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SYMPOSIUM
Year : 2020  |  Volume : 10  |  Issue : 1  |  Page : 7-11  

Lophomonas blattarum: A new flagellate causing respiratory tract infections


1 Department of Microbiology, Sri Venkateswara Institute of Medical Sciences and Sri Padmavathi Medical College (Women), Tirupati, Andhra Pradesh, India
2 Vice-Chancellor, Sri Balaji Vidyapeeth, Puducherry, India

Date of Submission06-Dec-2019
Date of Acceptance31-Jan-2020
Date of Web Publication20-May-2020

Correspondence Address:
Abhijit Chaudhury
Department of Microbiology, Sri Venkateswara Institute of Medical Sciences and Sri Padmavathi Medical College (Women), Tirupati - 517 507, Andhra Pradesh
India
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DOI: 10.4103/tp.TP_81_19

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   Abstract 


Lophomonas blattarum is a flagellate protozoan parasite which was originally described as a commensal in the gut of cockroaches. From the 1990s, reports started coming out of peoples Republic of China about its possible role in bronchopulmonary infections, and this was followed by reports from some other parts of the world as well. There had been some skepticism regarding the misidentification of bronchial ciliated epithelial cells as L. blattarum, but recent use of molecular diagnosis has come as an aid in clearing the controversy. This review focuses on the various aspects of the parasite including its biology, epidemiology, clinical manifestations, laboratory diagnosis, and the treatment aspects. Molecular diagnosis has recently been employed and more reports concerning its validation is needed. More basic research concerning the genomic and proteomic analysis is necessary to develop reliable molecular and serological tests for this parasite in future.

Keywords: Bronchopulmonary infections, epidemiology, laboratory diagnosis, Lophomonas blattarum, treatment


How to cite this article:
Chaudhury A, Parija SC. Lophomonas blattarum: A new flagellate causing respiratory tract infections. Trop Parasitol 2020;10:7-11

How to cite this URL:
Chaudhury A, Parija SC. Lophomonas blattarum: A new flagellate causing respiratory tract infections. Trop Parasitol [serial online] 2020 [cited 2020 Oct 31];10:7-11. Available from: https://www.tropicalparasitology.org/text.asp?2020/10/1/7/284618




   Introduction Top


Protozoan and helminthic infestation of the lung and respiratory tract can be seen worldwide, both in the immune-compromised as well as immune-competent individuals. A number of factors such as global immigration, increased number of immune-compromised people, international travel, global warming, and rapid urbanization of the cities have increased the susceptibility of the world population to parasitic diseases.[1] As a consequence, a number of new human parasites, in addition to other established pathogens are coming into limelight. Lophomonas blattarum is a new entity which has been proposed to be a cause of upper- and lower-respiratory tract infections in various reports from around the world, but controversies exist about its correct identification in the patients' samples. Although the first human case was reported in 1993 from China,[2] only one comprehensive review is available[3] regarding this parasite. Hence, the present article is an attempt to summarize the existing literature till 2019 and examine the taxonomy, morphology, epidemiology, clinical manifestations, diagnostic aspects, and treatment. This review is based on the PubMed search as of October 15, 2019 with the search term “Lophomonas,” which revealed 42 results.


   Taxonomy Top


L. blattarum, was first described by Samuel Stein in 1860 and was found to be a commensal in the intestines of cockroaches.[4] It is an anaerobic multiflagellate protozoan parasite belonging to the supergroup Excavata, first rank Parabasalia and second rank Cristamonadida. Two suborders, Lophomonadidae and Trichonymphina exist in Cristamonadida. There are two species belonging to Lophomonadidae: L. blattarum and Lonchura striata,[3],[5] which are commensals of cockroaches and termites.


