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Vector Control, Pest Management, Resistance, Repellents
Control of Cockroaches (Blattaria) in Sewers: APractical
Approach SystematicReview
HassanNasirian1,3, and ArefSalehzadeh2
1Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran,
Iran, 2Department of Medical Entomology, School of Medicine, Hamadan University of Medical Sciences, Hamadan, Iran, and
3Corresponding author, e-mail: hanasirian@yahoo.com
Subject Editor: Richard Johnson
Received 12 August 2018; Editorial decision 20 October 2018
Abstract
Periplaneta americana (L.) (Blattaria: Blattidae), the American cockroach, is the most important invasive urban pest
of sewer environments colonizing there with high significance of human public health and household allergens
need to be controlled. Therefore this practical approach systematic review perform internationally to highlight
and provide a detailed P.americana control in sewers. Among 474 searched papers, 129 of those were selected
to become this practical approach systematic review of the American cockroach control in sewers. To control the
American cockroaches, many studies have been conducted in various fields describing from an angle. The results
were classified and discussed in getting cockroaches from sewers into buildings and their elimination, insecticide
susceptibility, application of dust, bait and Inesfly paint insecticide formulations, biocontrol, and futuristic action
categories. Arecommending manner to achieve a successful P. americana cockroach control in sewers is using
a combination of Integrated Pest Management (IPM) strategies resulted in significant reductions of cockroach
infestations and asthma health outcomes. Use ofthe American cockroach breeding thelytok y, push–pull strategies
and an automated sewer robot, and integrating health into the future buildings may be new approaches ofthe
American cockroach control strategies.
Key words: American cockroach, Periplaneta americana, allergen, integrated pest management, IPM
Cockroaches (Blattaria) have a world-wide distribution especially
in the tropical and subtropical areas. They demonstrate extraordin-
ary adaptation to a wide range of habitats, reproduce rapidly, and
have lthy habits and a bad smell. Cockroaches have been proved
acting as probable carriers of the pathogenic or opportunistic bac-
teria and fungi found in nosocomial infections, and food-borne
poisoning mostly being drug resistant. They involve in human intes-
tinal parasites and intermediate hosts, and play a role as a major
source of allergens (Tachbele etal. 2006; Salehzadeh et al. 2007;
Fakoorziba et al. 2010; Kassiri and Kazemi 2012; Page 2012;
Pai 2013; Motevali Haghi et al. 2014a,b; Menasria et al. 2015;
Varadínová etal. 2015; Nasirian 2016; Atiokeng Tatang etal. 2017;
Davari etal. 2017a; Martínez-Girón etal. 2017; Nasirian 2017a,b;
Esty and Phipatanakul 2018; Nasirian 2018; Schapheer etal. 2018;
Sookrung etal. 2018). In addition to the great medical importance,
cockroaches are a common and important pest that inhabit various
public places (Wagan etal. 2017) and are one of the key group of
insect pests in sewer environments (Gul etal. 2017).
After developing and increasing the population of the cities and
expanding of industries and factories, the issue of environmental
pollution is becoming increasingly important. Effective collection
and treatment of urban waste water is essential to the health of our
rivers, lakes and coastal waters and to protect human health. The
collection of sanitary and human wastewaters is one of the most
important issues of urban and rural life due to the high levels of con-
tamination and pathogenic microorganisms toxicity and odor nuis-
ance to the network stakeholders and the public (Carrera etal. 2016,
EPA 2016, Shammay etal. 2016). So at rst the wastewaters need to
be decontaminated, and then returned into the ow of water in the
nature after their collecting and bringing out of the towns by sewers.
The most common worldwide cockroaches are the American
(Periplaneta americana), the German (Blattella germanica), the
Oriental (Blatta orientalis), and the brown-banded (Supella lon-
gipalpa) cockroaches (Sulaiman et al. 2011, Nasirian 2016).
Periplaneta americana (L.) (Blattaria: Blattidae) is one of the most
important synanthropic invasive and hygienic urban pests distrib-
uted worldwide. This pest species is an annoyance to human as
associates with diseases and allergies, and damages to clothes and
documents (Hwang and Chen 2004, Reierson etal. 2005, Baggio-
Deibler et al. 2018, Zhu et al. 2018). The American cockroaches
Journal of Medical Entomology, 56(1), 2019, 181–191
doi: 10.1093/jme/tjy205
Advance Access Publication Date: 20 November 2018
Review Article
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are also a prevailing species and important sources of household
allergens (Hubner-Campos etal. 2013, Carlson etal. 2017, Esty and
Phipatanakul 2018, Sookrung etal. 2018). Unlike the German cock-
roach being the most invading pests of human dwellings (Noureldin
and Farrag 2008, Paksa et al. 2012, Nazari etal. 2016, Tang etal.
2016, Sanei Dehkordi et al. 2017, Davari et al. 2018, Nasirian
2018), it is considerable that P.americana species is the most import-
ant pests of sewers. The appropriate conditions of the sewers such
as humidity, temperature, darkness of the environment, and presence
of plenty of water and food have made sewers as a suitable environ-
ment to the growth and reproduction of the American cockroaches.
In fact, a sewer is a perfect home for the American cockroaches. An
underground sewer system is insulated, warm in winter, and cool
in summer. Asewer provides protection from people and predators
with the possible exception of hungry rats. The substantial problem
is when these creatures exit the sewers and enter the people homes
and other buildings. A large-scale of P. americana cockroaches
migrates to human dwellings via breathing manholes of sewers.
