Pathogens of Medical Importance Identified in Hospital-Collected Cockroaches: A Systematic Review

1. Introduction

Cockroaches are ancient insects, with fossil evidence indicating that their lineage can be traced back to the Upper Carboniferous period. [1] Despite the passage of time, modern species have retained a high degree of morphological and physiological similarity to their ancestors. These insects possess the capacity to adapt to a diverse array of habitats, a trait that has enabled their survival in a multitude of environments. [2,3,4]

The majority of these insects inhabit tropical and subtropical regions of the globe. [4,5] Approximately 4,600 species have been identified, with over 99% classified as non-domestic. [6] Two notable examples are Blatella germanica (Linnaeus, 1767) and Periplaneta americana (Linnaeus, 1758) which are among the most common synanthropic cockroaches due to its abundance and cosmopolitan distribution. [5,7,8,9] The species in question inhabits a variety of environments that provide optimal conditions for its survival, including residential buildings, commercial premises, healthcare facilities, educational institutions, and food-handling establishments.10 These insects are omnivorous, with a preference for foods rich in starch and sugars. [3]

The World Health Organization (WHO) considers cockroaches a significant public health concern due to their role as mechanical vectors, capable of carrying potential pathogens on external and internal parts of their bodies. These pathogens include bacteria, fungi, protozoa, helminths, and viruses. [3,5,11]

The contamination of food, surfaces, and objects of human use with pathogens carried by cockroaches occurs when these insects come into contact with them and regurgitate portions of their partially digested food or deposit their feces on them. [3,12,13] Pathogens from these insects can cause diseases such as bacterial dysentery, giardiasis, amebiasis, and toxoplasmosis, as well as symptoms such as nausea, abdominal pain, vomiting, and diarrhea. [14,15] The presence of cockroaches is a common occurrence in hospitals, which raises concerns about the potential adverse implications for the health of patients and workers. [10,16,17,18]

In this regard, the World Health Organization (WHO) reports that healthcare-associated infections (HAIs) are responsible for approximately 40,000 deaths annually. It is estimated that 25% of HAIs occur in developing nations and between 5% and 15% in developed countries.[19] The predominant group of pathogens that cause these types of infections are bacteria, many of which are resistant to multiple antibiotics and have been isolated and identified from the bodies of cockroaches. [16,20,21,22,23]

The phenomenon of antibiotic resistance (AR) represents a significant global public health concern, with documented associations with elevated mortality rates, prolonged hospitalizations, diminished therapeutic options, increased economic costs, and the potential for hospital-acquired outbreaks. [24] The gravity of this issue is underscored by projections indicating that by 2050, AR is likely to account for 10 million deaths and inflict substantial financial burdens, with a disproportionate impact on low- and middle-income countries.[25]

The bacteria that most frequently cause infections in hospitalized patients include S. aureus, Streptococcus sp., Acinetobacter sp., S. coagulase negative, P. aeruginosa, E. coli, Proteus mirabilis, and K. pneumoniae. Some of these bacteria represent a global threat due to their increasing resistance to available antibiotics and their role in transmitting such resistance between bacteria of the same and different species. [26,27]

Over the past decade, there has been a notable increase in research related to the pathogens carried by cockroaches collected in various environments, including hospitals [6]. However; there has been a paucity of studies that have synthesized this information with the aim of facilitating access to it and enhancing the understanding and comprehension of personnel working in such health institutions. Accordingly, the objective of the present study was to describe the pathogens carried by cockroaches collected in hospitals in different parts of the world during the period 2000-2023 and their resistance mechanisms by means of a systematic review of the indexed literature.

2. Materials and Methods

2.1. Design

A systematic review of the literature was conducted to identify the pathogens and resistance mechanisms carried by cockroaches collected from hospitals in various parts of the world.

2.2. Methodology Used in the Search for Relevant Studies

The search strategy was conducted in accordance with the guidelines set forth in the PRISMA 2020 statement and through manual examination [28].

