Skip to main content
NCBI home page
Heliyon logoLink to Heliyon
. 2021 Sep 13;7(9):e07970. doi: 10.1016/j.heliyon.2021.e07970

Oral toxicity of various Stemona collinsiae crude extracts against nymph and adult stages of American cockroach, Periplaneta americana (Dictyoptera: Blattodea)

Anon Phayakkaphon b, Preeyanate Dathong b, Napasorn Ransibrahmanakul a, Nontapat Sarovath a, Yudthana Samung b, Aurapa Sakulpanich a,∗
PMCID: PMC8453207  PMID: 34585003

Abstract

Stemona collinsiae exhibits insecticidal resistance against various pests and insect vectors. However, insecticidal activity of S. collinsiae roots has not been tested for some insect vectors, including the American cockroach, Periplaneta americana. The synanthropic insect P. americana is a reservoir of pathogenic and non-pathogenic microorganisms and a cause of infectious diseases and cockroach allergy. This important vector transmits microorganisms to animals and humans to cause vector-borne diseases. This research involved detection of the nymphicidal and adulticidal activities of S. collinsiae root extracts against P. americana through oral administration. The effects of hexane, dichloromethane, ethanol, and water crude extracts were tested on final instar nymphs and adult P. americana. After P. americana ingested bait containing hexane and dichloromethane crude extracts, signs of toxicity occurred, such as hind leg shaking, whole-body tremor, immobility, abdomen swelling, and death. At 48 h, the nymphs and adult P. americana that ingested dichloromethane crude extract-containing bait showed corrected mortality of 65%–100% and 20%–100%, respectively. Whereas none of the nymphs and adult P. americana that ingested the water crude extract-containing bait died (0% corrected mortality). When we dissected alimentary canals of the dead P. americana that had ingested dichloromethane and hexane crude extract-containing baits, the foreguts were found to be swollen. TLC analysis showed the dichloromethane and hexane crude extracts contained the alkaloid didehydrostemofoline and unknown fluorescent substances. Phytochemicals from crude extracts were detected in extracts of dissected alimentary canals using thin-layer chromatography, and didehydrostemofoline alkaloid and unknown fluorescent substances were found in cockroaches that ingested dichloromethane- and hexane-containing baits. The cause of death of P. americana may be attributed to alkaloids and synergistic effects of other substances in S. collinsiae root extract. Mechanisms of action might include several pathways involved in nervous system function. Thus, dichloromethane and hexane crude extracts can be developed as alternative active ingredients in a natural insecticide for cockroach control.

Keywords: Stemona collinsae, Non-Tai-Yak, Nymphicide, Biopesticide, Cockroach control, Adulticidal activity, Nymphicidal activity, Didehydrostemofoline, Alkaloids

Stemona collinsae, Non-Tai-Yak, Nymphicide, Biopesticide, Cockroach control.

1. Introduction

Periplaneta americana is an omnivorous, synanthropic insect and an important insect vector. P. americana is found at approximately 60.9% in 14 provinces of Thailand (Tawatsin et al., 2001), and is globally distributed, including in Korea (Lee et al., 2003), China (Chompoosri et al., 2004), and Iran (Kassiri et al., 2014). P. americana prefers a warm climate with high humidity and prefers living in dark places. Cockroaches such as P. americana are indicators of poor hygiene and are often found in indoor and outdoor facilities, such as kitchens, restaurants, toilets, and sewers (Chompoosri et al., 2004; Sriwichai et al., 2002; Lee et al., 2003; Tawatsin et al., 2001). The cockroach's alimentary cavity and salivary glands are reservoirs for the habitation and propagation of both non-pathogenic and pathogenic microorganisms (Falsone et al., 2017; Tinker and Otteson, 2016; Gijzen and Barugahare, 1992; Bracke et al., 1979); thus, P. americana can carry several vector-borne diseases, such as food poisoning, parasitic diseases, and typhoid disease. Microorganisms such as Klebsiella, Pseudomonas, Escherichia coli, Proteus, Salmonella, Staphylococcus, Streptococcus, Strongyloides stercoralis, Ascaris lumbricoides, Trichuris trichiura, Isospora belli, Entamoeba histolytica, Entamoeba coli, and Iodamoeba butschlii (Kassiri et al., 2014; Malik et al., 2013; Chamavit et al., 2011; Pai et al., 2005) can be transmitted to humans and animals via mechanical and biological transmission (Pai et al., 2003; Tatfeng et al., 2005; Suntaravitun and Domaikaw, 2018; Zahraei-Ramazani et al., 2018: Malik et al., 2013; El-Sherbini andGneidy, 2012; Chamavit et al., 2011). Cockroaches mediate mechanical transmission when they climb over waste and sewage, which are sources of pathogenic and non-pathogenic microorganisms. Microorganisms, parasites, and their eggs can opportunistically attach to the skin, hair, legs, and wings of the cockroach and be transferred to human or animal foodstuffs by the insect when it is foraging, resulting in the spread of infectious diseases. In other cases, microorganisms can contaminate human and animal diets via secretions from cockroach salivary glands, i.e., biological transmission. P. americana is also a transport vector of Toxoplasma gondii (Chinchilla et al., 1994), the pathogenic protozoan that causes toxoplasmosis (Dubey, 2008). Cats, the definitive hosts, ingest T. gondii by eating infected raw meat, rodents, or arthropods, such as house flies and cockroaches (Hill and Dubey, 2002), and excrete the oocytes of T. gondii in their faeces. The faeces are then ingested by cockroaches (Wallace, 1972). When a pregnant woman comes into contact with oocytes via fecal-oral administration or exposure to cat feces, T. gondii may be transmitted from the mother to the unborn child, who is at risk of serious symptoms such as blindness, mental disability, hydrocephalus, chorioretinitis, intracerebral calcification, and physical disability (Dubey, 2008; Halonen and Weiss, 2013). Thus, the elimination of cockroaches can decrease the rate of transmission of T. gondii and other pathogenic microorganisms from cockroaches to animals and humans.

A well-known non-infectious disease associated with cockroaches is cockroach allergy (Srisuwatchari et al., 2020; Nasirian, 2017; Patel and Meher, 2016; Sookrung et al., 2014; Arruda et al., 2001; Schou et al., 1990). The exoskeleton, whole body, secretions, feces, and dust particles from dead cockroaches are all sources of allergens (Patel and Meher, 2016). The main allergen Per 1a has been extracted and isolated from the midgut and feces of P. americana (Sookrung et al., 2014), and other allergens have been found, including Per 2a, Per 3a, Per 6a, Per 7a, Per 9a, and Per 10a; these allergens may cause indoor allergy and asthma in infants, children, and adults (Arruda et al., 2001). After a patient receives allergens via contact and inhalation, the allergens react with immunoglobulin E (IgE) and non-IgE types, leading to the secretion of cytokines and chemokines. Allergic inflammation occurs, during which white blood cells are increasingly induced and move into the inflammation site, while mast cells release histamine. Finally, allergic symptoms such as a red rash, sneezing, rhinorrhea, allergic rhinitis, airway inflammation, bronchospasm, wheezing, and asthma appear (Srisuwatchari et al., 2020; Patel and Meher, 2016).

