Psychodid flies and their implicated role in human myiasis and pseudomyiasis

ABSTRACT

Several psychodid flies are commonly associated with human-inhabited environments and have been increasingly implicated in cases of human myiasis. However, the basic biology of psychodid larvae is not well-suited for survival in the human intestinal or urogenital tract, making true, prolonged myiasis unlikely. In this review, we performed a systematic literature review of published cases of purported myiasis caused by psychodid flies, their identification, associated clinical findings, and treatment. We also discuss the anatomy and lifecycle of psychodid flies in relation to their purported ability to use human tissue as a nutritive source and survive in the human alimentary or urogenital tracts. Based on the range of non-specific and varied reported clinical manifestations, lack of observed collections, life cycle patterns of psychodid flies, the mechanics of their mouthparts, and breathing requirements, we conclude that most cases likely represent incidental findings, or in rare cases possibly pseudomyiasis, rather than true myiasis, and provide recommendations for clinical evaluation and reporting so that disease misclassification and unnecessary therapy do not occur.

INTRODUCTION

Psychodid flies, commonly known as drain flies, moth flies, sewage flies, sink flies, and filth flies, are members of the subfamily Psychodinae in the cosmopolitan family Psychodidae within the order Diptera. As implied by their common names, some species in this group are well known to be closely associated with domestic and other human-inhabited environments (1–3). As a result, human encounters with psychodid flies in domestic habitats are common; this is evidenced by infestations being frequently addressed by pest control specialists and documented by photographers and naturalists (4, 5). Unlike the related phlebotomine sand flies (subfamily Phlebotominae) who feed on vertebrate blood and serve as vectors for the causative agent of leishmaniasis and other human diseases, psychodine flies are non-biting and have generally been regarded as having little significance to human health, other than as possible mechanical vectors for bacteria (6). However, there have been increasing reports of psychodines causing human myiasis throughout the twentieth century and continuing into the twenty-first century, and this potential role deserves further investigation (7).

Myiasis is defined as the use of human or other animal tissue as a nutritive source for developing fly larvae and can be broadly classified into three categories: obligatory, facultative, and pseudomyiasis (also termed accidental or incidental myiasis) (8). The first two categories are types of true myiasis in which fly larvae feed on host tissue. In obligatory myiasis, fly larvae require healthy tissue from a living host for development; causative agents include botflies in the family Oestridae (Oestrus, Cuterebra, and Dermatobia), as well as some members of Calliphoridae (Cordylobia, Cochliomyia) and Sarcophagidae (Wohlfahrtia). In facultative myiasis, fly larvae opportunistically feed on dead or dying tissues after oviposition or larviposition (deposition of eggs or larvae, respectively) on pre-existing wounds; normally, larvae of these flies feed on bacteria and particulate nutritive matter in carrion, dung, and decomposing organic matter.

In contrast to the types of true tissue-invasive myiasis described previously, pseudomyiasis refers to the incidental infestation (or appearance of infestation) of the human body with fly larvae that do not require vertebrate tissue as a nutritive source (7–9). A common form of pseudomyiasis occurs with accidental ingestion of fly larvae through contaminated food or water and subsequent passage of dead larvae in stool. The larvae are incapable of surviving in the gastrointestinal tract and therefore cannot cause true infestation, although they may cause temporary mucosal irritation. It is likely that all reports of intestinal myiasis represent pseudomyiasis. Another possible explanation for purported intestinal myiasis is oviposition on a freshly collected stool sample that has prolonged exposure to the environment. Many of these flies have short developmental cycles, and eggs deposited in the stool can hatch and develop into visible larvae within hours post oviposition, given the impression that they were passed in the stool (10). Sometimes, common synanthropic flies will lay eggs on exposed human waste (e.g., feces, soiled diapers, voided urine, and discarded menstrual hygiene products containing blood) and may be mistaken as representing myiasis. While these larvae may evoke concern from the observer, their presence is not generally indicative of actual infestation as female flies readily lay their eggs in rich organic matter. Lastly, pseudomyiasis may involve the colonization of organically rich substrates such as urinary catheters and, rarely, mucosal surfaces.

