First Report of Lophomonas spp. in German ( Germanica) Trapped in Hospitals, Northern Iran

Seyyed Farzad Motevalli-Haghi Mazandaran University of Medical Sciences Atyeh Shemshadian Mazandaran University of Medical Sciences Maryam Nakhaei Mazandaran University of Medical Sciences Roghiyeh Faridnia Mazandaran University of Medical Sciences Omid Dehghan Mazandaran University of Medical Sciences Majid Malekzadeh Shafaroudi MazUMS: Mazandaran University of Medical Sciences Mehrasa Nejadi Kelarijani Mazandaran University of Medical Sciences Seyed Hassan Nikookar Mazandaran University of Medical Sciences Hamed Kalani Mazandaran University of Medical Sciences Mahdi Fakhar (  [email protected] ) Mazandaran University of Medical Sciences https://orcid.org/0000-0002-4690-6938

Research Article

Keywords: Cockroaches, Blattella germanica, Parasitic agents, Lophomonas sp., Hospital

Posted Date: March 3rd, 2021

DOI: https://doi.org/10.21203/rs.3.rs-262720/v1

License:   This work is licensed under a Creative Commons Attribution 4.0 International License. Read Full License

Page 1/14 Version of Record: A version of this preprint was published at Journal of Parasitic Diseases on April 5th, 2021. See the published version at https://doi.org/10.1007/s12639-021-01381-2.

Page 2/14 Abstract

Cockroaches are considered to be important reservoirs for protozoan and helminth parasites ,particularly an emerging Lophomonas spp., protozoan parasite. German cockroaches, Blattella germanica (B. germanica), are domestic pest distributed worldwide. However, little information is available regarding the burden of Lophomonas spp. infestation among domestic population worldwide. The present study investigated parasitic agents, emphasizing Lophomonas spp. infestation among B. germanica in northern Iran. During spring and summer 2018, a total of 496 adults B. germanica (265 males and 231 females) were trapped by hand and glass traps from the teaching hospitals in Mazandaran, Sari, northern Iran. All cockroaches were identifed using taxonomic keys. Each cockroaches was anesthetized with chloroform and the alimentary tract removed. Each section was smeared onto a glass slide. All the smears were examined under light microscopy to determine the presence of the parasites. Ten genera of parasites were identifed from the trapped B. germanica; overall, 233 (47%) were found to be positive for helminths (n=135) and protozoa (n=98). The helminths included Aspiculuris tetraptera egg (67/233, 28.7%), Oxiuros sp. (39/233; 16.7%), Dentostomella translucida (17/233; 7.3%), and nematodes Ova (12/233; 5.2%). The protozoan parasites identifed Gregarina sp. (61/233; 26.2%), Entamoeba sp. (19/233; 8.2%), Blastocystis sp. (5/233; 2.1%), Lophomonas (4/233; 1.7%), Nyctotherus sp. (4/233; 1.7%), unclassifed fagella (5/233; 2.1%). Lophomonas spp. was detected within the gut of B. germanica, for the frst time, in Iran. It has previously been identifed in the gut of cockroaches a long time ago, however, this is the frst attempt to detect Lophomonas in cockroaches housing in hospitals. Thereby, it possibly presenting pose a serious respiratory infection risk for patients and health care personnel.

