the family Formicidae, order Hymenoptera. Ants are diversely spread among continents and biogeographic regions with more than 12,500 species in 290 genera belonging to 21 subfamilies having been identified thus far. Tropical areas and continental forests have the greatest influence on the presence of ant species diversity. In Thailand, 247 ant species distributed among 55 genera in nine subfamilies have been recorded.1-4 Six of these species (Aenictus artipus, Leptanilla thai, Lophomyrmex striatulus, Tetramorium ciliatum, Tetramorium flavipes, and Tetraponera 267 Downloaded from http://www.apjai-journal.org. For personal use only. No other uses without permission Asian Pac J Allergy Immunol 2015;33:267-75 notabilis) were originally described from Thai territories and are located in agricultural fields and forests.5 Invasive ants are exotic species that establish colonies outside their native areas and can cause a decline or a change in diversity, community, and populations of native invertebrates, vertebrates, and plants by their invasion and displacement.6 However, invasive ant species, such as Solenopsis geminata and Tetraponera rufonigra, can also play an important role in the impact on clinical hypersensitivity reaction.7, 8 The important invasive ant species are widely distributed worldwide (Table 1).9-11 Of these invasive ant species, Anoplolepis gracilipes (yellow crazy ant), Pheidole megacephala (big-headed ant), and Solenopsis geminata (tropical fire ant) are all present in Thailand.6 The yellow crazy ant is thought to decrease the diversity and population of native fauna and flora in ecosystems due to its replacement of natural native species, but information on its distribution is rarely reported. The medical importance of ant-induced hypersensitivity Thailand has a number of ants of medical importance. The red imported fire ant (Solenopsis invicta, Buren) is an important invasive ant species that is also present in many other parts of the world, and is considered to cause hypersensitivity in both children and adults. Other fire ants in the genus Solenopsis, including S. invicta, S. richteri, S. geminata, S. saevissima, S. xyloni, and S. aurea can cause allergic reactions.10, 12 Importantly, there is cross-reactivity among venoms of the Solenopsis species, such as S. xyloni and S. aurea, and other hymenoptera.13, 14 The tropical fire ant (S. geminata) is a natural native species with a wide distribution throughout Thailand whose stings can cause allergic reactions. Another group of ants that cause hypersensitivity belong to the genus Myrmecia, especially M. pilosula, which are found in Australia.15-17 However, the ant species that are most commonly responsible for anaphylaxis in Thai patients are Solenopsis geminata, Tetraponera rufonigra, and Odontoponera denticulata (Figure 1). Patients with stings from these ants were referred to tertiary care hospitals in Bangkok for immunotherapy, and ants were sent for species identification at the Faculty of Tropical Medicine, Mahidol University (unpublished data). All three species are aggressive ants with painful bites or stings. Both T. rufonigra and O. denticulata have a stinger at the end of the gaster (Figure 2). T. rufonigra-induced hypersensitivity has been reported in humans after stings and can cause severe anaphylaxis.18 The first case of T. rufonigra-induced anaphylaxis was reported from Thailand. The patient was a 17-month-old girl who presented with two episodes of urticaria, angioedema, dyspnea, and loss of consciousness.7 Species identification of the most common causative species of ant anaphylaxis in Thailand The most common causative species of ant anaphylaxis in Thai patients are Solenopsis geminata, Tetraponera rufonigra, and Odontoponera denticulata. S. geminata belongs to the family Formicidae, subfamily Myrmicinae, genus Solenopsis, species geminata. The morphology of Solenopsis can be confused with a smaller species of Monomorium, although Solenopsis is distinguished by the presence of a two-segmented petiole.19, 20 Identification of fire ant species is very difficult and involves evaluating the morphology of worker ants rather than just one specimen. S. geminata workers have a polymorphic size of 3–8 mm body length. The body has a reddish brown color and is mostly smooth and shiny, without sculpture. The head of the S. geminata worker is divided into two notches, while in S. invicta workers these notches are absent (Figure 2). The differentiation of tropical fire ant morphology is determined using worker ants but can also be characterized using molecular techniques based on mitochondrial DNA encoding cytochrome oxidase subunit I (COI) or the internally-transcribed spacer (ITS) gene.21 The differentiation of Solenopsis species by morphology alone is difficult and can often be confused with other species; therefore, molecular identification is now widely used. PCR amplification of the COI gene followed by cutting nucleotide sequences with the HinfI restriction enzyme can be used to distinguish S. invicta, S. geminata, and S. xyloni from Florida.22 However, even though molecular amplification is now widely used, it is expensive. T. rufonigra belongs to the family Formicidae, subfamily Ponerinae, genus Tetraponera, species rufonigra. It is black and shiny except on their alitrunk that has an orange line, which is the specific characteristic of T. rufonigra. Differentiation of 268 Downloaded from http://www.apjai-journal.org. For personal use only. No other uses without permission Hypersensitivity to ant stings Table 1. The geographical distribution of major invasive ant species. Ant species Geographical Range Reference(s) Native Invasive species Anoplolepis gracilipe* Africa, Tropical Africa, Asia, Australia, Caribbean, Indian