Acupuncture is associated with a positive effect on odour discrimination in patients with postinfectious smell loss—a controlled prospective study

Abstract

Introduction
Smell disorders are common in the general population and occur e.g., after infections, trauma or idiopathically Treatment strategies for smell loss range from surgery, medication to olfactory training, depending on the pathology, but they are limited This study examined the effect of acupuncture on olfactory function.

Methods
Sixty patients with smell loss following infections of the upper respiratory tract were included in this investigation Half of the study group were randomly assigned to verum acupuncture and the other half to sham acupuncture Olfaction was measured by means of the “Sniffin’ Sticks” test battery (odour threshold, discrimination and identification).

Results
Compared to sham acupuncture, verum was associated with an improvement of smell function as measured by the TDI score ( p = 0.039) The improvement was largely determined by improvement in odour discrimination, and was significantly better in patients with a shorter duration of the disorder.

Conclusion
The present results suggest that acupuncture is an effective supplementary treatment option for patients with olfactory loss.

Full text

Vol.:(0123456789)
1 3
European Archives of Oto-Rhino-Laryngology (2022) 279:1329–1334
https://doi.org/10.1007/s00405-021-06872-9
RHINOLOGY
Acupuncture isassociated withapositive effect onodour
discrimination inpatients withpostinfectious smell loss—a controlled
prospective study
TanjaDrews1,2 · ThomasHummel1· BettinaRochlitzer1,3· BettinaHauswald1· AntjeHähner1
Received: 5 February 2021 / Accepted: 4 May 2021 / Published online: 25 May 2021
© The Author(s) 2021
Abstract
Introduction Smell disorders are common in the general population and occur e.g., after infections, trauma or idiopathically
Treatment strategies for smell loss range from surgery, medication to olfactory training, depending on the pathology, but
they are limited This study examined the effect of acupuncture on olfactory function.
Methods Sixty patients with smell loss following infections of the upper respiratory tract were included in this investigation
Half of the study group were randomly assigned to verum acupuncture and the other half to sham acupuncture Olfaction was
measured by means of the “Sniffin’ Sticks” test battery (odour threshold, discrimination and identification).
Results Compared to sham acupuncture, verum was associated with an improvement of smell function as measured by the
TDI score (p = 0.039) The improvement was largely determined by improvement in odour discrimination, and was signifi-
cantly better in patients with a shorter duration of the disorder.
Conclusion The present results suggest that acupuncture is an effective supplementary treatment option for patients with
olfactory loss.
Keywords Acupuncture· Smell loss· Olfaction· Sniffin’ sticks
Introduction
Olfactory impairment is common in the general population
and results in a loss of quality of life [1, 2]. While there
are several valid and reliable tools available for the diagno-
sis of olfactory loss, the treatment possibilities of olfactory
dysfunction are limited Causes of smell disorders include
sinunasal diseases, acute infections of the upper respiratory
tract, head trauma, neurodegenerative diseases, medication
including chemotherapy, environmental factors and ageing
[3–5]. In effect, approximately 5% of the population are
estimated to exhibit functional anosmia with the prevalence
being highest in the older population [6, 7].
Treatment strategies for smell loss are related to the cause
of the disorder Particularly effective therapies are available
for chronic inflammation of the upper airway system includ-
ing surgery or topical or systemic anti-inflammatory medica-
tion [8, 9]. Interestingly, in clinical routine topical steroids
are used irrespective of the aetiology [10]. Another effective
method in treating various forms of smell loss is olfactory
training [11]. Systematic, repeated exposure to odours may
lead to an improvement of olfactory function in patients
with post-infectious, posttraumatic and neurodegenerative
smell loss [11–15]. Nevertheless, apart from these treatment
options, therapies for olfactory loss are relatively poorly
developed [16, 17].
Hence, the present study focuses on the treatment of
patients with postinfectious smell loss who represent one of
the largest groups of patients with olfactory disorders with
about 18–45% of patients presenting themselves with smell
loss [1]. Postinfectious smell loss is caused by an infection
of the upper respiratory tract (URTI) that persists after the
* Tanja Drews
Tanja.Drews@uniklinikum-dresden.de
1 Department ofOtorhinolaryngology, Smell andTaste
Clinic, Technische Universität Dresden, Technical
University ofDresden Medical School, Fetscherstrasse 74,
01307Dresden, Germany
2 Department ofOtorhinolaryngology,
Bundeswehrkrankenhaus Berlin, Scharnhorststr 13,
10115Berlin, Germany
3 Klinik Für Augenheilkunde, Städtisches Klinikum Görlitz,
Girbigsdorfer Str 1-3, Görlitz, Germany
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