Introduction

There are almost 4,500 species of cockroaches worldwide, 50 species of which have been recognized as domestic pests, but only a few of these species inhabit human dwellings such as (Blattella germanica), ( americana), Oriental cockroach ( orientalis), and Brown-banded cockroach ( longipalpa) (Gullan and Cranston 2005; Hamu et al. 2014; Kumie et al. 2002; Salehzadeh et al. 2007). Blattella germanica (: ) as a common domestic pest has been reported from all parts of Iran (Salehzadeh et al. 2007). Nocturnal German Cockroaches are light brown and relatively small (10–15 mm long) and have a shorter life span than other species. Differences in morphological characteristics of (left mandible, right tegmen, hind-wings, and cerci) have differentiated them from other similar species. (Lawless 1999; Martínez-Girón et al. 2017). Cockroaches act as a vector to transmit and harbor various pathogenic agents including bacteria, viruses, fungi, protozoa, and helminths (Al-bayati et al. 2011; Bala and Sule 2012; Chamavit et al. 2011; El-Sherbini 2011; Kinfu and Erko 2008; Pai et al. 2003). Cockroaches are known as intermediate hosts of several helminths. So far, numerous pathogen parasites such as Ascaris lumbricoides, Enterobius vermicularis, Hookworms, Strongyloides stercoralis, Hymenolepis nana, Taenia/Echinococcus sp., Trichuris trichiuraEntamoeba histolytica/ dispar, Entamoeba coli, Cryptosporidium sp. and Blastocystis spp. have been isolated from cockroaches, which are transported in mechanical method (Adenusi et al. 2018; Kinfu

Page 3/14 and Erko 2008). In addition, these are a cause of allergies and asthma (Jeong et al. 2015; Rabito et al. 2017). So far, Lophomonas spp., have been found in the sputum of patients with asthma (Martínez- Girón et al. 2007; Mirzazadeh et al. 2017). The Lophomonas spp. is a multi-fagellated parasite, infecting the lung of patients through inhaling of the dust. This parasite inhabits the hindgut of and cockroaches as an endocommensal (Alam-Eldin and Abdulaziz 2015; Strand and Brooks 1977; Wang et al. 2006).

Hospital usually provides suitable temperature, food, and water for cockroaches which are able to get nourishment from vomit, spit, phlegm, excrement, human entrails, and other diverse food sources. These cockroaches can often move between hospital wards, operating theatres, patients’ rooms, and food preparation and storage areas, frequently via gaps in walls such as pipe chases (Haghi et al. 2014; Oğuz et al. 2017). Different organophosphate, organocarbonate, and pyrethroid insecticides are used to control these species in hospitals. However, they have been developing resistance to these compounds (Arif et al. 2017).

There are several studies on Lophomonas spp. infection among the human population in Iran (Berenji et al. 2016; Ghafarian et al. 2018; Fakhar et al. 2019;). However, there is not any document about the prevalence of Lophomonas spp., in German cockroaches in Iran. Overall, limited information is available regarding the burden of Lophomonas spp. infestation among domestic cockroach population worldwide (Keighobadi et al. 2020). The aim of the present study therefore was to investigate parasitic agents with emphasizing to Lophomonas infestation among cockroaches from the teaching hospitals in Sari, Mazandaran Province, northern Iran. The fndings of the present study will shed light on the potential role of cockroaches in the mechanical transmission of intestinal parasites and help to design more efcient control intervention strategy to control of synanthropic German cockroaches.

Materials And Methods

Study design and trapping of cockroaches

This cross-sectional study was conducted between the spring and summer months of 2018 in 4 hospitals including Imam Khomeini, Bu Ali, Fatemeh Zahra, and Zareh under the supervision of the Mazandaran University of Medical Sciences (MAZUMS), Sari, Mazandaran province, northern Iran.

German cockroaches were caught using hand and glass traps from different parts of the hospitals, including laboratory, kitchen, infectious diseases ward, general surgery, and patients’ room, according to the previous studies (Smith and Appel 2008; Wang and Bennett 2006). Glass traps had a glass or plastic jar with 20 cm height and 15 cm in diameter constricted with funnel paper. To prevent cockroaches from escaping, the upper interior parts of the jars were lubricated with parafn oil. Malt juice and bread were placed inside the jars as a bait to attract the cockroaches. To lead cockroaches into the trap, two methods were used: 1) digging the ground and putting the glass trap in it at the same level with the ground. This method was not feasible due to stone or ceramic foors of hospitals; and 2) paper strips were put between the upper edge of the jar and the ground surfaces (Cochran and World Health 1999). Page 4/14 Transporting of cockroaches to the laboratory

Using sterile gloves, all cockroaches were taken into sterile glass or plastic containers and transferred to the laboratory. To prevent the spread of contamination, each container was used only for one cockroach. Having been taken to the laboratory, each of the cockroaches was anesthetized by the solution of chloroform, observed by stereomicroscope, and then identifed using taxonomic keys (Harwood and James 1979).