• The following keywords were established: cockroach, bacteria, hospital, pathogenic parasites, and antibiotic resistance. In order to optimize the retrieval of relevant information, the bibliographic citations of the articles examined were selected.
• The literature search was conducted using Google Scholar and electronic databases pertinent to the field of health, namely LILACS, the SciELO portal, and PubMed.
• The articles were identified based on their title, language, date of publication, and the time interval between January 2000 and April 2023 (the extreme years of the interval were included).
• Reports that met at least one of the exclusion criteria proposed by the authors of this study were excluded.
• The selected articles were found to meet all the inclusion criteria established by the authors of this work.

2.3. Inclusion Criteria for Studies

• Reports of isolation and identification of pathogenic organisms of medical importance from external or internal parts of cockroaches.
• Articles published in the period from January 1, 2000 to April 30, 2023. For the establishment of this period of time, we took into account what was described by Guzman et al.[6] who express that since 2000 there has been an increase in publications in Pubmed related to the topic of cockroaches and the pathogens identified from the body of these insects.
• Studies carried out with cockroaches collected in hospital environments, although the research also describes the capture of these insects in other places such as homes, hotels, markets, schools, or restaurants.
• Scientific reports from anywhere in the world that are published in the form of a thesis, scientific article or letter to the editor in English, Spanish or Portuguese.

2.4. Exclusion Criteria for Studies

• Articles in which the scientific name of the cockroach species collected is absent.
• Exclusively experimental research studies conducted in a laboratory setting on pathogens isolated from cockroaches collected in hospital settings.
• Publications that constitute review articles.

2.4. Statistical Analysis

• Microsoft Office Excel 2007 version was used to present the results in tables and figures.

3. Results

3.1. Search for Information

Figure 1 shows the flowchart of the selection process of the reports that make up the review based on the updated PRISMA guide [28]. Initially, using the established keywords, their combinations, date of publication and languages, 109 records on the subject were identified. Thirty-four articles were excluded because they were considered duplicates. In addition, 22 were eliminated because they were dissertations, conferences and book data.

The 53 reports resulting from the screening of the records were examined based on the inclusion and exclusion criteria previously established by the authors. Finally, 22 articles were selected for review. Most of the articles were published in Pubmed 65/109 (59.6%).

3.2. Distribution of Articles by Continent and Country

Table 1 shows that 95.4% of the research comprising the present review was conducted in developing nations [29]. Of these, 45.4% were published in countries on the Asian continent, while 39% and 23% were in African and American nations, respectively. Iran, Brazil and Ethiopia accounted for 59% of the studies involved in this review.

3.3. Cockroach Species Collected and Identified in the Studies Analyzed

Figure 2 shows that five cockroach species were identified in the 22 articles included in the review. [17,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50] B. germanica and P. americana were the most common, reported in 15 (68%) and 13 (59%) of the studies described, respectively. [17,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50] In seven studies (32%) more than one cockroach species was captured in the same hospital environment. [17,36,37,41,46,48,50]

B. germ: Blattella germanica; P: Periplaneta; P. amer: Periplaneta americana

3.4. Microorganisms Isolated and Identified from Cockroaches Collected in Hospitals

Table 1 shows the microorganisms isolated and identified from the bodies of cockroaches collected in hospitals. Bacteria represented the predominant group, being reported in 89% of the articles included in the review, followed by fungi and helminths with 13% and protozoa with 9%.

Bacteria of potential medical importance appearing in the greatest number of articles were: E. coli (11 articles), S. aureus (9 articles), Enterobacter aerogenes and K. pneumoniae (7 articles), P. aeruginosa and Citrobacter freundii (6 articles) and Enterobacter cloacae, Klebsiella oxytoca and Proteus vulgaris (5 articles). Enterococcus faecalis, Morganella morganii, Proteus mirabilis, Staphylococcus epidermidis, Streptococcus pneumoniae, Streptococcus pyogenes and Streptococcus agalactiae appear less frequently (Table 1).