   Morphology Top


The parasite exhibits both trophozoite and cyst stages; however, only the trophozoite stage can be seen in human tissue while both forms can be seen in the insect gut. The trophozoite is a round or pear-shaped structure and measures 20–60 μm in length and 12–20 μm in width. The cytoplasm has a granular appearance with phagocytosed food particles. At the apical zone, it has a tuft of numerous flagella which are irregularly arranged.[3],[6],[7] The outer flagella of the tuft are smaller and separate, and vibrate freely in the surrounding fluid medium and make the trophozoite to rotate forward swimming along its longitudinal axis. Details of the parasite body reveal that extending down the central axis is a trumpet-shaped body, the calyx. Arranged in rows and attached to the anterior end of the calyx is a tuft of flagella. Each flagellum possesses 11 filaments and ends in a typical basal body. The calyx membrane in the region of the basal bodies appears continuous, thick, and fibrous. Below this region, it is composed of a series of discrete longitudinally and obliquely arranged plates; these gather below the nucleus to form a bundle that extends posteriorly as the axial filament. Surrounding the calyx in the region of the nucleus is a specialized collar of cytoplasm known as the parabasal apparatus[8],[9] [Figure 1]. The cyst form which is found only in cockroaches and termites are spherical or oval and surrounded by a homogeneous membrane.[7]
Figure 1: The detailed structure of Lophomonas blattarum. Note the wine-glass-shaped calyx, axial filament, and parabasal “collar” of tubules, visible in the light microscope. (After Kudo[7] and Beams and Sekhon[8])

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Microscopy of clinical specimen

The morphology of the trophozoite stage has been primarily described in bronchopulmonary specimens such as sputum and bronchoalveolar lavage fluid. The parasite can be stained by Papanicolaou method or Wheatley s trichrome stain or by regular Giemsa or Wright stain. L. blattarum can be identified by its pyriform shape, granular cytoplasm with a large vacuole and the characteristic tuft of numerous and irregular flagella at the apical end [Figure 2]. In unstained fresh specimens, a characteristic to-and-fro movement can be seen.
Figure 2: (left) Flagellate protozoan parasite in fresh sputum sample. Note the pyriform shape, granular cytoplasm with a large vacuole and the tuft of flagella at the apical end (arrow). (Wet mount × 1200; bar, 15 μm). (Right) Similar flagellate protozoon in a sputum smear (Wheatley's trichrome srtain × 1000; bar, 15 μm). (Reproduced from Martinez-Giron and van Woerden)[3]

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There is an on-going controversy regarding the misidentification of bronchial ciliated epithelial cells as L. blattarum to the extent that Mu et al. have concluded that, “In the past 20 years, all the diagnosed cases as pulmonary L. blattarum infection reported in our country were misdiagnosed. Currently, there is no evidence to show L. blattarum as a pathogen resulting in pulmonary infection.”[10] This issue has been addressed by Li and Gao,[11] who have described the differentiating features between these two closely resembling structures mentioned in [Table 1]. These morphological differences can be seen in light microscopy [Figure 3] and [Figure 4].
Table 1: Distinguishing features between Lophomonas blattarum and ciliated epithelial cells[11]

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Figure 3: A ciliated bronchial ciliated cell and Lophomonas blattarum in wet mount of sputum specimen: (left) Ciliated bronchial cell-note the columnar shape, and terminal bar and inserted cilia at the apical end. (Right) Lophomonas blattarum– note the oval shape, granular cytoplasm with phagocytosed particles and a tuft of flagella (arrow) (×1000; bar: 6 μm) (Reproduced from Martinez-Giron and van Woerden)[3]

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Figure 4: Stained sample of sputum showing ciliated bronchial cells (left) and Lophomonas blattarum (right). The cilia are regularly oriented, whereas the flagella have an irregular arrangement (Papanicolaou stain × 1000; bar, 12 μm). (Reproduced from Martinez-Giron and van Woerden)[3]

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   Epidemiology Top


L. blattarum is a normal inhabitant of the hindgut of common species of cockroaches which include Blatta orientalis, Periplaneta americana, and Blattella germanica, as well as of termites. Cyst forms of the parasite have been demonstrated in insect gut[12] and the cysts have also been found in the environment.[13] It can be logically deduced that the parasite is excreted through the insect feces, and the cystic form can survive in the external environment for varying periods. The cysts of this protozoa are spread by contaminated food and clothing. Therefore, someone could be infected easily by breathing the dust containing L. blattarum. In the favorable environment inside the human host, excystation occurs and the trophozoites are set free, thus initiating the infection process. The domestic environment is a favorite residing place for cockroaches, and it is a well-known fact that these insects are important biological and mechanical carriers of pathogenic parasite species.[14],[15]