The differentiation between true myiasis and pseudomyiasis can have important clinical and behavioral implications. While true myiasis requires larval removal and potentially surgery and tissue debridement, pseudomyiasis rarely requires medical intervention. Similarly, different strategies are indicated for preventing true myiasis compared with pseudomyiasis. For these reasons, it is important to fully understand the nature of all myiasis cases in order to make sound patient care decisions, prevent occurrence/recurrence, and document cases in the medical record and/or scientific literature. To this end, we review the published literature on cases of purported myiasis due to psychodid larvae to understand the commonly reported associations and clinical manifestations. We also review the life history and morphology of psychodid larvae to investigate their ability to cause true human obligatory or facultative myiasis.

LIFE HISTORY OF PSYCHODID FLIES IN RELATION TO CLAIMS OF MYIASIS

The subfamily Psychodinae occupies a broad range of ecological niches, and its constituent species are highly diverse in morphology. Despite this diversity, a few generalizations regarding their life history can be made herein. They undergo a complete metamorphosis during their existence, with egg, larva, pupa, and adult stages. After hatching, the larvae undergo molting three times, for a total of four instars (larval stadia) before pupation. It is predominantly the larval stages that have been implicated in cases of human myiasis, although pupae have occasionally been reported. Adults emerge from the pupal cases and are able to mate within hours. Developmental periods have been reported for only a few species of Psychodinae. Not surprisingly, some of the most detailed information is available for synanthropic species. Williams (11) reported the duration of the life cycle of laboratory-reared Clogmia albipunctata to be at least 17 days, with larval development requiring between 12 and 15 days (11). Vaillant (12) observed the same species, also in a controlled environment, and found the complete life cycle to last 17 days and that adults live for approximately 10 days (12). Later, Sehgal et al. (13) reared C. albipunctata in a laboratory at 22°C and recorded the duration of larval development as 16–17 days, with the pupal stage lasting 5–6 days (13). More recently, Azmiera et al. (14) reviewed life cycle data for Psychoda alternata and other Psychoda species as the data pertain to forensic studies (14). In all cases, developmental time depends on temperature and availability of nutrients (3, 6, 14).

Psychodid larvae are mainly detritivores (i.e., feeding on detritus), while the adults are non-feeding, typically short-lived, and remain close to the larval habitat, as long as levels of moisture and nutrients remain suitable for oviposition and larval development. Some common names such as “drain fly,” “sewer fly,” and “trickle filter fly” are often used in reference to Psychodidae at large, but it is important to note that this is inaccurate, as these names are originally applied to a few synanthropic species. Clogmia albipunctata is known as the drain fly or sewer fly due to its affinity for these microhabitats (2, 11), while these names have also been used for Psychoda albipennis, which is frequently found in human-impacted habitats (1). Furthermore, Psychoda alternata and some closely related species are called trickle filter flies, owing to their success in colonizing sewage treatment filters (15). These comparatively well-known species normally occur in persistent moist or shallow-water microhabitats, especially in environments related to the trash disposal and wastewater infrastructure. Kitchens, latrines, toilets, showers, and floor drains are readily invaded where sufficient nutrition has accumulated and is accessible to adult flies for oviposition; however, the exact location where the larvae are feeding and developing may be hidden from view (e.g., in the plumbing; Fig. 1). The larvae feed on bacteria and biofilms resulting from deposits of human waste or other decaying organic material (2, 3, 6).

Fig 1.

Diagram of a restroom toilet fixture, indicating a common location for the development of psychodid larvae and pupae. The life cycle of these flies, including eggs (right), larvae, pupae, and adults, is shown in the inset.

PSYCHODID LARVAL MORPHOLOGY IN RELATION TO CLAIMS OF MYIASIS

General characteristics of Psychodinae larvae include a well-developed, completely exposed (visible) head capsule and a trunk (thorax and abdomen) with annulated segments (Fig. 2). Each segment bears a sclerotized (hardened), dorsal plate and a series of conspicuous bristles (11, 12). Often the bristles become caked in detritus from the larval habitat, playing a role in camouflage as well as in resistance to desiccation (3, 12); however, this varies depending on whether the larvae are crawling in the moist substrate or suspended in standing water (Supplemental Video S1).

Fig 2.

