Endoscopic Lacrimal Silicone Tube Intubation in Patients with Primary Acquired Nasolacrimal Duct Obstruction: A Retrospective Study

doi:10.21203/rs.3.rs-4829423/v1

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Endoscopic Lacrimal Silicone Tube Intubation in Patients with Primary Acquired Nasolacrimal Duct Obstruction: A Retrospective Study

https://doi.org/10.21203/rs.3.rs-4829423/v1

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Background: A lacrimal endoscope is the only instrument that can be used to observe the luminal side of the lacrimal duct. Lacrimal tube intubation (LTI) surgery using a lacrimal endoscope is less invasive than a dacryocystorhinostomy. However, in LTI surgery for PANDO, the risk factors for poor outcomes although it remains unclear. This study aimed to determine the outcomes and risk factors of primary acquired nasolacrimal duct obstruction (PANDO) treated with LTI.

Methods: This retrospective study was performed at Saitama Medical University Hospital. We enrolled 102 patients (75 females; mean age 72.1±9.0) who were diagnosed with unilateral PANDO and underwent LTI surgery using lacrimal endoscope between August 2016 and January 2020. Preoperatively, the lacrimal pathways were washed with a normal saline solution and samples obtained were cultured. The obstruction sites in the lacrimal pathway were determined endoscopically. Eight weeks after LTI, samples obtained from a piece of the removed lacrimal tube were cultured. We identified the bacterial cultures observed before and after the surgery. We examined risk factors for re-occlusion in patients with PANDO during the first 6 months after surgery.

Results: Ninety-four (92.2%) sides successfully passed the lacrimal syringing test 6 months after surgery. In univariate and multivariate analyses, the risk factors for lacrimal duct re-occlusion were diabetes mellitus (p=0.02, 0.04, respectively) and the presence of granulomatous changes on endoscopy (p<0.001, 0.02, respectively). All 11 patients with PANDO and diabetes mellitus had positive lacrimal tube culture results.

Conclusion: LTI failure was more common in patients with diabetic complications or when granulation was observed on lacrimal duct endoscopy.

bacterial population

dacryoendoscope

diabetes mellitus

lacrimal obstructive disease

lacrimal endoscope

lacrimal tube intubation

nasolacrimal duct obstruction

Obstruction or stenosis of the nasolacrimal system causes epiphora; therefore, topical antibiotics or surgical treatment may be selected. Dacryocystorhinostomy (DCR) restores tear drainage by bypassing blockage in the nasolacrimal duct through the creation of a bony ostium and is the main treatment options for patients with primary acquired nasolacrimal duct obstruction (PANDO). Lacrimal tube intubation (LTI) was first introduced by Keith (1) who used this technique as an alternative to DCR in patients with PANDO; LTI has since become an established alternative treatment option. In recent years, combined lacrimal duct endoscopy has been used and its success rate has been improving. The reported success rate of LTI in patients with PANDO ranges from 40–97%.(2–7) The timing of the tube removal is reportedly between 1 week and various years, with 2–6 months post-intubation being the most common removal period.(6–9) In DCR surgery, previous studies have suggested that inflammation and postoperative infection, such as Pseudomonas spp. Infection,(10) lacrimal scarring,(11) and fibrosis due to prolonged silicone intubation (10, 11) might be associated with surgical failure. Additionally, surgical failure is associated with old age,(12) allergy to medications,(13) prior ocular surgery (13) and a history of diabetes mellitus.(12, 13)

However, in LTI surgery for PANDO, it has been reported that older age (14) and Pseudomonas spp. infection of the silicone tube (15) are risk factors for poor outcomes although it remains unclear what other patient characteristics may be involved. This study aimed to examine the outcomes and risk factors of LTI surgery performed using a lacrimal endoscope.

This retrospective study was approved by the Ethics Committee of Saitama Medical University Hospital (20091.01) and was conducted in accordance with the provisions of the Declaration of Helsinki. All the participants provided written informed consent for the surgical procedure. The need for informed consent pertaining to study enrollment was waived by the Ethics Committee of Saitama Medical University owing to the retrospective design of the study.