Nowadays, P.americana not only is a domiciliary pest but also
the most frequent species in sewers which colonize there turning into
suitable environment for reproduction and growth with high sig-
nicance of human public health throughout the world, especially
in metropolitan areas neglecting maintenance of manholes for long
periods. They frequently invade surrounding buildings after mov-
ing from sewers (Reierson etal. 2005, Tee etal. 2011b, Bueno-Marí
et al. 2013, Dehghani et al. 2014, Lupo 2017, Alias and Retnani
2018). When cockroaches are occupying sewers and, more impor-
tantly, escaping from sewers, solving the problem is not as easy as
we would think required control measures. Treating the sewers with
insecticides can become a political and regulatory issue, involving
coordination with the sewer authority. The older the sewers, the
more likely it is to be infested with cockroaches, and the more dif-
cult it will be to solve the problem (Williams 2016).
To control P. americana, many studies have been conducted in
various elds which has been published in separate papers or notes
and describe from an angle of the topic such as getting cockroaches
from sewers into buildings and their elimination, sewer cockroach
population size and age-class structure, ghting measures such as
insecticide susceptibility, application of dust, bait and Inesy paint
insecticide formulations, possible plant essential oil application and
biocontrol, and futuristic actions such as integrating health into the
future buildings and future techniques for control of cockroaches.
Each of them can be a good lever for P.americana control measures.
Putting the all levers of control on the table in order to use the best
optimized P.americana control that encountered conditions require
to be used. Therefore this practical approach systematic review per-
form internationally to highlight and provide a detailed of the cock-
roach control in sewers between July 2017 and July2018.
Materials and Methods
Paper Collection and Selection forReview
At the rst step, some special phrases or key words like ‘sewers’, ‘cock-
roaches’, ‘medical importance of cockroaches’, ‘Periplaneta ameri-
cana’, ‘American cockroach’, ‘medical importance of Periplaneta
americana’, ‘insecticide susceptibility’, and ‘control of P.americana
or American cockroaches in sewers’ were used to search the relevant
papers or notes from websites like Scopus, PubMed, Web of Science,
Google Scholar, Springer, Elsevier, ScienceDirect and academic
assemblies between July 2017 and July 2018. In the second step,
some special phrases or key words were selected among the con-
tent of the searched papers after carefully reading. Then they were
used as new key words or phrases to seek the new papers about the
subject of the study. Of the 474 papers from the above-mentioned
websites, 129 papers were selected to become this practical approach
systematic review study of sewer cockroach control.
Paper Data Extraction and Classification
The papers were dedicated to having sewer cockroach control were
read carefully and their contents were extracted and categorized
using Nasirian (2017a,b; 2018) methodology (Nasirian 2017a,b,
Nasirian 2018). Results of cockroach control in sewers which were
extracted and classied in separate distinct categories, and their
extensive description represented in the section of the results sum-
marized in Table1.
Results and Discussion
Getting Cockroaches From Sewers Into Buildings and
Their Elimination
Having cockroaches in a sewer system would not be a problem, if
cockroaches stayed put. But they do not stay put. The American
cockroaches have only one generation per year. Adults and nymphs
of the American cockroaches are active throughout a year (Tee etal.
2011b). Adults and fully-grown cockroach nymphs migrate from
sewers into buildings for food, shelter and overwintering (Williams
2016). The movements of cockroach density rates between the man-
holes of sewers also correlate with the mean daily minimum tem-
perature (Tee etal. 2011b).
An effective tactic to reduce cockroach allergen exposures is
eliminating the cockroaches (Sever et al. 2007). As cockroaches
afliate with food, water, and shelter sources. Therefore potential
cockroach food, water, and shelter sources should be eliminated as
well as elimination and closing of crevices or cracks (Orkin 2018).
To eliminate the cockroaches’ water sources and entering points,
any cracks or holes in the drain pipes would be located by using
a ashlight and would be sealed with appropriate caulk. Standing
water attracts cockroaches; so any leaky faucets would be xed.
Crevices and holes around the drain pipes would be sealed with
caulk, plaster or cement. Any gaps around the pipes would be
looked for and lled with silicone sealant or urethane foam. Any
space around the pipes and holes in the walls where they come
through the walls would be sealed by using expanding insulation
foam (TICLP 2017). After that, a very thorough inspection of the
areas should be inspected. Evaluating the situation and making a
customized highly effective treatment plan will correlate with the
needs (Orkin 2018). Exterior treatments, drain cleaning and treat-
ments, drain traps, and interior inspections are steps of the solutions
to eliminate the cockroaches represented briey by Lupo (2017)
that depending on the circumstances need to be accurately imple-
mented (Lupo 2017).
