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letter2021
EARXXX10.1177/01455613211031024Ear, Nose & Throat JournalOu and Huang

Case Report
Ear, Nose & Throat Journal
2023, Vol. 102(12) NP591­–NP595
Nasal Maggot Infection in a Patient With © The Author(s) 2021
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Nasal Non-Hodgkin’s Lymphoma sagepub.com/journals-permissions
DOI: 10.1177/01455613211031024
https://doi.org/10.1177/01455613211031024
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Jing Ou, Master of Medicine1 , and Yan Huang, Doctor of Medicine2

Abstract
We describe a case of nasal non-Hodgkin’s lymphoma in a 79-year-old Chinese patient accompany with nasal myiasis. The first
2 biopsies in this case were false negative. Subsequently, nasal maggots developed in this patient. After removing all maggots under
nasal endoscopy, the patient continued to have recurrent fever and was transferred to a higher hospital for further treatment, in
which he received a third biopsy. Unfortunately, several hours after the biopsy, the patient died for severe nasal bleeding. The final
biopsy result indicated the neoplasm of the left nasal cavity was non-Hodgkin’s lymphoma. This case illustrates the importance of
repeated biopsies for nasal non-Hodgkin’s lymphoma if necessary. Nasal myiasis is a secondary disease of nasal non-Hodgkin’s
lymphoma in this case.

Keywords
nasal, non-Hodgkin’s lymphoma, myiasis, biopsy

Background lymphoma is difficult to diagnose at the early stage, or even

misdiagnose this disease due to its nonspecific clinical mani-
Lymphoma is a malignant tumor of the immune system. Lym-
festations. The clinical manifestations of this disease can be
phoma arises from lymph nodes and lymphoid tissues, and its
divided into 3 phases. Patients with nasal NHL present with a
occurrence is mostly related to some malignant transformation
common cold or nasosinusitis with intermittent nasal obstruc-
of immune cells generated by the proliferation and differentia-
tion and watery or bloody secretions in prodromal stage. In the
tion of lymphocytes in the immune response process.
active phase, nasal obstruction is aggravated in these patients,
Lymphoma is divided into Hodgkin’s lymphoma (HL) and
and nasal mucosa swelling, purulent and smelly nasal dis-
non-Hodgkin’s lymphoma (NHL) based on histopathological
charge, granuloma, erosion, ulceration, necrosis, nasal septum,
characteristics. Non-Hodgkin’s lymphoma occurs in the extra-
or palate perforation also can be found in the nasal cavity, while
nodal tissues mainly, and NHL accounts for about 3% of all
the general condition is not too bad. In the terminal stage, the
cancer cases in the population.1 The head and neck region is the
mucosa, cartilage, bone of the midline in the nasal cavity, and
second common site for primary extranodal lymphoma after
the adjacent tissues are damaged severely, which leads to local
the gastrointestinal tract.2
disfiguration, cachexia, and systemic failure. Indeed, the
Thereinto, nasal NHL also belongs to primary extranodal
lymphoma.3 The incidence of nasal NHL accounts for 23%
to 31% of nasal malignancy in Asia,4 and it has high degree
1
of malignancy.5 Nasal NHL is divided into 3 subtypes accord- Department of Otorhinolaryngology, Luoding People’s Hospital, Luoding,
China
ing to immunohistochemistry, which include diffuse large 2
Department of Otorhinolaryngology–Head and Neck Surgery, Guangdong
B-cell lymphoma, peripheral T-cell lymphoma, and NK(Na- Provincial People’s Hospital and Guangdong Academy of Medical Sciences,
tural Killer )/T-cell lymphoma. NK/T cells are the most com- Guangzhou, China
mon source of nasal NHL in China, which accounts for more Received: May 23, 2021; revised: June 14, 2021; accepted: June 21, 2021
than 90%.6
Nasal NK/T-cell lymphoma is common in Asia, Spain, and Corresponding Author:
Yan Huang, Department of Otorhinolaryngology-Head and Neck Surgery,
South America, especially in China, but it is rare elsewhere.7-9 Guangdong Provincial People’s Hospital and Guangdong Academy of Medical
Although the prevalence is not low in the above areas, we still Sciences, Guangzhou 510000, China.
can find some literatures10,11 that report that nasal NK/T-cell Email: [email protected]

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2NP592 Ear, NoseEar, Nose &Journal
& Throat Throat102(12)
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Figure 1. (A) A gray-red neoplasm that was anabrotic on the surface and easy to bleed when being touched in the left nasal cavity. (B) The
mucosa of nasopharynx was smooth.

nonspecific inflammation and necrosis of nasal tissues contrib-

ute to the difficulty of early diagnosis of nasal NHL. Now, we
present a case of nasal NHL accompany with nasal myiasis,
which fails to make an accurate diagnosis in early stage.