A total of 102 patients (75 females; mean age 72.1 ± 9.0 years; age range, 57 to 89 years) who were diagnosed unilateral PANDO and underwent LTI surgery using lacrimal endoscope between August 2016 and January 2020 were included. Patients with a history of paranasal sinus injury, eyelid trauma, or bilateral PANDO were excluded. No patient had any history of acute dacryocystitis or functional nasolacrimal duct obstruction. All the patients were diagnosed with unilateral lacrimal passage obstruction. The demographic and clinical characteristics of the patients, including age, sex, systemic and ocular medical histories, and systemic and local predisposing factors, were collected from their medical records.

The diagnosis of lacrimal passage obstruction was based on a lacrimal syringing test and endoscopic examination. The detailed diagnostic procedure was as follows. First, using a 23G Nakamura’s lacrimal washing single-sized needle (Inami, Tokyo, Japan) filled with saline solution, the lacrimal pathway was washed to determine whether it was obstructed. We washed the lacrimal pathway with a normal saline solution and cultured the reflux from the lacrimal pathway (preoperatively). Lacrimal obstructive disease was diagnosed when saline solution did not reach the nasal cavity. After anesthetizing the lacrimal duct with 2% lidocaine, a lacrimal endoscope (Fibertech, Chiba, Japan) was inserted into the lacrimal duct to confirm the obstruction location. Based on previous reports, endoscopic findings were described as follows: mucus, fibrotic membrane, stones, and granulation.(16, 17)

In all patients, lacrimal surgery was performed to perforate the obstruction using a lacrimal endoscope and to intubate the lacrimal pathway. LTI was performed as described previously.(7) LTI surgery was successful in all cases. For intubation, we used LACRIFAST® (Kaneka Medical Products, Osaka, Japan) with a lacrimal tube. After lacrimal surgery, the lacrimal pathway was syringed with normal saline every 2 weeks to prevent occlusion and lacrimal tube infection for 8 weeks. All patients received topical 0.3% gatifloxacin and 0.1% fluorometholone four times a day for 8 weeks. Eight weeks later, the lacrimal tube was removed by syringing through the lacrimal pathway. The extracted lacrimal tube was divided into three parts based on the distance from the punctal portion immediately after removal: up to 20 mm (from the puncta to the lacrimal sac), up to 40 mm (in the nasolacrimal duct), and > 40 mm (in the nasal cavity). The second sample (postoperative culture) was cultured. We evaluated the outcome of the procedure 6 months after the surgery. Surgical “success” was defined as successful fluid irrigation of the lacrimal pathway without reflux. Surgical “failure” was defined as the absence of fluid in the nasal cavity during irrigation of the lacrimal pathway.

All statistical analyses were performed using the JMP version 12® (SAS Institute, Tokyo, Japan). All data are expressed as means ± standard deviation. The Mann–Whitney U test was used to compare the mean age between the LTI surgery success and failure groups. Fisher’s exact test was used to compare sex distribution, history of lacrimal surgery, allergic conjunctivitis, hypertension, and diabetes mellitus rates, and lacrimal endoscopy findings. It was also used to determine the bacterial detection rate before and after surgery. A logistic regression model was used to calculate the adjusted odds ratio with a 95% confidence interval (CI) for patient-and lacrimal endoscopy finding-related risk factors associated with LTI failure. A multivariate logistic regression model was used to adjust for all the potential confounding factors. Statistical significance was set at p < 0.05.

Table 1 shows patient characteristics. A total of 94 (92.2%) patients had surgical success and 8 (7.8%) had surgical failure. None of the patients with surgical failure passed the lacrimal syringing test 6 months after surgery. Six patients exhibited reflex discharge during the lacrimal syringe test. The mean age, sex distribution, history of lacrimal surgery, and allergic conjunctivitis rates were comparable between the success and failure groups. The incidence rates of hypertension and diabetes mellitus were significantly higher than surgical failure group than success group (p = 0.005, 0.03, respectively). The rates of lacrimal endoscopy and granulation of the nasolacrimal duct were significantly higher than those in the surgical failure group than success group (p = 0.004); four non-diabetic patients had stones on lacrimal endoscopy, and all of them were in the success group.