Fighting Measures
Many researches to achieve appropriate and effective insecticides
control against cockroaches using newer methods are still ongoing
(Buczkowski etal. 2001). Various registered aqueous sprays, dusts,
and baits are applied to sewer shafts for the American cockroach
control (Rust etal. 1991, Reierson etal. 2005). The use of spraying
insecticides, and re and fogging is the most popular method in sew-
ers. Due to the high population density of P. americana cockroach
species in sewers as a result of suitable warm and humid environ-
ment, the choice of an appropriate and effective insecticide is neces-
sary for its control. Resistance of cockroaches to insecticides also can
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Table1. Results of category data extracted and classified about cockroach control in sewers
Category References
Getting cockroaches from sewers into buildings and their elimination Tee etal. 2011b, Williams 2016, Lupo 2017, TICLP 2017, Orkin
2018
Insecticide susceptibility
Resistance of P.americana to cyclodiene Thompson etal. 1993
Susceptibility of P.americana to lambda-cyhalothrin, permethrin, del-
tamethrin, cyuthrin and alpha-cypermethrin
Vythilingam and Sutivigit 1994
Susceptibility of P.americana and B.germanica to commercially dish-
washing liquids and cleaners
Baldwin and Koehler 2007
Resistance of P.americana to imidacloprid, deltamethrin, pronil and
Metarhizium anisopliae
Syed etal. 2014
Resistance of P.americana to malathion Tahir etal. 2017
Effectivity of long-lasting insecticide-treated nets against non-target
household insects including P.americana
Sharma etal. 2006
Application of dust formulations Schoeld and Crisafulli 1980, Rust etal. 1991, Reierson etal. 2005
Application of bait formulations
Application of abamectin bait against P.americana Koehler etal. 1991
Application of neonicotinyl baits (pronil 0.05% and imidacloprid
2.15% gel baits) against P.americana
Reierson etal. 2005
Application of dust consisting of pyrethrins, piperonyl butoxide, boric
acid, and diatomaceous earth against P.americana
Reierson etal. 2005
Application of bait formulation containing abamectin B1, orthoboric acid,
or propoxur against P.americana
Appel etal. 2005
Application of pronil 0.03% (Goliath gel) against P.americana Srinivasan etal. 2005
Application of gel baits (0.01 and 0.05% pronil, and 0.6% indoxacarb)
against P.americana
Bayer etal. 2012
Application of indoxacarb 0.6% gel bait (Advion) against P.americana Anikwe etal. 2014
Application of Potassium alum against P.americana Salama 2015
Application of Beauveria bassiana bait formulation against P.americana Wang etal. 2016
Bait preference of P.americana to insecticides and natural foods Porusia etal. 2017
Application of insecticidal bait to reduce asthma of cockroach exposure Rabito etal. 2017
Application of Inesy paint insecticide formulations Delacour-Estrella etal. 2014, Hazra 2018
Application of plant essential oils as insect repellents
Repellency of N,N-diethylphenylacetamide (DEPA) against P.americana Prakash etal. 1990
Application of essential oil of Alpinia calcarata against P.americana Paranagama and Sujantha Ekanayake 2004
Fumigant effects of Allium sativum, Allium cepa, Thymus vulgaris,
Origanum dubium, Rosemarinus ofcinalis and Brassica nigra against
P.americana
Yilmaz and Tunaz 2013
Biocontrol
Releasing of Aprostocetus hagenowii parasitoid against P.americana Reierson etal. 2005
Investigating parasitism of P.americana oothecae by Evania
appendigaster
Fox and Bressan-Nascimento 2006
Investigating parasitism of Steinernema carpocapsae nematodes against
P.americana and B.germanica
Maketon etal. 2010
Release of Aprostocetus hagenowii parasitoids against P.americana Tee etal. 2011a
Evaluating of Metarhizium anisopliae, M.robertsii and Beauveria bassi-
ana against P.americana
Hubner-Campos etal. 2013
Evaluating of B.bassiana and M.anisopliae conidial suspensions against
P.americana
Hernández-Ramírez etal. 2007
Evaluating of M.anisopliae IP46 strain against P.americana Gutierrez etal. 2016
Evaluating of M.anisopliae (the JAB68 isolate) and B.bassiana (the
IBCB35 isolate) against P.americana
Baggio-Deibler etal. 2018
The challenges of nding environmentally safe treatments Hwang and Chen 2004, Reierson etal. 2005, Hernández-Ramírez
etal. 2007, Maketon etal. 2010, Kumar Reddy and Lee 2012,
Amin etal. 2014, Angelakis and Snyder 2015, Rani etal. 2017,
Davari etal. 2018, Orkin 2018
Futuristic actions
Integrating health into the future buildings Heidari etal. 2017
Future techniques for control of cockroaches
The parthenogenesis of domiciliary P.americana cockroaches Katoh etal. 2017
P.americana exhibits automixis-type thelytoky Tanaka and Daimon 2018
An automated sewer robot conduct any inspection of the sewage pipeline Mongeau etal. 2014, Vaani etal. 2017
The use of push–pull strategies in IPM Cook etal. 2007
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be delayed or avoided by using an appropriate insecticide (Tee etal.
2011b, Bueno-Marí etal. 2013).
Insecticide susceptibility (Thompson et al. 1993, Vythilingam
and Sutivigit 1994, Baldwin and Koehler 2007, Syed etal. 2014,
Tahir etal. 2017), effectivity of long-lasting insecticide-treated nets
(LLINs) (Sharma etal. 2006), application of dust, bait and Inesy
paint insecticide formulations (Schoeld and Crisafulli 1980,
Koehler etal. 1991, Rust etal. 1991, Appel etal. 2005, Reierson etal.
2005, Srinivasan etal. 2005, Bayer etal. 2012, Anikwe etal. 2014,
Delacour-Estrella etal. 2014, Salama 2015, Wang etal. 2016, Porusia
etal. 2017, Rabito etal. 2017, Hazra 2018) and plant essential oils
as insect repellents (Prakash etal. 1990, Paranagama and Sujantha
Ekanayake 2004, Yilmaz and Tunaz 2013), and biocontrol (Reierson
etal. 2005, Fox and Bressan-Nascimento 2006, Hernández-Ramírez
etal. 2007, Maketon etal. 2010, Tee etal. 2011a, Hubner-Campos
et al. 2013, Gutierrez et al. 2016, Baggio-Deibler et al. 2018) are
ghting measures that their extensive description represented and
discussed in the following items (Table1).