Therefore, eliminating cockroaches and terminating their life cycle, for instance via mechanical traps and chemical insecticides, is an important strategy for controlling and preventing cockroach vector-borne diseases. Insects can receive chemical insecticides via ingestion, contact, and inhalation. The ingestion pathway, usually using oral bait, is convenient, ready to use, and simple for insect control. The bait does not widely diffuse in air and good insect control should have a low ecological impact (Revay et al., 2015). The toxic bait is contained in closed containers which are safe for humans and pets. After insects eat the toxic bait, the toxic insecticides are absorbed and distributed to the tissue (Champman, 1998). Irregular symptoms occur, leading to the death of the insect. Insecticidal activity via the ingestion route is an interesting basic route and toxic bait products are available in the market. Accordingly, the bait method was used in this research. Natural chemicals from insecticidal plants are sources of synthetic insecticides such as pyrethroids and imidacloprid. In Thailand, there is a high diversity of insecticidal plants, including Stemona collinsiae (Stemonaceae), which has been traditionally used as an insecticide and insect repellant to protect food. Furthermore, the root extract has been used as a pesticide for eliminating beetles and pests in pepper plantations (Inthachub and Duyfjes, 2011). Recent scientific reports revealed that S. collinsiae root extract can be used to kill pests such as Plutella xylostella (Jiwajinda et al., 2001; Phattharaphan et al., 2010), Spodoptera exigua (Brem et al., 2002), and insect vectors such as Parasarcophaga ruficornis (Sakulpanich et al., 2017) and Chrysomya megacephala (Sakulpanich et al., 2016), but its insecticidal activity against P. americana has never been reported. Thus, in this research, we studied the nymphicidal and adulticidal activities of various S. collinsiae root extracts against final instar nymph and adult stage P. americana via oral administration. The crude extracts were produced using a sequential reflux extraction method, and phytochemicals in each crude extract were detected with thin-layer chromatography (TLC). Bait mixed with each crude extract was fed to P. americana to observe the resulting mortality and signs of toxicity, including irregularities of the internal organs.

2. Materials and methods

2.1. Plant materials

2.1.1. Stemona collinsiae preparation

Roots of S. collinsiae were harvested from Ubon Ratchathani, Thailand, from December 2018 to January 2019, and the roots and aerial parts were arranged as herbarium for identification. The roots were first cleaned with tap water and then dried using an electric fan to eliminate excess water on the surface of the roots and cut up into small pieces. Next, they were dried in a hot air oven at 55 ± 1 °C for 72 h. The small dry pieces of root were ground and sieved using a #30 mesh sieve, and the powdered root was used in further reflux extraction processes.

The herbarium of S. collinsiae root and aerial parts was identified and deposited in the Forest and Plant Conservation research office, Department of National Parks, Wildlife and Plant conservation with voucher specimens BKF No. 196976.

2.1.2. Preparation of hexane, dichloromethane, ethanol, and water crude extracts using sequentially reflux extraction method (modified from Sakulpanich et al., 2017)

Hexane, dichloromethane, ethanol, and purified water were used as extractants. For hexane extraction, powdered root (300 g) was placed in a round-bottom flask, 1000 ml of hexane was added, and the top of the flask was covered with a cold condenser. The flask was soaked in a 60–70 °C water bath for 1 h, then the liquid extract was passed through a filter paper and the filtrate collected in a bottle and protected from light. The filtrate was tested for alkaloids by analyzing a 2 ml aliquot using thin-layer chromatography (TLC) and Dragendorff’s spray reagent. A new aliquot of hexane was added into the extraction residue, and the flask was re-immersed in the water bath for 1 h. The extraction and filtration process were repeated until all alkaloids were exhaustively extracted from the extraction residue. The complete extraction was confirmed by TLC and Dragendorff’s spray reagent. The collected filtrates were concentrated using a rotary evaporator under reduced pressure at 40 ± 1 °C. Then, the hexane crude extract was dried on a water bath at 70 ± 1 °C, poured into a tightly sealed glass container, protected from light, and kept in a refrigerator at 4 °C.

For dichloromethane, ethanol, and water extraction, the extraction process was repeated using the same steps as described in the hexane extraction. The dichloromethane, ethanol, and water were changed when alkaloid-testing showed a negative result in the final filtrate. The water crude extract was dried using lyophilization.

2.2. Ethical consideration statement

The animal protocol was established under ethical principles and guidelines for the use of animals provided by the National Research Council of Thailand and all animal experiments were performed in accordance with the protocols approved by the Animal care and Use Committee of Thammasat University: Protocol No. 005/2020 and the Animal care and Use Committee of Faculty of Tropical Medicine, Mahidol University: Protocol No. 001/2021 Certificate No. FTM-ACUC 005/2021.

2.3. Periplaneta americana rearing

Periplaneta americana were collected from Ratchaburi, Thailand. The cockroach species were identified by an Entomologist, Yudthana Samung, who works in Department of Medical Entomology, Faculty of Tropical Medicine, Mahidol University. The species identification was performed following the handbook of domiciliary cockroach species in Thailand (Asahina, 1983). P. americana were reared by Anon Phayakkaphon who works in the Department of Medical Entomology, Faculty of Tropical Medicine, Mahidol University; they were provided with dry cat food (Purina® Friskies® for adult cats, Nestlé, Thailand) and water. They were maintained and bred in plastic boxes (30 × 30 × 30 cm) with lids on the top. Petroleum jelly was smeared on the inside wall of each plastic box to prevent the cockroaches escaping. The plastic boxes containing P. americana were placed in a cockroach-rearing room at the Department of Medical Entomology, Faculty of Tropical Medicine, Mahidol University, under ambient temperatures (27–30 °C), 70%–90% humidity, and a photoperiod of a 12:12 h dark: light cycle. Final instar nymphs and adult P. americana were used for oral toxicity tests using the bait method (Seanmanot et al., 2018; Thavara et al., 2007).

2.4. Oral toxicity based on bait method

2.4.1. Bait preparation

Each type of crude extract was homogenously mixed with glucose. The range of concentration, 1–50% w/w was tested. Two-fold serial dilutions were prepared (6 concentrations per two-fold dilution). The range of concentration of the crude extract, which produced the range of corrected mortality between 10-90% (Finney, 1971), was selected for calculating LC50. Finally, 3 g of each concentration of the bait was weighed and placed in a disposable plastic Petri dish (90 × 15 mm) (สำนักงานคณะกรรมการอาหารและยา, 2538).

2.4.2. Bioassay

Bioassay (modified from Ko et al., 2016; Anikwe et al., 2014; Srinivasan et al., 2005; ประกาศสำนักงานคณะกรรมการอาหารและยา, 2538).

A group of 10 final instar nymphs (unsexed) and a group of 10 adult P. americana (mixed sexes) were used in the test. A cup of water was placed in the testing box. The P. americana were released into the box and starved for 24 h before testing. After 24 h, the bait was placed in the box, and signs of toxicity and mortality were observed at 1, 2, 4, 12, 24, 48, and 72 h. The dead P. americana were detected by prodding them with forceps. Signs of death were as follows: P. americana did not respond to prodding, were immobile, and were unable to return to a normal posture. P. americana in the negative control group received only glucose. All experiments were repeatedly performed for three replications.

A group of 10 final instar nymphs (unsexed) and a group of 10 adult P. americana (mixed sexes) were used in the test. A cup of water was placed in the testing box. The P. americana were released into the box and starved for 24 h before testing. After 24 h, the bait was placed in the box, and signs of toxicity and mortality were observed at 1, 2, 4, 12, 24, 48, and 72 h. The dead P. americana were detected by prodding them with forceps. Signs of death were as follows: P. americana did not respond to prodding, were immobile, and were unable to return to a normal posture. P. americana in the negative control group received only glucose. All experiments were repeatedly performed for three replications.

2.5. Comparison of the dissected alimentary canals from the extract-treated group and negative control group

The dead P. americana were dissected and their alimentary canals removed. P. americana in the negative control group were killed by freezing in a refrigerator at -20 °C before dissection, then fixed onto the dissection board with pins. The dissection was performed by longitudinally cutting from the abdomen using medical scissors, and the exoskeleton and fat tissue were gradually removed using forceps. The alimentary canals from P. americana in the extract-treated group were compared with those from negative control group.

The images of P. americana and the dissected alimentary canal were taken using a Canon EOS 500D digital SLR camera (Canon, Japan). The SNZ745T stereomicroscope 10x (Nikon, China) with microscope camera MDX503 and iWorks software (Lanoptik Technologies Ltd., China) was used for enlarging the images.

2.6. Determination of alkaloids in crude extracts and dissected alimentary canal using TLC

2.6.1. Preparation of hexane, dichloromethane, ethanol, and water crude extract solutions

The hexane, dichloromethane, ethanol, and water extract solutions were prepared at a concentration of 1 mg/ml. The hexane and dichloromethane crude extracts were dissolved in dichloromethane, whereas the ethanol and water crude extracts were dissolved in 70% ethanolic solvent. In the case of water crude extract, a sonication bath was used for dissolving.

