Population Explosions of Tiger Moth Lead to Lepidopterism Mimicking Infectious Fever Outbreaks

<div><p>Lepidopterism is a disease caused by the urticating scales and toxic fluids of adult moths, butterflies or its caterpillars. The resulting cutaneous eruptions and systemic problems progress to clinical complications sometimes leading to death. High incidence of fever epidemics were associated with massive outbreaks of tiger moth <i>Asota caricae</i> adult populations during monsoon in Kerala, India. A significant number of monsoon related fever characteristic to lepidopterism was erroneously treated as infectious fevers due to lookalike symptoms. To diagnose tiger moth lepidopterism, we conducted immunoblots for tiger moth specific IgE in fever patients’ sera. We selected a cohort of patients (n = 155) with hallmark symptoms of infectious fevers but were tested negative to infectious fevers. In these cases, the total IgE was elevated and was detected positive (78.6%) for tiger moth specific IgE allergens. Chemical characterization of caterpillar and adult moth fluids was performed by HPLC and GC-MS analysis and structural identification of moth scales was performed by SEM analysis. The body fluids and chitinous scales were found to be highly toxic and inflammatory in nature. To replicate the disease in experimental model, wistar rats were exposed to live tiger moths in a dose dependant manner and observed similar clinico-pathological complications reported during the fever epidemics. Further, to link larval abundance and fever epidemics we conducted cointegration test for the period 2009 to 2012 and physical presence of the tiger moths were found to be cointegrated with fever epidemics. In conclusion, our experiments demonstrate that inhalation of aerosols containing tiger moth fluids, scales and hairs cause systemic reactions that can be fatal to human. All these evidences points to the possible involvement of tiger moth disease as a major cause to the massive and fatal fever epidemics observed in Kerala.</p></div

Tiger moth habitats and cointegration of larval versus epidemic waves.

<p>(A) Geographical range of <i>A</i>. <i>caricae</i> (marked as red) includes Indo-Australian tropics to Queensland and Vanuatu (Ref. 18 & 48). (B) Abundance of tiger moth caterpillars infested on <i>F</i>. <i>hispida</i> in Kerala during the year 2009. (C). The mean larval abundance cointegrate with total number of fever cases in selected districts of Kerala (marked as A-D) from the year 2009 to 2012. All the regions from hilly terrains to low lying lands of Kerala are heavily distributed with host plants that have close proximity to houses with illuminated lights. The maps were created using ArcGIS 10 software.</p

Toxic responses in experimental rats.

<p>(A-B) Regeneration of megakaryocytes in response to platelet reduction was evident with larger megakaryocytes with irregular multilobulated nucleus and more prominent nucleoli in spleen and bone marrow respectively. (C-D) Mean megakaryocyte volume represented by Leishman-Giemsa positive cells (per field@400×) in spleen (<i>n</i> = 60) and bone marrow (<i>n</i> = 120) respectively. (E) Pneumonitis caused due to extensive proliferation of lymphocytes in the peribronchial region (br, bronchiole). (F) Hepatic tissue reports centrilobular necrosis characterized by prominent ballooning, swollen granular cytoplasm with fading nuclei and nuclear infiltration (cv, central vein). (G) Mild acute renal tubular necrosis illustrated by destroyed cells in proximal tubules (pr). (H) Toluidine blue-positive mast cells (inset red arrow) scattered in lung tissue. (I) Mean mast cell recruitment (per field@400×) in lung tissue of control and toxin groups (<i>n</i> = 120). Asterisks indicate significant difference, <i>t</i>-test, <i>P <</i> 0.05. Fig A,B = magnification 1000× and scale bar = 8 <i>μ</i>m. Fig E-G = 200× and 100 <i>μ</i>m. Fig H = 400× and 20 <i>μ</i>m.</p

Unrestricted Cointegration Rank Test (Trace) by methods of Johansen and Juselius.

<p>Unrestricted Cointegration Rank Test (Trace) by methods of Johansen and Juselius.</p

Tiger moth and toxic components.

<p>(A) <i>A</i>. <i>caricae</i> showing its characteristic white discal-spotted forewings and black-spotted yellow hind wings. (B) Final instar forage on pioneer host leaves is active at night but elusive during day light. Larva is blackish with red prothorax and a central black stripe in which on each segment two black spots arranged longitudinally (Ref. 18). The photographs were originally taken by P J Wills (Fig A & B). (C) Lamellar type represents majority of the scales on the head, thorax, wings and abdomen (magnification 100×) (D) Scales on the female ovipositor were mostly of piliform type (magnification 500×). (E) Defensive fluids released from specific bleeding points. Broad arrow show hairy tufts or “<i>flechettes</i>” (piliform type) and narrow ones denote the toxic secretions from teguments. The photograph was originally taken by Anjana Mohan (Fig E).</p

Tiger moth specific IgE in human sera.

<p>(A) Immunoblot shows no specific IgE reaction of healthy control serum against tiger moth total protein extract. (B) Specific IgE reaction of patient’s serum against tiger moth total protein extract. The patient was a 40 year old male diagnosed negative for chikungunya, HbsAg and leptospirosis but his total IgE level was > 2,500 IU/mL. (C) Another patient positive to tiger moth specific IgE. A 39 year old male presented with complaints of high grade fever, headache and myalgia. Basic bloods showed thrombocytopenia (≈52000) with deranged liver enzymes and marginally elevated creatinine levels. (D) No bands were detected on moth extract against IgE hypersensitive serum to other allergens (IgE level was > 2,500 IU/mL). (E) No specific IgE reaction of fever control serum (IgE level was < 200 IU/mL) against tiger moth total protein extract. (F) Serum pre-incubated with tiger moth protein show no specific IgE reaction but the same serum (not pre-incubated) showed tiger moth specific IgE response. (G) Serum from patient shows no specific IgE reaction against cockroach total protein but that showed a previously positive IgE response against tiger moth protein. (H) Serum from patient shows no specific IgE reaction against <i>Hyblea</i> moth total protein but that showed a previously positive IgE response against tiger moth total protein. (I) β-actin loading control. (J) Tiger moth specific 42 and 40 kDa IgE bands were prominent when blotted with fever patient serum. (K) The above membrane (J) was further blotted against monoclonal anti-β-actin antibody followed by blotting with secondary anti-mouse IgG AP-linked antibody. No further binding of β-actin was observed at 42 kDa region.</p