Insecticide Susceptibility
Unlike the German cockroaches which its insecticide susceptibility
or resistance has been well studied, a few studies have been per-
formed in the eld of insecticide susceptibility or resistance against
the American cockroaches. There are few studies being also available
about the efcacy of insecticide formulations against P.americana in
sewers (Tee etal. 2011b, Bueno-Marí etal. 2013). Vythilingam and
Sutivigit (1994) reported that P.americana was susceptible to namely,
lambda-cyhalothrin, permethrin, deltamethrin, cyuthrin, and alpha-
cypermethrin pyrethroids. The susceptibility level based on LC50 were
observed as the lambda-cyhalothrin > permethrin > deltamethrin >
cyuthrin > alpha-cypermethrin order. Lambda-cyhalothrin was the
most effective and alpha-cypermethrin was the least effective against
P. americana (Vythilingam and Sutivigit 1994). However, a study
exhibited a moderate levels of resistance (2.0-fold) to deltamethrin
against P. americana (Syed etal. 2014). Excluding bed bugs, 100%
mortality was detected in nontarget household insects including the
American cockroaches by cone bioassaytests.
Cyclodiene insecticide resistance in the American cockroaches is
related with a single base pair replacement in the GABA receptor
or chloride ion channel gene Rdl (Thompson etal. 1993). In many
parts of the world, the control of cockroaches discontinue with
diazinon and chlorpyrifos applications (Reierson etal. 2005). Unlike
the German cockroaches, the commercially available formulations
of dishwashing liquids and cleaners were not effective against the
American cockroaches (Baldwin and Koehler 2007). Imidacloprid
and deltamethrin (2.0-fold), and pronil (3.9-fold) exhibited moder-
ate level of resistance against adult P.americana (Syed etal. 2014).
Findings of topically applied entomopathogenic Metarhizium
anisopliae (Hypocreales: Clavicipitaceae) also emphasize a distinct
resistance of nymphs of the American cockroach to M.anisopliae
(Gutierrez et al. 2016). The American cockroach populations also
exhibited resistance against malathion with signicantly higher
activities of insecticide detoxifying enzymes which were recorded
compared to the susceptible control population. The elevated levels
and higher enzymatic activity of glutathione S-transferases (GSTs),
monooxygenases, and nonspecic esterases are the possible reasons
for resistance of malathion and enzymes involved in resistance devel-
opment (Tahir etal. 2017).
Briey, P. americana is being emerged resistant to cyclodiene,
deltamethrin, pronil, imidacloprid and malathion insecticides, and
entomopathogenic M. anisopliae (Thompson et al. 1993, Baldwin
and Koehler 2007, Syed etal. 2014, Gutierrez etal. 2016, Tahir etal.
2017). Certainly, a lot of studies need to be done in the future. Unlike
the American cockroaches, there are numerous studies performed in
the eld of insecticide resistance against the German cockroaches.
Currently it is well documented that the German cockroaches are
being emerged resistant to a wide groups of insecticides including
organophosphates, carbamates, pyrethroids, phenyl pyrazoles, spi-
nosad, neonicotinoids, and oxadiazines (Nasirian et al. 2006a–e;
Nasirian etal. 2009; Limoee et al. 2010; Nasirian 2010; Nasirian
etal. 2011; Paksa etal. 2011, 2012; Ladonni etal. 2013; Naqqash
etal. 2016; Nazari etal. 2016; Sanei Dehkordi etal. 2017).
Although the commercially available formulations of cleaners
and dishwashing liquids were equally toxic to adult B. germanica
cockroaches getting 83–100% mortality with 100% cleaner via an
immersion application and 92–100% mortality at 1% dishwashing
liquid. However, they were not effective against the adult American
cockroaches except for immersion application of dishwashing liquid
resulted in a 0.24% LC50 (Baldwin and Koehler 2007).
During recent years, LLINs, treated at factory level with insec-
ticide either coated around or incorporated into bers, have been
started to conquer the problems of low retreatment rates, washing,
and erratic dose of the insecticide resulting in the dilution of efcacy
of the conventional insecticide-treated mosquito nets. Excluding bed
bugs, 100% mortality was detected in nontarget household insects
including the American cockroaches by cone bioassay tests. In addi-
tion to LLINs are highly effective against malaria vectors they mod-
erately impact against non-target household insects (Sharma etal.
2006).
Sewers are being sought to use approved strategies of Integrated
Pest Management (IPM) and the materials with minimal envi-
ronmental impact and low mammalian toxicity can be used. The
persistence and efcacy of insecticides in sewers depend on sev-
eral factors like the rate of organic matters, formulation type, the
kind of active matter, the type of cockroach populations, and cli-
matic conditions. It seems emerging of insecticide resistance is the
most factors that affects the persistence and efcacy of insecticides.
Microencapsulated diazinon and aqueous sprays of wettable pow-
der chlorpyrifos provide an excellent control of cockroaches for at
least 9 mo. Emulsiable concentrate and microencapsulated and
chlorpyrifos sprays provide >94.0% reductions of cockroaches for
a year (Rust etal. 1991). The product combining piperonyl butox-
ide with tetramethrin and alfacipermetrin (pyrethroids) also achieve
excellent results with cockroach control while the insecticide persis-
tence effects achieve during 1 mo in sewers. These results concord-
ance with outcomes of the other former studies (Rust etal. 1991,
Fahiminia etal. 2010, Bueno-Marí etal. 2013). Obviously, the effec-
tiveness of the insecticide formulations for 1-mo control is very little
time that this time should be increased. Diazinon and clorpyrifos
(organophosphate) insecticides reduce the cockroach populations
for only 1wk (Bueno-Marí etal. 2013). It may be due to insecticide
resistance (Tahir etal. 2017) and inadequate insecticide doses.