Table 1

Basic patient characteristics
Charanteristics	Success (n = 94)	Failure (n = 8)	p-value
Age	71.9 ± 8.9	74.0 ± 10.6	*0.39
Sex
Male (n = 27)	26	1	^†0.67
Female (n = 75)	68	7	^†0.67
History of lacrimal surgery (n = 14)	13	1	^†1.00
Allergic conjunctivitis (n = 16)	13	3	^†0.10
Hypertension (n = 28)	22	6	^†0.005
Diabetes (n = 11)	8	3	^†0.03
Finding of lacrimal endoscopy
mucos (n = 28)	24	4	^†0.21
granulation (n = 11)	7	4	^†0.004
false passage (n = 10)	9	1	^†0.58
*Mann-Whitney U ^†Fisher's exact test

Table 2 shows the results of multivariate analyses of risk factors for surgical outcomes. The mean age, sex distribution, history of lacrimal surgery, allergic conjunctivitis, and hypertension rates were comparable between the LTI success and failure groups. Patients with PANDO and diabetes mellitus were more likely to have failed LTI compared to their counterparts without diabetes mellitus (p = 0.04). The lacrimal endoscopy and nasolacrimal duct granulation rates were significantly higher than those in the surgical failure group than success group (p = 0.02). Sub-analysis was performed for patients with diabetes, revealing no differences in blood glucose (before and 2 h after a meal) and hemoglobin A1c levels, or in antidiabetic drug use, between the successful and failed LTI surgery groups (Table 3). None of the patients with diabetes mellitus received insulin injections. The odds ratio for LTI failure in patients with PANDO and diabetes mellitus was 11.67 (95% CI: 1.21–112.51, p = 0.04). In the finding of lacrimal endoscopic surgery, the odds ratio for failure of LTI surgery with mucosa, false passages of lacrimal pathway, and formation of granulation were 1.04, 2.61, 17.94, respectively (Table 4).

Table 2

Results of univariate and multivariate
Charanteristics	Univariate		Multivariate
	95%CI	p-value	95%CI	p-value
Age	-0.12–0.05	0.53	-0.01–0.01	0.88
Female	-0.40–1.97	0.31	-0.39–0.49	0.43
History of lacrimal surgery	-1.54–0.85	0.91	-3.35–0.32	0.36
Allergic conjunctivitis	-1.63–0.75	0.79	-0.70–2.88	0.16
Hypertension	0.07–1.63	0.03	-0.90–1.41	0.54
Diabetes	0.07–1.72	0.02	0.19–3.49	0.04
Finding of lacrimal endoscopy
mucos	0.68–12.58	0.13	-3.27–0.80	0.43
granulation	2.55–60.67	< 0.001	0.99–5.93	0.02
false passage	0.12–12.24	0.79	-0.82–2.95	0.54
CI: confidence interval

Table 3

Profile of diabetes mellitus before the lacrimal tube insertion surgery
	Univariate p-value	Multivariate p-value
Blood glucose
Before the meal	0.23	0.62
2 hours after meal	0.62	0.44
HbA1c	0.23	0.29
Use of antidiabetic drug	0.48	0.55

Table 4

Odds ratio of risk factor
	Univariate		Multivariate
	Odds ratio (95%CI)	p-value	Odds ratio	p-value
Diabetes mellitus	6.45(1.30-32.08)	0.04	11.67(1.21-112.51)	0.04
Hypertension	9.82(1.85–52.2)	0.001	1.91(0.24–15.14)	0.54
Findings of lacrimal endoscope
mucos	2.91(0.68–12.58)	0.13	1.04(0.10-11.03)	0.70
granulation	12.42(2.55–60.67)	< 0.001	17.94(1.49-215.31)	0.02
false passage	1.34(0.115–12.24)	0.79	2.61(0.12–58.64)	0.54
CI: confidence interval