and Pacific (Yellow crazy ant) Asia? Ocean 91 Dinoponera gigantea Amazonian states 92 Hypoponera sp. Brazil, Malaysia 93, 94 95, 96 Linepithema humile South America, Africa, Asia, North America, Atlantic and Pacific (Argentine ants) Argentina Ocean, North Carolina (US) Myrmecia pilosula Far East, Australia 47, 66, 71 Odontomachus bauri Caracas, Venezuela 71, 97 Virginia, North and South Carolina (US), Georgia 98, 99 Pachycondyla chinensis (Chinese Japan, Asia needle ant) Pachycondyla sennaarensis (US) West Africa Australia, Iran, Saudi Arabia 100, 101 Africa Australia, North and South America, Caribbean, 10 (Samsum ants) Pheidole megacephala (Big-headed ant) Indian and Pacific Ocean Pseudomyrmex ejectus Brazil 71 Rhytidoponera metallica Queensland (Australia) 71 Southern California (US) 13 Solenopsis geminata Central, North Asian islands including Indonesia, Taiwan, Pacific 44, 102-104 (Tropical fire ant) and South island, Florida, Hawaii, Caribbean, and Thailand Solenopsis aurea America, Asia Solenopsis invicta South America (Red imported fire ant) Solenopsis richteri Spain, southern China, southeast Asia, Brisbane, 13, 105-107 Australia, North American western states, Brazil South America Saudi Arabia, Mississippi, Alabama, North America 13, 44, 108 (Black imported fire ant) Solenopsis saevissima São Paolo (Brazil) 109, 110 Solenopsis xyloni Southwestern states (US), Mexico 13, 44 Sri Lanka, Thailand 7, 18 Wasmannia auropunctata Central and South Africa, Caribbean, Pacific Ocean, South and North 111, 112 (Little fire ant) America America Tetraponera rufonigra * Origin of the yellow crazy ant is unknown although some studies indicate it is from tropical Asia. T. rufonigra and O. denticulata can be done by the body shape, color, and the number of nodes on the petiole segments. T. rufonigra has two nodes on the petiole segment while, O. denticulata has a single node (Figure 1). Moreover, O. denticulata has a narrow node with a small spine on the petiole segment. Ant sting and venom isolation The tropical fire ant (S. geminata) is an aggressive fire ant with a painful sting that is potentially life threatening.23 Normally, anaphylactic reactions caused by ants occur in patients that come into contact with the ant venom during stinging.24 In general, the constituents of ant venom responsible for anaphylaxis are composed of spray acid and alkaloids derived from piperidine.25,26 The ant venom is usually injected from a poison gland located at the posterior part of the ant (gaster), which secretes various chemicals from different compartments depending on whether the ant is a queen or a worker.20 The main toxic chemicals from an S. geminata queen were identified by gas chromatography–mass spectrometry and included 2alkyl-6-methylpiperidine alkaloids, -lactone, and -pyrone, which were originally identified as components of the S. invicta queen attractant pheromone.19 Ant whole body extract (WBE) or the induced secretion of poison from the posterior gland has been used for ant immunotherapy.27-29 This isolated venom is collected by a micro-glass tube during induced ant stinging,29, 30 and might be useful for 269 Downloaded from http://www.apjai-journal.org. For personal use only. No other uses without permission Asian Pac J Allergy Immunol 2015;33:267-75 (A) Solenopsis geminata (B) Tetraponera rufonigra (C) Odontoponera denticulata Figure 1. Species of ants most often responsible for anaphylaxis in Thai patients. immunotherapy or testing the cross-reactivity to other hymenoptera, although it is difficult to isolate and the activity is easily lost.31, 32 Currently, S. invicta WBE is commercially available for skin testing.25, 33, 34 Ant allergens Ant venoms are composed of various biologically active peptides and protein components with each ant species having a variety of major allergenic proteins. The most frequently studied ant venom components are from fire ants with the venom of the red imported fire ant (S. invicta) being the most extensively investigated.35 Each S. invicta sting transfers 0.04 to 0.11 µL of venom and 10 to 100 ng of proteins.36 The alkaloid part of the S. invicta venom causes a sterile pustule at the sting site, and has cytotoxic and hemolytic properties.37 The protein part is composed of four major allergens, i.e., Sol i 1, Sol i 2, Sol i 3, and Sol i 4.38 Sol i 1 is a 37-kDa protein with phospholipase A1 activity that comprises 2–5% of the total venom protein.39 Sol i 2 is a 26-kDa protein that is also present in the venom of other species but is dissimilar to the other sol allergens. This allergen comprises 67% of the total venom proteins. Sol i 3 is a 24-kDa protein that is a member of the antigen 5 family and comprises 20% of the total venom protein. Sol i 4 has a 13-kDa molecular mass and comprises 9% of the total venom proteins, which are different from the other sol allergens.14 There are still limited data on protein allergens from ants in Asia, especially those in Thailand where T. rufonigra and S. geminata are the most common causative species of ant anaphylaxis.8 T. rufonigra protein allergen was characterized and identified by immunoblot assay and showed a dominant active protein of approximately 120 kDa.7 A study of S. geminata allergen revealed that it was composed of four venom proteins: Sol gem 1, Sol gem 2, Sol gem 3, and Sol gem4 with molecular weights of 37, 28, 26, and 16 kDa, respectively.40 Of these, Sol gem 2 has a dimer form with a molecular weight of 28/15 kDa (under non-reducing and reducing condition). The amino acid sequence analysis of Sol gem 2 exhibited a degree of homology with the Sol i 2 allergen of S. invicta and their allergenic properties are probably similar. A study of Myrmecia ant venom identified many venom allergens