Application of Dust Formulations
A great way to treat cockroach in the crevices and small cracks is
to be dust. Various powders, dusts, and dusters for control of cock-
roaches are to be boric acid, Delta Dust, Drione Dust, bellow dust-
ers, and electric dusters. Pyrethrins, the active ingredients of the
pyrethrum insecticide, are very effective in killing insects but are
quite harmless to mammals. When combined with silica gel to form
Drione powder, they can be applied for long-term against insects
(Schoeld and Crisafulli 1980). Drione dust is a very safe product
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and also very effective which remains effective as long as it stays dry.
An appropriate proprietary dust formulation as little as 50–100g/
manhole including boric acid 35.5%, diatomaceous earth 50%,
piperonyl butoxide 10.0%, and pyrethrins 2.0% blown into the
system with a commercial DeVilbis sprayer provide >98% control
for at least 3 mo (Reierson et al. 2005). Apowder of synergized
pyrethrins plus silica gel mixture, boric acid and bendiocarb resulted
in an excellent control for at least 1 mo; however, cockroach infesta-
tion returned after 3–6 mo of treated shafts. Obviously, the effective-
ness of the insecticide formulations for 1 mo control is very little
time that this time should be increased. As in the fall populations of
the adult cockroaches being the lowest, treatments provide the best
results (Rust etal. 1991).
Application of Bait Formulations
Although there is a report using baits failed to provide consistent con-
trol of the American cockroaches due to application problems (Rust
etal. 1991) or the insect growth regulators (IGRs) are not be recom-
mended as an active materials for the control of the American cock-
roaches in sewers (Bueno-Marí et al. 2013). However, the results of
eld studies have been indicated that the baits are effective against
the cockroaches (Nasirian et al. 2006b, Nasirian 2007, 2008; Wan-
Norakah etal. 2017; Davari etal. 2018) and also the American cock-
roach species in sewers.
Neonicotinyl and abamectin baits provided rapid success effec-
tive control of P. americana and relatively inexpensive in sewers.
MaxForce FC Roach Killer (pronil 0.05%) and Pre-Empt, IMAGEL
(imidacloprid 2.15%) gel baits provide ≥96% control for 6 mo or
longer (Reierson etal. 2005).
Granular ant bait formulations (containing abamectin B1,
orthoboric acid, or propoxur) are clearly toxic to the American and
German cockroaches. The gel bait formulation of pronil 0.03%
(Goliath) when exploited at the adequate dosages on cement, mud,
thatch and wood surfaces could cause >80% mortality of P.ameri-
cana cockroaches in places possessing these types of surfaces. The
American cockroaches greatly preferred the commercially available
gel baits (0.05% pronil and 0.6% indoxacarb) for feeding over dog
food. The gel bait of indoxacarb 0.6% was highly effective against
the American and German cockroaches. Periplaneta americana cock-
roaches ingest the potassium alum affecting mortality. Laboratory
and eld studies demonstrated the high efcacy of a B. bassiana
bait formulation against the American and German cockroaches.
Although it is important to maximize the bait consumption, the fac-
tors enhancing secondary mortality and contacting toxicity should
also be considered (Koehler etal. 1991, Appel etal. 2005, Reierson
etal. 2005, Srinivasan etal. 2005, Bayer et al. 2012, Anikwe etal.
2014, Salama 2015, Wang etal. 2016).
Baits compared with spray applications possess benets being
inexpensive, ready and easy to use, widely available, having low
toxicity and negative side effects, and not needing to apply by a
technician (Davari et al. 2018). The applied insecticidal bait for-
mulations provided sustained cockroach elimination during 12 mo
and resulted in reduction of asthma morbidity (Rabito etal. 2017).
Compared with controls, a eld trial placement of boric acid gran-
ules to a courtyard eliminate cockroaches with a signicant cock-
roach antigen reduction of buildings (Carlson etal. 2017).
Toxic gel baits are one effective control method for cockroach
control. Periplaneta americana are thought to prefer toxic baits over
other food sources (Porusia etal. 2017). According to the labora-
tory experiments, the baits were accepted by cockroaches as a food
source (Varadínová etal. 2015). However, eld P.americana strains
tended to visit natural foods more often, and laboratory strains vis-
ited insecticide baits more frequently. Field and laboratory strains
of P.americana cockroaches are not fully attracted to the gel baits
when other foods are available around their harborage. Therefore,
it needs to be minimized the availability of other food sources when
applying gel baits around the cockroach harborage (Porusia etal.
2017). Areasonable manner is using a combination of IPM strate-
gies with strong vector control management such as reforming and
cleaning of the environment, spraying, and applying the bait formu-
lations recommending for effective cockroach pest control including
P.americana (Nasirian 2016, Davari etal. 2018).
To achieve an effective treatment, the gel baits must be applied as
a narrow band restricted just below the cover, not deep within. Solid
and granular baits administrating by devices or gel baits distributing
by cards lower in the manholes of sewers are not as effective. Gel
baits which were covered with fungus retrieved from sewer man-
holes months later stayed toxic indicating prolonged success efcacy
against nymphs emerging afterward. Regardless of active ingredient
degradation, revival of cockroach populations in some manholes of
sewers appearing as a result of the baits may be consumed (Reierson
etal. 2005). Therefore, there is a need for replacement of the baits.
Application of Inesfly Paint Insecticide Formulations
An Inesy paint insecticide is a contact insecticide, specically formu-
lated for effective, economic, and long-term control. Today, however,
insecticidal paints are receiving renewed interest for their potential
use against disease vectors. This interest can be attributed to several
factors, of which safety of Inesy paint insecticides, low concentra-
tion of active ingredients, organic solvent free, active ingredient grad-
ual releasing, and low application frequency, along with the concerns
that should be addressed before this intervention tool achieves wide-
spread application (Hazra 2018). When sewer cockroaches come
in contact with Inesy paint insecticide the mucus secreted by the
insect’s feet will dissolve the polymers designed to hold the insecti-
cide micro-particles on the treated surface, and the insecticide is then
absorbed into the insect’s feet killing them typically within 24 to 48h.
