Jou nal o
Clinical Medicine
A icle
Diagnos ic Accu acy S udy Compa ing Hys e osalpingo-Foam
Sonog aphy and Hys e osalpingog aphy o Fallopian Tube
Pa ency Assessmen
Julia Ramos 1,2, Cinzia Caliga a 1,2, Es he San ama ía-López 1,2 , C is ina González-Ra ina 1,2,3,*,
Nicolás P ados 1,2,3, F ancisco Ca anza 1,2, Víc o Blasco 1,2 and Manuel Fe nández-Sánchez 1,2,3,4
Ci a ion: Ramos, J.; Caliga a, C.;
San ama ía-López, E.;
González-Ra ina, C.; P ados, N.;
Ca anza, F.; Blasco, V.;
Fe nández-Sánchez, M. Diagnos ic
Accu acy S udy Compa ing
Hys e osalpingo-Foam Sonog aphy
and Hys e osalpingog aphy o
Fallopian Tube Pa ency Assessmen . J.
Clin. Med. 2021,10, 4169. h ps://
doi.o g/10.3390/jcm10184169
Academic Edi o : Jacek Szama owicz
Recei ed: 30 July 2021
Accep ed: 10 Sep embe 2021
Published: 15 Sep embe 2021
Publishe ’s No e: MDPI s ays neu al
wi h ega d o ju isdic ional claims in
published maps and ins i u ional a il-
ia ions.
Copy igh : © 2021 by he au ho s.
Licensee MDPI, Basel, Swi ze land.
This a icle is an open access a icle
dis ibu ed unde he e ms and
condi ions o he C ea i e Commons
A ibu ion (CC BY) license (h ps://
c ea i ecommons.o g/licenses/by/
4.0/).
1IVIRMA Se illa, A enida Amé ico Vespucio 19, ES-41092 Se ille, Spain; [email p o ec ed] (J.R.);
[email p o ec ed] (C.C.); es he [email p o ec ed] (E.S.-L.); [email p o ec ed] (N.P.);
[email p o ec ed] (F.C.); ic o [email p o ec ed] (V.B.);
[email p o ec ed] (M.F.-S.)
2Fundación IVI, Ins i u o de In es igación Sani a ia La Fe, ES-46026 Valencia, Spain
3Depa men o Molecula Biology and Biochemical Enginee ing, Uni e sidad Pablo de Ola ide,
ES-41013 Se ille, Spain
4Depa men o Su ge y, Uni e sidad de Se illa, ES-41004 Se ille, Spain
*Co espondence: [email p o ec ed]; Tel.: +34-954-286-274; Fax: +34-954-285-084
Abs ac :
In oduc ion: Simpli ied ul asound-based in e ili y p o ocols ha appea o p o ide
enough in o ma ion o plan e ec i e managemen ha e been desc ibed. Thus, he objec i e o his
s udy is o compa e he diagnos ic accu acy o he hys e osalpingo- oam sonog aphy (HyFoSy)
in ubal pa ency es ing wi h he adi ional hys e osalpngog aphy (HSG) o es ablishing a new
diagnos ic s a egy in in e ili y. Ma e ial and Me hods: P ospec i e obse a ional diagnos ic accu acy
was pe o med in a p i a e e ili y clinic in which 106 women unde going a p econcep ionally isi
we e ec ui ed. All o hem had low isk o ubal disease, had pe o med an HSG and we e nega i e
o Chlamydia achoma is an ibody. Main ou come measu es we e ubal pa ency and pain g ade.
Resul s: E alua ion o ubal pa ency by HyFoSy showed a o al conco dance wi h he esul s o he
p e ious HSG in 72.6% (n= 77), and a o al disco dance o 4.7% (n= 6), wi h he in e - es ag eemen
Kappa equal o 0.57, which means mode a e conco dance. Among he pa ien s, 59.1% did no epo
pain du ing he p ocedu e, while he emaining 48.1% indica ed pain in di e en deg ees; pa ien s
usually epo less pain and only 6.6% desc ibed mo e pain wi h HyFoSy han wi h HSG (OR 6.57
(CI 95% 3.11–13.89)). Clinical ou comes a e pe o ming HyFoSy we e no a ec ed. Conclusions:
HyFoSy is in conco dance wi h HSG ega ding ubal pa ency esul s and i is a less pain ul echnique
han HSG. HyFoSy is mo e economical and can be pe o med in an exam oom only equipped wi h
an ul asound scanne . Based on hese esul s, HyFoSy could be he i s -choice diagnos ic op ion o
assess ubal pa ency in pa ien s wi h low isk o ubal disease.