The first report of human infection originated from China in 1993[2], and subsequently, the majority of the reports have been from China with 138 cases,[16],[17],[18] with a few reports from Spain and Peru,[16] and in recent years from Mexico,[19] Iran,[20] Turkey,[21] and India.[22],[23] Although cases seem to be concentrated in China, isolated reports from Europe, the America, and other parts of Asia suggest that infections may be spread out in the globe, given the ubiquitous presence of the cockroach population worldwide.


   Clinical Features Top


A review of the existing literature[3],[16],[17],[18],[19],[20],[21],[22],[23] reveals that among the patients, there were no significant differences by gender and with age ranging from 9 days to 95 years. Immunosuppression in any form is an important risk factor and includes patients with kidney allograft transplantation, long-term corticosteroid treatment, chemotherapy with cytotoxic drugs, hepatic transplantation, allogeneic hematopoietic stem cell transplantation, and HIV infection.[11] Underlying lung disease like tuberculosis[22] can also play an important role by lowering immune status.

The bronchopulmonary site is most commonly infected given the nature of entry of the pathogen by inhalation. As per the case reports, some infrequent sites affected include maxillary sinus, urinary tract, and uterus.[11] The clinical manifestations include fever (38°C-39°C), cough, expectoration, chest pain, and shortness of breath. The expectoration is usually white or yellow and purulent and sometimes blood tinged. Thus, the clinical symptoms are unremarkable and similar to other respiratory conditions such as bronchial asthma, pneumonia, bronchiectasis, or pulmonary abscesses.[3] The X-ray and computed tomography imaging features of the patients show ground-glass opacity, patchy consolidation, and patchy or streaky shadows distributed in bilateral lungs.[16] Bronchoscopy examination has shown narrowing of the bronchial orifice, congestion and edema, and yellowish-white necrosis of mucosa. In blood examination, marked eosinophilia is not a constant finding, being present in 21.5%–35% cases only.[3],[11] This may be due to the immunosuppression observed in the majority of the patients.


   Laboratory Diagnosis Top


  1. Microscopy of Specimen: The definitive diagnosis of Lophomonas infection relies heavily on conventional light microscopy using unstained and stained preparations. Sputum and bronchoalveolar lavage fluid are the routine specimens which are commonly employed for any respiratory tract infection. Pyriform-shaped structures with granular cytoplasm and a tuft of flagella at one end raises a strong suspicion of Lophomonas along with the typical to-and-fro movement. However, care must be taken to distinguish it from bronchial ciliated epithelial cells (see above), with which it may be frequently confused[11]
  2. Culture: The parasite is difficult to grow, but a culture method had been devised by Lorenc in 1938[24] as described by Kirby.[25] Briefly, 0.8% salt solution with yeast added for food is used as the culture medium. The yeast needs to be grown separately in lemon juice diluted with an equal amount of tap water. Before using the yeast for culture, it has to be washed repeatedly with water by centrifugation, resuspended in salt solution and then added to the salt solution for culture. There should not be an over-excess of yeast in the medium.[25] Apart from this, the animal model for this parasite is not known.


Nucleic acid amplification

The lack of any molecular diagnostic evidence of Lophomonas infections in previous reports had always cast a shadow on the reliability of microscopic evidence alone.[11] This controversial issue seems to have been answered in a recent article from Iran by Fakhar et al.[26] In a patient with upper respiratory tract infection, they demonstrated the organism and also detected the nucleic acid by PCR in the nasal discharge. They designed a pair of primers for genus-specific detection of Lophomonas spp. by aligning of small subunit ribosomal RNA (SSU rRNA) sequence of two Lophomonas species: L. blattarum and L. striata. The forward primer was: (F) 5′-GAG AAG GCG CCT GAG AGA T-3′ and the reverse primer was:® 5′-ATG GGA GCA AAC TCG CAG A-3′. With this, they were able to demonstrate a 214-bp band. This is the first report of molecular diagnosis of Lophomonas infection which has addressed an important lacuna in diagnostic criteria and future reports are awaited to substantiate the finding.