Photomicrograph of a larval Clogmia albipunctata showing the sclerotized head capsule and conical posterior, as well as segmentation with annuli and tergal plates.

Their mouthparts include toothed mandibles operating in an oblique plane and a conical, brush-like labrum operating in a vertical plane (Fig. 3A). The specific shape of the mandible is dependent on the feeding behavior and source of nutrition (16, 17). In mature (fourth instar) Clogmia albipunctata, for example, each mandible has a series of apical to subapical, blade-like dentations (Fig. 3A) used for scraping the biofilm from a hard surface or shredding decaying organic matter, suspended or otherwise, into fine particles before ingestion (11, 12). This is achieved by repeated, often rapid opening and closing of the mandibles and labrum (Supplemental Video S2).

Fig 3.

Morphological features of larval Clogmia albipunctata (Williston, 1893). A: head capsule with partially extended mouthparts, ventral view. B: posterior abdominal division with flabellar processes and associated float setae resting at the water surface, exposing posterior spiracles to the atmosphere. Scale bars: 0.1 mm

All psychodid larvae have only the anterior-most and posterior-most spiracles functional, which is the most common arrangement among Diptera larvae (16). Larvae of Psychodinae have their posterior spiracles modified as extended tubes enclosed by a sclerotized cone (Fig. 2). In this arrangement, the spiracular openings are paired, directed posteriorly, and flanked by two pairs of movable clavate processes. Each of these clavate processes is set with a fringe of hydrophobic setae (Fig. 3B) that lay flat on the water surface, thereby keeping the posterior end of the larva and the spiracular openings exposed to the atmosphere so that the larvae can breathe (Supplemental Video S3). Another function of the clavate processes and hydrophobic setae is to trap an air bubble as the larva becomes submerged. This allows gas exchange to occur while the larva is fully submerged at shallow depths (11) ( Supplemental Video S3) Despite this adaptation, psychodid larvae are not known to have the ability to remain submerged for extended periods of time. In fact, Williams (11) found that Clogmia albipunctata larvae were only able to remain submerged for approximately 24 hours, after which they died without access to surface air (11).

Based on their structure and function, mouthparts of Psychodinae larvae are suited for feeding on fine particulate organic matter, while their posterior spiracles and associated structures are adapted for life in shallow aquatic habitats. When the larvae are at rest with their posterior end on the water surface, they may ingest suspended food particles. Otherwise, they actively crawl on wet surfaces or are fully submerged in search of nutrition. They are clearly not adapted to live for extended periods of time in oxygen-poor environments without an interface with the atmosphere, such as within the human alimentary canal or urogenital tract.

IMPLICATED SPECIES AND EPIDEMIOLOGY OF REPORTED CASES

The reported cases of myiasis caused by psychodid flies have been documented nearly worldwide but are most common in the Middle East, North Africa, and Southeast Asia. Cases are notably absent or sparse from the Americas (Table 1). The most commonly implicated species are described as follows.

TABLE 1.