with post-translational processing, and found that most allergen activity was caused by disulfide-linked heterodimers.41 Ant venom nomenclature The International Union of Immunological Studies Allergen Nomenclature Subcommittee (IUIS) has assigned official names to fire ant allergens based on venom proteins: 1 was assigned to phospholipase A1B; 2 was assigned to Sol i 2 homologous proteins; 3 was assigned to antigen 5related proteins; and 4 was assigned to Sol i 4 homologous proteins.42 A revision of the nomenclature of allergenic components of Myrmecia should be done to conform to the IUIS guidelines.43 Cross-reactivity among Solenopsis species In addition to S. invicta, four other species of Solenopsis, including S. richteri (black imported fire ant), S. xyloni (southern fire ant), S. aurea (desert fire ant), and S. geminata (tropical fire ant) also cause allergic reactions.44 Regarding the structure of S. richteri allergens, Sol r 1 and Sol r 3 are similar to Sol i 1 and Sol i 3 allergens from S. invicta, respectively, while the Sol r 2 allergen of S. richteri and S. invicta have less homology.44 There is no allergen that is analogous to 270 Downloaded from http://www.apjai-journal.org. For personal use only. No other uses without permission Hypersensitivity to ant stings Sol i 4 in S. richteri even though the venom allergens of S. richteri and S. invicta appear to be allergenically similar.45 A study of S. xyloni allergic reactions showed that serum from patients with reactions to stings by S. xyloni were reactive to Sol i 1 and Sol i 3, but were only marginally reactive to Sol i 2.44 Allergic reactions from S. aurea stings are reported occasionally, but data is limited. Nonetheless, cross-reactivity between allergens of S. aurea and S. invicta, especially Sol 1 and Sol 3, have been reported.44 The structures of four S. geminata venom proteins appear to be similar to the Sol i 1, Sol i 2, Sol i 3, and Sol i 4 allergens of S. invicta. The Sol gem 2 allergen from S. geminata venom was characterized and shown to have allergenic properties similar to those of Sol i 2 from S. invicta.40 Sol i 2 has 72.3% amino acid sequence homology with Sol gem 2 and 78.2% sequence homology with Sol r 2.46 In summary, there are some sequence differences between the Sol 2 and Sol 4 antigens of all fire ant venoms, but IgE antibodies against fire ant venoms are highly crossreactive. Indeed, reactions to stings from any fire ant species can cause sensitization to other species. Cross-reactivity between Solenopsis species and other ants Ants of the genus Pachycondyla are a major cause of ant hypersensitivity in Asia and the Middle East.47,48 Studies of cross-reactivity between Pachycondyla and imported fire ants are controversial, however. A study from Korea revealed no cross-reactivity,49 but another study from the Middle East showed cross-reactivity between Pachycondyla sennaarensis and imported fire ant venom by immunoblot testing.50 Ants of the genus Myrmecia are the predominant cause of ant hypersensitivity in Australia.51 Allergens from these ants are complex with highly basic peptides.42, 52 However, no evidence of cross-reactivity between Myrmecia and fire ant venom was found in allergic patient sera.46 Figure 2. Morphological outline of the tropical imported fire ant (Solenopsis geminata). Tropical fire ant (S. geminata) workers are usually used for species identification. S. geminata has the sting apparatus at the end of gaster and the number of petiole segments is usually used for species identification. (A) S. geminata workers have a 2-segmented petiole and two notches on the head. (B) The ant body is divided into four parts including head, alitrunk, petiole, and gaster. 271 Downloaded from http://www.apjai-journal.org. For personal use only. No other uses without permission Asian Pac J Allergy Immunol 2015;33:267-75 Cross-reactivity between Solenopsis species and other hymenoptera Cross-reactivity among insects and unique ant allergens have been established for some hymenoptera venoms with studies reporting crossreactivity among major proteins of vespids (yellow jackets) and S. invicta. The Sol i 1 allergen of S. invicta is a phospholipase related to those found in vespid venom with 33–38% amino acid identity.39, 53 A study reported cross-reactivity between Sol i 1 and vespid phospholipase with clinical significance.54 Sol i 3 is a member of the antigen 5 family with 43–50% amino acid sequence identity with vespid antigen 5.14, 55, 56 Sol i 3, however, has few conserved areas in common with vespid antigen 5, and there is a lack of IgE cross-reactivity between the two allergens.56, 57 Clinical presentation of ant hypersensitivity Hymenoptera sting-induced anaphylaxis has been reported worldwide, as well as in Thailand,58 with studies revealing cases of ant-induced severe hypersensitivity reactions.7, 59 Reactions to ant hypersensitivity can be divided into immediate- and delayed-type hypersensitivity reactions. Immediate reactions occur within 1–4 hours after ant stings, and can be further divided into normal local reactions (pain, swelling, erythema, heat, and sterile pustules at sting sites), large local reactions (a reaction larger than 10 cm in diameter persisting for longer than 24 hours), generalized cutaneous reactions (pruritus and urticaria), and systemic reactions (anaphylaxis).35 There have been many previous reports of imported fire ant-induced hypersensitivity reactions and anaphylaxis. A large study of 20,755 cases with fire ant stings estimated that 413 patients (2%) had anaphylaxis.60 Another study showed that S. invictainduced hypersensitivity reactions were the cause of death in 83 of 29,300 patients in a physician survey.61 Infants and elderly people are at risk of indoor imported