Keywo ds:
ubal pa ency; hys e osalpingo-con as sonog aphy; hys e osalpingo- oam sonog aphy;
hys e osalpingog aphy; HyFoSy; HSG
1. In oduc ion
Imaging diagnos ics a e an essen ial pa o con empo a y medicine. Ul asound-
based examina ion plays a special ole in gynecology and i s use has been inc easing,
pa icula ly in he e alua ion o in e ili y. T adi ionally, he co ne s ones o in es iga ion
o an in e ile couple ha e been g ouped in o se e al es ing ca ego ies, wi h he e alu-
a ion o u e ine a chi ec u e and ubal pa ency being one o he mos impo an ones [
1
].
Tubal abno mali ies a e seen in 25–35% o emale sub e ili y pa ien s [
1
]. Tubal disease
encompasses a ange o pa hologies, wi h pel ic in lamma o y disease (PID) as he mos
common cause; i is usually asymp oma ic, and i s main causal agen is Chlamydia achoma-
J. Clin. Med. 2021,10, 4169. h ps://doi.o g/10.3390/jcm10184169 h ps://www.mdpi.com/jou nal/jcm
J. Clin. Med. 2021,10, 4169 2 o 8
is [
2
]. O he possible causes o ubal in e ili y a e endome iosis, p e ious pel ic su ge y,
ib oids and pel ic ube culosis [3].
Lapa oscopy wi h ch omope uba ion (LC) is he gold-s anda d echnique o ubal
assessmen , bu because i is an in asi e, expensi e and iskie echnique [
1
,
4
] i was
eplaced by HSG, which has been used o decades. This la e p ocedu e has lowe
diagnos ic accu acy han LC [
5
], is unable o de ec abno mal o a ies o myome ium
and in ol es adia ion exposu e, discom o o e en abdominal pain [
6
]. Conside ing he
disad an ages o HSG, hys e osalpingo-con as sonog aphy (HyCoSy) was in oduced
as an al e na i e o ou pa ien ubal assessmen as i a oids he p e iously men ioned
isks. HyCoSy, using a mix u e o ai and saline solu ion, has an accu acy compa able o
ha o HSG [
7
], allows he eal- ime obse a ion o he pel ic o gans h ough ul asound
and i pe o ms be e han HSG when de ec ing abno mali ies in he u e ine ca i y [
8
].
Howe e , HyCoSy is mo e ope a o -dependen han he wo o he echniques. A his poin ,
i is impo an o highligh ha all hese me hods ha e echnical limi a ions, so scien i ic
socie ies ecommend u he e alua ion wi h a second echnique in case o abno mal esul s
o es ablish a co ec diagnosis and ind he bes ea men s a egy o he pa ien [1].
Di e en con as media ha e been p o en e ec i e bu ha e become no longe
a ailable o di e en easons [
9
]. In 2007, a non-emb yo oxic gel known as ExEm
®
gel
(GynaecologIQ, Del , The Ne he lands) was de eloped. Because ul asound scans (US)
o good-quali y a an accep able p ice we e ob ained, hys e osalpingo- oam sonog aphy
(HyFoSy) has been es ablished as a sa e and less pain ul al e na i e and has become
widely adop ed in in e ili y clinics and ou pa ien se ings, sho ening wai ing imes o
ea men ini ia ion [
10
]; mo eo e , i s easibili y, ole abili y and sa e y ha e been al eady
demons a ed [11–13].
The abili y o pe o m mos in e ili y diagnoses by ul asound in he ambula o y
se ing is no only a ac i e and bene icial o pa ien s, bu also o he heal hca e sys em.
Thus, he objec i e o his s udy is o es ima e he diagnos ic accu acy o HyFoSy in ubal
pa ency es ing and compa e i o he accu acy o adi ional HSG o es ablishing a new
diagnos ic s a egy in in e ili y ea men .
2. Ma e ials and Me hods
2.1. Pa ien s
This s udy was app o ed by he ins i u ional E hics Commi ee o he Hospi al Uni e -
si a io Vi gen Maca ena (Se ille, Spain) and all pa ien s signed an in o med consen o m
(in e nal E hics Commi ee numbe 2071). One hund ed and six pa ien s we e ec ui ed
be ween June 2013 and Feb ua y 2017 in ou e ili y cen e (Figu e 1). The inclusion c i e ia
we e ha ing a p e ious HSG pe o med in less han a yea , a nega i e se ology o IgG
and IgM Chlamydia achoma is and being pa ien s wi h low isk o ubal disease. Risk o
ubal disease was assessed pe o ming a US and exhaus i e anamnesis (no e idence o
PID o o he pel ic diseases such as hyd osalpinx, adnexal pa hology, p e ious abdominal
su ge y o endome iosis).