Purported myiasis cases caused by psychodid flies^c

Causative agent	Country	Patient age/sex	Myiasis type	Clinical manifestations (co-existing conditions)	Larval collection	Treatment	Ref.
Clogmia albipunctata	Canada; travel to Iraq and Afghanistan	57 /M	Urogenital	None; complained of passing larvae via his urethra	Recovery of larvae after urination	Ivermectin	(18)
Clogmia albipunctata	China	26 /F	Oral	None; larvae found in the mouth while brushing teeth (dental caries)	Recovery of larvae during flushing of tooth root with saline	Saline flush	(19)
Clogmia albipunctata	China	50 /F	Urogenital	Frequent micturition and urgency; complained of larvae in morning urine × 2 months (UTI)	Recovery of larvae in urine (collected in a clean container)	Broad-spectrum antibiotics	(20)
Clogmia albipunctata	Egypt	24 /F	Urogenital	Complained of motile, dark, worm-like organisms in urine intermittently × 2 yr, associated with dysuria and frequent micturition	Recovery of larvae and pupae in urine (collected in a clean container)	Ivermectin	(21)
Clogmia albipunctata	Egypt	36 /M	Intestinal	Abdominal pain, bloating, and diarrhea with intermittent constipation	Recovery of larvae in the stool/toilet floor	Ivermectin, nitazoxanide, and saline purgative	(22)
Clogmia albipunctata	Egypt	F	Urogenital	Dysuria, fever, and periurethral and genital itching; complained of motile dark larvae in urine × 2 months	Recovery of larvae after urination	Antibiotics and antiseptics	(23)
Clogmia albipunctata	India	24 /F	Urogenital	Complained of motile, dark, worm-like objects in urine × 3 months; no other symptoms	Recovery of larvae after urination	Ivermectin	(24)
Clogmia albipunctata	Japan	69 /F	Urogenital	Lower abdominal pain, cloudy urine, and hematuria × multiple years; complained of finding black–brown motile “worms” in urine	Recovery of larvae in toilet water after urination	None	(25)
Clogmia albipunctata	Japan	48 /F	Intestinal	N/A	N/A	N/A	(26)
Clogmia albipunctata	Malaysia	41 /F	Intestinal	Abdominal colic; complained of “worms” on the toilet floor after defecation	Recovery of larvae on the toilet floor	Albendazole	(27)
Clogmia albipunctata	Malaysia	7 /M	Intestinal	Vomiting larvae	Recovery of larvae in vomitus	N/A	(28)
Clogmia albipunctata	Mexico	13 /F	Urogenital	Bradypsychia, bradylalia, hallucinations, delirium, and somnolence (meningitis, NOS)	Recovery of larvae and pupae from the urinary catheter and by cystoscopy; bladder biopsy revealed chronic inflammation	Ivermectin	(29)
Clogmia albipunctata	Netherlands (ex: Mexico)	18 /F	Urogenital	Complained of small moving objects in menses secretions; no other symptoms	Recovery of larvae in menstrual secretions after bathing	None	(30)
Clogmia albipunctata	Nigeria	M	Nasopharyngeal	Nasal irritation; complained of larvae from nostrils	Recovery of larvae from nostrils by the patient	N/A	(31)
Clogmia albipunctata	Palestine	28 /F	Urogenital	Mild abdominal pain and burning sensation during urination; (pregnancy)	Recovery of larvae after urination and inside the house	Antibiotics, antiseptic therapy, and hydration	(32)
Clogmia albipunctata	South Africa	F (elderly)	Nasopharyngeal	Sensation of movement in the nose; chronic black nasal discharge	Recovery of larvae after nasal irrigation	None (environmental controls)	(33)
Clogmia albipunctata	Taiwan	21 /M	Intestinal	Abdominal pain; anal itching	Recovery of larvae after defecation	Mebendazole for initially suspected enterobiasis	(34)
Clogmia albipunctata	Turkey	43 /F	Urogenital and gastrointestinal	Perianal and periurethral/genital itching; complained of larvae in urine and feces × 2 months	Recovery of larvae after urination and defecation	Unspecified antibiotics	(35)
Pericoma sp.	India	12 /M	Urogenital	Frequent urination, sensation of incomplete bladder emptying, and weight loss; complained of “worms” in urine × 2 months	Recovery of larvae in urine collected in a sterile container	Broad-spectrum antibiotics	(36)
Psychoda albipennis	Egypt	21 /M	Urogenital	Urinary tract discharge and burning micturition	Recovery of larvae after urination	N/A	(37)
Psychoda albipennis	India	19 /F	Urogenital	Dysuria, fever, and periurethral and genital itching; complained of live “worms” in urine × 2–3 yr	Recovery of larvae after urination; bladder washings by cystoscopy	Ivermectin	(38)
Psychoda albipennis	Iran	9 /F	Urogenital	Dysuria; complained of motile black–gray particles in urine	Recovery of larvae after urination	N/A	(39)