fire ant stings. A review of local newspapers in the United States between 1991 and 2004 revealed 10 indoor fire ant stings that were previously unreported and 10 stings that were reported in the medical literature. Six of the 20 patients died within one week after hypersensitivity reactions occurred.62 Immediate reactions from the stings of ants other than imported fire ants have also been reported. Ants of the genus Pachycondyla are the most common cause of anaphylaxis in tropical areas of Asia and the Middle East. Pachycondyla sennaarensis was the cause of anaphylaxis in 31 United Arab Emirates patients with positive skin tests and specific IgE antibodies to this ant,63 and Pachycondyla chinensis induced large local reactions after stings in 1.6% of patients in Korea. Another study showed that 7 of 327 patients (2.1%) had systemic immediate reactions and that four patients had anaphylaxis.64 Ants of the genus Myrmecia in Australia caused several deaths from anaphylaxis.65,66 Fatal anaphylaxis from the southern fire ant or S. xyloni in the United States was also reported.67 Nonfatal immediate reactions from S. xyloni were also shown in other studies.68, 44 Other native fire ants (S. aurea and S. geminata) caused immediate hypersensitivity reactions in studies from the United States69, as did harvester ants (genus Pogonomyrmex) and oak ants (Pseudomyrmex species).70, 71 Delayed reactions usually occur more than 4 hours after ant stings and cause dermatitis, arthralgia, and lymphadenopathy from serum sickness, renal abnormalities, and vasculitis, respectively.72 Serum sickness from fire ant attacks was reported in the United States73 and nephrotic syndrome occurred in a child two weeks after being stung by a fire ant.74 Diagnosis of ant-induced hypersensitivity Diagnosis of ant-induced hypersensitivity can be performed by documenting a patient history of allergic reaction to ant stings, by physical examination, or through the use of in vivo and/or in vitro tests. A history of the circumstances of the sting, including where it occurred, what the individual was doing, and the nature of the ant habitat, should be asked. Identification of the causative ant should be determined by an entomological specialist. Physical examination for evidence of ant stings should also be completed. Vital signs, as well as respiratory and gastrointestinal signs and symptoms, should be carefully examined for evidence of anaphylaxis. Skin lesions, such as pseudopustules at the sting site within 24 hours after being stung, can also help diagnose imported fire ant stings. A widely used in vivo method to diagnose fire ant-sting hypersensitivity includes skin testing using imported fire ant WBE. The result is positive when the skin-prick test is performed using a concentration of 1:1000 (w/v) of imported fire ant WBE. If the skin-prick test result is negative, an intradermal skin test using concentrations of 1:1,000,000 to 1:1000 (w/v) of the imported fire ant WBE should be performed.75 272 Downloaded from http://www.apjai-journal.org. For personal use only. No other uses without permission Hypersensitivity to ant stings Serum specific IgE to imported fire ant venom can be used as an in vitro test to diagnose hypersensitivity to imported fire ants. The sensitivity of serum specific IgE is lower than skin testing and therefore, is only recommended when skin testing cannot be done or interpreted. Serum specific IgE testing can also help in diagnosis of imported fire ant allergy in suspected cases with negative skin-test results.76 Twenty-nine percent of adults with a history of fire ant exposure without systemic reactions had a positive skin-test result.77 A study revealed that 24% of non-allergic control cases had positive specific-IgE test results for imported fire ant venom.54 Skin testing and serum specific IgE should not be performed without a clinical history of allergic reactions from imported fire ants because of the high degree of asymptomatic IgE production in an exposed population.68, 78 The skin-prick test was used to diagnose P. chinensis anaphylaxis in Korea and higher P. chinensis-specific IgE levels were observed in patients with anaphylaxis compared with patients with large local reactions or the asymptomatic population.48 The ant-sting challenge test is used for patients with a history of ant anaphylaxis but negative skin testing and serum specific IgE results. It has not been used extensively because of the chance of provoking serious allergic reactions. Specialized centers are required for sting challenges.79, 80 Management of ant-induced hypersensitivity Management of ant-induced hypersensitivity can involve either immediate treatment for anaphylaxis or preventive treatment. Immediate treatment for anaphylaxis includes epinephrine at a dosage of 0.01 mg/kg to a maximum of 0.3 mg for children and 0.3 to 0.5 mg for adults.81, 82 An epinephrine auto-injector should be prescribed for patients with histories of severe allergic reactions. Other medications, including antihistamines and bronchodilators, should be given as symptomatic treatments. Late-phase anaphylaxis can be prevented by corticosteroids. Supportive treatments should follow standard guidelines for anaphylaxis, including fluid resuscitation, oxygen therapy, and placing the individual in a recumbent position.82 Local reactions can be treated by local wound care, including wound dressing, topical or systemic antibiotics for secondary infection, cold compression to reduce local swelling, and topical corticosteroids to limit the swelling of large local reactions. Pseudopustules from fire ant stings should be kept clean and intact to prevent secondary bacterial infection.75 Preventive measures for the treatment of ant anaphylaxis include