2.6.2. Preparation of dichloromethane alimentary canal extracts

Didehydrostemofoline is very soluble in dichloromethane; thus, dichloromethane was selected to extract the didehydrostemofoline from the dissected alimentary canals. The dissected alimentary canals of the dead nymph and adult P. americana in the treated groups and negative control group were soaked in dichloromethane. Dichloromethane (1 mL) was added to a container with the dissected alimentary canal, which was then shaken using a vortex for 3 min, and the dichloromethane liquid extract was pipetted into a new container. A new aliquot of dichloromethane was added to the container and shaken for 3 min, and the extraction was repeated three times. The collected dichloromethane liquid extract of the alimentary canal was dried using a rotary evaporator under reduced pressure and at 40 °C. Dichloromethane (1 mL) was added to the dry residue, and the alkaloids in the dichloromethane alimentary canal extract solutions were tested with TLC.

2.6.3. TLC method

Amounts of 20 μL of the dichloromethane alimentary canal extract solution, 10 μL of didehydrostemofoline, 10 μL of hexane, dichloromethane, and water crude extract solution, and 20 μL of ethanol crude extract solution were spotted onto a silica gel GF254 TLC plate (Merck, Germany) by Linomat 5 applicator (Camag®, Switzerland). The TLC plate was developed in a TLC tank containing a mixture of dichloromethane, methanol, water, and 10% NH4OH in the ratio 70: 25: 5: 0.1. The developed TLC plate was dried and detected under visible and UV light at 254 nm and 366 nm, respectively. Then, the TLC was sprayed with Dragendorff’s reagent to detect the alkaloids. The development of an orange band indicated the presence of an alkaloid. TLC images were taken and recorded by TLC Visualizer (Camag®, Switzerland) and the TLC performance was controlled by WinCats software (Camag®, Switzerland). TLC was performed by the authors and was performed repeatedly for three replications.

2.7. Parameter and statistical analysis

The percentage of observed mortality was calculated. The data were corrected using Abbott’s formula (Abbott, 1925). The percentages of corrected mortality were calculated and shown as mean ± SD or range as min-max. Signs of toxicity, morphological changes and abnormal behaviour were observed. The onset of action and time to death were recorded and compared with the negative control group. The severity level of morphological and behaviour changes including signs of toxicity were considered and divided into groups. The percentage of the P. americana in each group was calculated. Probit analysis using the Probit analysis program, March 1987 version (Raymond, 1985), was performed to calculate the median lethal concentrations (LC50) at a 95% confidence limit of upper (UCL) and lower (LCL) confidence limits. Results with p-value < 0.05 are considered statistically significant.

3. Results

3.1. Oral toxicity based on bait method

Each type of extract resulted in different mortality percentages and nymphicidal and adulticidal activity levels. Forty-eight hours after treatment of the final instar nymphs with baits containing hexane, dichloromethane, ethanol, or water crude extract, we observed percentage corrected mortalities of 0%–30%, 65%–100%, 7%–13%, and 0%–0% respectively. The adult P. americana at 48 h after treatment with the baits containing hexane, dichloromethane, ethanol, or water crude extract displayed percentage corrected mortalities of 11%–54%, 20%–100%, 0%–40%, and 0%–0%, respectively. The mortality of P. americana that ingested the ethanol crude extract was less than those that consumed the dichloromethane and hexane extract baits. When the dichloromethane and hexane extract baits were suddenly placed in the test boxes, P. americana retreated. After 15–30 min, a few P. americana gradually approached and ate the bait, and 48–72 h after placing the bait, all P. americana that ingested the bait had died with a swollen abdomen. The baits containing the highest concentrations of dichloromethane and hexane extracts showed the most potent repellent effect. P. americana ate the bait mixed with the low-concentration ethanol crude extract and showed symptoms of leg shaking and body tremors, but 48 h later, the symptoms had disappeared and no dead P. americana were seen. Both the final instar nymph and adult P. americana that received the dichloromethane crude extract displayed the highest percentage corrected mortality. All P. americana in the water crude extract-treated group and in the negative control group (0%–0% of corrected mortality) survived and did not show any signs of toxicity.

All P. americana that ingested the bait containing hexane and dichloromethane crude extracts, and some that consumed the ethanol crude extract, showed toxicity symptoms, such as excited movement, body elevation, hind leg shaking, whole-body tremors, immobility, and abdomen swelling. Compared with the P. americana in the negative control group (Figure 1A), the P. americana that ingested the dichloromethane and hexane crude extract-containing baits showed clear abdomen swelling (Figure 1B). At the highest concentration (50% w/w) of each crude extract, the onset time of the excited movement and shaking symptoms appeared at 13–15 min after eating the bait containing dichloromethane crude extract, which occurred faster than the ethanol crude extracts (34–40 min). At 1–3 h after consuming the bait containing the dichloromethane crude extract, the swollen abdomen occurred. The shortest duration of time-to-death was 24 h which was found in the P. americana in the dichloromethane extract-treated group. At 24–72 h, the majority of P. americana in the ethanol extract treated group had not died, but they presented immobility.

Figure 1.

Figure 1

Open in a new tab

Comparison between (A) the adult P. americana in the negative control group and (B) the adult P. americana receiving the dichloromethane crude extract and clearly showed the abdomen swelling (black arrow).

Severe effects were found, such as inflating of the peritoneum, which led to a tear of the integument (1%) (Figure 2A) or leakage of adipose tissue from the intersegmental membrane (1%) (Figure 2B). The protrusion of anal organs (Figure 2C) occurred more frequently than both of the severe effects. The inflating of the peritoneum and leaking of adipose tissue happened in some P. americana that had repeatedly ingested the toxic bait containing low concentrations (1.0% w/w–2.5% w/w) or ate the bait containing dichloromethane crude extract at the high concentration (50% w/w).

Figure 2.

Figure 2

Open in a new tab

The severe effect in the adult P. americana causing from the ingestion of toxic bait. (A) inflating of peritoneum and tearing of exoskeleton which happened with P. americana, eating repeatedly the dichloromethane bait, and (B) leaking of adipose tissue (black arrow) and (C) the protruded anus part (black arrow) was frequently occurred in the hexane and dichloromethane crude extract-treated group.

Three main signs of toxicity that developed after oral administration represented three levels of symptom severity, from most to least severe: (1) swollen abdomen, (2) apathy and absence of movement, (3) defensive behaviour and rapid locomotion. The percentage of P. americana that displayed each sign is presented in Table 1. After P. americana ate the bait mixed with dichloromethane, hexane, and ethanol crude extracts, there was sequentially apathy and motionlessness, followed by swelling of the abdomen, and those showing a swollen abdomen usually died within 72 h. The symptom of abdomen swelling was an irreversible effect.

Table 1.

The percentage of the signs of toxicity divided into three levels in each group of P. americana ingesting the different extracts, observed at 24 and 48 h.