Among several insecticides with different formulations and
active substances including Bio-blaticida 100SC (containing dif-
lubenzuron), Diptron EC20 (containing clorpyrifos), Ecorex alfa
(containing alphacypermethrin, tetrametrin, and piperonyl butox-
ide), Empire 20 (containing clorpyrifos), Inesy 5 AIGR (contain-
ing diazinón, clorpyrifos, and pyriproxyfen), Serpa D60 (containing
diazinón), and Sumilarv 10 EC (containing pyriproxyfen) apply to
sewer shafts for controlling the American cockroaches. The paints
with and without insecticide, Inesy, provide an optimal reduction
for up to 3 mo (P<0.001) observing the best products for P.ameri-
cana cockroach populations control. Therefore, it should be noted
that the cockroach population reductions, as well as the insecticide
persistence effect, were similar in both types of paints in sewers
(Bueno-Marí etal. 2013). Paints with insecticide also provide inter-
estingly an optimal control of the American cockroach populations
for 3 mo (Bueno-Marí etal. 2013).
One single application of 50–70g Inesy paint 5 AIGR per spot
provided long-term control of Blatta orientalis cockroach popula-
tions for 9 mo at this pest infestation of Zaragoza areas in Spain
(Delacour-Estrella etal. 2014).
Application of Plant Essential Oils as Insect
Repellents
DEPA (N,N-diethylphenylacetamide) displayed residual repel-
lency for 4 wk against P. americana cockroaches at 0.5 mg/cm2
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concentration (Prakash et al. 1990). Essential oils, produced by
plants, have been exhibited to have insecticidal, attractant or repel-
lent properties. These effects are presumed to produce through their
interaction with receptors of octopamine. In insects which octopa-
mine is an important biogenic monoamine the functions are as
neurohormones, neurotransmitters and neuromodulators (Gross
etal. 2014). Briey essential oils of Alpinia calcarata (Zingiberales:
Zingiberaceae) freshly cut rhizomes which identied as camphene,
camphor, fenchyl acetate 1,8-cineole, β-pinene and α-pinene showed
repellant properties in P.americana. Essential oils of Allium sativum
(Lamiales: Lamiaceae), Brassica nigra (Brassicales: Brassicaceae)
plant and allyl isothiocayanate monoterpenoid component have
potential as fumigant insecticidal effects against the American cock-
roaches (Paranagama and Sujantha Ekanayake 2004, Yilmaz and
Tunaz 2013). To achieve practical use, these results need to be evalu-
ated by the eld studies.
Recently it has been proved that the Pogostemon cablin
(Lamiales: Lamiaceae) essential oil of leaves, Artemisia arborescens
and A. santolina (Asterales: Asteraceae), Apiaceae (Apiales) plants,
and their major components have good potential as repellents or
natural insecticide sources (Yeom etal. 2012, Liu etal. 2015, Yeom
et al. 2015) for the German cockroach control, until they will be
legally and ofcially used, take a lot of time (Nazari etal. 2016).
The German cockroaches also exhibited high values of repellency
exposing to treated lter paper with catnip plant, Nepeta cataria
(Lamiales: Lamiaceae), the individual nepetalactone isomers or
essential oil. Of the two evaluated nepetalactone isomers (Z,E- and
E,Z-nepetalactone), B. germanica were the most responsive to the
E, Z isomer (Schultz etal. 2006). These studies should also be tested
in P.americana and to achieve practical use the results need to be
evaluated by the eld studies.
Biocontrol
It is well-known that control with natural enemies is less aggressive
and can currently be exploited with less risk than other methods
such as chemical control which is the main technique used world-
wide to control post-embryonic pest stages (Baggio-Deibler et al.
2018). Chemical control also provide only temporary control, it is
recommended that it should be accompanied by other control meth-
ods (Ross and Cochran 1992).
Although there was a report that the natural enemies may be
inappropriate in the sewer environment. There was no measurable
effect on populations of cockroaches in sewer environments after
releasing of Aprostocetus hagenowii (Hymenoptera: Eulophidae)
parasitoid which was reportedly effective on the American and
smokybrown cockroaches (Periplaneta fuliginosa), but it may be
inappropriate due to lack of effectiveness in sewer environment here
(Reierson etal. 2005).
So far, natural enemies of P.americana including Evania appendi-
gaster (Hymenoptera: Evaniidae) and A.hagenowii, the parasitoids
of P. americana oothecae; Steinernema carpocapsae (Rhabditida:
Steinernematidae) entomopathogenic nematodes; and Metarhizium
anisopliae and Beauveria bassiana (Hypocreales: Clavicipitaceae)
entomopathogenic fungi have been successfully used to control
P.americana cockroaches (Hwang and Chen 2004, Reierson et al.
2005, Fox and Bressan-Nascimento 2006, Hernández-Ramírez etal.
2007, Maketon etal. 2010, Tee etal. 2011a, Hubner-Campos etal.
2013, Gutierrez etal. 2016, Tee and Lee 2017, Baggio-Deibler etal.
2018). But when the natural enemies were applied in the form of
baits or along with the baits achieved more successfully results than
natural enemies alone (Hwang and Chen 2004, Hernández-Ramírez
etal. 2007, Maketon et al. 2010). The application of E. appendi-
gaster parasitoid of the American cockroaches oothecae habitats
such as sewers accompanied with baits resulted in effective reduction
of the American cockroach populations (Hwang and Chen 2004).