immunotherapy and re-sting avoidance. Immunotherapy with imported fire ant WBE is considered for adults and children with systemic reactions to ants who have shown positive results by skin testing or specific IgE antibodies.75 This recommendation is the same as the immunotherapy recommended for hymenoptera hypersensitivity. Children ≤16 years of age with isolated cutaneous systemic reactions from ant stings do not require immunotherapy because of the low risk of subsequent systemic reactions.83, 84 Nevertheless, children with cutaneous reactions from fire ant stings with a significant exposure risk may be considered for treatment with imported fire ant immunotherapy.75 The dosing schedule for imported fire ant immunotherapy is not uniform because of the rapidity of the build-up phase. Most expert recommendation protocols indicate treatment once or twice weekly until a maintenance dose is reached. A maintenance dose of 0.5 ml of 1:100 (w/v) imported fire ant WBE is recommended. If treatment failure occurs, increased doses can be considered.85 Some recommendations suggest 0.5 ml of 1:10 (w/v) imported fire ant WBE as a maintenance dose.86, 87 In endemic areas with a high incidence of imported fire ant stings, the rapid increase of the dose protocol or a rush schedule in the maintenance phase is preferable to the conventional schedule. A 2-day rush protocol with imported fire ant immunotherapy showed good safety and efficacy.86 A 1-day rush immunotherapy protocol in children and adults was also safe and effective.88, 89 Imported fire ant immunotherapy can be advanced to the maintenance phase within only 1–2 days by rush protocol. The duration of immunotherapy is usually 3–5 years. For patients at risk of re-exposure, the recommendation for discontinued immunotherapy is when the results of skin testing or serum specific IgE for fire ants are negative.90 Currently, there is insufficient data on the efficacy of immunotherapy for ant species other than the imported fire ant, and therefore, exposure avoidance—such as not disturbing ant nests, allowing nests to be removed by trained professionals, avoiding walking barefoot or with sandals, and wearing long pants and long-sleeved shirts when working outdoors—should be 273 Downloaded from http://www.apjai-journal.org. For personal use only. No other uses without permission Asian Pac J Allergy Immunol 2015;33:267-75 recommended to ant hypersensitivity patients. 11. Rhoades RB, Stafford CT, James FK, Jr. Survey of fatal anaphylactic reactions to imported fire ant stings. Report of the Acknowledgments This review was a part of the study “Ant hypersensitivity in Thailand: species and allergen identification by detecting patients’ antibody reaction to the tropical fire ant compared with the imported fire ant” supported by the Thailand Research Fund (TRF, grant number MRG5580064). We thank Emeritus Prof. Dr. Wanpen Chaicumpa for advice and for reviewing the manuscript. We also thank Yudthana Samung for ant species identification, and Vatcharin Nakphong for the fire ant image (Figure 2). Thanks to Mr. Paul Adams for proofreading this manuscript. Fire Ant Subcommittee of the American Academy of Allergy and Immunology. The J Allergy Clin Immunol. 1989;84:159-62. 12. Tankersley MS. The stinging impact of the imported fire ant. Curr Opin Allergy Clin Immunol. 2008;8:354-9. 13. More DR, Kohlmeier RE, Hoffman DR. Fatal anaphylaxis to indoor native fire ant stings in an infant. Am J Forensic Med Pathol. 2008;29:62-3. 14. Hoffman DR. Allergens in Hymenoptera venom XXIV: the amino acid sequences of imported fire ant venom allergens Sol i II, Sol i III, and Sol i IV. J Allergy Clin Immunol. 1993;91:71-8. 15. Street MD, Donovan GR, Baldo BA, Sutherland S. Immediate allergic reactions to Myrmecia ant stings: immunochemical analysis of Myrmecia venoms. Clin Exp Allergy. 1994;24:590-7. 16. Jones TH, Devries PJ, Escoubas P. Chemistry of venom alkaloids References in the ant, Megalomyrmex foreli (Myrmicinae) from Costa Rica. J 1. Chem Ecol. 1991;17:2507-18. Kritsaneepaiboon S, Saiboon S. Ant species (Hymenoptera: Formicidae) in a longkong(Meliaceae: Aglaia dookkoo Griff.) 2. 17. Wiese MD, Davies NW, Chataway TK, Milne RW, Brown SG, plantation. Songklanakarin J Sci Technol. 2000;22:393-6. Heddle RJ. Stability of Myrmecia pilosula (Jack Jumper) ant Watanasit S, Trirat N. Diversity of ants (Hymenoptera: venom for use in immunotherapy. J Pharm Biomed Anal. Formicidae) in two rubber plantations in Songkhla Province, 2011;54:303-10. Southern Thailand. Songklanakarin J Sci Technol. 2011;33:151- 18. 61. 3. following ant bites. Ceylon Med J. 2011;56:34-5. Thongphak D, Kulsa C. Diversity and Community Composition of 19. Cruz-Lopez L, Rojas JC, De La Cruz-Cordero R, Morgan ED. Ants in the Mixed Deciduous Forest, the Pine Forest and the Para Behavioral and chemical analysis of venom gland secretion of Rubber Plantation at Chulaborn Dam, Chaiyaphum Province, the queens of the ant Solenopsis geminata. J Chem Ecol. Northeastern Thailand. Int J Env Rural Dev. 2014;5:72-6. 4. 5. 2001;27:2437-45. Torchote P, Sitthicharoenchai D, Chaisuekul C. Ant species 20. Brindis Y, Lachaud JP, Gomez YGB, Rojas JC, Malo EA, Cruz- diversity and community composition in three different habitats: Lopez L. Behavioral and olfactory antennal responses of mixed deciduous forest, teak plantation and fruit orchard. Tropical Solenopsis geminata (Fabricius) (Hymenoptera: Formicidae) Natural History. 2010;10:37-51. workers to their dufour gland secretion. Neotrop Entomol. Jaitrong W, Yamane S. Review of the Southeast Asian species of the Aenictus javanus and Aenictus philippinensis species groups 6. 2008;37:131-6. 