Table 5 shows the bacterial species detected pre- and postoperatively. In the successful LTI group, Staphylococcus epidermidis, Streptococcus oralis, Corynebacterium spp. and Candida parapsilosis were the most common bacterial species detected postoperatively (p < 0.001, 0.007, < 0.001, < 0.001, respectively). In this group, the rate of bacteria detected postoperatively was significantly lower than that detected preoperatively (p = 0.03). Table 6 shows the results of bacterial cultures obtained from patients with and without diabetes mellitus. In patients without diabetes mellitus, S. epidermidis, S. oralis, Corynebacterium spp., and C. parapsilosis were the most commonly detected species postoperatively (p < 0.001, 0.003, 0.003, and 0.001, respectively). In the diabetes mellitus group, the number of bacteria detected postoperatively was comparable to that detected pre-operatively (p = 0.13). However, all patients had positive postoperative cultures.

Table 5

Result of bacterial culture pre and post lacrimal surgery
	Failure (n = 8)			Success (n = 94)
	Pre operative	Post operative	p-value (pre vs post)	Pre operative	Post operative	p-value (pre vs post)
Staphylococcus aureus	1	1	1.00	12	13	0.83
Staphylococcus epidermidis	3	1	0.24	30	7	< 0.001
Streptococcus anginosus	1	0	0.30	1	0	0.32
Streptococcus oralis	0	1	0.30	0	7	0.007
Corynebacterium spp	2	1	0.52	10	29	< 0.001
Serratia marcescens	0	0		1	0	0.32
Moraxella catarrhalis	0	0		1	0	0.32
Pseudomonas aeruginosa	0	0		2	0	0.16
Haemophilus influenzae	0	0		2	0	0.16
Klebsiella oxytoca	0	1	0.30	1	0	0.32
Candida parapsilosis	0	1	0.30	1	15	< 0.001
No detective	1	2	0.52	32	19	0.03
Fisher’s exact test was used for the bacterial detection rate

Table 6

Result of bacterial culture with and without diabetes mellitus
	With diabetes mellitus			Without diabetes mellitus
	Pre operative	Post operative	p-value (pre vs post)	Pre operative	Post operative	p-value (pre vs post)
Staphylococcus aureus	3	2	0.54	10	12	0.64
Staphylococcus epidermidis	1	0	0.30	32	8	< 0.001
Streptococcus anginosus	1	0	0.30	1	0	0.32
Streptococcus oralis	0	0		0	8	0.003
Corynebacterium propinquum	3	6	0.19	9	24	0.003
Serratia marcescens	0	0		1	0	0.31
Moraxella catarrhalis	0	0		1	0	0.31
Pseudomonas aeruginosa	1	0	0.30	1	0	0.31
Haemophilus influenzae	0	0		1	0	0.31
Klebsiella oxytoca	0	1	0.31	1	0	0.31
Candida parapsilosis	0	2	0.13	1	14	< 0.001
No detective	2	0	0.13	31	21	0.10
Fisher’s exact test was used for the bacterial detection rate

In this study, the rate of LTI surgical failure was increased in patients with diabetes mellitus and granulation observed on lacrimal endoscopy. All patients with PANDO and diabetes mellitus had positive postoperative cultures.