Psychoda albipennis	Libya	10 /F	Urogenital	Pain, discomfort, and dysuria; motile larvae in urine × 1 yr	Recovery of larvae after urination (home and hospital)	Urinary tract antiseptics, hydration	(40)
Psychoda albipennis	Saudi Arabia	42 /M	Urogenital	Complained of passing “worms” in urine × 3 weeks	Recovery of larvae after urination	Nitrofurantoin, hydration	(41)
Psychoda albipennis	Turkey	29 /M	Urogenital	Urinary incontinence	Recovery of larvae after urination	N/A	(42)
Psychoda albipennis	Turkey	15 /M	Urogenital	Complained of passing “worms” in urine × 3 months	Recovery of larvae after urination	N/A	(43)
Psychoda albipennis	Turkey	29 /M	Urogenital	Frequent urination and left flank pain; complained of passing worms in urine × 3 days	Recovery of larvae after urination	None	(44)
Psychoda albipennis	Turkey	20 /F	Urogenital	Nausea, vomiting, and dysuria; complained of motile objects in urine	Recovery of larvae after urination	Antibiotics, urinary antiseptics	(45)
Psychoda albipennis	Turkey	50 /F	Urogenital	N/A [post-urinary bladder surgery]; complained of motile objects in urine	Recovery of larvae in urine	Antibiotics, urinary antiseptics	(46)
Psychoda albipennis	Turkey	28 /F	Urogenital	Nausea, vomiting, abdominal pain, dysuria, and suprapubic tenderness; complained of moving worms in urine × 2 weeks	Recovery of larvae after urination	Antibiotics, urinary antiseptics	(47)
Psychoda albipennis	Turkey	10 /F	Urogenital	Painful and frequent urination and genital pruritus; complained of white and black worms in urine	Recovery of larvae in 24-hour urine and observed collection	Urinary tract antiseptics, hydration	(48)
Psychoda albipennis	Turkey	42 /M	Urogenital	Erectile dysfunction, groin pain, and pollakiuria; complained of passing motile larvae in urine	Recovery of larvae after urination	Antibiotics, urinary antiseptics	(49)
Psychoda albipennisa	Turkey	M	Urogenital	Dysuria; complained of passing black-grayish mobile particles in urine × 2 months	Recovery of larvae after urination	Cefpodoxime proxetil and methenamine hydromethylene citrate	(50)
Psychoda albipennis	Turkey	64 /M	Urogenital	Discomfort during urination; complained of passing larva-like organisms in urine	Recovery of larvae after urination	Antibiotics and urinary antiseptics	(51)
Psychoda albipennis	Turkey	21 /F	Urogenital	Right costo-lumbar pain, vaginal irritation, dysuria, polyuria, hematuria, vomiting, and diarrhea	Recovery of larvae after urination	Extracorporeal shockwave lithotripsy for nephrolithiasis	(52)
Psychoda alternata	Iraq	35 /M	Urogenital	Dysuria, frequent micturition, burning sensation in the urethra, and fever	Recovery of larvae after urination	N/A	(53)
Psychoda alternata	USA	M	Nasopharyngeal	None	Recovery of larvae in sputum	N/A	(54)
Psychoda sexpunctata	Japan	N/A	Intestinal	N/A	Recovery of larvae from a digestive tube	N/A	(55)
Psychoda sp.	China	12 /M	Urogenital	Measles	Recovery of larvae in urine	N/A	(56)
Psychoda sp.	Egypt	19 /F	Urogenital and gastrointestinal	Nausea and epigastric pain	Recovery of larvae in vomitus, stool, urine, and menstrual blood	None	(57)
Psychoda sp.	Egypt	44 /M	Urogenital	Complained of passing “worms” in urine	Recovery of larvae after urination	Ivermectin	(58)
Psychoda sp.	Egypt	9 /F	Urogenital	Dysuria	Recovery of larvae after urination	Ivermectin	(58)
Psychoda sp.	Egypt	23 /M	Urogenital	Urinary discharge and dysuria; previous surgery for kidney stones; passing “worms” in urine	Recovery of larvae after urination	Ivermectin	(58)
Psychoda sp.	Egypt	18 /M	Urogenital	Complained of passing “worms” in urine	Recovery of larvae after urination	Ivermectin	(58)
Psychoda sp.	Egypt	68 /M	Urogenital	Hematuria, and dysuria	Recovery of larvae after urination	Ivermectin	(58)
Psychoda sp.	Iran	26 /F	Urogenital	UTI, stomach pain, malodorous reddish vaginal discharge, and polyuria	Recovery of larvae after urination	N/A	(59)
Psychoda sp.	Libya	9 /F	Urogenital	Genital pruritis; passing “dark worms” in urine	Recovery of larvae after urination	N/A	(60)
Psychoda sp.	Turkey	53 /F	Urogenital	Dysuria; complained of passing “worms” in urine × 2 weeks	Recovery of larvae in urine collected directly in a clean cup	Urinary antiseptics	(61)
Psychodidae, undet.b	USA	31 /M	Urogenital	Complained of passing a larva in the urine associated with midstream interruption of flow; a previous episode of hematuria	Recovery of larvae after urination	Ivermectin	(62)