1330 European Archives of Oto-Rhino-Laryngology (2022) 279:1329–1334
1 3
infection has passed [18]. The exact pathological mechanism
is unclear but its possible lesion sites include damage to
the sustentacular cells or the olfactory receptor neurons in
the mucosa or the olfactory bulb [19, 20]. URTI-associated
smell loss typically occurs after the fifth decade of life and
is seen more frequently in women than in men [18]. About
25% of these patients describe parosmia, possibly due to the
partial loss of olfactory receptors [21]. In addition to olfac-
tory training, treatment strategies include vitamin A nasal
drops or systemic alpha-lipoic acid [22, 23].
Sporadically, acupuncture has been used in postinfectious
olfactory loss [24]. Acupuncture is an important part of tra-
ditional Chinese medicine Those that use needle acupunc-
ture believe that every living being is filled with the energy
“Qi” that flows within the body along meridians on which
the individual acupuncture points are located Diseases are
explained by disruptions in the flow of Qi [25, 26].
The needling of acupuncture points has been shown to be
associated with analgesic and relaxing effects It is, therefore,
not only positive for the body but similarly for the men-
tal state of the patient Needling stimulates nerves, which
results in an activation of the central nervous system [27].
The procedure involves the application of 10–20 needles
to certain cutaneous points, where they remain for about
30min [28]. The points are determined by palpation The
procedure is repeated on different days There should be a
noticeable effect, for example in the form of improvement
of symptoms, after about 8 sessions on different days [29].
Side effects are rare, with only about 3% of treated patients
describing pain, local infections and hematoma [28].
So far there are only a few studies, that will now be
described, that have examined the effect of acupuncture
on smell disorders in a controlled way However, previous
results already indicate a positive effect of this approach
In the study by Vent etal., 15 patients with postinfectious
smell loss were treated with acupuncture and compared
to 15 patients who had been treated with Vitamin B After
10weeks of acupuncture treatment, there was a significant
improvement in smell function in the acupuncture group
compared to the Vitamin B group [30]. However, the signifi-
cance of this study was questioned later [31]. A non-blinded
control condition was used in a study by Dai etal who
reported olfactory improvement in postinfectious patients
after acupuncture compared to a patient group without treat-
ment [32]. Hauswald etal applied acupuncture in the context
of a non-randomized, non-controlled study in a larger group
of patients with various aetiologies of smell loss [33]. They
reported a significant improvement in olfactory function,
especially in postinfectious smell loss Anzinger used laser
acupuncture on healthy subjects in a double-blinded single-
application approach and found a positive, acute effect on
olfaction which was measured using the Sniffin’ Sticks Test
[34]. Furthermore, in a case report smell improvement in
one patient receiving acupuncture treatment was reported,
this was based, however, on self-assessment [35].
The aim of this single-centre, prospective, placebo-con-
trolled, patient-blinded study was to investigate the change
of olfactory function in patients with postinfectious smell
loss following 12 acupuncture sessions, twice per week,
each 30min long Based on previous reports, we expected
that acupuncture has a positive effect on smell function in
postinfectious patients.
Methods
Patients
Sixty subjects were recruited consecutively between August
2012 and February 2013 at the Smell and Taste Clinic of
the Department of Otorhinolaryngology of the TU Dres-
den All patients had received the diagnosis of postinfec-
tious smell loss following a detailed, structured history and
a full otorhinolaryngological examination including nasal
endoscopy [36]. Inclusion and exclusion criteria are listed in
Table1 All participants provided written informed consent
The study was approved by the Ethics Committee of the
Medical Faculty of the TU Dresden (ethics approval number
EK 78,032,012).
Olfactory testing
The “Sniffin’ Sticks” test battery was applied before and
after treatment involving tests for odour threshold, odour
discrimination and odour identification [37]. The sum of
Table 1 Inclusion and exclusion criteria
Inclusion criteria Exclusion criteria
Smell loss directly following an URTI Symptom-free interval
18years of age or older URTI during the study period
Written informed consent Neurological diseases that may impair the sense of smell (e.g Parkinson’s or
Alzheimer’s disease)
Absence of chronic infection of the nasal cavities or sinuses Dermatological problems that may complicate the application of the needles
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