Group of P. americana Time of observation The percentage of P. americana, observed at 24th and 48th hour
Final-instar nymph
 Adult P. americana
Swollen abdomen Apathy and absence of movement Defense behavior and rapid locomotion Swollen abdomen Apathy and absence of movement Defense behavior and rapid locomotion
Hexane treated group 24th hour 11.1–55.0 (29.2 ± 1.7) 25.0–77.8 (56.8 ± 2.3) 0.0–20.0 (11.0 ± 0.1) 16.7–60.0 (20.7 ± 1.5) 57.2–88.9 (71.6 ± 1.4) 0.0–10.0 (4.5 ± 0.2)
48th hour 21.7–60.0 (39.3 ± 1.6) 25.0–73.3 (50.7 ± 2.0) 0.0–5.0 (2.7 ± 0.2) 16.7–60.0 (38.0 ± 1.9) 42.5–80.7 (61.8 ± 1.6) 0.0–0.0 (0.0 ± 0.0)
Dichloromethane treated group 24th hour 35.0–100.0 (74.0 ± 2.8) 0.0–30.0 (16.8 ± 1.2) 0.0–0.0 (0.0 ± 0.0) 10.0–85.0 (31.5 ± 2.9) 10.0–90.0 (57.2 ± 2.9) 0.0–20.0 (8.4 ± 0.7)
48th hour 50.0–100.0 (84.0 ± 2.7) 0.0–15.0 (10.0 ± 0.8) 0.0 ± 0.0 (0.0 ± 0.0) 20.0–95.0 (33.0 ± 2.2) 20.0–80.0 (54.0 ± 2.2) 0.0–0.0 (0.0 ± 0.0)
Ethanol treated group 24th hour 0.0–33.3 (17.2 ± 1.4) 20.0–88.9 (60.8 ± 2.9) 0.0–80.0 (37.0 ± 3.2) 0.0–30.0 (16.0 ± 1.3) 10.0–70.0 (42.0 ± 2.6) 0.0–60.0 (30.0 ± 2.5)
48th hour 0.0–20.0 (8.4 ± 0.7) 20.0–88.9 (56.4 ± 2.5) 0.0–80.0 (40.5 ± 2.8) 0.0–30.0 (12.0 ± 1.3) 10.0–70.0 (36.0 ± 2.6) 0.0–60.0 (30.0 ± 2.5)
Water treated group 24th hour 0.0–0.0 (0.0 ± 0.0) 0.0–0.0 (0.0 ± 0.0) 100 (100.0 ± 0.0) 0.0 ± 0.0 (0.0 ± 0.0) 0.0 ± 0.0 (0.0 ± 0.0) 100 (100.0 ± 0.0)
48th hour 0.0–0.0 (0.0 ± 0.0) 0.0–0.0 (0.0 ± 0.0 100 (100.0 ± 0.0) 0.0 ± 0.0 (0.0 ± 0.0) 0.0 ± 0.0 (0.0 ± 0.0) 100 (100.0 ± 0.0)
Glucose treated group (Negative control) 24th hour 0.0–0.0 (0.0 ± 0.0) 0.0–0.0 (0.0 ± 0.0) 100 (100.0 ± 0.0) 0.0 ± 0.0 (0.0 ± 0.0) 0.0 ± 0.0 (0.0 ± 0.0) 100 (100.0 ± 0.0)
48th hour 0.0–0.0 (0.0 ± 0.0) 0.0–0.0 (0.0 ± 0.0) 100 (100.0 ± 0.0) 0.0 ± 0.0 (0.0 ± 0.0) 0.0 ± 0.0 (0.0 ± 0.0) 100 (100.0 ± 0.0)
Open in a new tab

Range presented in range of min-max.

(…) presented as mean ± SD.

At 24 h, the P. americana, ingesting the dichloromethane crude extract, showed the highest percentage of the swelling abdomen (35.0–100.0% in final instar nymph and 10.0–85.0% in the adult stage) and the lowest percentage of defence effect and fast movement (0.0%). At 48 h, the number of P. americana, showing apathy and motionlessness, decreased (0.0–15.0% in final instar nymph and 20.0–80.0% in the adult stage) while the percentage of the swelling abdomen increased (50.0–100.0% in final instar nymph and 20.0–95.0% in the adult stage). At 24 and 48 h, the ethanol crude extract predominantly produced the highest percentage of apathy and motionlessness (20.0–88.9% in final instar nymph and 10.0–70.0% in the adult stage) while the percentage of the swelling abdomen was lowest, compared with the dichloromethane and hexane crude extract treated groups. The P. americana eating the water crude extract and the P. americana in the negative control group eating only the glucose did not show any sign of toxicity (0% of swelling abdomen, apathy and motionlessness) and still showed fast movement and reactions to stimulants (100% of defence effect with fast movement).

3.2. Comparison of the dissected alimentary canals in the extract-killed P. americana and the P. americana in the negative control group

After the P. americana in the hexane- and dichloromethane-treated groups died with swollen abdomens, they were dissected to study the internal organs. We found that their foreguts were swollen compared with those in the water crude extract-treated and negative control groups, which showed no swelling (Figure 3). Some P. americana in the ethanol-treated group with swollen abdomens were dissected, and the foregut was found to be swollen in a similar manner to that of the P. americana in the dichloromethane- and hexane-treated groups. Black digested food was observed in the foreguts of the ethanol-, dichloromethane-, and hexane-treated groups but was not seen in the foreguts of the negative control group, which ate only glucose (Figure 3).

Figure 3.

Figure 3

Open in a new tab

The dissected alimentary canals of (A) the final instar nymphs and (B) the adult P. americana in the hexane crude extract-treated group, the dichloromethane crude extract-treated group and the negative control group receiving only glucose.

3.3. Determination of alkaloids in the crude extracts and the dissected alimentary canal using TLC method

The orange bands appeared after spraying the TLC plate with Dragendorff's spray reagent (Figure 4C), which indicated the presence of alkaloids. Quenching bands were seen under light at 254 nm (Figure 4A). Orange and quenching bands were seen at the same position (Rf = 0.41) in the didehydrostemofoline reference substance (Row No. 9), hexane crude extract (Row No. 6), and dichloromethane crude extract (Row No. 7), including the extracts of the dissected alimentary canals from the adult P. americana (Row No. 2 and 3) and final instar nymphs (Row No. 12 and 13) that ingested the hexane and dichloromethane crude extract-containing baits.

Figure 4.

Figure 4

Open in a new tab

TLC pattern of the crude extracts and the extracts from the dissected alimentary canals which was observed under (A) UV 254 nm, (B) 366 nm and (C) after sprayed with dragendorff's spray reagent. 1 = Adult P. americana ingesting glucose. 2 = Adult P. americana ingesting hexane bait. 3 = Adult P. americana ingesting dichloromethane bait. 4 = Adult P. americana ingesting ethanol bait. 5 = Adult P. americana ingesting water bait. 6 = Hexane crude extract. 7 = Dichloromethane crude extract. 8 = Ethanol crude extract. 9 = Didehydrostemofoline reference substance. 10 = Water crude extract. 11 = Final-instar nymph ingesting glucose. 12 = Final-instar nymph ingesting hexane bait. 13 = Final-instar nymph ingesting dichloromethane bait. 14 = Final-instar nymph ingesting ethanol bait. 15 = Final-instar nymph ingesting water bait.

An orange band corresponding to didehydrostemofoline alkaloid was apparent in the dichloromethane crude extract and P. americana that ingested bait containing hexane and dichloromethane crude extracts, while the water crude extract did not show this band. All extracts from dissected alimentary cavities exhibited the didehydrostemofoline band at Rf = 0.41, except those of the final instar nymph and adult P. americana that ate the bait containing the water crude extract (Row No. 5 and 15). The highest concentration of didehydrostemofoline was found in the extract from the alimentary canal of adult P. americana that consumed dichloromethane bait (Row No. 3), followed by that of the final instar nymphs that ingested the dichloromethane bait (Row No.13).

Under light at 366 nm (Figure 4B), blue and purple fluorescent bands appeared at Rf = 0.73 and Rf = 0.75, respectively. Both fluorescent bands appeared in the row containing the dichloromethane crude extract (Row No. 7) and the alimentary canal extracts of adult P. americana (Row No. 3) and final instar nymphs (Row No. 13) that ingested the dichloromethane crude extract. The highest fluorescence intensity occurred for the alimentary canal extract from the adult P. americana that ate the dichloromethane crude extract (Row No. 3), and the second highest intensity was seen for the gut extract of final instar nymphs that consumed the dichloromethane crude extract (Row No. 13).