21. Molecular phylogeny of Crematogaster subgenus Decacrema ants 78. (Hymenoptera: Formicidae) and the colonization of Macaranga McNatty A, Abbott KL, Lester PJ. Invasive ants compete with and (Euphorbiaceae) trees. Mol Phyl Evol. 2003;27:441-52. 22. Sanchez-Peña SR, Chacón-Cardosa MC, Resendez-Perez D. Oecologia. 2009;160:187-94. Identification of fire ants (Hymenoptera: Formicidae) from Wanotayan K, Malainual N, Sassa-deepang T, Boonchoo S, Northeastern Mexico with morphology and molecular markers. Jirapongsananuruk O, Vichyanond P. Anaphylaxis to venom of Tetraponera ruflonigra ant: A case report. J Allergy Clin Immunol Florida Entomologist. 2009;92:107-15. 23. 2005; 115: S39. 8. Mullins RJ, Brown SG. Ant venom immunotherapy in Australia: the unmet need. Med J Aust. 2014;201:33-4. Puranitee P, Vilaiyuk S, Kamchaisatian W, Manuyakorn W, 24. Haymore BR, McCoy RL, Nelson MR. Imported fire ant Teawsomboonkit W, Sasisakunporn C, et al. Reported Ant Re- immunotherapy prescribing patterns in a large health care system sting Reaction in Thai Children with Ant Anaphylaxis Receiving during a 17-year period. Ann Allergy Asthma Immunol. Immu J Allergy Clin Immunol 2012; 115: AB228. 9. Feldhaar H, Fiala B, Gadau J, Mohamed M, Maschwitz U. (Hymenoptera, Formicidae, Aenictinae). ZooKeys. 2012;193:49- modify the trophic ecology of hermit crabs on tropical islands. 7. Ratnatilaka GA, Herath RR, Dias RK. Severe anaphylaxis 2009;102:422-5. Holway DA, Lach L, Suarez AV, Tsutsui ND, Case TJ. The 25. Hoffman DR. Allergens in Hymenoptera venom. XVII. Allergenic causes and consequences of ant invasions. Ann Rev Ecol and Syst. components of Solenopsis invicta (imported fire ant) venom. J 2002;33:181-233. Allergy Clin Immunol. 1987;80:300-6. 10. Hoffman DR. Ant venoms. Curr Opin Allergy Clin Immunol. 26. Schultz DR, Arnold PI, Wu MC, Lo TM, Volanakis JE, Loos M. 2010;10:342-6. Isolation and partial characterization of a polysaccharide in ant 274 Downloaded from http://www.apjai-journal.org. For personal use only. No other uses without permission Hypersensitivity to ant stings venom (Pseudomyrmex sp.) that activates the classical 38. Hoffman DR, Dove DE, Jacobson RS. Allergens in complement pathway. Mol Immunol. 1979;16:253-64. Hymenoptera venom: XX. Isolation of four allergens from 27. Wanandy T, Gueven N, Davies NW, Brown SG, Wiese MD. imported fire ant (Solenopsis invicta) venom. J Allergy Clin Pilosulins: A review of the structure and mode of action of venom peptides from an Australian ant Myrmecia pilosula. Toxicon. Immunol. 1988;82:818-27. 39. Hoffman DR, Sakell RH, Schmidt M. Sol i 1, the phospholipase 2015;98:54-61. 28. allergen of imported fire ant venom. J Allergy Clin Immunol. Cabrera A, Williams D, Hernandez JV, Caetano FH, Jaffe K. 2005;115:611-6. Metapleural- and postpharyngeal-gland secretions from workers of 40. Sukprasert S, Uawonggul N, Jamjanya T, Thammasirirak S, the ants Solenopsis invicta and S. geminata. Chem Biodivers. Daduang J, Daduang S. Characterization of the allergen Sol gem 2 2004;1:303-11. from the fire ant venom, Solenopsis geminata. J Venom Anim 29. Hoffman DR, Dove DE, Jacobson RS. Allergens in Hymenoptera venom. XX. Isolation of four allergens from imported fire ant (Solenopsis invicta) venom. J Allergy Clin Toxins Trop Dis. 2012;18:325-34. 41. Davies NW, Wiese MD, Brown SGA. Characterisation of major Immunol. peptides in ‘jack jumper’ ant venom by mass spectrometry. 1988;82:818-27. Toxicon. 2004;43:173-83. 30. Pan J, Hink WF. Isolation and characterization of myrmexins, six 42. Allergen nomenclature. IUIS/WHO Allergen Nomenclature isoforms of venom proteins with anti-inflammatory activity from the tropical ant, Pseudomyrmex triplarinus. Toxicon. Subcommittee. Bull World Health Organ. 1994;72:797-806. 43. 2000;38:1403-13. Thomas W. Allergen nomenclature. Allergy. 1995;50:765-74. 31. Stafford CT, Wise SL, Robinson DA, Crosby BL, Hoffman DR. 44. Hoffman DR. Reactions to less common species of fire ants. J Safety and efficacy of fire ant venom in the diagnosis of fire ant allergy. J Allergy Clin Immunol. 1992;90:653-61. Allergy Clin Immunol. 1997;100:679-83. 45. 32. Goncalves Paterson Fox E, Russ Solis D, Delazari Dos Santos L, Hoffman DR, Smith AM, Schmidt M, Moffitt JE, Guralnick M. Allergens in Hymenoptera venom. XXII. Comparison of venoms Aparecido Dos Santos Pinto JR, Ribeiro da Silva Menegasso A, from two species of imported fire ants, Solenopsis invicta and Cardoso Maciel Costa Silva R, et al. A simple, rapid method for richteri. J Allergy Clin Immunol. 1990;85:988-96. the extraction of whole fire ant venom (Insecta: Formicidae: 46. Hoffman DR. Hymenoptera venom allergens. Clin Rev Allergy Solenopsis). Toxicon. 2013;65:5-8. Immunol. 2006;30:109-28. 33. Hoffman DR, Jacobson RS, Schmidt M, Smith AM. Allergens in 47. Shek LP, Ngiam NS, Lee BW. Ant allergy in Asia and Australia. Curr Opin Allergy Clin Immunol. 2004;4:325-8. Hymenoptera venoms. XXIII. Venom content of imported fire ant 48. Cho YS, Lee Y-M, Lee C-K, Yoo B, Park H-S, Moon H-B. whole body extracts. Ann Allergy. 1991;66:29-31. Prevalence of Pachycondyla chinensis venom allergy in an ant- 34. Arseneau AM, Nesselroad TD, Dietrich JJ, Moore LM, Nguyen S, infested area in Korea. J Allergy Clin Immunol. 2002;110:54-7. Hagan LL, et al. A 1-day imported fire ant rush immunotherapy schedule with and without premedication. Ann Allergy Asthma 35. King TP, Hoffman D, Lowenstein H, Marsh DG, Platts-Mills TA, 49. Yun YY, Ko SH, Park JW, Hong CS. Anaphylaxis to venom of Immunol. 2013;111:562-6. the Pachycondyla species ant. J Allergy Clin Immunol. Stafford CT. Hypersensitivity to fire ant venom. Ann Allergy 1999;104:879-82. 50. Reunala T, Brummer-Korvenkontio H, Saarinen K, Räsänen L, Asthma Immunol. 