1331European Archives of Oto-Rhino-Laryngology (2022) 279:1329–1334
1 3
the scores from the three subtests resulted in the TDI-score
(Threshold, Discrimination and Identification).
Acupuncture treatment
Subjects were randomly attributed to treatments so that one
half received verum acupuncture and the other half received
sham acupuncture, sham meaning that fake points, rather
than actual acupuncture points were needled Both groups
underwent acupuncture 12 times with approximately 2 ses-
sions per week The acupuncture as well as the sham acu-
puncture consisted of needling specific points using sterile
acupuncture needles This was performed by the same person
in every session, and in every session the same points were
needled.
After completion of the study treatment, patients who
had received the placebo condition were offered the verum
acupuncture following the conclusion of the study.
The points chosen for the verum acupuncture were com-
parable to those used in previous studies and can be seen
in Image 1 [30, 33]. All points were used symmetrically on
both sides of the body.
The points used in the sham acupuncture were the same
points used in the ACUSAR- study [38]. The points used are
listed in Table2.
Statistical analysis
The data were analysed using SPSS 27.0 (SPSS Inc., Chi-
cago, Ill, USA) If not mentioned otherwise, all data are
shown as means ± standard deviation (SD) or numbers (%),
significance level was set at p < 0.05 (two-tailed test) Pear-
son statistics were used for correlational analyses.
Results
Sixty patients, 23 males and 37 females were included in
the study The verum group was comprised of 17 hypos-
mic patients and 13 functionally anosmic patients, the sham
acupuncture group of 2 normosmic, 14 hyposmic and 14
anosmic patients All patients completed the study without
any exception.
No adverse effects were encountered during the acupunc-
ture sessions Descriptive statistics of the patient groups at
baseline are shown in Table3.
When comparing the change of TDI scores before and
after treatment the verum group performed better than the
sham acupuncture group (F = 4.45, p = 0.04) Concern-
ing individual subtests, only odour discrimination was
significantly different between the two groups (F = 9.48,
p = 0.003), but not odour threshold (F = 2.61, p = 0.11) and
odour identification (F = 0.93, p = 0.34) These results can
Image 1 Verum-points on face and ear (Bl 3, LG23, Di 20, NP 12,
Op 16), on the arm (Di 4, Lu 7) and on the leg (MP 6, Ma 44)
Table 2 Verum and placebo acupuncture points
Location Acupuncture Points Points for
sham acu-
puncture
Head Bladder 3 /
Governing Vessel 23 /
Large intestine 20 /
Extra point 12 /
Ear Ear 16 /
Arm Lung 7 Deltoideus
Large intestine 4 Upper Arm
Leg Spleen 6 Thigh 1
Stomach 44 Thigh 2
Back / Back 1
/ Back 2
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

1332 European Archives of Oto-Rhino-Laryngology (2022) 279:1329–1334
1 3
be seen in Fig 1 With regard to a clinically significant
improvement on an individual level, 6 of 30 subjects from
the verum group (20%) exhibited improvement of more
than 5.5 points in the TDI score, whereas only 3 of 30 sub-
jects exhibited improvement in the placebo group (10%)
[39]. While this is not a statistically significant result, it
does deserve mention.
When analysing data across both groups there was a
significant correlation between the change of TDI scores
and the duration of the disease (r = − 0.4, p = 0.001) wit h
Table 3 descriptive statistics
at baseline before treatment;
TDI: summated score from
odour threshold, discrimination,
and identification; standard
deviation in brackets
Verum acupuncture Sham acupuncture p-value
Age in years 63.0 (13.6) 66.3 (10.1) 0.29
duration of smell loss in years 3.9 (4.3) 5.1 (5.3) 0.34
TDI score 17.12 (5.62) 17.47 (6.99) 0.86
Odour Threshold 2.08 (1.68) 2.29 (1.79) 0.84
Odour Discrimination 8.37 (2.53) 8.03 (2.99) 0.75
Odour Identification 6.67 (2.83) 7.13 (3.57) 0.60
Fig 1 Mean differences (scores
after treatment minus scores
before acupuncture) of olfac-
tory test results with Standard
Errors; * shows significant
results
Fig 2 Correlation between
changes in TDI scores and dura-
tion of smell loss
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