4. Discussion

Stemona collinsiae and crude extracts including alkaloids such as didehydrostemofoline, stemofoline, and hydroxystemofoline (Kongkiatpaiboon et al., 2011; Schinnerl et al., 2007; Greger, 2006; Sastraruji et al., 2005; Seger et al., 2004; Pham et al., 2002; Jiwajinda et al., 2001) exhibit insecticidal activity against pests and important insect vectors (Sakulpanich et al., 2016, 2017; Phattharaphan et al., 2010; Vo et al., 2010; Brem et al., 2002; Jiwajinda et al., 2001), but P. americana has never been tested with S. collinsiae. This study was the first report that presented the nymphicidal and adulticidal activities of S. collinsiae root extracts against P. americana. The highest didehydrostemofoline content was in the dichloromethane crude extract and was followed by hexane and ethanol crude extracts while the absence of didehydrostemofoline was found in the water crude extract. The dichloromethane crude extract presented the highest potency against P. americana followed by the hexane and ethanol crude extracts. All P. americana in the groups that received water crude extract and only the glucose survived. The least amount of didehydrostemofoline was found in the ethanol crude extract because the didehydrostemofoline was not exhaustively extracted in the previous extraction with dichloromethane extractant. The lowest didehydrostemofoline content in the ethanol crude extract slightly affected the mortality rate in the P. americana. Therefore, didehydrostemofoline was the cause of death in the P. americana that ingested the toxic baits, especially the dichloromethane crude extract-containing bait. Interestingly, the phytochemicals possessed blue and purple fluorescent bands on TLC, which were most prominent in the dichloromethane crude extract, including extracts from the dissected alimentary cavity of the final instar nymph and adult P. americana ingesting the bait containing dichloromethane crude extract. Thus, it is possible that the unknown blue and purple fluorescent phytochemicals were also the cause of death in the dichloromethane treated P. americana. These fluorescent phytochemicals and other phytochemicals, such as stilbenoids and rotenoid flavonoids, might synergize the insecticidal activity of the alkaloids. Recently, stilbenoids isolated from Vitis vinifera canes reportedly exhibited insecticidal activity against Spodoptera littoralis larvae (Pavela et al., 2017); however, its effects on S. collinsiae are unclear and should be investigated in further experiments.

The oral toxicities of the S. collinsiae root extracts were novel, as evident from the findings. Signs of toxicity were observed, including hind leg shaking, body tremors, undirected and fast movement, immobility, paralysis, abdomen swelling, and finally death. The strongest toxicity signs were seen in P. americana that ate the dichloromethane crude extract-containing bait, and the strength was directly associated with the concentrations of didehydrostemofoline and unknown fluorescent substances. These toxicity symptoms are similar to those reported for nitromethylene heterocycle insecticides and neonicotinoids such as imidacloprid. The latter produces irregular and strong excitatory responses, such as abdominal quivering, wing flexing, uncontrollable preening, leg tremor, violent whole-body shaking, as well as depressive paralytic responses, such as prostration, immobility, paralysis (Tan et al., 2007; Schroeder and Flatum, 1984). Didehydrostemofoline containing pyrrolo[1,2-a]azepine (Schinnerl et al., 2007; Seger et al., 2004) or other alkaloids has some functional groups or pharmacophores similar to nitromethylene heterocycle insecticides and neonicotinoids comprising imidazolidine rings with electronegative atoms and N-containing cyclic/acyclic substituents (Schroeder and Flatum, 1984). Furthermore, alkaloids such as muscarine, tubocurarine, conitine, and nicotine generally act on the nervous and muscle systems. Thus, the insecticidal activity of S. collinsiae root extract is a result of alkaloids that induce neonicotinoid-like signs of toxicity.

The toxicity of didehydrostemofoline and stemofoline alkaloids which occurred from the inhibitory activity of acetylcholinesterase was reported (Kongkiatpaiboon et al., 2013). When considering other mechanisms behind the stimulation of nicotinic receptors and according to IRAC (IRAC, 2020), insect nicotinic acetylcholine receptor agonists and allosteric activators are of interest. Imidacloprid activates nicotinic acetylcholine receptor desensitized (nAChRD), while methyllicaconitine interacts with nicotinic acetylcholine receptor nondesensitized (nAChRN). Neonicotinoids, such as acetamiprid and clothianidin, are able to interact with α-bungarotoxin-insensitive nicotinic acetylcholine receptors both nAChR1 and nAChR2 to induce a biphasic current-voltage curve, whereas imidacloprid produces a monophasic current-voltage curve (Tan et al., 2007; Thany et al., 2007; Thany, 2009; Thany and Tricoire-Leignel, 2011). In comparison with this research, in terms of hyper-excitation, the cockroaches treated with the dichloromethane and hexane extracts in our study showed toxicity signs in the early stages, followed by lethargy. Because of the chemical structure-activity relationship, it is possible that the alkaloids within the S. collinsiae root extracts, especially the dichloromethane and hexane crude extracts, activate the nicotinic acetylcholine receptors, such as nAChRD and nAChRN, in the thoracic ganglia, or nAChR1 and nAChR2 in the DUM neurons. The mechanisms of action of the alkaloids isolated from S. collinsiae that interact with nicotinic acetylcholine receptors, and their structure-activity relationships, should be explored in further experiments.

Other insecticidal phytochemicals, such as stilbenoids (e.g., stemofurans A−K, dihydrostilbenes, stilbostemins A) and rotenoid flavonoids (e.g., stemonacetal, stemonal, and stemonone) (Zraunig et al., 2014; Pangkam and Chimsook, 2013; Pacher et al., 2002; Shiengthong et al., 1974), were found in S. collinsiae which exhibit inhibitory activity on mitochondrial complex I electron transport (IRAC, 2020). The S. collinisae root extracts, especially the dichloromethane crude extracts, were found to comprise alkaloids and other unknown compounds but they might also contain rotenoids. The alkaloids, rotenoids, and unknown substances could produce synergistic effects and promote the insecticidal activity of S. collinsiae root extracts.

In this research, irregular and prominent swelling of the abdomen and foregut was surprisingly found in all dead P. americana. These symptoms were irreversible and important causes of death in P. americana, especially those that ate the bait mixed with the dichloromethane crude extract. The protrusion of the anal organ and leakage of adipose tissue were a result of the excess foregut swelling and the swollen foregut being pressed against the internal organs/adipose tissue. The swelling of the abdomen and foregut was not found in the negative control group or water crude extract group but the milder effect was noticed in the ethanol crude extract group. The swollen abdomen and foregut in P. americana that ingested the dichloromethane crude extract may have resulted from didyhydrostemofoline and other alkaloids which disturbed the function of neurotransmitters and the nervous system as well as crop hydrostatic pressure, transient pressure, and hemolymphic osmotic pressure which affected crop volume and crop emptying time because the muscles of the foregut and anterior midgut, including those involved in peristaltic movement, are controlled by the stomodeal nervous system, while the release of air from the crop during the feeding process is controlled by the pharyngeal and proventriculus nervous pathways. Pressure in the hemolymph influences the hydrostatic pressure gradient in the crop lumen and the anterior part of the midgut and leads to the opening of the proventricular valve (Davey and Treherne, 1964). Interference with the function of the foregut occurred consecutively. Moreover, crop emptying is regulated by the osmotic pressure of the hemolymph, which is controlled by dietary factors. At high hemolymphic osmotic pressure, the crop emptying time is prolonged (Champman, 1998), and the absorption of toxicants and the severity of toxicity increase. However, the actual cause of the abdomen and foregut swelling is uncertain.

Unexpectedly, the bait containing hexane and dichloromethane crude extracts as active ingredients showed cockroach-repellent properties, as both the final instar nymphs and adult P. americana retreated from these crude extracts, which affected the LC50 calculation. The relationship between the concentration of the crude extract and oral toxicity was dose-independent. Therefore, the LC50 values calculated in this research do not represent the actual values. In contrast, the ethanol and water crude extracts including glucose did not show repellent properties, and the starved P. americana ate the bait soon after it was placed in the boxes. Both the dichloromethane and hexane crude extract-containing baits, which possessed an odor and repellent activity, contained high concentrations of didehydrostemofoline and blue and purple fluorescent phytochemicals. Thus, we preliminarily presumed that the odor and repellent effect might be produced by the alkaloids or the unknown fluorescent substances. Likewise, repellent hetisine alkaloid was reported to repel Tribolium casteneum (Ulubelen et al., 2001). However, insecticidal compounds in the dichloromethane and hexane crude extracts should be isolated and the repellent compounds separated to remove the characteristic odor that disturbs P. americana, allowing bait containing only the isolated insecticidal compounds to be prepared and tested. The calculation of LC50 should subsequently be renewed to obtain the actual value.