Case Report
A 79-year-old man presented to the outpatient department of
Otolaryngology in Luoding People’s Hospital in September
2020 complaining of persistent nasal obstruction, purulent dis-
charge, and weight loss for about 6 months. We found much
purulent and bloody secretions and a gray-red neoplasm which
was anabrotic on the surface and easy to bleed when being
touched in the left nasal cavity by endoscopy. The mucosa of
the nasopharynx was smooth in this patient (Figure 1). And
then nasal and sinus computed tomography (CT) scan and
biopsy were carried on this patient. Computed tomography
showed a slight thickening of the left nasopharyngeal wall, and
unknown dense shadow in the left nasal cavity, and bilateral
nasosinusitis (Figure 2). The subsequent biopsy result sug-
gested that the specimen was a small amount of necrotic tissue. Figure 2. Slight thickening of the left nasopharyngeal wall, and unknown
dense shadow in the left nasal cavity, and bilateral nasosinusitis.
After anti-infective therapy of 9 days in the outpatient depart-
ment, the patient still showed no improvement and then was
hospitalized in the Department of Otolaryngology in Luoding be alleviated very well. Postoperatively, the patient returned to
People’s Hospital. the hospital regularly for nasal endoscopy examination and
Physical examination showed no significant lymphadenec- regular medication that included oral antibiotic, prednisone,
tasis in the whole body. Chest CT scan and ultrasound of heart eucalyptol enteric-coated tablets, and intranasal glucocorticoid.
and abdomen also showed no significant lymphadenectasis. About one month after surgery, this patient came to our
HIV test showed negative. And Enterobacter cloacae was hospital for reexamination due to high fever. By nasal endo-
found in the left nasal cavity. Bilateral sinus opening operation scopy examination, the patient presented with a nasal myiasis
under nasal endoscope was performed in this patient after the infestation (Figure 3) and was immediately hospitalized again.
contraindications to surgery were excluded. During the opera- The removal of crawling maggots was performed with the help
tion, we performed a biopsy of the neoplasm deeply in the left of forceps under nasal endoscopy. More than 100 larvae were
nasal cavity again. But the pathological examination result withdrawn. And another bacteria Escherichia coli was found in
showed necrotic tissues once again. After anti-infective therapy the left nasal cavity. The level of LDH(lactate dehydrogenase)
and intravenous dripping of glucocorticoids for 3 days, this was 440 U/L, while the normal level was 114 to 240 U/L.
patient was discharged after improvement of nasal obstruction, Systemic treatment using intravenous dripping ceftriaxone
but the symptoms of bloody and purulent rhinorrhea could not (1000 mg bid), metronidazole(0.5 g every 8 hours) and
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this patient still died on the day. The subsequent biopsy result
showed the neoplasm of the left nasal cavity was NHL (Figure
4).