J. Clin. Med. 2021,10, 4169 3 o 8
J. Clin. Med. 2021, 10, x FOR PEER REVIEW 3 o 9
Figu e 1. Flowcha o eligible pa icipan s. HyFoSy: hys e osalpingo- oam sonog aphy; HSG: hys e osalpingog aphy; IUI: in au e ine insemina ion; IUI-D: in au e ine
insemina ion wi h dono semen; IUI-H: in au e ine insemina ion wi h husband o pa ne ’s semen.
106 women assessed o
elegibili y
106 pa ien s included and
HyFoSy pe o med
6 Pa ien s wi h bila e al occlusion (5.7%)
Conco dance in 2 Pa ien s
wi h HSG (33.3%)
No conco dance in 4 Pa ien s
wi h HSG (66.6%)
3 pa ien s ollowed IUI:
- 2 IUI-D wi h 1 p egnancy (50%)
- 1 IUI-H wi h no p egnancy (0%)
17 pa ien s wi h unila e al pa ency (16%)
7 ollowed IUI:
- 3 IUI-D wi h 2 p egnancies (66.7%)
- 4 IUI-H wi h no p egnancies (0%)
83 Pa ien s wi h bila e al pa ency (78.3%)
41 ollowed IUI:
- 17 IUI-D wi h 9 p egnancies (52.9%)
- 24 IUI-H wi h 5 p egnancies (20.8%)
Figu e 1.
Flowcha o eligible pa icipan s. HyFoSy: hys e osalpingo- oam sonog aphy; HSG: hys e osalpingog aphy;
IUI: in au e ine insemina ion; IUI-D: in au e ine insemina ion wi h dono semen; IUI-H: in au e ine insemina ion wi h
husband o pa ne ’s semen.
2.2. Technique
The HyFoSy p ocedu e was always pe o med by he same ained clinicians and
unde he same condi ions. P io o he examina ion, a 2-dimensional ul asound (IUI-US)
was achie ed o assess pel ic ana omy. All US we e pe o med using a Gene al Elec ic
Voluson 730 p oV sys em equipped wi h a olume ic 4–9 MHz endo aginal p obe (IC5-9H
H40422LL).
The oam con as was p epa ed and pe o med a oom empe a u e as p e iously
desc ibed [
14
]. In mos cases, we used he GIS ca he e (Smi h Medical, Uni ed Kingdom),
which is included in he ExEm
®
Foam ki , bu in pa ien s in whom i was no possible o
in oduce i , we needed an al e na i e one, such as he Gyne ics
®
(#4219 Em ac Delphin
Emb yo ans e ca he e ) o Ki aza o
®
(4.7F 230 mm T ial EC-PRO Ca he e ), which a e
so e and na owe . The slow in oduc ion o 5 mL o oam in one bolus in o he endome-
ial ca i y was enough o achie e co ec isualiza ion. We pe o med a longi udinal
u e us ul asound analysis o e alua e ha oam was passing h ough i and no in o he
agina. Then, we s udied a ans e se sec ion o he u e us o loca e he ubes. Finally, we
checked o oam dispe sion a ound he o a ies and inside he pe i oneal ca i y. The gel
usually main ained i s echogenici y long enough, be ween 5 and 12 min, o allow image
acquisi ion. We de ined ubal pa ency as gel oam spillage om he imb ia ending, seen
as luid low su ounding he o a y and i s collec ion in pel is. Dis al ubal blockage was
de ined as absence o spillage. In he e en o appa en co nual blockade, we p oceeded
ollowing he sugges ion ha adding an addi ional oam injec ion may co ec he ubal
spasms [15].
A he end o he p ocess, pa ien s had o ill ou a ques ionnai e abou he expe ienced
pain. Pa ien s had o choose a alue om 0 o 10 using isual analogue scale (VAS) o
desc ibe he pain expe ienced in bo h echniques: HyFoSy and HSG. No analgesics we e
indica ed p io o he pe o mance o he echnique.
2.3. Clinical Ou comes
A e ubal pa ency diagnosis, i y-one pa ien s unde wen in au e ine insemina ions
(IUI) as shown in Figu e 1. A maximum o 4 IUI we e pe o med be o e being e e ed o an
J. Clin. Med. 2021,10, 4169 4 o 8
in i o
e iliza ion (IVF) ea men . Clinical p egnancy a e calcula ed as he pe cen age o
p egnancy women pe in au e ine insemina ion wi h dono semen (IUI-D) and in au e ine
insemina ion wi h husband o pa ne ’s semen (IUI-H) pe o med we e compa ed wi h
ou indica o s o alida e he ubal pa ency diagnosis.