1333European Archives of Oto-Rhino-Laryngology (2022) 279:1329–1334
1 3
better outcome in patients with a shorter duration of the
olfactory loss (Fig 2).
Discussion
The present results indicated that acupuncture has a posi-
tive effect on olfactory function in patients with postin-
fectious smell loss We found a significant improvement in
general olfactory performance as well as an improvement
in odour discrimination in verum acupuncture compared
to sham treatment On an individual level, verum acupunc-
ture increased olfactory function in 20% of the subjects
compared to 10% of subjects who had sham acupuncture
Further, the treatment response correlated negatively with
the duration of smell loss—the longer the smell loss the
less likely it was to achieve a positive treatment response
A similar relation between the duration of olfactory loss
and improvement of olfactory function has been reported
several times [15, 40]. Acupuncture appeared to be useful
independently from the patients´ age.
The results of our study confirm some of the findings
of previous studies. The present research tried to avoid
several issues that limited the significance of previous
studies, e.g., lack of a control group, heterogeneous
patient groups, or low case numbers [30, 32–34]. We,
therefore, included a homogenous, thoroughly diag-
nosed patient group with postinfectious smell loss, and
a patient-blinded control condition to minimize possi-
ble bias. The therapy was well accepted by the patients,
which can be seen from the lack of dropouts and the
absence of side effects.
It is interesting to note that odour discrimination, but
not odour threshold, improved in response to acupunc-
ture An explanation could be that odour discrimination
appears to involve higher-level cognitive functions to a
higher degree compared to odour thresholds [41]. Acu-
puncture has previously been shown to have effects on
cognitive function tested with the Mini-Mental State
Examination Test in patients following a stroke [42, 43].
Therefore, it might be hypothesized that acupuncture has
positive effects on the cognitive processing of odours
For example, the outcome of the test might have been
positively modified by different levels of attention and
concentration.
Acupuncture is an important part of traditional Chi-
nese medicine When analysing this form of treatment,
it is important to remember that the classical scientific
proof is difficult to obtain when the foundation of the treat-
ment includes something that evades measurement It is,
however, possible to focus on the effects of the treatment,
which is what was done in this study.
Conclusion
The present results suggest that acupuncture is helpful in
patients with postinfectious olfactory loss. The shorter
the time span between smell loss and treatment, the more
likely it is for the treatment to have a positive effect.
With hardly any negative side effects being described,
acupuncture should be considered as a supplementary
treatment.
Future studies need to determine whether the observed
increase of olfactory sensitivity is temporary or is lasting
for a longer period of time.
Funding Open Access funding enabled and organized by Projekt
DEAL.
Declarations
Conflict of interest The authors declare that they have no conflict of
interest.
Ethical approval The study was carried out in accordance with the
Code of Ethics of the World Medical Association (1964 Declaration of
Helsinki and later amendments) The study was approved by the Ethics
Committee at the Medical Faculty of the TU Dresden (Ethics Approval
No. EK 78032012) The study design was presented to the volunteers
in written form and written informed consent was obtained from each
individual participant.
Informed consent Written informed consent was obtained from each
individual participant.
Open Access This article is licensed under a Creative Commons Attri-
bution 4.0 International License, which permits use, sharing, adapta-
tion, distribution and reproduction in any medium or format, as long
as you give appropriate credit to the original author(s) and the source,
provide a link to the Creative Commons licence, and indicate if changes
were made. The images or other third party material in this article are
included in the article’s Creative Commons licence, unless indicated
otherwise in a credit line to the material. If material is not included in
the article’s Creative Commons licence and your intended use is not
permitted by statutory regulation or exceeds the permitted use, you will
need to obtain permission directly from the copyright holder. To view a
copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/.
References
1. Nordin S, Brämerson A (2008) Complaints of olfactory disor-
ders: epidemiology, assessment and clinical implications. Curr
Opin Allergy Clin Immunol 8(1):10–15
2. Croy I, Nordin S, Hummel T (2014) Olfactory disorders and
quality of life–an updated review. Chem Senses 39(3):185–194
3. Damm M, Temmel A, Welge-Lüssen A etal (2004) Olfactory
dysfunctions Epidemiology and therapy in Germany, Austria
and Switzerland. HNO 52(2):112–20
4. Bernhardson BM, Tishelman C, Rutqvist LE (2007) Chem-
osensory changes experienced by patients undergoing cancer
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