Novelty of repellent activity from S. collinsiae crude extract based on the concentration was also found in this research. P. americana were obviously killed by S. collinsiae crude extract via oral administration using a bait form. P. americana has self-grooming behavior (Zhukovskaya, 2014). It is an omnivorous insect and opportunistic feeder (Bell and Adiyodi, 1982). It could ingest a residue of the crude extract attached to its antenna, foreleg, midleg, hindleg, wing, abdomen, corpse, exuviae, or other diet. Thus, aerosol was also a form of interest, but the suitable concentration, stability, and shelf-life of the insecticidal phytochemicals in the crude extract should be selected and detected. Besides, didehydrostemofoline, having a molecular mass less than 500, and lipophilicity, could penetrate from integument via pore canal and gland including a soft intersegmental membrane. It was absorbed and distributed to the target site. It was accumulated in the lipid tissue of P. americana. For the development of an aerosol formulation, contact toxicity should be tested for finding the evidence of efficacy of S. collinsiae against P. americana in the next experiment.

5. Conclusions

The dichloromethane and hexane crude extracts showed high toxicity to P. americana. The ethanol crude extract was less toxic, while the water crude extract was non-toxic to P. americana. The dichloromethane and hexane crude extracts killed the final instar nymph and adult P. americana and, thus, can terminate their life cycle and could be applied for insect control. The alkaloids found in S. collinsiae root extracts act as neurotoxins and cause irregular symptoms and death in P. americana. Didehydrostemofoline alkaloid is reported to possess acetylcholinesterase-inhibiting activity; however, other phytochemicals may also be responsible for the insecticidal activity, including rotenoids, flavonoids, and other unknown fluorescent substances, which may also synergistically promote the insecticidal properties. The mechanisms of actions of the phytochemicals in S. collinsiae root extract might involve the nicotinic acetylcholine receptor modulator, nicotinic acetylcholine receptor allosteric modulator-site I, and mitochondrial complex I electron transport inhibitors. However, this needs further study because it was unclear which mechanisms were involved.

S. collinsiae roots contain an abundance of various insecticidal phytochemicals. This plant provides interesting raw materials for the development of alternative insecticides against the final instar nymph and adult P. americana via oral administration or in the form of a toxic bait or other form such as aerosol. This study found the repellent activity of the S. collinsiae hexane and dichloromethane crude extract. It can be used as a raw material in repellent products for repelling P. americana. The S. collinsiae root extract showed insecticidal and repellent activities against P. americana based on the concentration of the crude extract and the type of phytochemicals in the crude extract.

Declarations

Author contribution statement

Anon Phayakkaphon and Yudthana Samung: Contributed reagents, materials, analysis tools or data, Performed the experiments.

Preeyanate Dathong, Napasorn Ransibrahmanakul, Nontapat Sarovath: Performed the experiments.

Aurapa Sakulpanich: Conceived and designed the experiments; Performed the experiments; Analyzed and interpreted the data; Contributed reagents, materials, analysis tools or data; Wrote the paper.

Funding statement

This work was supported by Faculty of Pharmacy, Thammasat University Research Fund under the Specific Field Research Scholar: Research Unit in Medicinal Chemistry and Natural Products Research Unit, Contact No. Pharm TU-S 1/2019.

Data availability statement

Data included in article/supplementary material/referenced in article.

Declaration of interests statement

The authors declare no conflict of interest.

Additional information

No additional information is available for this paper.

Acknowledgements

We have to thank Assoc. Prof. Dr. Jiraporn Ruangsittichai and Assoc. Prof. Dr. Arom Jedsadayanmata for supporting and facility. Finally, we are deeply grateful to the program of Phytopharmaceutical Sciences and the department of Pharmacognosy, faculty of Pharmacy, Mahidol University which allowed us to use high-performance thin-layer chromatography (HPTLC) apparatus for the detection of phytochemicals with TLC method.