Regarding fungi, two articles reported the identification of the species Aspergillus niger from the external part of cockroaches, while Candida glabrata, Candida krusei and Aspergillus fumigans were isolated in a different study from those analyzed in the review. The remaining members of this group were not classified at the species level but at the genus level, such as Mucor spp, Penicillium spp and Rhizopus spp (Table 1).

Helminths harmful to human health were identified: Enterobius vermicularis (eggs, larvae and adults) and Ancylostoma duodenale (larvae) in two and one of the studies analyzed, respectively. In addition, the presence of organisms belonging to the genera Ascaris (adults) and Taenia were detected (Table 1).

Regarding protozoa, the presence of Lophomonas blattarum and Entamoeba coli was identified in two and one of the studies, respectively. In other studies, organisms such as Blastocystis spp., Cyclospora spp., and Cystoisospora spp. were reported (Table 1).

Isolation and identification of medically important microorganisms from the external and internal parts of cockroaches was reported in 12 (55%) of the 22 articles reviewed. In all studies, pathogens were detected in both body parts of these vectors. [17,32,33,34,39,40,42,43,44,45,47,50]

One article (4.5%) reported the identification of viruses (rotavirus) carried by cockroaches on the external and internal parts of their bodies. [40]

3.5. Antibiotic Resistance and Mechanisms of Resistance in Bacteria Identified in Cockroaches

Antibiotic resistance in bacteria isolated and identified from cockroaches collected in hospitals was addressed in 64% (14/22) of the studies included in this review (Table 1).

Figure 3 shows that gram-negative bacteria were identified in the highest percentage of the articles analyzed where AR is reported. In this regard, E. coli stands out with 8 studies (57%), followed by K. pneumoniae and P. aeruginosa, which are described in 4 (29%) and E. cloacae in 3 (21%). In the case of gram-positive bacteria, S. aureus appears in 5 studies (36%).

AR in bacteria was frequently observed in antibiotic groups such as penicillins, cephalosporins, aminoglycosides, amphenicols, tetracyclines and quinolones. [17,30,31,32,33,39,40,45,46]

Regarding antibiotic resistance mechanisms, the BlaZ gene coding for beta-lactamase enzymes and the production of extended-spectrum beta-lactamases were detected in one and two studies, respectively. [17,45,50] These enzymes are responsible for the resistance mechanism characterized by inactivation of the antibiotic. [51] On the other hand, the presence of genes coding for Penicillin-binding proteins involved in the resistance mechanism called target site modification [51], appears in one investigation. [48] Two articles reported the presence of tet (K) and tet (L) genes encoding proteins involved in the mechanism of antibiotic efflux through the energy-dependent pump. In addition, these studies were able to identify the tet (M) and tet (O) genes involved in the mechanism of target site alteration that protects the ribosome from the action of the antibiotic.[17,48,52] Finally, the mechanism of resistance (target site modification) to colistin mediated by the mcr-1 gene was detected in E. coli isolates. [50,53]

3.6. Methods Used in the Identification of Microorganisms Identified in Cockroaches

Table 1 shows that in 17 of the 18 studies (94%) bacteria were identified by seeding in culture media (general and differential), Gram staining (GS) and Conventional Biochemical Tests (CBT). In addition, five of the 17 articles referred above (29.4%) used other techniques such as Analytical Profile Index (API), Serological Tests and PCR. In one of the 18 investigations, only the culture media seeding method and MALDI-TOF technology were used.

For the identification of fungi, methods based on seeding in culture media and examination of macroscopic and microscopic characteristics of the growths were used. Protozoa and helminths were classified using direct parasitologic methods, and rotaviruses were identified using ELISA technology (Table 1).

3.7. Methods Used to Detect Antibiotic Resistance and its Mechanisms in Bacteria Identified in Cockroaches

As shown in Table 1, the predominant method used to detect antimicrobial resistance was the use of disk diffusion (Kirby Bauer). This method was used in 12 of the 14 studies in which AR was investigated. On the other hand, PCR was used in three of the 12 articles (25%) and the Etest method in one of the 14 studies (7.1%). It is worth noting that one of the studies reviewed did not report the method used to detect AR (Table 1).