1334 European Archives of Oto-Rhino-Laryngology (2022) 279:1329–1334
1 3
chemotherapy: a qualitative interview study. J Pain Symptom
Manage 34(4):403–412
5. Ogawa T, Rutka J (1999) Olfactory dysfunction in head injured
workers. Acta Otolaryngol Suppl 540:50–57
6. Landis BN, Konnerth CG, Hummel T (2004) A study on
the frequency of olfactory dysfunction. Laryngoscope
114(10):1764–1769
7. Brämerson A, Johansson L, Ek L, Nordin S, Bende M (2004)
Prevalence of olfactory dysfunction: the skövde population-
based study. Laryngoscope 114(4):733–737
8. Fokkens WJ, Lund VJ, Mullol J etal (2012) European Position
Paper on Rhinosinusitis and Nasal Polyps 2012. Rhinol Suppl
23:3
9. Fokkens W, Desrosiers M (2019) Harvey R EPOS2020: develop-
ment strategy and goals for the latest European Position Paper on
Rhinosinusitis. Rhinology 57(3):162–168
10. Damm M, Schmitl L, Müller CA, Welge-Lüssen A, Hummel T
(2019) Diagnostics and treatment of olfactory dysfunction. HNO
67(4):274–281
11. Hummel T, Rissom K, Reden J, Hähner A, Weidenbecher M, Hüt-
tenbrink KB (2009) Effects of olfactory training in patients with
olfactory loss. Laryngoscope 119(3):496–499
12. Haehner A, Tosch C, Wolz M etal (2013) Olfactory training in
patients with Parkinson’s disease. PLoS One 8(4):e61680
13. Geißler K, Reimann H, Gudziol H, Bitter T, Guntinas-Lichius
O (2014) Olfactory training for patients with olfactory loss after
upper respiratory tract infections. Eur Arch Otorhinolaryngol
271(6):1557–1562
14. Altundag A, Cayonu M, Kayabasoglu G etal (2015) Modified
olfactory training in patients with postinfectious olfactory loss.
Laryngoscope 125(8):1763–1766
15. Damm M, Pikart LK, Reimann H etal (2014) Olfactory training is
helpful in postinfectious olfactory loss: a randomized, controlled,
multicenter study. Laryngoscope 124(4):826–831
16. Hummel T, Whitcroft KL, Andrews P etal (2017) Position paper
on olfactory dysfunction. Rhinology, Suppl 25(2017):1–30
17. Daramola OO, Becker SS (2015) An algorithmic approach to the
evaluation and treatment of olfactory disorders. Curr Opin Oto-
laryngol Head Neck Surg 23(1):8–14
18. Hummel T, Hüttenbrink KB (2005) Olfactory dysfunction due
to nasal sinus disease Causes, consequences, epidemiology, and
therapy. HNO 53(Suppl 1):S26-32
19. Brann DH, Tsukahara T, Weinreb C etal (2020) Non-neuronal
expression of SARS-CoV-2 entry genes in the olfactory system
suggests mechanisms underlying COVID-19-associated anosmia.
Sci Adv. https:// doi. org/ 10. 1126/ sciadv. abc58 01
20. Tian J, Pinto JM, Cui X etal (2016) Sendai Virus Induces Per-
sistent Olfactory Dysfunction in a Murine Model of PVOD via
Effects on Apoptosis, Cell Proliferation, and Response to ants.
PLoS One 11(7):e0159033
21. Hong SC, Holbrook EH, Leopold DA, Hummel T (2012) Dis-
torted olfactory perception: a systematic review. Acta Otolaryngol
132(Suppl 1):S27-31
22. Hummel T, Whitcroft KL, Rueter G, Haehner A (2017) Intranasal
vitamin A is beneficial in post-infectious olfactory loss. Eur Arch
Otorhinolaryngol 274(7):2819–2825
23. Hummel T, Heilmann S, Hüttenbrink KB (2002) Lipoic acid in
the treatment of smell dysfunction following viral infection of the
upper respiratory tract. Laryngoscope 112(11):2076–2080
24. Tanaka O, Mukaino Y (1999) The effect of auricular acupuncture
on olfactory acuity. Am J Chin Med 27:19–24
25. Hesse HP (2007) Akupunktur. In: Likar R, Wendtner F, Wenzel
G, Ausserwinkler M, Sittl R (eds) Bernatzky G. Nichtmedika-
mentöse Schmerztherapie – Komplementäre Nethoden in der
Praxis. Springer Verlag, Wien, p S 385-390