References

  1. ประกาศสำนักงานคณะกรรมการอาหารและยา เรื่อง หลักเกณฑ์การทดสอบประสิทธิภาพของวัตถุอันตราย. (2538, 26 กันยายน). ราชกิจจานุเบกษา. เล่ม 112 ตอนที่ 77ง. (In Thai language)
  2. Abbott W.S. A method of computing the effectiveness of an insecticide. J. Am. Mosq. Contr. Assoc. 1925;3(2):265–267. [PubMed] [Google Scholar]
  3. Anikwe J.C., Adetoro F.A., Anogwih J.A., Makanjuola W.A., Kemabonta K.A., Akinwande K.L. Laboratory and field evaluation of an indoxacarb gel bait against two cockroach species (Dictyoptera: blattellidae, Blattidae) in Lagos, Nigeria. J. Econ. Entomol. 2014;107(4):1639–1642. doi: 10.1603/ec13457. [DOI] [PubMed] [Google Scholar]
  4. Arruda L.K., Vailes L.D., Ferriani V.P.L., Santos A.B.R., Pomés A., Chapman M.D. Cockroach allergens and asthma. Curr. Opin. Allergy Clin. Immunol. 2001;107(3):419–428. doi: 10.1067/mai.2001.112854. [DOI] [PubMed] [Google Scholar]
  5. Asahina S. Handbook Series No. 5. 1983. Domiciliary cockroach species in Thailand. Promotion of provincial health services project; p. 12. [Google Scholar]
  6. Bell W.J., Adiyodi K.G. Chapman & Hall; New York: 1982. The American Cockroach. [Google Scholar]
  7. Bracke J.W., Cruden D.L., Markovetz A.J. Intestinal microbial flora of the American cockroach, Periplaneta americana L. Appl. Environ. Microbiol. 1979;38(5):945–955. doi: 10.1128/aem.38.5.945-955.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brem B., Seger C., Pacher T., Hofer O., Vajrodaya S., Greger H. Feeding deterrence and contact toxicity of Stemona alkaloids a source of potent natural insecticides. J. Agric. Food Chem. 2002;50:6383–6388. doi: 10.1021/jf0205615. [DOI] [PubMed] [Google Scholar]
  9. Chamavit P., Sahaisook P., Niamnuy N. The majority of cockroaches from the Samutprakarn province of Thailand are carriers of parasitic organisms. Excli J. 2011;10:218–222. [PMC free article] [PubMed] [Google Scholar]
  10. Champman R.F. fourth ed. Cambridge University Press; Cambridge: 1998. The Insects: Structure and Function; pp. 38–68. [Google Scholar]
  11. Chinchilla M., Guerrero O.M., Castro A., Sabah J. Cockroaches as transport hosts of the protozoan Toxoplasma gondii. Rev. Biol. Trop. 1994;42(1-2):329–331. PMID: 7480943. [PubMed] [Google Scholar]
  12. Chompoosri J., Thavara U., Tawatsin A., Sathantriphop S., Yi T. Cockroach surveys in the northern region of Thailand and guangxi province of China. Southeast Asian J. Trop. Med. Publ. Health. 2004;35(Suppl 2):46–49. PMID: 15906633. [PubMed] [Google Scholar]
  13. Davey Y.K.G., Treherne J.E. Studies on crop function in the cockroach (Periplaneta americana L.) J. Exp. Biol. 1964;41:513–524. [Google Scholar]
  14. Dubey J.P. The history of Toxoplasma gondii—the first 100 years. J. Eukaryot. Microbiol. 2008;55(6):467–475. doi: 10.1111/j.1550-7408.2008.00345.x. [DOI] [PubMed] [Google Scholar]
  15. El-Sherbini G.T., Gneidy M.R. Cockroaches and flies in mechanical transmission of medical important parasites in Khaldyia Village, El-Fayoum, Governorate, Egypt. J. Egypt. Soc. Parasitol. 2012;42(1):165–174. doi: 10.12816/0006304. [DOI] [PubMed] [Google Scholar]
  16. Falsone L., Colella V., Napoli E., Brianti E., Otranto D. The cockroach Periplaneta americana as a potential paratenic host of the lungworm Aelurostrongylus abstrusus. Exp. Parasitol. 2017;182:54–57. doi: 10.1016/j.exppara.2017.09.023. [DOI] [PubMed] [Google Scholar]
  17. Finney D.J. Cambridge University Press; Cambridge, England: 1971. Probit Analysis. [Google Scholar]
  18. Gijzen H.J., Barugahare M. Contribution of anaerobic protozoa and methanogens to hindgut metabolic activities of the American cockroach, Periplaneta americana. Appl. Environ. Microbiol. 1992;58(8):2565–2570. doi: 10.1128/aem.58.8.2565-2570.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Greger H. Structural relationships, distribution and biological activities of Stemona alkaloids. Planta Med. 2006;72(2):99–113. doi: 10.1055/s-2005-916258. [DOI] [PubMed] [Google Scholar]
  20. Halonen S.K., Weiss L.M. Toxoplasmosis. Handb. Clin. Neurol. 2013;114:125–145. doi: 10.1016/B978-0-444-53490-3.00008-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hill D., Dubey J.P. Toxoplasma gondii: transmission, diagnosis and prevention. Clin. Microbiol. Infect. 2002;8(10):634–640. doi: 10.1046/j.1469-0691.2002.00485.x. [DOI] [PubMed] [Google Scholar]
  22. Inthachub P., Duyfjes B.E.E. In: Flora of Thailand Volume Eleven Part One. Santisuk T., Larsen K., editors. Prachachon Co. Ltd.; Bangkok: 2011. Stemonaceae; pp. 74–99. [Google Scholar]
  23. IRAC-Insecticide Resistance Action Committee . 2020. The IRAC Mode of Action Classification.https://irac-online.org/modes-of-action/ accessed. [Google Scholar]
  24. Jiwajinda S., Hirai N., Watanabe K., Santisopasri V., Chuengsamarnyart N., Koshimizu K., Ohigashi H. Occurrence of the insecticidal 16, 17-didehydro-16(E)-stemofoline in Stemona collinsiae. Phytochemistry. 2001;56(7):693–695. doi: 10.1016/s0031-9422(00)00443-x. [DOI] [PubMed] [Google Scholar]
  25. Kassiri H., Kassiri A., Kazemi S. Investigation on American cockroaches medically important bacteria in Khorramshahr hospital, Iran. Asian Pac. J. Trop. Dis. 2014;4(3):201–203. [Google Scholar]
  26. Ko A.E., Schal C., Silverman J. Diet quality affects bait performance in German cockroaches (Dictyoptera: blattellidae) Pest Manag. Sci. 2016;72(10):1826–1836. doi: 10.1002/ps.4295. [DOI] [PubMed] [Google Scholar]
  27. Kongkiatpaiboon S., Rojsanga P., Pattarajinda V., Gritsanapan W. Acetylcholinesterase inhibitory activity of didehydrostemofoline, stemofoline alkaloids and extracts from Stemona collinsiae Craib roots. Pharm. J. 2013;5(2):56–59. [Google Scholar]
  28. Kongkiatpaiboon S., Schinnerl J., Felsinger S., Keeratinijakal V., Vajrodaya S., Gritsanapan W., Brecker L., Greger H. Structural relationships of Stemona alkaloids: assessment of species-specific accumulation trends for exploiting their biological activities. J. Nat. Prod. 2011;74(9):1931–1938. doi: 10.1021/np2004374. [DOI] [PubMed] [Google Scholar]
  29. Lee D.K., Lee W.J., Sim J.K. Population densities of cockroaches from human dwellings in urban areas in the Republic of Korea. J. Vector Ecol. 2003;28(1):90–96. [PubMed] [Google Scholar]
  30. Malik K., Jamil A., Arshad A. Study of pathogenic microorganisms in the external body parts of American cockroach (Periplaneta americana) collected from different kitchens. IOSR J. Pharm. Biol. Sci. 2013;7(6):45–48. [Google Scholar]
  31. Nasirian H. Infestation of cockroaches (Insecta: blattaria) in the human dwelling environments: a systematic review and meta-analysis. Acta Trop. 2017;167:86–98. doi: 10.1016/j.actatropica.2016.12.019. [DOI] [PubMed] [Google Scholar]
  32. Pacher T., Seger C., Engelmeier D., Vajrodaya S., Hofer O., Greger H. Antifungal stilbenoids from Stemona collinsae. J. Nat. Prod. 2002;65(6):820–827. doi: 10.1021/np0105073. [DOI] [PubMed] [Google Scholar]
  33. Pai H.H., Chen W.C., Peng C.F. Isolation of bacteria with antibiotic resistance from household cockroaches (Periplaneta americana and Blattella germanica) Acta Trop. 2005;93:259–265. doi: 10.1016/j.actatropica.2004.11.006. [DOI] [PubMed] [Google Scholar]
  34. Pai H.H., Ko Y.C., Chen E.R. Cockroaches (Periplaneta americana and Blattella germanica) as potential mechanical disseminators of Entamoeba histolytica. Acta Trop. 2003;87:355–359. doi: 10.1016/s0001-706x(03)00140-2. [DOI] [PubMed] [Google Scholar]
  35. Pangkam N., Chimsook T. The structure activity relationship and cytotoxicity between stemonal and 6-deoxyclitoriacetal. Adv. Mater. Res. 2013;699:698–702. [Google Scholar]
  36. Patel S., Meher B.R. A review on emerging frontiers of house dust mite and cockroach allergy research. Allergol. Immunopathol. 2016;44(6):580–593. doi: 10.1016/j.aller.2015.11.001. [DOI] [PubMed] [Google Scholar]
  37. Pavela R., Waffo-Teguo P., Biais B., Richard T., Me´rillon J.M. Vitis vinifera canes, a source of stilbenoids against Spodoptera littoralis larvae. J. Pest. Sci. 2017;90:961–970. [Google Scholar]
  38. Pham H.D., Yu B.W., Chau V.M., Ye Y., Qin G.W. Alkaloids from Stemona collinsae. J. Asian Nat. Prod. Res. 2002;4(2):81–85. doi: 10.1080/10286020290027344. [DOI] [PubMed] [Google Scholar]