Discussion
Myiasis is a disease caused by fly larvae (maggots) parasitic on
human and vertebrate host tissues or organs, which usually
occurs in areas with poor sanitary conditions.12 The common
infection locations of myiasis include eye, ear, nose, vagina,
urethra, colon, and so on. Although the distribution of this
disease is worldwide,13,14 nasal myiasis is rare in our country,12
not to mention nasal NHL accompany with nasal myiasis.
Nasal myiasis is not difficult to diagnose, and the basis of
diagnosis is that the maggots are found in the nasal cavity or
nasopharynx. The signs and symptoms of nasal myiasis include
nasal and/or facial pain, bloody or mucopurulent nasal secre-
tion, epistaxis, foul smell, and anosmia, which are usually
related to the presence and movement of the larvae.13,15 The
surfaces of maggots carry some bacteria that may cause nasal
and nasopharynx infection. The nasal cavity is close to the
Figure 3. The black arrow showed the maggots in the left nasal cavity.
sinuses, eyeballs, meninges, and skull. Once the fly maggots
migrate into and invade these position, they may lead to serious
consequences such as purulent meningitis, even death.16 Endo-
scopic removing maggots, nasal irrigation, anti-infective ther-
apy, and the treatment of the primary disease are the main
treatments for nasal myiasis. It’s reported that the risk factors
of myiasis are open wounds, scabs, suppurative lesions, and
ulcers contaminated with secretions and bloody remnants.17
In this case, we suppose the nasal smelly secretions, which
exist in this patient with nasal NHL, attract flies to drill into
nasal cavity and lay eggs, and then lead to larva accidental
parasitism. We can find other nasal myiasis cases with other
primary diseases.15,17,18 Therefore, chronic wasting diseases
may be important risk factors for nasal myiasis.
The staging of HL and NHL (Ann Arbor Classification) are
as follows. Stage I includes one node (I) or single extranodal
lesion without nodal involvement (IE). Stage II includes 2 or
more nodal groups on the same side of the diaphragm (II), or
single extranodal lesion with adjacent nodes involvement, with
Figure 4. Large necrosis was observed in this neoplasm tissue. A few or without other nodal groups on the same side of the dia-
lymphocytes were observed locally, of which morphology was rela-
phragm involvement (IIE). Stage III includes nodes groups
tively simple. The chromatin of lymphocytes was deeply stained, while
the nucleoli were not obvious, and the cytoplasm was small. The on both sides of the diaphragm (III), or with limited related
pathological diagnosis was considered as non-Hodgkin’s lymphoma of extranodal lesions involvement (IIIE), or with spleen involve-
the left nasal cavity. ment (IIIS), or with both involvements (IIIEþS). Stage IV
includes diffuse extranodal lesion involvement, with or without
lymphadenectasis, or single extranodal lesion involvement
defervescence drugs for 10 days was also performed. Where- with distant lymphadenectasis.19,20 According to this staging
after, the nasal myiasis infestation was completely resolved. classification, this case that we report belongs to the stage IE.
However, the patient continued to have recurrent fever. Subse- Although the stage IE of NHL usually has a bad prognosis, it’s
quently, the patient was transferred to Guangdong Provincial reported that the median survival for the stage IE of this disease
People’s Hospital for further treatment and received a third is 7 years and 9 months after active treatments.21 However, this
biopsy of the left nasal mucosa. About 2 hours after the biopsy, patient died for massive nasal bleeding about only 8 months
the patient had severe nasal bleeding and cardiac and respira- after the onset, which was significantly lower than that of
tory arrest. Although active rescue treatments were performed, above.
4NP594 Ear, NoseEar, Nose &Journal
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One reason also the most important reason is that we fail to References
make an accurate diagnosis in the early stage of this disease, 1. Rabkin CS, Devesa SS, Zahm SH, Gail MH. Increasing incidence of
which results in failure to receive the appropriate treatment in non-Hodgkin’s lymphoma. Semin Hematol. 1993;30(4):286-296.
time such as combination chemotherapy, and so on. It’s 2. Salplahta D, Comanescu MV, Anghelina F, Ionita E, Mogoanta
reported to be a diagnostic challenge for extranodal NK/T cell CA, Anghelina L. Non-Hodgkin lymphomas of Waldeyer’s ring.
lymphoma.22 Although we perform 2 biopsies in the first treat- Rom J Morphol Embryol. 2012;53(4):1057-1060.
ment hospital, we both get 2 negative false results. Too much 3. Kim GE, Koom WS, Yang WI, et al. Clinical relevance of
necrotic tissues in this patient of nasal NHL lead to the failure three subtypes of primary sinonasal lymphoma characterized
of biopsies. Biopsy in non-necrotic areas after adequately by immunophenotypic analysis. Head Neck. 2004;26(7):
removing necrotic tissue is vital to improve the diagnostic 584-593.
efficiency of nasal NHL. Nasal NHL cells are deemed to infil- 4. Mukaratirwa S, van der Linde-Sipman JS, Gruys E. Feline nasal
trate along the walls of blood vessels,23 which might be a and paranasal sinus tumours: clinicopathological study, histomor-
potential cause of massive nasal bleeding afterward. And the phological description and diagnostic immunohistochemistry of
concomitant nasal myiasis not only confuses the diagnosis but 123 cases. J Feline Med Surg. 2001;3(4):235-245.
also aggravates the inflammation of nasal cavity and nasophar- 5. Vidal RW, Devaney K, Ferlito A, Rinaldo A, Carbone A. Sino-
ynx. Two different bacterial infections have been found suc- nasal malignant lymphomas: a distinct clinicopathological cate-
cessively in the nasal cavity of this patient. Maggots might be gory. Ann Otol Rhinol Laryngol. 1999;108(4):411-419.
the intermediate host of these bacteria. As it’s mentioned in 6. You JY, Chi KH, Yang MH, et al. Radiation therapy versus che-
other case report, myiasis patients have bacterial infection.24 motherapy as initial treatment for localized nasal natural killer
Maggots could eat and damage tissues of nasal cavity during (NK)/T-cell lymphoma: a single institute survey in Taiwan. Ann
parasitism, which might be another reason for massive nasal Oncol. 2004;15(4):618-625.
bleeding of this patient. 7. Au WY, Weisenburger DD, Intragumtornchai T, et al. Clinical
Another reason is probably that the Ann Arbor classification differences between nasal and extranasal natural killer/T-cell
system is less accurate in predicting the prognosis of patients lymphoma: a study of 136 cases from the international per-
with aggressive NHL.25 International Prognostic Index (IPI) ipheral T-cell lymphoma project. Blood. 2009;113(17):
seems to be more suitable for identification, which is based 3931-3937.
on age, tumor stage, serum LDH level, performance status, and 8. Lima M. Aggressive mature natural killer cell neoplasms: from
the number of extranodal lesions sites. The IPI identifies 4 risk epidemiology to diagnosis. Orphanet J Rare Dis. 2013;8:95.
groups with predicting 5-year survival rates of 73%, 51%, 43%, 9. Li YX, Liu QF, Fang H, et al. Variable clinical presentations of
and 26%.25 In this case, the patients is older than 60 years, and nasal and Waldeyer ring natural killer/T-cell lymphoma. Clin
the serum LDH level is 1.2 times more than normal, and the Cancer Res. 2009;15(8):2905-2912.
performance status is classified as 2, and he has B symptoms 10. Lisowska G, Zieba N, Stryjewska-Makuch G, Scierski W,
that include temperature >38.3  C and the loss of more than Miskiewicz-Orczyk K, Misiolek M. Natural killer (NK)//T-
10% of body weight recently. The IPI of this patient is 3, which cell lymphoma, nasal type, with periorbital involvement: a
is considered as a high-medium risk. It indicates this patient has case report and literature review. Am J Case Rep. 2020;21:
a bad prognosis. e926599.
11. Wong D, Parry LA, Bloch AE, Agar N. Extranodal NK/T cell
Conclusion lymphoma, nasal type, with retrobulbar extraconal phlegmon and
naso-oral fistula. BMJ Case Rep. 2019;12(3):e227160.
Any nasal inflammation of unknown etiology, especially with 12. Shao-gang LI, Zhao-yong WU, Jing-yi LI. Four cases of Myiasi-
nasal mucosa necrosis, should not be ignored the possibility of sin Beijing and review of literature. J Clin Exp Med. 2018;17(14):
nasal NHL. It’s very necessary to repeated biopsies for accurate 1558-1561.
diagnosis. Specific infections such as nasal myiasis might 13. Francesconi F, Lupi O. Myiasis. Clin Microbiol Rev. 2012;25(1):
occur on basis of nasal NHL. 79-105.
14. Salmanzadeh S, Rahdar M, Maraghi S, Maniavi F. Nasal myiasis:
Declaration of Conflicting Interests a case report. Iran J Public Health. 2018;47(9):1419-1423.
The author(s) declared no potential conflicts of interest with respect to 15. Serafim RA, Do ESR, de Mello R, Collin SM, Deps PD. Case
the research, authorship, and/or publication of this article. report: nasal myiasis in an elderly patient with atrophic rhinitis
and facial sequelae of leprosy. Am J Trop Med Hyg. 2020;102(2):
Funding 448-450.
The author(s) received no financial support for the research, author- 16. White ZL, Chu MW, Hood RJ. Nasal myiasis: a case report. Ear
ship, and/or publication of this article. Nose Throat J. 2015;94(7):E24-E25.
17. Lubis RR, Albar MY, Darlan DM. Massive orbital myiasis arising
ORCID iD from nasal myiasis in an Indonesian patient with diabetes. Am J
Jing Ou https://orcid.org/0000-0003-3583-3566 Ophthalmol Case Rep. 2019;13:147-150.
Ou and Huang
Ou and Huang NP5955