Microscopic examination

Afterwards, cockroach bodies were washed completely and separately using 1 mL of sterile isotonic saline and their intestinal tract were removed using dissection. The dissection was performed using special scissors under a stereo microscope. The complete alimentary canal was removed and the foregut, midgut, and hindgut were cut longitudinally to expose the internal surface. Each internal surface was then smeared onto a glass slide. A drop of normal saline was added and each wet smear was examined under a light microscope with 100x & 400x magnifcation to examine the existence of protozoa and helminths. In the case of Lophomonas spp. or other protozoa, the smears were stained by Giemsa staining method to confrm the correct identifcation. To identify adult helminth isolated from the intestine of the German cockroaches, they were fxed in AFA (mixture of alcohol, formalin, and acetic acid) solution processed in lacto-phenol (Chinchilla et al. 1994) and were studied as permanent mounts.

Results

Frequency and contamination rate of the cockroaches

A total of 496 German cockroaches (265 males and 231 females) were trapped from different parts of the hospitals and examined in terms of intestinal parasites. Furthermore, among places which the cockroaches had been collected, the most contaminated cockroaches were belonged to kitchen (67/125; 53.6%) followed by restaurant (53/104; 50.1%) (Table 1).

Parasites species characterization

Overall, 233 (47(% cockroaches were found to be positive at least for one parasite including helminths (135/233; 57.9%) and protozoa (98/233; 42.1%). The morphological characteristics were assessed in both wet and stained smears to identify helminths and protozoa. In general, 10 genera of parasites were isolated from the cockroach specimens, including 4 genera of helminths including Aspiculuris tetraptera (67/233, 28.7%), Oxiuros sp. (39/233; 16.7%), Dentostomella translucida (17/233;7.3%), and nematodes Ova (12/233;5.2%), and 6 genera of protozoa including Gregarina sp. (61/233; 26.2%), Entamoeba sp. (19/233; 8.2%), Blastocystis sp. (5/233;2.1% ), Lophomonas (4/233;1.7%), Nyctotherus sp. ( 4/233;1.7%), unclassifed fagella (5/233;2.1%) . Parasitic agents identifed in the gut of the cockroaches (Figure 1) have been presented in Table 2 and 3. Additionally, the 40 cockroaches (17.2%) were found to be positive

Page 5/14 for both protozoa and helminths. Some parasites found in the gut of German cockroaches have been presented in Figure 2.

Discussion

Our results showed about half (47%) of German cockroaches (Blattella germanica) were contaminated with at least one parasite. Therefore, these cockroaches have a potential role in the mechanical transmission of several helminths and parasitic protozoa to humans. However, some of them are non- pathogen for humans (El-Sherbini and Gneidy 2012; Perfetti 2015). In the present study, the most common protozoan and helminth were Gregarina (26.2%) and Aspiculuris tetraptera (28.7 %), respectively, that are non-pathogen for humans. Moreover, cockroaches would have been contaminated during their nocturnal movements from one ward to another and to other areas including toilets, general surgery, dining room (self-service), and patient rooms (Cochran and World Health 1999). Several researches have proposed that cockroaches act as carriers of important pathogens for human, including Entamoeba histolytica (Kinfu and Erko 2008; Pai et al. 2003), Toxoplasma gondii (Chinchilla et al. 1994), Cryptosporidium parvum and Balantidium coli (El-Sherbini and Gneidy 2012). Due to the diversity of cockroaches-borne pathogenic parasites, there are different clinical disorders in humans that may even cause death (Adenusi et al. 2018; Kinfu and Erko 2008).