^a The larva in this manuscript is misidentified; based on the available images, it is likely C. albipunctata.

^b The larva pictured in this case is Stupkaiella, a non-synanthrophic psychodid genus.

^c M—male, F—female, N/A—not available, Ref—reference, UTI—urinary tract infection.

Clogmia albipunctata, a common species living closely alongside and benefiting from humans (synanthropic) has a near-worldwide distribution and has been implicated as a cause of nasopharyngeal, urogenital, and intestinal myiasis from the Netherlands (30), Palestine (32), Egypt (21–23), Turkey (35), Nigeria (31), South Africa (33), China (19, 20), Taiwan (34), Japan (25, 26), India (24), Malaysia (27, 28), Canada (18), and Mexico (29). This species is often reported under its synonym Telmatoscopus albipunctatus.

Psychoda albipennis is another common and widely distributed species (1) and has been implicated in urogenital myiasis in Egypt (37), India (38), Iran (39), Turkey (42–52, 61), Saudi Arabia (41), and Libya (40). Psychoda alternata has been implicated in nasopharyngeal myiasis in the USA (54) and urogenital myiasis in Iraq (53). Psychoda sexpunctata has been implicated as a cause of gastrointestinal myiasis in Japan (55). Additional members of the genus Psychoda not specificated have been implicated in gastrointestinal and urogenital myiasis in Egypt (57, 58), Libya (60), Iran (59), Turkey (61), and China (56).

Pericoma, as currently delineated, is restricted to the Palearctic (region including Europe, Africa north of the Sahara, and Asia north of the Himalayas). There is one reported case of urinary myiasis caused by Pericoma from India (36); in that report, the organism was not identified at the species level. Interestingly, evaluation of the images in that case report by one of the current authors (G.C.) has shown the specimen to be misidentified; it actually represents a specimen of Clogmia.

CLINICAL MANIFESTATIONS ASSOCIATED WITH PURPORTED CASES OF MYIASIS CAUSED BY PSYCHODID FLIES

A wide variety of clinical manifestations and comorbidities have been associated with reported cases of myiasis caused by the larvae of psychodid flies (Table 1). To date, cases comprise primarily urogenital myiasis, with rare reports of oral, intestinal, and nasopharyngeal myiasis.

In cases of purported urogenital myiasis, several patients were asymptomatic or symptoms were not reported (18, 24, 30, 35, 41, 43, 44, 56, 58, 62). When symptoms were present, the most common complaints were dysuria, itching, burning, and vaginal discharge during urination (23, 32, 37, 40, 45, 47, 48, 51–53, 58, 60, 63), followed by frequent micturition, polyuria, and pollakiuria (frequent, abnormal urination during the day), often with urgency (20, 21, 37, 49, 52, 53, 59). Less common complaints included fever (23, 53), nausea (45, 47, 57), epigastric pain (57), vomiting (45, 47, 52), diarrhea (52), cystitis (25), hematuria (52, 58), urinary incontinence (42), abdominal or groin pain (32, 38, 47, 49), erectile dysfunction (49), and neurological disorders such as bradypsychia, bradylalia, hallucinations, and delirium (29). Other comorbidities associated with purported urogenital cases included pregnancy (32), post urinary bladder surgery or surgery for kidney stones (46, 58), measles (56), and enterobiasis (48). Of note, most cases were diagnosed solely on the presence of motile larvae in urine (Table 1), and it was not usually clear if the urine was captured directly or retrieved from the environment (e.g., toilet bowl). However, there were several cases in which urine was purportedly collected into a clean container (20, 22, 36, 40, 48), and there were two unusual cases in which larvae were retrieved directly from the bladder/bladder washings during cystoscopy (29, 63). Thus, it appears as though psychodid larvae can enter the human bladder and urethra at least on a temporary basis, particularly if they have a port of entry (e.g., catheter). The resulting colonization would result in inflammation as to be expected from any foreign body contamination. However, it is unlikely that they could survive for extended periods of time based on their anatomy (described previously) and eventual need for oxygen, and none of these reports specifically describe a pathology associated with feeding by the larvae.