18. Katabi A, Aguirre M, Obeidat Y, Al-Ourani M, Assad S, Zeid F. 22. Gomes PS, Caselhos S, Vide AT, Fonseca R. Extranodal natural
Nasal myiasis in myasthenic crisis, a case report and literature killer/T cell lymphoma, nasal type: a diagnostic challenge. BMJ
review. Respir Med Case Rep. 2020;31:101212. Case Rep. 2019;12(11):e232404.
19. Carbone PP, Kaplan HS, Musshoff K, Smithers DW, Tubiana M. 23. Zhang YJ, Hu WH, Liu H, et al. Clinical features and prognosis of
Report of the committee on Hodgkin’s disease staging classifica- nasal type NK/T cell lymphoma [in Chinese]. Zhonghua Zhong
tion. Cancer Res. 1971;31(11):1860-1861. Liu Za Zhi. 2006;28(1):50-53.
20. Smithers DW. Summary of papers delivered at the conference on 24. Uysal S, Ozturk AM, Tasbakan M, et al. Human myiasis in
staging in Hodgkin’s disease (Ann Arbor). Cancer Res. 1971; patients with diabetic foot: 18 cases. Ann Saudi Med. 2018;
31(11):1869-1870. 38(3):208-213.
21. Hu W, Chen M, Luo F. Multivariate analysis of prognosis of patients 25. International Non-Hodgkin’s Lymphoma Prognostic Factors
with stage IE non-Hodgkin’s lymphomas of the nasal cavity [in Project. A predictive model for aggressive non-Hodgkin’s lym-
Chinese]. Zhonghua Zhong Liu Za Zhi. 2001;23(3):240-243. phoma. N Engl J Med. 1993;329(14):987-994.