In this study, diabetes mellitus was associated with an increased risk of LTI surgical failure. In previous reports, surgical failure of endoscopic DCR was associated with old age,(12, 18) allergy to medications,(13) duration of symptoms,(18) duration of intubation,(19) pre-existing sinus or nasal abnormalities,(20) previous trauma or nasal surgery,(18) prior ocular surgery,(13) and a history of diabetes mellitus.(12, 13)

In this study, older age was not a risk factor for surgical failure. A previous study divided participants into those aged 50–60 years (18) and those aged ≥ 61 years.(12) In the present study, none of the patients with PANDO and diabetes mellitus, and only three patients without diabetes mellitus, were younger than 61 years. The age distribution in the study sample precluded meaningful analyses for the effects of age on the risk of LTI failure. The large proportion of older adults included in this study may be due to the fact that LTI can be performed under local anesthesia, making it more accessible to older patients, compared to DCR, which requires general anesthesia. A previous study reported that LTI is associated with older age in patients with lacrimal stenosis.(14) However, the average age in the previous study was 59.68 ± 10.7 years (range, 21 to 87 years); in the present study patients were older.

In previous reports, hypertension (41.06%) was the most common systemic disease comorbid with PANDO, followed by neoplasms (18.74%), and diabetes mellitus (10.90%).(21) Two previous studies suggested that diabetes mellitus was a risk factor for re-obstruction after DCR surgery.(12, 13) First, slow wound healing in patients with diabetes mellitus may increase the risk of granulation and scar tissue formation at the osteotomy site, disrupting the natural healing process of the osteotomy edges in DCR surgery, leading to osteotomy obstruction.(13) Second, diabetes mellitus predisposes patients to wound ulceration and other chronic diseases, while a hyperglycemic state impairs both fibroblast and endothelial cell functions, involved in granulation tissue organization and wound vascularization. Chronic non-healing wounds are common among patients with diabetes mellitus owing to impaired blood flow, pericyte loss, and decreased vascularization.(22, 23) Overall, poor wound healing may cause prolonged inflammation and mucosal changes. In this study, the endoscopic findings indicated that lacrimal granulation and inflammation were the leading risk factors for surgical failure. Inflammation after LTI surgery may be caused either by bacterial contamination or mechanical stress induced by the tube. Silicone tube intubation does not induce significant histopathological changes of the lacrimal sac.(24) However, Kim et al. (25) reported that if the inflammation is not controlled after LTI, removal of the silicone tube should be performed, as the silicone tube itself can induce an inflammatory reaction and stimulate granulation tissue. Moreover, in patients with chronic dacryocystitis, chronic inflammation with fibrosis is the most common histopathological finding in biopsies of the lacrimal sac wall.(26) Severe fibrosis caused by inflammation can make re-epithelialization more difficult, even when properly reconstructed.(7) Linberg et al. (27) suggested that a long duration of PANDO causes severe and irreversible anatomical changes in the entire duct, causing difficulties in reconstruction and remodeling. In a review article, diabetes mellitus was associated with increased inflammatory biomarker levels and increased risk of diabetes complications.(28) Additionally, signs of inflammation, such as conjunctival injection and discharge of pus around the silicone tubes and puncta after LTI, may increase the risk of surgical failure.(25) Kim et al. (25) reported that in the cases of systemic or ocular diseases that can induce inflammation, special postoperative care is needed. We speculate that inflammation and mucosal damage caused by mechanical stress from tubing, as well as diabetes-related inflammation, can lead to re-obstruction of the nasolacrimal duct.

Lacrimal endoscopy enables the determination of the exact site and extent of obstruction anywhere along the lacrimal drainage system by allowing direct visualization of the passage. The presence of mucus, debris, stones, edema, or fibrosis can lead to the narrowing or complete obstruction of the lacrimal drainage system.(25) Lacrimal endoscopic findings revealed that obstruction in the nasolacrimal duct could be caused by secretory substances, such as mucus and stones, as well as structural changes, such as fibrotic membranes and stenosis.(16, 17) The success rate of the secretory group was significantly lower than that of the structural group.(17) In the present study, granulation was identified as a risk factor for secretory changes. It has been reported that in patients with PANDO with false passages, lacrimal endoscopy-guided silicone tube intubation is safer and more effective.(16) In this study, false passages on lacrimal endoscopy were not a risk factor for surgical failure. Lacrimal endoscopy allows direct confirmation of findings and is considered a useful tool for performing surgery and for predicting prognosis.