1996;77:87-95. Lestringant G, Hoffman DR. Characterization of IgE-binding 34. deShazo RD, Butcher BT, Banks WA. Reactions to the stings of allergens the imported fire ant. New Engl J Med. 1990;323:462-6. venoms: Comparative analyses of alkaloidal in Samsum ant venom. Immunol.2005;115:S108. 37. Brand JM, Blum MS, Fales HM, MacConnell JG. Fire ant components. Toxicon. 1972;10:259-71. Reference no. 51-112 in online version 275 Downloaded from http://www.apjai-journal.org. For personal use only. No other uses without permission J Allergy Clin Downloaded from http://www.apjai-journal.org. For personal use only. No other uses without permission Hypersensitivity to ant stings 51. Brown SG, van Eeden P, Wiese MD, Mullins RJ, Solley GO, Puy 68. Lockey RF. Systemic reactions to stinging ants. J Allergy Clin R, et al. Causes of ant sting anaphylaxis in Australia: the Australian Immunol. 1974;54:132-46. Ant Venom Allergy Study. Med J Aust. 2011;195:69-73. 69. Helmly RB. Anaphylactic reaction to fire ant. Hawaii Med J. 52. Inagaki H, Akagi M, Imai HT, Taylor RW, Kubo T. Molecular 1970;29:368-9. cloning and biological characterization of novel antimicrobial 70. Pinnas JL, Strunk RC, Wang TM, Thompson HC. Harvester ant peptides, pilosulin 3 and pilosulin 4, from a species of the sensitivity: In vitro and in vivo studies using whole body extracts Australian ant genus Myrmecia. Arch Biochem Biophys. and venom. J Allergy Clin Immunol. 1977;59:10-6. 2004;428:170-8. 71. 53. Schmidt M, Sakell RH, Hoffman DR. The sequence of Sol i 1 the Suiter DR, et al. Adverse reactions to ants other than imported fire cross-reactive allergen of imported fire ant venom. J Allergy Clin ants. Ann Allergy Asthma Immunol. 2005;95:418-25. Immunol. 2004;113:S73. 54. 72. Reisman RE, Livingston A. Late-onset allergic reactions, including serum sickness, after insect stings. J Allergy Clin Hoffman DR, Dove DE, Moffitt JE, Stafford CT. Allergens in Hymenoptera venom: XXI. Cross-reactivity and Immunol. 1989;84:331-7. multiple 73. reactivity between fire ant venom and bee and wasp venoms. J M, McConnell TJ, Hoffman 1999;131:424-9. DR. Immunologic 74. Swanson GP, Leveque JA. Nephrotic syndrome associated with characterization of the recombinant fire ant venom allergen Sol i ant bite. Tex Med. 1990;86:39-41. 3. Allergy. 2003;58:342-9. 56. Hoffman DR. Allergens in Hymenoptera venom XXV: The amino 75. Golden DB, Moffitt J, Nicklas RA, Freeman T, Graft DF, Reisman acid sequences of antigen 5 molecules and the structural basis of RE, et al. Stinging insect hypersensitivity: a practice parameter update 2011. J Allergy Clin Immunol. 2011;127: 852-4. antigenic cross-reactivity. J Allergy Clin Immunol. 1993;92:707-16. 57. deShazo RD, Williams DF, Moak ES. Fire ant attacks on residents in health care facilities: a report of two cases. Ann Intern Med. Allergy Clin Immunol. 1988;82:828-34. 55. Schmidt Klotz JH, deShazo RD, Pinnas JL, Frishman AM, Schmidt JO, 76. Reisman RE. Insect sting allergy: the dilemma of the negative skin Weber RW. Solenopsis invicta. Ann Allergy Asthma Immunol. test reactor. J Allergy Clin Immunol. 2001;107:781-2. 2003;91:A-6. 77. Stafford CT, Moffitt JE, Bunker-Soler A, Hoffman DR, Thompson 58. Poachanukoon O, Paopairochanakorn C. Incidence of anaphylaxis in the emergency department: a 1-year study in a university WO. Comparison of in vivo and in vitro tests in the diagnosis of hospital. Asian Pac J Allergy Immunol. 2006;24:111-6. imported fire ant sting allergy. Ann Allergy. 1990;64:368-72. 59. Piromrat K, Chinratanapisit S, Trathong S. Anaphylaxis in an 78. James FK, Jr., Pence HL, Driggers DP, Jacobs RL, Horton DE. emergency department: a 2-year study in a tertiary-care hospital. Imported fire ant hypersensitivity. Studies of human reactions to fire ant venom. J Allergy Clin Immunol. 1976;58:110-20. Asian Pac J Allergy Immunol. 2008;26:121-8. 79. 60. Stafford CT, Hutto LS, Rhoades RB, Thompson WO, Impson LK. Rueff F, Przybilla B, Muller U, Mosbech H. The sting challenge Imported fire ant as a health hazard. South Med J. 1989;82:1515- test in Hymenoptera venom allergy. Position paper of the 9. Subcommittee on Insect Venom Allergy of the European Academy of Allergology and Clinical Immunology. Allergy. 61. Rhoades RB, Stafford CT, James FK, Jr. Survey of fatal 1996;51:216-25. anaphylactic reactions to imported fire ant stings. J Allergy Clin 80. Valentine MD. Insect-sting anaphylaxis. Ann Intern Med. Immunol. 1989;84:159-62. 1993;118:225-6. 62. Rupp MR, deShazo RD. Indoor fire ant sting attacks: a risk for 81. Kemp SF, Lockey RF, Simons FE. Epinephrine: the drug of frail elders. Am J Med Sci. 2006;331:134-8. choice for anaphylaxis. A statement of the World Allergy 63. Dib G, Guerin B, Banks WA, Leynadier F. Systemic reactions to Organization. Allergy. 2008 ;63:1061-70. the Samsum ant: An IgE-mediated hypersensitivity. J Allergy Clin 82. Lieberman P, Nicklas RA, Oppenheimer J, Kemp SF, Lang DM, Immunol. 1995;96:465-72. 64. Cho YS, Lee YM, Lee CK, Yoo B, Park HS, Moon HB. Bernstein DI, et al. The diagnosis and management of anaphylaxis Prevalence of Pachycondyla chinensis venom allergy in an ant- practice parameter: 2010 update. J Allergy Clin Immunol. 2010;126:477-80.e1-42. infested area in Korea. J Allergy Clin Immunol. 2002;110:54-7. 65. 66. Brown SG, Wu QX, Kelsall GR, Heddle RJ, Baldo BA. Fatal 83. Golden DB, Kagey-Sobotka A, Norman PS, Hamilton RG, anaphylaxis following jack jumper ant sting in southern Tasmania. Lichtenstein LM. Outcomes of allergy to insect stings in children, Med J Aust. 2001;175:644-7. with and without venom immunotherapy. N Engl J Med. 2004;351:668-74. McGain F, Winkel KD. Ant sting mortality in Australia. Toxicon. 84. Valentine MD, Schuberth KC, Kagey-Sobotka A, Graft DF, 2002;40:1095-100. 67. More DR, Kohlmeier RE, Hoffman DR. Fatal anaphylaxis to Kwiterovich KA, Szklo M, et al. The Value of immunotherapy indoor native fire ant stings in an infant. Am J Forensic Med with venom in children with allergy to insect stings. New Engl J Patho. 