   Treatment Top


Metronidazole has been used successfully at the usual dose of 500 mg every 8 h orally for 7–10 days in adults, and 7.5 mg/kg every 8 h in children. A single intravenous dose of 15 mg/kg over 1 h (as a loading dose), followed by 7.5 mg/kg every 6 h has also been used.[3] Tinidazole has also been used as an alternative drug.


   Conclusion Top


Parasites are not considered important causes of respiratory tract infections, and the recognition of L. blattarum adds a new dimension to this belief. Although considered a pathogen in immunocompromised hosts, some cases have also been documented in immunocompetent individuals. Respiratory tract infections in an immunocompromised patient may be due to a myriad of microorganisms, and hence, it is important to consider other traditional pathogens before coming to a definitive conclusion. Co-infection is a distinct possibility and in such doubtful cases response to a course of metronidazole or related agents can help in determining the pathogenic role of this parasite. The same approach can be employed in cases where differentiation from bronchial ciliated epithelium cells poses a problem. With only one report of molecular diagnosis,[26] it is imperative to test all cases of suspected L. blattarum for nucleic acid detection using the above mentioned or some other primers. In addition, the development of serological tests for the detection of either antigen or antibody will pave the way for confirmation of microscopic diagnosis. As more reports start emanating from other parts of the world, more concerted research on these aspects needs to be taken for this new flagellate protozoan parasite.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
   References Top

1.
Cheepsattayakorn A, Cheepsattayakorn R. Parasitic pneumonia and lung involvement. Biomed Res Int 2014;2014:874021. doi:10.1155/2014/874021.  Back to cited text no. 1
    
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Chen SX, Meng ZX. Bronchopulmonary Lophomonas blattarum infection: A case report (in Chinese). Chin J Parasitol Parasit Dis 1993;11:28.  Back to cited text no. 2
    
3.
Martinez-Girón R, van Woerden HC. Lophomonas blattarum and bronchopulmonary disease. J Med Microbiol 2013;62:1641-8.  Back to cited text no. 3
    
4.
Gile GH, Slamovits CH. Phylogenetic position of Lophomonas striata Bütschli (Parabasalia) from the hindgut of the cockroach Periplaneta americana. Protist 2012;163:274-83.  Back to cited text no. 4
    
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Adl SM, Simpson AG, Farmer MA, Andersen RA, Anderson OR, Barta JR, et al. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol 2005;52:399-451.  Back to cited text no. 5
    
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Brugerolle G, Lee JJ. Phylum parabasalia. In: Lee JJ, Leedale GF, Bradbury P, editors. An Illustrated Guide to the Protozoa. 2nd ed. Vol. 2. Lawrence: USA, Society of Protozoologists; 2000. p. 1196-250.  Back to cited text no. 6
    
7.
Kudo RR. Observations of Lophomonas blattarum a flagellate inhabiting the colon of the cockroach Blatta orientalis. Arch Protistenkd 1926;53:504-5.  Back to cited text no. 7
    
8.
Beams HW, Sekhon SS. Further studies on the fine structure of Lophomonas blattarum with special reference to the so-called calyx, axial filament, and parabasal body. J Ultrastruct Res 1969;26:296-315.  Back to cited text no. 8
    
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Kessel RG, Beams HW. Freeze fracture and scanning electron microscope studies on the nuclear envelope and perinuclear cytomembranes (parabasal apparatus) in the protozoan, Lophomonas blattarum. J Submicrosc Cytol Pathol 1990;22:367-78.  Back to cited text no. 9
    
10.
Mu XL, Shang Y, Zheng SY, Zhou B, Yu B, Dong XS, et al. A study on the differential diagnosis of ciliated epithelial cells from Lophomonas blattarum in bronchoalveolar lavage fluid. Zhonghua Jie He He Hu Xi Za Zhi 2013;36:646-50.  Back to cited text no. 10
    