The addition of 3 and 5% boric acid to the cockroach diets along
with B. bassiana produced 82.0 and 92.0% of mortality, respec-
tively which had a good acceptance by the American cockroaches
(Hernández-Ramírez et al. 2007). Releasing of A. hagenowii par-
asitoid were also more effective when releases were made at high
and middle levels of sewer manholes than at a low level which was
placed at the sewer manhole midpoint (Tee etal. 2011a).
The American cockroach oothecae parasitism is affected by host
density and days of E.appendigaster parasitoid lifetime. The greatest
reproductive efciency of E.appendigaster females happened in the
rst 14 d of their lifetime. The parasitism rates decrease with increas-
ing the host density (Fox and Bressan-Nascimento 2006). Reduced
progeny survival of E.appendigaster parasitoid due to host canni-
balism did not alter the parasitoid’s oviposition of females priority
for newly cockroach eggs (Tee and Lee 2017). Therefore, in overall
to achieve more successful results the releases of parasitoid or natu-
ral enemies need frequently to be repeated with appropriate time
intervals or it accompanied with the baits, the baits also replaced
with the appropriate time intervals.
The Challenges of Finding Environmentally Safe
Treatments
The challenges of nding environmentally safe treatments that
do not affect urban waters is a very controversial topic. Although
valuable researches and reviews about removing the pollutants and
insecticides from the urban waters have been implemented. There
are valuable treatment technologies and strategies for removal and
degradation of persistent and toxic pesticides using nanoparticles
and nanotechnology-based multifunctional and highly efcient pro-
cesses (Kumar Reddy and Lee 2012, Amin et al. 2014, Angelakis
and Snyder 2015, Rani et al. 2017). The unique characteristics of
nanomaterials such as large surface areas, size, shape, and dimen-
sions making them particularly attractive for urban water treatment
applications (Amin etal. 2014). The degradation techniques of insec-
ticides are now advanced using nanomaterials of various kinds such
as TiO2 and Fe and found to be excellent adsorbents and efcient
photocatalysts for degrading more or less whole insecticides as well
as their toxic metabolites. It is noteworthy that such methodologies
are economic, fast and very efcient (Rani etal. 2017).
While it would seem that is wiser to use the strategies that do
not lead to environmental contamination from the beginning, in
order to solve the problems that human being faced. The actions of
these kinds are eliminating of potential cockroach food, water, and
shelter sources, closing of crevices or cracks (Orkin 2018), applying
materials with minimal environmental impact and low mammalian
toxicity (Reierson etal. 2005), having low toxicity and negative side
effects including baits (Davari etal. 2018) as well as achieving more
successfully results by using natural enemies in the form of baits or
along with the baits than natural enemies alone (Hwang and Chen
2004, Hernández-Ramírez etal. 2007, Maketon etal. 2010).
Futuristic Actions
Integrating Health Into the Future Buildings
For promoting healthy environments and behaviors, and mitigat-
ing adverse health outcomes, the building designers must redesign,
renovate, and reconstruct the future buildings. A key priority in
Journal of Medical Entomology, 2019, Vol. 56, No. 1186
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designing, building, and operating of new and existing buildings also
should be based on the health and wellbeing of building occupants.
Strategies of green infrastructures, smart buildings, and larger sys-
tems should be changed serving and supporting public health goals.
To promote health at the level of individual buildings, interventions
are also in a manner of enhancing indoor environmental quality and
providing opportunities for physical activity.
To measure a building’s health impacts and navigate the various
programs with using metrics, a ‘healthy building’ is being built with
multiple co-benets relating to the energy efciency, environment,
economy, planning, society, and transportation (Heidari etal. 2017).
Future Techniques for Control of Cockroaches
Facultative parthenogenesis which may be observed in many animal
phyla is an asexual mode of reproduction that females generate off-
spring without mating with male partner (Katoh etal. 2017) and play
an important role in the evolution of insect sex, sociality, and strate-
gies of reproduction (Tanaka and Daimon 2018). Parthenogenesis is
frequently more popular than sexual reproduction in some eusocial
and subsocial insects (Katoh etal. 2017). As American cockroaches
belong to the superfamily Blattoidea diverging into eusocial termites
and showing facultative parthenogenesis, it is well-suited to address
this reproductive issue (Katoh etal. 2017). Atype of parthenogen-
esis which offspring are produced by females without fertilization
named as thelytoky are being exhibited in some cockroach species.
Astudy result demonstrates that the American cockroaches exhibit
automixis-type thelytoky in which diploidy restoring by gamete
duplication or terminal fusion (Tanaka and Daimon 2018).
Bringing together various elements of different pest management
strategies and providing a framework for their effective deployment
are tactics of push–pull strategies. In the push strategy, stimuli like
alarm pheromones, anti-aggregation pheromones, antifeedants, ovi-
position deterrents, non-host volatiles, and visual distractions are
used to mask host apparency or repel or deter the pests away from
the resource. In the pull strategy, highly apparent and attractive
stimuli like aggregation or sex pheromones, host volatiles, gustatory
or oviposition stimulants, and visual stimulants are simultaneously
used to attract the pests to other areas such as traps or trap crops
concentrating and facilitating elimination there (Cook etal. 2007).