Clinical manifestations associated with purported cases of intestinal myiasis are general including nausea, abdominal pain, gastroenteritis, bloating, and diarrhea, with or without intermittent constipation. In a patient from Egypt, larvae were recovered in stool after defecation in a pit latrine. The patient’s household has two kinds of toilets, a pit latrine and a standard toilet; the patient reportedly uses the pit latrine, while his wife and children, who had no complaints of larvae being found in their stool, use the toilet (22). In another patient from Malaysia, larvae were reportedly collected in vomitus (28). In one patient the larvae were reported from various bodily fluids (vomitus, stool, urine, and menstrual blood) over seven days, but no specifics on where the larvae were collected from nor any discussion on hygiene concerns of the patient (57). One patient also reported abdominal colic; in this case, the fly larvae were found on the “toilet floor” and not in the toilet after defecation (27).

Cases of purported nasopharyngeal myiasis usually involved some kind of nasal irritation or the sensation of something moving in the nose (31, 33). One patient complained of chronic nasal discharge (33). In one case, larvae were recovered in sputum in an otherwise presumably healthy patient (54). One case of purported oral myiasis was in an asymptomatic patient who recovered larvae after brushing her teeth (19). Further examination of this patient revealed significant dental caries, and numerous psychodid larvae were retrieved following saline flushing of the tooth root; however, it is likely these larvae contaminated the area after using water for oral hygiene that was from a faucet colonized with larvae.

DISCUSSION

In this review, we have described the general structure and function of the mouthparts in psychodid fly larvae, as well as their feeding habits and the atmospheric conditions required for them to breathe. Given these biological features in conjunction with the time duration required for the larvae to develop, it is unlikely that psychodid larvae could survive, let alone further develop, in the human alimentary or urogenital tracts. We have also reviewed the published cases of purposed myiasis attributed to psychodid larvae and note that most appear to be based on finding larvae in the environment following urination or defecation, especially when there is no evidence suggesting the larvae were observed or collected by trained medical personnel. Only a few were identified in situ or in observed collections by medical professionals. Thus, is it not possible to draw definitive conclusions as to the nature of the cases and whether they represent pseudomyiasis or facultative myiasis. This is, unfortunately, a problem with most cases of urogenital and intestinal myiasis, as the diagnosis is often based on finding larvae in the environment. The implicated species are usually saprophagous and thus expected to be found in dirty or contaminated water, human or animal feces, or on biofilms growing in moist environments (10), and it is generally believed the presence of these saprophagous larvae in toilets, bathtubs, latrines, and other environmental sources represents contamination of a clinical specimen (e.g., oviposition or larviposition on a stool specimen post-defecation) (64, 65). Larvae recovered in vomitus may be incidental following irritation after the consumption of larvae in contaminated food or water sources. Complicating this assessment is that many flies that depend on human or animal feces as a larval food source have rapid development, and larvae may be present as early as a few hours after oviposition (10).

In some cases, intestinal myiasis has been defined as the spurious passage of ingested larvae (e.g., cheese fly larvae, Piophilus casei) (10, 65). In these cases, there may be inflammation of the intestinal mucosa due to secretions by the larvae and potential physical damage caused by cuticular spines, but there is no evidence that the larvae actually use human intestinal tissue as a nutritive source during passage (10).

In rare instances, cases of intestinal myiasis have been described when flies deposit eggs or larvae in soiled diapers or around the anal opening in patients presenting with poor hygiene (66), but in these cases, the larvae are likely feeding on fecal material and not intestinal tissue or skin and would thus be considered cases of pseudomyiasis rather than true myiasis. Larvae may also feed on biofilms such as those present on indwelling catheters and medical devices. Psychodid larvae were obtained from a urinary catheter from a Mexican patient (18), and larvae were obtained by cystoscopy, suggesting that they entered the bladder through the catheter. The bladder mucosa was noted to be inflamed, giving rise to the possibility that local irritation had occurred from the physical presence of the larvae.