In the present study, S. epidermidis was detected less frequently after surgery in the surgical success group. The detection rates of S. oralis, Corynebacterium spp., and C. parapsilosis increased postoperatively, compared to pre-operatively, and we suppose that S. oralis and C. parapsilosis were derived from the nasal cavity. We assumed that topical gatifloxacin administration effectively reduced S. epidermidis contamination, but that the Corynebacterium spp. may be resistant to this drug. In this study, all Corynebacterium spp. detected in the tube samples were resistant to quinolone antibiotics. Previous studies have suggested that postoperative infection and inflammation, especially Pseudomonas spp. infection,(10, 15) might affect the outcomes of nasolacrimal surgery. Moreover, the isolation of P. aeruginosa from silicone tube biofilms is associated with a high rate (50%) of surgical failure.(29) In the in vitro experiments, only S. aureus and P. aeruginosa formed biofilms after 12 weeks on silicon tubes incubated in culture media containing various bacteria.(30) The detection of P. aeruginosa in postoperative lacrimal tubes is considered a risk factor for surgical failure. P. aeruginosa was not detected in this study. All patients with diabetes had positive postoperative cultures. Patients with diabetes are also susceptible to infection within the orbit,(31) so residual bacteria in the tear ducts may have prolonged the inflammation and granulation of the lacrimal mucosa.

The present study has certain limitations. First, the retrospective and single-center design limited our ability to draw definitive conclusions regarding risk factors for LTI surgery. Diabetes mellitus was a risk factor of LTI re-obstruction. However, the duration of diabetes mellitus could not be considered due to the retrospective nature of the study. The duration of diabetes mellitus may affect outcomes in this patient group by affecting the duration and extent of inflammation of the lacrimal mucosa. It has been reported that the duration of PANDO is a risk factor for surgical failure in DCR surgery,(18) but the duration of symptoms could not be considered in this study. Second, there was selection bias in patients with diabetes mellitus. Patients with diabetes and good glycemic control were selected for this study because surgery was not performed in patients with poor glycemic control. None of the included patients received insulin injections. Therefore, hemoglobin A1c and blood glucose levels before and 2 h after meals were comparable in the surgical success and failure groups in this study. Third, the postoperative observation period was 6 months, reducing our ability to assess the long-term outcomes. A long-term prospective multicenter study is needed to validate these results.

We demonstrated that the surgical failure rate of LTI was increased in patients with PANDO and diabetes mellitus or granulation observed on lacrimal endoscopy. Lacrimal endoscopy allows direct confirmation of findings and is a useful tool not only for surgery, but also for predicting LTI outcomes.

Dacryocystorhinostomy, DCR, Lacrimal tube Insertion, LTI, primary acquired nasolacrimal duct obstruction, PANDO.

Ethics approval and consent to participate

This study was performed in accordance with the Declaration of Helsinki and was approved by the ethical committee of the Saitama Medical University. All the participants provided written informed consent for the surgical procedure. The need for informed consent pertaining to study enrollment was waived by the Ethics Committee of Saitama Medical University owing to the retrospective design of the study.

Consent for publication

Not applicable

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Funding

No funding was received by any of the authors for the writing of this manuscript.

Acknowledgements

We would like to thank Honyaku Center Inc. for English language editing.

Author contributions

Conceptualization, S. I.; methodology, S. I.; software, S. I.; validation, S. I. and K. S.; formal analysis, S. I., S. T., and K. S.; investigation, S. I.; resources, S. I.; data curation, S. I. and S. T.; writing—original draft preparation, S. I.; writing—review and editing, S. I. and S. T.; visualization, S. I.; supervision, S. T. and K. S.; project administration, K. S. All authors have read and agreed to the published version of the manuscript.

Competing Interests

The authors declare no conflicts of interest regarding the publication of this article.

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No competing interests reported.

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Endoscopic Lacrimal Silicone Tube Intubation in Patients with Primary Acquired Nasolacrimal Duct Obstruction: A Retrospective Study

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