The detection of genes and enzymes that indicate the antibiotic resistance mechanism present in the bacteria analyzed was performed in five of the 22 studies (22.7%). [17,37,45,48,50] The PCR technique was used in three of them, [17,37,48] in one the Double Disc Synergy Test (DDST) [45] and in another article RT-PCR and DDST. [50]

4. Discussion

A systematic review of pathogens of medical importance isolated from cockroaches collected in hospitals in different parts of the world over a 24-year period was performed. A literature search strategy similar to that used by other authors in reviews of isolated fly, cockroach, and beetle pathogens was established for the selection of studies. [54,55,56] This allowed a thorough process of identification, screening, and selection of articles based on the inclusion and exclusion criteria proposed by these authors.

Ninety-five percent of the studies in the review come from developing countries [29] in the Americas, Africa, and Asia. [17,30,31,32,33,34,35,36,38,39,40,41,42,43,44,45,46,47,48,49,50]. Similar findings have been reported by different authors in their respective review articles. [55,56,57] In the countries where these studies were conducted, there are socioeconomic factors that negatively affect the health conditions found in second and third level hospital facilities. [17,30,38,39,40,58] The presence of cockroaches in hospitals, parasites in their integument and gastrointestinal tract is an indicator of poor sanitation in health facilities. [1,44] On the other hand, there are reports of cockroaches collected in hospitals in Japan, France, and Poland [37,59,60] showing that this phenomenon is independent of the geographical location and economic situation of nations, which becomes an epidemiological alert for developed countries.

B. germanica and P. americana were the predominant cockroach species in the studies included in this review. [17,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50] Both are recognized as the most abundant of this group of insects worldwide. [7,8,9] Trade and the ability of both species to adapt to a wide range of conditions have played a key role in their distribution. [1,2,3,4,5,11,61] Blatta orientalis, Periplaneta fuliginosa, and Periplaneta japonica are other species considered to be of medical importance with limited worldwide distribution reported in the articles reviewed. [1,2,36,37,48,50]

In seven of the 22 articles analyzed (32%), several species of cockroaches coexisting in the same hospital facility and carrying pathogens of medical importance were captured. [17,36,37,41,46,48,50] This fact could increase the likelihood of the spread and mechanical transmission of these organisms in the hospital environment. The high infestation of P. americana in the drainage system of hospitals, as well as its size, 3 to 4 times larger than B. germanica, could facilitate this phenomenon. [17] On the other hand, Karimi et al. [36] collected 305 cockroaches in three hospitals in Iran belonging to the species P. americana (65.6%), B. germanica (12.1%) and Blatta. orientalis (22.3%). The first and second mentioned species were caught in corridors, laundry rooms, basements, food stores, and facilities. However, the third species predominates in places where the temperature is colder in relation to the collection sites of the other two species. The difference in habitat is another aspect that favors the spread of pathogens by cockroaches.

Cockroaches host and carry a variety of pathogens on the external and internal parts of their bodies, such as bacteria, infective forms of helminths, fungi, protozoa, and rotavirus, as reported by several authors. [55,57] The nocturnal habits of these vectors, their reproductive capacity, the ease with which they enter synanthropic places (homes, restaurants, hospitals, etc.), the ingestion of a wide variety of foods, including waste, and their free movement over a wide range of surfaces such as floors, tables, pipes, ceilings, cracks, and corridors condition the contact with ubiquitous microorganisms. [1,11,23,58] In addition, many pathogens can persist for months on dry inanimate surfaces, depending on the optimal conditions of temperature, humidity and amount of inoculum, which facilitates the contact of cockroaches with them and consequently favors their mechanical vector capacity. [1,3,11,37,44,61,62] In this sense, different authors in their research do not find statistically significant differences between the distribution of potentially pathogenic bacteria identified on the outside and inside of the body of cockroaches captured in hospitals. [17,33,39,40,43]