Despite these considerations, we identified a single reported case from India (37) where larvae were observed in the bladder wash fluid after diffuse ulceration was observed by cystoscopy. The patient did not have a history of current or recent catheterization, suggesting a possible case of incidental myiasis, although it is possible the wash fluid itself was the source of contamination.

Similar to the gastrointestinal and urogenital cases of myiasis involving psychodids, most reported cases of oral myiasis were based on the recovery of larvae during toothbrushing or rinsing rather than from human tissue. Given the information presented previously on the biology of psychodid flies, one must consider contamination of the toothbrush or mouth during the rinsing process with larvae living within the faucet. In one case of suspected oral myiasis from France, larvae were also found in a water collection container that was used for, among other things, brushing the patient’s teeth. The authors concluded that this was not a true case of myiasis and emphasized the importance of indisputable parasitological–clinical examinations demonstrating lesions caused by the suspected agent (67). Similarly, in one case of suspected nasopharyngeal myiasis caused by C. albipunctata, the larvae were recovered after the use of a nasal irrigation device (33), suggesting possible contamination of the water source or the device itself. There was the single aforementioned case of oral myiasis from China (20), which described the recovery of larvae from a tooth root socket during saline flushes, suggesting contamination of the area after using water containing larvae.

Based on these cases, we conclude that one must be cautious before determining psychodid fly larvae, or any fly larvae, as the direct cause of the patient’s ailments, in the absence of corroborated, unequivocal epidemiological, parasitological, and clinical evidence. Physicians and clinicians should take this information into consideration before subjecting their patients to unnecessary physical or chemotherapeutic treatment. Furthermore, laboratorians should be cognizant of this when larvae are received into the laboratory. Identification of fly larvae can be challenging, but it is important for laboratorians to be able to separate those flies that can cause obligatory or facultative myiasis from those that likely cause pseudomyiasis or represent incidental findings from the environment. If this is not possible, the specimens should be sent to a reference laboratory that can carry out the process of identification. Identification of fly larvae is beyond the scope of this work, and the readers are directed to other works that describe this (8, 9, 68). Broadly speaking however, fly larvae that use human tissue as a nutritive source lack a well-defined, sclerotized head capsule; lack prominent bristles; and do not possess posterior spiracles directed posteriorly away from the body of the larva (68). It is recommended that fly larvae, and insects in general, that are not of medical concern be reported as such so as not to create a potentially false connection between the organism and any symptoms the patient may be experiencing (8). Suggested reports could include verbiage such as “arthropod/insect, not of medical importance” or “organism is not a known human parasite” or similar (8). Despite the organisms in these instances not having any clinical relevance, such reporting could help alleviate any concerns the patient may have. Clinicians and laboratorians should also exercise caution before publishing cases claiming psychodid flies reported from clinical specimens are the causative agent of myiasis. A critical evaluation of the situation is required, which may include consultation with an experienced parasitologist or medical entomologist. Some factors to consider include, but not limited to, a precise and correct identification of the suspected causal agent, detailed information on how the specimen was found and collected, and any clinical correlation, including duration before and after the finding of the larvae.

It is also hoped that academic journals apply rigorous scrutiny of data before publishing cases of myiasis caused by psychodid larvae. An accurate genus-level identification should be made, and high-quality images should be included. The review process for such papers should also include input from entomologists familiar with the biology and epidemiology of these flies and microbiologists or parasitologists with expertise in myiasis.

SUPPLEMENTAL MATERIAL

The following material is available online at https://doi.org/10.1128/jcm.01200-23.

Supplemental Video S1. jcm.01200-23-s0001.mov.

Live psychodid larvae.

Supplemental Video S2. jcm.01200-23-s0002.mov.

Moving mouthparts of Clogmia albipunctata.

Supplemental Video S3. jcm.01200-23-s0003.mov.

Posterior spiracles using hydrophobic setae to capture an air bubble used in respiration.

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