Due to P. americana exhibits automixis-type thelytoky, use of
this P.americana advantage, push–pull strategies and an automated
sewer robot, and integrating health into the future buildings (Cook
etal. 2007, Heidari etal. 2017, Vaani etal. 2017, Tanaka and Daimon
2018), they may be new approaches of P.americana control strate-
gies in the future as futuristic actions. It is well documented that the
cockroaches are threatening human health (Nasirian 2010, Nasirian
2016, Davari et al. 2017a, Nasirian 2017a, Schapheer etal. 2018),
similar leishmaniosis, mosquitoes, myiasis, tick-borne diseases,
pediculosis, and scabies (Poudat and Nasirian 2007; Telmadarraiy
etal. 2007; Soleimani-Ahmadi etal. 2009; Nasirian etal. 2014a,b;
Shayeghi et al. 2016; Davari et al. 2017b; Martínez-Girón etal.
2017; Gholamian-Shahabad etal. 2018). Cockroach exposure is an
important asthma trigger (Rabito etal. 2017), particularly for chil-
dren with asthma living in homes of cockroach infested. Integrating
health into the future buildings and the described below future tech-
niques are the futuristic actions for control of cockroaches.
Although sanitation has been proved not to possess a direct
relationship with the domiciliary cockroach infestation levels (Lee
and Lee 2000). While cockroaches produce some allergens to be
accumulated within their tiny feces and may be persisted invisible
in the environment (Varadínová etal. 2015). Buffer environmental
conditions of urbanization allow pest insects expanding their distri-
bution. Several various pest insects, such as synanthropic cockroach
organisms, have expanded their distributions by human-modied
habitats. Suitable microhabitats for domiciliary cockroaches are gen-
erated by human settlements to help them for surviving and estab-
lishing to overall of the climatic restrictions (Schapheer etal. 2018).
In addition, the buildings of the future must redesign, renovate, and
reconstruct for promoting healthy environments and behaviors, and
mitigating adverse health outcomes (Heidari etal. 2017). They will
be designed and constructed in a way that they are cockroach-proof
or impossible to their entering and the survivals are inconceivable.
As P.americana has a unique reproduction exhibiting automixis-
type thelytoky which diploidy is remade by gamete duplication or
terminal fusion (Tanaka and Daimon 2018), in the future it may be
a new approach as a P.americana control. The new investigations in
this context through articial feeding (Nasirian and Ladonni 2006,
Nasirian etal. 2008) may be experimentally performed.
A challenge to locomote animals and engineer seeking in design-
ing agile robots is the information integration from structures of
dynamic sensory operating on a moving body. The sensor mechani-
cal tuning is critical for effective control as a tactile sensor is a physi-
cal linkage mediating mechanical interactions between environment
and body (Mongeau etal. 2014). Asewer automated robot conduct-
ing any inspection of sewer lines for cracks, corrosion obstacles, etc.
and clearing any blockage within (Vaani etal. 2017) are needed. It
is hoped that the robot will be used for control of cockroaches in
the future. The tactics of push–pull strategies are bringing together
various elements of different pest management strategies and provid-
ing a framework for their effective deployment (Cook etal. 2007).
They are the future techniques which may be used for control of the
American cockroaches in sewers.
Finally a reasonable manner is using a combination of IPM strat-
egies with strong vector control management such as reforming and
cleaning of the environment, spraying, and applying the bait formu-
lations recommending for effective cockroach pest control includ-
ing P.americana (Nasirian 2016, Rabito etal. 2017, Davari et al.
2018). Asuccessful tactic to eliminate cockroach allergen exposures
is elimination of cockroaches (Sever etal. 2007). Implementing an
IPM intervention including education of residents, intensive profes-
sional sanitation and extensive insecticidal bait applications resulted
in signicant reductions of cockroach infestation levels and allergens
(Arbes et al. 2003). Environmental and multifaceted interventions
have also demonstrated improvement in asthma health outcomes
(Arbes etal. 2003, Morgan etal. 2004, Eggleston etal. 2005, Sever
etal. 2007, Rabito etal. 2017).
Conclusion
It is well documented that the cockroaches are threatening human
health. Cockroaches have proved as potential carriers of the patho-
genic or opportunistic bacteria and fungi discovered in nosocomial
infections, food-borne poisoning and diseases mostly being drug-
resistant, human intestinal parasites and intermediate hosts, and
play a role as a major source of allergens causing asthma and other
human long-term health issues.
Periplaneta americana is the most important synanthropic inva-
sive and hygienic urban pests. This pest species is an annoyance
to human associating with diseases and allergy, and damaging to
clothes and documents. Periplaneta americana species is also the
most important pests of sewer environments colonizing there with
high signicance of human public health and source of household
allergens that need to be controlled. To control P.americana, many
Journal of Medical Entomology, 2019, Vol. 56, No. 1 187
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studies have been conducted in various elds which has been pub-
lished in separate papers or notes describing from an angle of the
topics. Each of them can be a good lever of P. americana control
measures. Putting the all levers of its control on the table pro-
vide possible using in required conditions. Therefore this practical
approach systematic review perform internationally to highlight and
provide a detailed of the control of cockroaches in sewers.
Unlike the German cockroaches which its insecticide resistance
has been well studied, a few studies have been performed in the eld
of insecticide susceptibility or resistance against the American cock-
roaches needing to be done in the future. Arecommending manner to
achieve a successful P.americana cockroach control in sewers is using
a combination of IPM strategies with strong vector control manage-
ment such as masterly resident education, intensive sanitation, environ-
mental and multifaceted interventions, extensive insecticide spraying
and bait formulations resulted in reductions of cockroach infestation
levels, allergens and asthma health outcomes. As P. americana has a
unique reproduction and exhibits automixis-type thelytoky, use of this
P.americana advantage, push–pull strategies and an automated sewer
robot, and integrating health into the future buildings, it may be a new
strategy of P.americana control in the future as futuristic actions.
Acknowledgments
This work did not receive any technical or nancial support from any institu-
tion and was done by the rst author at his own personal expense. The authors
declare that they have no conict of interest.
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