  39. Phattharaphan N., Pitiyont B., Visetson S. Potential of Stemona sp. for Plutella xylostella control. J. Biopestic. 2010;3(1):278–281. [Google Scholar]
  40. Raymond M. Preséntation d’ un programme d’ analyse log-probit pour microordinnateur. Cah. ORSTOM, Ser. Ent. med et Parasitol. 1985;22(2):117–121. [Google Scholar]
  41. Revay E.E., Schlein Y., Tsabari O., Kravchenko V., Qualls W., De-Xue R., Beier J.C., Traore S.F., Doumbia S., Hausmann A., Müller G.C. Formulation of attractive toxic sugar bait (ATSB) with safe EPA-exempt substance significantly diminishes the Anopheles sergentii population in a desert oasis. Acta Trop. 2015;150:29–34. doi: 10.1016/j.actatropica.2015.06.018. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Sakulpanich A., Attrapadung S., Gritsanapan W. Insecticidal activity of Stemona collinsiae root extract against Parasarcophaga ruficornis (Diptera: sarcophagidae) Acta Trop. 2017;173:62–68. doi: 10.1016/j.actatropica.2017.05.027. [DOI] [PubMed] [Google Scholar]
  43. Sakulpanich A., Attrapadung S., Gritsanapan W. Larvicidal activity evaluation of Stemona collinsae root extract in third-instar larva of Blow fly (Chrysomya megacephala) Planta Med. 2016;82(1):P846. [Google Scholar]
  44. Sastraruji T., Jatisatienr A., Pyne S.G., Ung A.T., Lie W., Williams M.C. Phytochemical studies on Stemona plants: isolation of stemofoline alkaloids. J. Nat. Prod. 2005;68(12):1763–1767. doi: 10.1021/np050361y. [DOI] [PubMed] [Google Scholar]
  45. Schinnerl J., Brem B., But P.P., Vajrodaya S., Hofer O., Greger H. Pyrrolo- and pyridoazepine alkaloids as chemical markers in Stemona species. Phytochemistry. 2007;68(10):1417–1427. doi: 10.1016/j.phytochem.2007.03.002. [DOI] [PubMed] [Google Scholar]
  46. Schou C., Lind P., Enrique F.C., Lockey R.F., Henning L. Identification and purification of an important cross-reactive allergen from american (Periplaneta americana) and German (Blattella germanica) cockroach. J. Allergy Clin. Immunol. 1990;86(6):935–946. doi: 10.1016/s0091-6749(05)80157-5. [DOI] [PubMed] [Google Scholar]
  47. Schroeder M.E., Flatum R.F. The mode of action and neurotoxic properties of the nitromethylene heterocycle insecticides. Pestic. Biochem. Physiol. 1984;22(2):148–160. [Google Scholar]
  48. Seanmanot S., Insung A., Pumnuan J., Tawatsin A., Thavara U., Phumee A., Gay F., Tachaboonyakiat W., Siriyasatien P. Insecticidal activity of Thai botanical extracts against development stages of German cockroach, Blattella germanica (L.) (Orthoptera: blattellidae) Southeast Asian J. Trop. Med. Publ. Health. 2018;49(1):46–49. [Google Scholar]
  49. Seger C., Mereiter K., Kaltenegger E., Pacher T., Greger H., Hofer O. Two pyrrolo[1, 2-α] azepine type alkaloids from Stemona collinsae Craib: structure elucidation, relationship to asperagamine A, and a new biogenetic concept of their formation. Chem. Biodivers. 2004;1(2):265–279. doi: 10.1002/cbdv.200490023. [DOI] [PubMed] [Google Scholar]
  50. Shiengthong D., Donavanik T., Uaprasert V., Roengsumran S., Massy-Westropp R.A. Constituents of Thai medicinal plants - III new rotenoid compounds - stemonacetal, stemonal and stemonone. Tetrahedron Lett. 1974;15(23):2015–2018. [Google Scholar]
  51. Sookrung N., Khetsuphan T., Chaisri U., Indrawattana N., Reamtong O., Chaicumpa W., Tungtrongchitr A. Specific B-cell epitope of per a 1: a major allergen of American cockroach (Periplaneta americana) and anatomical localization. Allergy Asthma Immunol. Res. 2014;6(4):325–332. doi: 10.4168/aair.2014.6.4.325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Srinivasan R., Jambulingam P., Subramanian S., Kalyanasundaram M. Laboratory evaluation of fipronil against Periplaneta americana & Blattella germanica. Indian J. Med. Res. 2005;122(1):57–66. PMID: 16106092. [PubMed] [Google Scholar]
  53. Srisuwatchari W., Kwanthong P., Bunnag C., Pacharn P., Jirapongsananuruk O., Visitsunthorn N. Association between skin prick test and serum specific immunoglobulin E to American cockroach allergens in allergic rhinitis patients. Allergol. Immunopathol. 2020;48(2):170–174. doi: 10.1016/j.aller.2019.07.007. [DOI] [PubMed] [Google Scholar]
  54. Sriwichai P., Nacapunchai D., Pasuralertsakul S., Rongsriyam Y., Thavara U. Survey of indoor cockroaches in some dwellings in Bangkok. Southeast Asian J. Trop. Med. Publ. Health. 2002;33(Suppl 3):36–40. [PubMed] [Google Scholar]
  55. Suntaravitun P., Dokmaikaw A. Prevalence of intestinal parasites and associated risk factors for infection among rural communities of Chachoengsao province, Thailand. Kor. J. Parasitol. 2018;56(1):33–39. doi: 10.3347/kjp.2018.56.1.33. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Tan J., Galligan J.J., Hollingworth R.M. Agonist actions of neonicotinoids on nicotinic acetylcholine receptors expressed by cockroach neurons. Neurotoxicology. 2007;28(4):829–842. doi: 10.1016/j.neuro.2007.04.002. [DOI] [PubMed] [Google Scholar]
  57. Tatfeng Y.M., Usuanlele M.U., Orukpe A., Digban A.K., Okodua M., Oviasogie F., Turay A.A. Mechanical transmission of pathogenic organisms: the role of cockroaches. J. Vector Borne Dis. 2005;42(4):129–134. [PubMed] [Google Scholar]
  58. Tawatsin A., Thavara U., Chompoosri J., Kong-ngamsuk W., Chansang C., Paosriwong S. Cockroach surveys in 14 provinces of Thailand. J. Vector Ecol. 2001;26(2):232–238. [PubMed] [Google Scholar]
  59. Thany S.H., Tricoire-Leignel H. Emerging pharmacological properties of cholinergic synaptic transmission: comparison between mammalian and insect synaptic and extrasynaptic nicotinic receptors. Curr. Neuropharmacol. 2011;9(4):706–714. doi: 10.2174/157015911798376343. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Thany S.H., Lenaers G., Raymond-Delpech V., Sattelle D.B., Lapied B. Exploring the pharmacological properties of insect nicotinic acetylcholine receptors. Trends Pharmacol. Sci. 2007;28(1):14–22. doi: 10.1016/j.tips.2006.11.006. [DOI] [PubMed] [Google Scholar]
  61. Thany S.H. Agonist actions of clothianidin on synaptic and extrasynaptic nicotinic acetylcholine receptors expressed on cockroach sixth abdominal ganglion. Neurotoxicology. 2009;30:1045–1052. doi: 10.1016/j.neuro.2009.06.013. [DOI] [PubMed] [Google Scholar]
  62. Thavara U., Tawatsin A., Bhakdeenuan P., Wongsinkongman P., Boonruad T., Bansiddhi J., Chavalittumrong P., Komalamisra N., Siriyasatien P., Mulla M.S. Repellent activity of essential oils against cockroachs (dictyoptera: blattidae, blattellidae, and blaberidae) in Thailand. Southeast Asian J. Trop. Med. Publ. Health. 2007;38(4):663–673. [PubMed] [Google Scholar]
  63. Tinker K.A., Ottesen E.A. The core gut microbiome of the American cockroach, Periplaneta americana, is stable and resilient to dietary shifts. Appl. Environ. Microbiol. 2016;82(22):6603–6610. doi: 10.1128/AEM.01837-16. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Ulubelen A., Meriçli A.H., Meriçli F., Kilinçer N., Ferizli A.G., Emekci M., Pelletier S.W. Insect repellent activity of diterpenoid alkaloids. Phytother Res. 2001;15(2):170–171. doi: 10.1002/ptr.688. [DOI] [PubMed] [Google Scholar]
  65. Vo D.T., Hsu W.H., Abu-Basha E.A., Martin R.J. Insect nicotinic acetylcholine receptor agonists as flea adulticides in small animals. J. Vet. Pharmacol. Therapeut. 2010;33(4):315–322. doi: 10.1111/j.1365-2885.2010.01160.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Wallace G.D. Experimental transmission of Toxoplasma gondii by cockroaches. J. Infect. Dis. 1972;126(5):545–547. doi: 10.1093/infdis/126.5.545. [DOI] [PubMed] [Google Scholar]
  67. Zahraei-Ramazani A.R., Saghafipour A., Vatandoost H. Control of American cockroach (Periplaneta americana) in municipal sewage disposal system, Central Iran. J. Arthropod Borne Dis. 2018;12(2):172–179. PMID: 30123811; PMCID: PMC6091800. [PMC free article] [PubMed] [Google Scholar]
  68. Zhukovskaya M.I. Grooming behavior in American cockroach is affected by novelty and odor. Scient. World J. 2014;2014:329514. doi: 10.1155/2014/329514. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Zraunig A., Pacher T., Brecker L., Greger H. Phenylbenzofuran-type stilbenoids from Stemona species. Phytochem. Lett. 2014;9:33–36. [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

Data included in article/supplementary material/referenced in article.

Articles from Heliyon are provided here courtesy of Elsevier

RESOURCES