2008;29:62-3. Med. 1990;323:1601-3. a Downloaded from http://www.apjai-journal.org. For personal use only. No other uses without permission Asian Pac J Allergy Immunol 2015;33:267-75 85. Steigelman DA, Freeman TM. Imported fire ant allergy: case 99. Bertelsmeier C, Guenard B, Courchamp F. Climate change may presentation and review of incidence, prevalence, diagnosis, and boost the invasion of the Asian needle ant. PLoS One. current treatment. Ann Allergy, Asthma Immunol. 2013;111:242- 2013;8:e75438. 5. 100. Al-Shahwan M, Al-Khenaizan S, Al-Khalifa M. Black (samsum) 86. Tankersley MS, Walker RL, Butler WK, Hagan LL, Napoli DC, ant induced anaphylaxis in Saudi Arabia. Saudi Med J. Freeman TM. Safety and efficacy of an imported fire ant rush 2006;27:1761-3. immunotherapy protocol with and without prophylactic treatment. 101. Alsharani M, Alanazi M, Alsalamah M. Black ant stings caused by J Allergy Clin Immunol. 2002;109:556-62. 87. Pachycondyla sennaarensis: a significant health hazard. Ann Triplett RF. Sensitivity to the imported fire ant: successful Saudi Med. 2009;29:207-11. treatment with immunotherapy. South Med J. 1973;66:477-80. 88. 102. Lai LC, Hua KH, Yang CC, Huang RN, Wu WJ. Secretion Judd CA, Parker AL, Meier EA, Tankersley MS. Successful profiles of venom alkaloids in Solenopsis geminata (Hymenoptera: administration of a 1-day imported fire ant rush immunotherapy Formicidae) in Taiwan. Environ Entomol. 2009;38:879-84. protocol. Ann Allergy Asthma Immunol. 2008;101:311-5. 103. Perfecto I, Vandermeer J. Discovery dominance tradeoff: the case 89. Dietrich JJ, Moore LM, Nguyen S, Hagan LL, Tankersley MS. of Pheidole subarmata and Solenopsis geminata (Hymenoptera: Imported fire ant hypersensitivity: a 1-day rush immunotherapy Formicidae) schedule without premedication. Ann Allergy Asthma Immunol. 2011;40:999-1006. pastures. Environ Entomol. Moffitt JE, Barker JR, Stafford CT. Management of imported fire Solenopsis geminata (hymenoptera: formicidae) as part of the ant allergy: results of a survey. Ann Allergy Asthma Immunol. natural enemy complex responsible for successful biological 1997;79:125-30. control of many tropical irrigated rice pests. Bull Entomol Res. 2009;99:503-12. 91. Chen Y. Global potential distribution of an invasive species, the 105. Ross KG, Shoemaker DD. Estimation of the number of founders yellow crazy ant (Anoplolepis gracilipes) under climate change. of an invasive pest insect population: the fire ant Solenopsis Integr Zool. 2008;3:166-75. invicta in the USA. Proc Biol Sci. 2008;275:2231-40. 92. Haddad Junior V, Cardoso JL, Moraes RH. Description of an 106. Valles SM, Oi DH, Plowes RM, Sanchez-Arroyo H, Varone L, injury in a human caused by a false tocandira (Dinoponera gigantea, Perty, 1833) with a revision on Conant P, et al. Geographic distribution suggests that Solenopsis folkloric, pharmacological and clinical aspects of the giant ants of the genera invicta is the host of predilection for Solenopsis invicta virus 1. J Paraponera and Dinoponera (sub-family Ponerinae). Rev Inst Invertebr Pathol. 2013;113:232-6. 107. Kemp SF, deShazo RD, Moffitt JE, Williams DF, Buhner WA, Med Trop Sao Paulo. 2005;47:235-8. 93. neotropical 104. Way MJ, Heong KL. Significance of the tropical fire ant 2009;103:535-6. 90. in Braga DL, Louzada JN, Zanetti R, Delabie J. Rapid evaluation of 2nd. Expanding habitat of the imported fire ant (Solenopsis ant diversity in land use systems in southern Bahia, Brazil. invicta): a public health concern. J Allergy Clin Immunol. 2000;105:683-91. Neotrop Entomol. 2010;39:464-9. 94. Chen CD, Nazni WA, Lee HL, Hashim R, Abdullah NA, Ramli R, 108. Chen L, Hu QB, Fadamiro HY. Reduction of venom alkaloids in et al. A preliminary report on ants (Hymenoptera: Formicidae) Solenopsis richterix-Solenopsis invicta hybrid: an attempt to recovered from forensic entomological studies conducted in identify new alkaloidal components. J Agric Food Chem. different ecological habitats in Malaysia. Trop 2010;58:11534-42. Biomed. 109. Fox EG, Bueno OC, Yabuki AT, de Jesus CM, Solis DR, Rossi 2014;31:381-6. 95. Rowles AD, Silverman J. Argentine ant invasion associated with ML, et al. General morphology and ultrastructure of the venom loblolly pines in the southeastern United States: minimal impacts apparatus and convoluted gland of the fire ant, Solenopsis saevissima. J Insect Sci. 2010;10:24. but seasonally sustained. Environ Entomol. 2010;39:1141-50. 96. Silverman J, Brightwell RJ. The Argentine ant: challenges in 110. Pesquero MA, Dias AM. Geographical transition zone of managing an invasive unicolonial pest. Annu Rev Entomol. Solenopsis fire ants (Hymenoptera: Formicidae) and Pseudacteon fly parasitoids (Diptera: Phoridae) in the state of Sao Paulo, Brazil. 2008;53:231-52. Neotrop Entomol. 2011;40:647-52. 97. Rodriguez-Acosta A, Reyes-Lugo M. Severe human urticaria 1892) 111. Derstine NT, Troyer EJ, Suttles CN, Siderhurst LA, Jang EB, (Hymenoptera: Formicidae) venom. Int J Dermatol. 2002;41:801- Siderhurst MS. Field trapping the little fire ant, Wasmannia produced by ant (Odontomachus bauri, Emery auropunctata. J Insect Sci. 2012;12:93. 3. 98. Nelder MP, Paysen ES, Zungoli PA, Benson EP. Emergence of the 112. Fabres G, Brown WL. The recent introduction of the pest ant introduced ant Pachycondyla chinensis (Formicidae: Ponerinae) as Wasmannia auropunctata into New Caledoni. Aust J Entomol. a public health threat in the Southeastern United States. J Med 1978;17:139-42. Entomol. 2006;43:1094-8. b Downloaded from http://www.apjai-journal.org. For personal use only. No other uses without permission
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