The results of the present study showed that the German cockroach had high distribution in the different parts of the examined hospitals that was consistent with the previous study (Haghi et al. 2014). The largest numbers of cockroaches collected from Imam Khomeini and Bu Ali Hospitals, Mazandaran Province, northern Iran, were found in the restaurant and kitchen as compared to other places (Table 1). In this study, 47% of cockroaches were contaminated with parasites. In a study on the cockroaches collected from Samutprakarn Province, Thailand, (Chamavit et al. 2011) showed that 54.1% of cockroaches were contaminated with different parasites and play an important role in their prevalence. The contamination of cockroaches with parasitic agents was identifed 75.6% in southwestern Ethiopia (Hamu et al. 2014), 47.82% in Turkey (Oğuz et al. 2017). The prevalence of 8% and 12.24% were reported in American cockroaches respectively by (Rina S 2015). Overall, researchers in a review study showed that the global contamination of cockroaches ranges from 49 to 55%. Moreover, the global contamination of German cockroaches was between 40 and 70% (Nasirian 2017).

Several species can be found in the gut of German cockroaches, most important of which are Nyctotherus sp., Gregarina spp., Entamoeba spp., Cryptosporidium spp., Lophomonas spp., and Balantidium coli (van Woerden et al. 2020). In the present study, the protozoa prevalence in the gut of German cockroaches was 35.9% as compared to that of 56.1% in Thailand (Chamavit et al. 2011), 96% in Turkey (Oğuz et al. 2017), and 27.4% in southwestern Ethiopia (Hamu et al. 2014). Our results showed that the contamination of cockroaches with helminths in northern Iran was higher than that reported in other countries (Chamavit et al. 2011; Hamu et al. 2014; Oğuz et al. 2017). In Martínez-Girón and colleagues (2017) study, some protozoa was found in German cockroach digestive tract, of them the highest prevalence rate was related to Nysctotherus spp. (91.8%) and followed by Gregarina spp. (64.5%).

Page 6/14 Moreover, the lowest prevalence rate was related to Lophomonas spp. (13.6%). Moreover , the results of a recent study on the faecal pellets of the German cockroaches in Spain, showed 6.8 % of these to be infected with Lophomonas cyst (van Woerden et al. 2020) which is relatively consistent with the present study. Among other protozoan that were found in the study, the highest prevalence rate was belonged to Nysctotherus spp. (34.4%) followed by Gregarina spp. (18%). Lophomonas is a commensal parasite of cockroaches gastrointestinal tract that contaminates the environment, food and clothes by ejecting cysts. Following inhalation of cysts, it causes respiratory infection in humans (Xue et al. 2014). The main clinical symptoms of this new emerging protozoan in the respiratory tract include fever, cough, weakness, weight loss, and hemoptysis. Individuals at risk of lophomoniasis infection are often immunocompromised and transplant recipients (Talebian et al. 2018; Xue et al. 2014).

According to the evidence available at the Iranian National Registry Center for Lophomoniasis (INRCL) in Mazandaran Province, the prevalence of Lophomonas infection among patients suffering from respiratory disorders who referred to this center from Mazandaran, the place of the present study, is about 14% (unpublished data). This could confrm that at least one of the sources of infection in this area is contact with /close to German cockroaches infected with this protozoan parasite and can be considered as a potential hazard and even possibly as nosocomial infection for patients admitted to these hospitals. Therefore, the fght against these carriers will be more important than ever. The usage of traps is the best way to control the population of German cockroach in the environment, including hospitals. Convenient use, cheapness, non-toxicity are the advantages of these traps. The application of these traps reduces the use of insecticides (Mahmoud 2013).

In a study on gut of Bllatella germanica in Turkey other parasitic agents, including Blastocystis sp., Entamoeba spp., and nematodes ova were found (Oğuz et al. 2017). Previous studies reported low contamination of cockroaches with helminths compared to protozoa ,where the prevalence rate was 0.8% for Strongyloidesstercoralis and 0.3% Ascaris lumbricoides (Chamavit et al. 2011; Salehzadeh et al. 2007). In this study, Aspiculuris tetraptera (23.1%) and Dentostomella translucida (6.2%) had the highest frequency among the helminths isolated from the gut of German cockroach. Overall, these domestic pests can harbor many pathogenic and nonpathogenic agents and therefore should be eliminated from important places such as hospitals to avoid the distribution of some parasites to human, particularly Lophomonas spp. as pathogenic protozoan parasite. As a whole, control of cockroaches will substantially minimize the spread of parasites caused by helminths and protozoa in hospitals environment.