26. Stux G, Stiller N, Pothmann R, Jayasuriya A (1985) Akupunk-
tur—Lehrbuch und Atlas 2 Auflage. Springer Verlag, Berlin-
Heidelberg, p S 10–16-S 29–33
27. Stux G (2007) Akupunktur—Einführung, 7th edn. Springer-Ver-
lag, Berlin, p S.9–36-S.57–186
28. Stux G, Stiller N, Berman B, Pomeranz B (2008) Akupunktur –
Lehrbuch und Atlas, 7th edn. Springer Verlag, Berlin
29. Stör W, Irnich D (2009) Acupuncture: basics, practice, and evi-
dence. Schmerz 23(4):405–418
30. Vent J, Wang DW, Damm M (2010) Effects of traditional Chinese
acupuncture in post-viral olfactory dysfunction. Otolaryngol Head
Neck Surg 142(4):505–509
31. Silas J, Doty RL (2010) No evidence for specific benefit of acu-
puncture over vitamin B complex in treating persons with olfac-
tory dysfunction. Otolaryngol Head Neck Surg 143(4):603
32. Dai Q, Pang Z, Yu H (2016) Recovery of Olfactory Function in
Postviral Olfactory Dysfunction Patients after Acupuncture Treat-
ment. Evid Based Complement Alternat Med. https:// doi. org/ 10.
1155/ 2016/ 49860 34
33. Hauswald B, Tänzer K, Hüttenbrink KB (1998) Die Ergeb-
nisse der Akupunktur bei Patienten mit Hyp-bzw Anosmien.
In: Hauswald B, Tänzer K, Hüttenbrink KB (eds) Allergische
Erkrankungen von Haut und Schleimhäuten—Akupunktur im
Dialog. Hippokrates-Verlag, Stuttgart, p S 67-71
34. Anzinger A, Alberecht J, Kopietz R etal (2009) Effects of lasern-
eedle acupuncture on olfactory sensitivity of healthy human
subjects: a placebo-controlled, double-blinded, randomized trial.
Rhinology 47:153–159
35. Lin PS, Luo SD, Huang OY (2019) The application of bo’s
abdominal acupuncture on post-viral olfactory disorder after
steroid treatment failure: a case study. J Chin Med 30(2):119–129
36. Welge-Luessen A, Leopold DA, Miwa T (2013) Smell and Taste
Disorders - Diagnostic and Clinical Work-Up. In: Welge-Luessen
A, Hummel T (eds) Management of Smell and Taste Disorders - A
Practical Guide for Clinicians. Thieme, Stuttgart, pp 49–57
37. Hummel T, Sekinger B, Wolf SR, Pauli E, Kobal G (1997) “Snif-
fin” sticks’: olfactory performance assessed by the combined
testing of odor identification, odor discrimination and olfactory
threshold. Chem Senses 22:39–52
38. Brinkhaus B, Witt CM, Ortiz M etal (2010) Acupuncture in sea-
sonal allergic rhinitis (ACUSAR)–design and protocol of a ran-
domised controlled multi-centre trial. Forsch Komplementmed
17(2):95–102
39. Gudziol V, Lötsch J, Hähner A, Zahnert T, Hummel T (2006)
Clinical significance of results from olfactory testing. Laryngo-
scope 116(10):1858–1863
40. Reden J, Mueller A, Mueller C, Konstantinidis I, Frasnelli J, Lan-
dis BN, Hummel T (2006) Recovery of olfactory function follow-
ing closed head injury or infections of the upper respiratory tract.
Arch Otolaryngol Head Neck Surg 132(3):265–269
41. Hedner M, Larsson M, Arnold N etal (2010) Cognitive factors in
odour detection, odour discrimination, and odour identification
tasks. J Clin Exp Neuropsychol 32(10):1062–1067
42. Liu F, Li ZM, Jiang YJ, Chen LD (2014) A meta-analysis of acu-
puncture use in the treatment of cognitive impairment after stroke.
J Altern Complement Med 20(7):535–44
43. Zhou L, Zhang YL, Cao HJ, Hu H (2013) Treating vascular
mild cognitive impairment by acupuncture: a systematic review
of randomized trials. Zhongguo Zhong Xi Yi Jie He Za Zhi
33(12):1626–30
Publisher’s Note Springer Nature remains neutral with regard to
jurisdictional claims in published maps and institutional affiliations.
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