In fact, bacteria were the most frequently identified group in the studies included in the review. Several authors acknowledge the predominance of these microorganisms among the pathogens isolated from cockroaches. [1,5,11] This finding is not surprising given the high prevalence of these infectious agents in healthcare-associated infections. [19,20] However, Elgderi et al. [32] captured specimens of P. americana from hospitals and homes in Tripoli, Libya, show no evidence that insects from hospitals are more likely to carry bacteria than those from homes. This suggests that the presence of these pathogens in these insects is primarily related to the sanitary conditions of the environments they inhabit.

Bacteria commonly identified in the review articles were: E. coli, S. aureus, E. aerogenes, K. pneumoniae, P. aeruginosa, C. freundii, E. cloacae, K. oxytoca, and P. vulgaris, all of which are known to cause human infections, particularly in the hospital setting. [63,64,65,66,67] K. pneumoniae and S. aureus cause nosocomial pneumonia; P. aeruginosa causes surgical wound and burn infections; E. coli causes urinary tract infections; and both E. aerogenes and E. cloacae are opportunistic microorganisms that commonly cause infections in patients admitted to health care facilities. [54,63] These pathogens have been isolated from cockroaches collected from various parts of the hospital, such as the operating room, intensive care unit, and neonatal unit. [30,31,39]

Several review articles suggest that cockroaches may play an important role in hospital-acquired parasitosis. Carzola et al. [44] identified enteroparasites of medical importance in P. americana cockroaches captured in Venezuela. Among the parasites identified were E. vermicularis and trophozoites of the protozoan Lophomona blattarum isolated from patients with pulmonary disease in Iran, China, Spain, India, and Peru. [49,68]

The studies analyzed in this research show the presence of fungi of medical importance carried by cockroaches collected in hospitals. Mycoses in hospital environments are common over the world, mainly caused by Aspergillus spp. and Candida spp. [57] In the same line, Motevali et al. [41] demonstrated the presence of different species of fungi A. flavus, A. niger, A. fumigatus, C. albicans and C. glabrata in B. germanica and P. americana collected from three hospitals in Iran.

Viruses (rotaviruses) were identified in only one study in this review. This finding is the first report of identification of these infectious agents in cockroaches collected from hospitals in Ghana. [40] Rotavirus causes severe and fatal diarrhea in young patients worldwide and accounts for half of all hospitalizations for this condition in children under 5 years of age in developed countries. It is also responsible for approximately 25% of all hospital-acquired viral infections, particularly in immunocompromised children. [57] However, the scarce detection of viruses in the articles included in this review may be due to the fact that the identification of pathogens in cockroaches tends to focus on bacteria, helminths, fungi and protozoa due to the availability of resources and ease of diagnosis. [1,11,40,58]

AR in bacteria is responsible for 70,000 patient deaths annually. [25] This phenomenon is reported in 14 articles in the current study, and mainly in bacteria of the ESKAPE group (Enterobacter spp., E. coli, K. pneumoniae, S. aureus and P. aeruginosa). [69] Moreover, other bacteria that are potentially harmful to humans have also been described: H. alvei, P. vulgaris, S. marcescens, S. pneumoniae, S. agalactiae, and S. pyogenes. These factors combine to create a global health risk associated with AR.