11.
Li R, Gao ZC. Lophomonas blattarum infection or just the movement of ciliated epithelial cells? Chin Med J (Engl) 2016;129:739-42.  Back to cited text no. 11
    
12.
Romeiro A, Solé-Cava A, Sousa MA, de Souza W, Attias M. Ultrastructural and biochemical characterization of promastigote and cystic forms of Leptomonas wallacei n. sp. isolated from the intestine of its natural host Oncopeltus fasciatus (Hemiptera: Lygaeidae). J Eukaryot Microbiol 2000;47:208-20.  Back to cited text no. 12
    
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Rogerson A, Detwiler A. Abundance of airborne heterotrophic protists in ground level air of South Dakota. Atmos Res 1999;51:35-44.  Back to cited text no. 13
    
14.
Kinfu A, Erko B. Cockroaches as carriers of human intestinal parasites in two localities in Ethiopia. Trans R Soc Trop Med Hyg 2008;102:1143-7.  Back to cited text no. 14
    
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Graczyk TK, Knight R, Tamang L. Mechanical transmission of human protozoan parasites by insects. Clin Microbiol Rev 2005;18:128-32.  Back to cited text no. 15
    
16.
Xue J, Li YL, Yu XM, Li DK, Liu MF, Qiu JF, et al. Bronchopulmonary infection of Lophomonas blattarum: A case and literature review. Korean J Parasitol 2014;52:521-5.  Back to cited text no. 16
    
17.
Li ZL, Lin MX, Guan JH. Pulmonary infection of Lophomonas blattarum in a case of diffuse bronchioloalveolar cell carcinoma. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 2014;32:5.  Back to cited text no. 17
    
18.
Wen SH, Shi LW, Liu CX. Report of a case with pulmonary infection of Lophomonas blattarum in children. Zhonghua Er Ke Za Zhi 2016;54:464-5.  Back to cited text no. 18
    
19.
Saldaña NG, Mendoza FJO, Larrauri FR, Trujillo DM, Montoya EV, de La Garza EA, et al. Bronchopulmonary infection by Lophomonas blattarum in a pediatric patient after hematopoietic progenitor cell transplantation: first report in Mexico. J Thorac Dis 2017;9:E899-902.  Back to cited text no. 19
    
20.
Berenji F, Parian M, Fata A, Bakhshaee M, Fattahi F. First case report of sinusitis with Lophomonas blattarum from Iran. Case Rep Infect Dis 2016;2016:2614187.doi:10.1155/2016/2614187.  Back to cited text no. 20
    
21.
Zorbozan O, Uysal A, Bacakoǧlu F, Turgay N, Töz S. Lophomonas blattarum associated broncho-pulmonary infection after immunotherapy: A case report and a smart-phone based video of trophozoite. Turkiye Parazitol Derg 2019;43:44-6.  Back to cited text no. 21
    
22.
Verma S, Verma G, Singh DV, Mokta J, Negi RS, Jhobta A, et al. Dual infection with pulmonary tuberculosis and Lophomonas blattarum in India. Int J Tuberc Lung Dis 2015;19:368-9.  Back to cited text no. 22
    
23.
Tyagi R, Anand KB, Teple K, Negi RS. Lophomonas blattarum infection in immunocompetent patient. Lung India 2016;33:667-8.  Back to cited text no. 23
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24.
Lorenc W. Untersuchungen an flagellaten aus dem Genus Lophomonas: 1. Zucht von Lophomonas blattarum stein ausserhalb des wirtstieres etc. Zool Pol 1938;3:225-50.  Back to cited text no. 24
    
25.
Kirby H. Materials and Methods in the Study of Protozoa. Berkeley: USA, University of California Press; 1950. p. 24-5.  Back to cited text no. 25
    
26.
Fakhar M, Nakhaei M, Sharifpour A, Kalani H, Banimostafavi ES, Abedi S, et al. First molecular diagnosis of lophomoniasis: The end of a controversial story. Acta Parasitol 2019;64:390-3.  Back to cited text no. 26
    


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