1.
2.
3.
4.
5.
6.
Terms and Conditions
Springer Nature journal content, brought to you courtesy of Springer Nature Customer Service Center GmbH (“Springer Nature”).
Springer Nature supports a reasonable amount of sharing of research papers by authors, subscribers and authorised users (“Users”), for small-
scale personal, non-commercial use provided that all copyright, trade and service marks and other proprietary notices are maintained. By
accessing, sharing, receiving or otherwise using the Springer Nature journal content you agree to these terms of use (“Terms”). For these
purposes, Springer Nature considers academic use (by researchers and students) to be non-commercial.
These Terms are supplementary and will apply in addition to any applicable website terms and conditions, a relevant site licence or a personal
subscription. These Terms will prevail over any conflict or ambiguity with regards to the relevant terms, a site licence or a personal subscription
(to the extent of the conflict or ambiguity only). For Creative Commons-licensed articles, the terms of the Creative Commons license used will
apply.
We collect and use personal data to provide access to the Springer Nature journal content. We may also use these personal data internally within
ResearchGate and Springer Nature and as agreed share it, in an anonymised way, for purposes of tracking, analysis and reporting. We will not
otherwise disclose your personal data outside the ResearchGate or the Springer Nature group of companies unless we have your permission as
detailed in the Privacy Policy.
While Users may use the Springer Nature journal content for small scale, personal non-commercial use, it is important to note that Users may
not:
use such content for the purpose of providing other users with access on a regular or large scale basis or as a means to circumvent access
control;
use such content where to do so would be considered a criminal or statutory offence in any jurisdiction, or gives rise to civil liability, or is
otherwise unlawful;
falsely or misleadingly imply or suggest endorsement, approval , sponsorship, or association unless explicitly agreed to by Springer Nature in
writing;
use bots or other automated methods to access the content or redirect messages
override any security feature or exclusionary protocol; or
share the content in order to create substitute for Springer Nature products or services or a systematic database of Springer Nature journal
content.
In line with the restriction against commercial use, Springer Nature does not permit the creation of a product or service that creates revenue,
royalties, rent or income from our content or its inclusion as part of a paid for service or for other commercial gain. Springer Nature journal
content cannot be used for inter-library loans and librarians may not upload Springer Nature journal content on a large scale into their, or any
other, institutional repository.
These terms of use are reviewed regularly and may be amended at any time. Springer Nature is not obligated to publish any information or
content on this website and may remove it or features or functionality at our sole discretion, at any time with or without notice. Springer Nature
may revoke this licence to you at any time and remove access to any copies of the Springer Nature journal content which have been saved.
To the fullest extent permitted by law, Springer Nature makes no warranties, representations or guarantees to Users, either express or implied
with respect to the Springer nature journal content and all parties disclaim and waive any implied warranties or warranties imposed by law,
including merchantability or fitness for any particular purpose.
Please note that these rights do not automatically extend to content, data or other material published by Springer Nature that may be licensed
from third parties.
If you would like to use or distribute our Springer Nature journal content to a wider audience or on a regular basis or in any other manner not
expressly permitted by these Terms, please contact Springer Nature at
onlineservice@springernature.com