Bacterial resistance in cockroach species to a wide range of antibiotics such as penicillin, tetracycline, gentamicin, ceftaroline, aztreonam, chloramphenicol, cefepime, ceftazidime, erythromycin, ampicillin, and amickacin is highlighted. [17,30,31,32,33,38,39,44,45] Prado et al. [30] isolated 15 species of enterobacteria from P. americana captured in a public hospital in Brazil. Antibiotic susceptibility testing revealed resistance to most of the antimicrobials tested in the study. Abdolmalekiet et al. [17] provided the first report of phenotypic and genotypic evaluation of antibiotic resistance in Methicillin-Resistant Staphylococcus aureus (MRSA) isolates from external and internal parts of P. americana and B. germanica collected in hospitals. The isolates also showed a high prevalence of resistance to the antibiotic penicillin, ceftaroline, tetracycline, gentamicin and trimethoprim-sulfamethoxazole. In the neonatal ward of a hospital in the capital of Ethiopia, 400 cockroaches of the species B. germanica were collected. Of these, K. pneumoniae, K. oxytoca, Providencia rettgeri, C. diversus, Citrobacter spp., E. cloacae, P. aeruginosa, E. coli, E. aeroginosa, S. aureus, and Acinetobacter spp. were identified, and multidrug resistance was observed in all of them. [45] The above indicates that cockroaches may be involved in the spread of AR among bacteria. [70]

A bacterial strain may develop multiple mechanisms of resistance to one or more antibiotics, and an antibiotic may be inactivated by different mechanisms in different bacterial species. Therefore, knowledge of these mechanisms is necessary as a fundamental step for the effective treatment of diseases with antimicrobial drugs. [69] In this review, the detection of AR mechanisms in bacteria was found in five of the 18 studies dealing with antibiotic resistance [17,37,45,48,50].

In Nigeria, using phenotypic methods, they found a mechanism of inactivation of beta-lactam drugs by the expression of extended-spectrum beta-lactamases (ESBL). [45] Chehelgerdi et al. [48] described for the first time antibiotic resistance in Iran by phenotypic and genotypic pathways in Streptococcus spp. isolated from cockroaches collected from hospital environments. These authors identified genes involved in the mechanisms of resistance to penicillins (pbp), tetracyclines (tet K, tet M, tet O, and tet L ), macrolides (erm and mef), and streptogramins A and B (rplV) using PCR technique. In Tunisia, the production of BLEE (blaCTX-M1) and the presence of mcr-1 genes responsible for the colistin resistance mechanism in the E. coli ST648 lineage were described for the first time. [50]

In terms of the methods used to identify microorganisms and determine antibiotic susceptibility profiles in bacteria, conventional technologies such as seeding in culture media, Gram staining, conventional biochemical tests, and direct parasitological methods predominated. A possible explanation for this phenomenon is that these are the techniques used in developing countries, which were the basic scenarios in which the research was carried out. On the other hand, advanced technologies that provide better diagnostic quality and faster results (API [32,37,42], PCR [17,48,50] and MALDI-TOF [50]) were not available to most of the laboratories in the studies analyzed in this review. This fact affects the quality of the results, since in many cases the microorganism can only be identified at the genus level, which prevents us from knowing whether they are of medical importance. In addition, there are probably other pathogens that cannot be identified due to technological limitations.

On the other hand, in the detection of enzymes and genes that indicate the presence of antibiotic resistance mechanisms, it was observed that four articles included in this review employ the PCR technique, three of which correspond to developing countries [17,48,50] carried out in the period 2017-2021. However, in Japan, this technology was used for the same purpose in 2009. [37] It is undeniable that these studies allow the identification of new pharmacological targets and the design of specific antibiotics to provide more precise treatments to combat infections caused by bacteria. [71]

The current research has the following limitation: in many studies, the nomenclature of the identified microorganisms was described down to the genus, which did not allow us to know the species and, consequently, its medical importance. For this reason, the analysis of the results emphasizes pathogens identified down to the species level.

5. Conclusions

Cockroaches in hospitals all over the world might carry potentially pathogenic organisms, which are recognized as etiological agents of human diseases belonging to the groups of bacteria, fungi, helminths, and protozoa. This reinforced the notion that the presence of these insects in healthcare facilities represents a potential risk due to their involvement in healthcare associated infections and as reservoirs of multidrug-resistant bacteria. Given the scarcity of publications on the subject addressed in this review, it is necessary to increase and deepen the study of pathogens of medical importance in cockroaches, a topic of importance for global health. .