Conclusion

Cockroaches act an important carrier for pathogenic and non-pathogenic agents. The presence of cockroaches in hospitals poses a serious risk for patients and health care personnel. However, the transmission of pathogens to humans has not been confrmed. Therefore, further studies are needed to assess the role of cockroaches in the transmission of protozoa and helminths to humans. Lophomonas spp. was detected in the gut of German cockroaches for the frst time in Iran. Consequently, this poses a

Page 7/14 respiratory infection risk for patients and health care personnel. The serious control of the cockroach’s population may dramatically reduce the burden of parasitic infections to humans in hospital environments. These fndings will increase the awareness and knowledge of health systems and encourage them to seriously eliminate cockroaches and other insects from hospitals.

Declarations

Acknowledgements

We are grateful to the Vice Chancellor of Research of the MAZUMS for providing fnancial support of the present study (Grant no: 3259). Also, the authors thank all colleagues for their kind contribution in the Iranian National Registry Center for Lophomoniasis (INRCL), and Toxoplasmosis Research Centre at MAZUMS.

Author’s contribution

MF, SFM and MN designed all steps of the project. MN, SFM, MMS, HK and RF writing the original draft. ASH, OD, SHN, and MNK trapped of the cockroaches, isolated and examined the parasites. All authors read, revised, and approved the fnal manuscript.

Compliance with ethical standards

Confict of interest

None declared.

Ethical approval

This study was reviewed and approved by the Ethics Committee of the Mazandaran University of Medical Sciences (Code: IR.MAZUMS.REC.1398.537). This research was conducted humanely, in line with the “Guidelines for Ethical Treatment of in Applied Behaviour and Welfare Research” that have been developed by the International Society for Applied Ethology.

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Tables

Table 1. Frequency and contamination rate of German cockroaches (Blattella germanica) according to different parts of the hospitals in Mazandaran Province, northern Iran

No. of positive (%) No. of examined Place

67 (53.6) 125 Kitchen

53 (50.1) 104 Restaurant

98 (49.7) 197 Powerhouse

8 (20.51) 39 Hospital wards

7 (22.6) 31 Rest room

233 (47) 496 Total

Page 11/14 Table 2. Helminths isolated from the gut of German cockroaches (Blattella germanica) captured in the hospitals in Mazandaran Province, northern Iran

Helminths No. of positive Percentage

Aspiculuris tetraptera Adult 4 1.7%

Egg 63 27%

Oxiuros sp. Adult 13 5.6%

Larva 7 3%

Ova 19 8.1%

Dentostomella translucida 17 7.3%

Nematodes Ova 12 5.2%

Total 135 57.9%

Table 3. Protozoa isolated from the gut of German cockroaches (Blattella germanica) captured in the hospitals in Mazandaran Province, northern Iran

Percentage No. of positive Protozoa

26.2% 61 Gregarina sp.

5.6% 13 Cyst Entamoeba sp.

2.6% 6 Trophozoite

2.1% 5 Blastocystis sp.

1.7% 4 Lophomonas sp.

1.7% 4 Nyctotherus sp.

2.1% 5 Unclassifed fagella

42.1% 98 Total

Figures

Page 12/14 Figure 1

Alimentary canal of a German cockroach (Blattella germanica)

Page 13/14 Figure 2

Some parasites observed in the wet smear prepared from the gut of German cockroaches. A: Aspiculuris tetraptera Egg; B: The adult stage of Aspiculuris tetraptera; C: Lophomonas spp. trophozoites; D: Gregarina sp.; E: Dentostomella translucida. Images A, C, D, and E under ×400 magnifcation and image B under ×40 magnifcation.

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