2.4. S a is ical Analysis
S a is ical analysis was pe o med acco ding o ubal pa ency and pain g ade. Tubal
pa ency was desc ibed as bila e al pa ency, unila e al pa ency, o no pa ency. Pain esul s
we e assessed using he isual analogue scale (VAS) and classi ied in o ou g oups o be
analyzed as an o dinal ca ego ical ou come acco ding o Engels e al. [
13
]: no pain (VAS 0),
mild pain (VAS 1–3), mode a e pain (VAS 4–6) o se e e pain (VAS 7–10). The side o he
pa ency was no ed o dis inguish ag eemen be ween echniques. Fo desc ip i e s a is ics,
da a a e p esen ed as he means and he 95% IC o hei di e ence. Each compa ison
gene a ed a di e en p- alue. In all cases, p- alues
≤
0.05 we e conside ed signi ican .
Wilcoxon ma ched-pai s signed- anks es was used o analyze he da a. The e is no
published da a abou co ela ion be ween HyFoSy and HSG esul s o pa ien ou come
ha can help us calcula e be o ehand he sample size. Because i is an explo a o y s udy,
we included a minimum o 100 pa ien s. We analyzed conco dance wi h he weigh ed
Kappa index [
16
]. We used he S a is ical Package o Social Sciences e sion 22 (SPSS,
USA) so wa e o da a analysis.
3. Resul s
The cha ac e is ics o he pa ien s ( emale age, BMI and in e ili y du a ion) a e sum-
ma ized in Table 1.
Table 1. Pa ien cha ac e is ics.
Mean (n= 106) S anda d De ia ion
Age (y) 34.71 ±3.68
Body mass index (kg/m2)24.11 ±4.54
In e ili y du a ion (y) 2.30 ±1.70
The e alua ion o ubal pa ency by HyFoSy showed a o al conco dance wi h he
esul s o he p e ious HSG in 72.6% (n= 77) o he cases (Table 2). On he o he hand,
we also desc ibed a o al disco dance o 4.7% o he p ocedu es (n= 5); 3.8% (n= 4) we e
diagnosed wi h a bila e al obs uc ion by HyFoSy while bo h o hei ubes we e pa en
acco ding o HSG es , and 0.9% (n= 1) was diagnosed wi h unila e al pa ency, bu in a
di e en ube depending on he es pe o med. The in e - es ag eemen Kappa was 0.57,
showing a mode a e conco dance.
Table 2. Pa ency esul s.
n= 106 Pa ien s
Pa ency du ing HyFoSy
Bila e al Obs uc ion
(n= 6; 5.7%)
Unila e al
Obs uc ion (n= 17;
16%)
Bila e al Pa ency
(n= 83; 78.3%)
Pa ency du ing HSG
Bila e al obs uc ion (n= 5; 4.7%) 2 (1.9%) * 3 (2.8%) 0 (0.0%) **
Unila e al obs uc ion (n= 15; 14.2%) 0 (0.0%) 3 (2.8%) * 11 (10.4%)
1 (0.9%) **
Bila e al pa ency (n= 86; 81.1%) 4 (3.8%) ** 10 (9.4%) 72 (67.9%) *
Wilcoxon ma ched-pai s signed- anks es (p< 0.001); in e - es ag eemen Kappa index (0.57); * o al conco dance; ** o al disco dance.
J. Clin. Med. 2021,10, 4169 5 o 8
Conce ning he ca he e used du ing he echnique, 57.5% o he p ocedu es we e
pe o med wi h he cannula co esponding o he ExEm
®
Foam ki , 37.5% wi h a Ki aza o
®
and 0.05% wi h a cannula belonging o Gyne ics®.
Du ing he pe iod o he s udy, 59.1% o he pa ien s did no epo pain du ing he
p ocedu e, while he emaining 48.1% indica ed pain in di e en deg ees, as shown in
Table 3. When pa ien s we e asked abou he pain, hey had expe ienced du ing p e ious
HSG, 50% o he esponses indica ed he same pain, 43.4% answe ed ha hey su e ed lees
and only he emaining 6.6% desc ibed mo e pain wi h HyFoSy han wi h HSG (OR 6.57
(CI 95% 3.11–13.89)).
Table 3. Pain esul s.
n= 106 Pa ien s
Pain du ing HyFoSy
No Pain
(n= 55; 51.9%)
Mild Pain
(n= 44; 41.5%)
Mode a e Pain
(n= 6; 5.7%)
Se e e Pain
(n= 1; 0.9%)
Pain du ing HSG
No pain (n= 37; 34.9%) 31 (29.2%) 6 (5.6%) 0 (0.0%) 0 (0.0%)
Mild pain (n= 22; 20.8%) 2 (2.0%) 19 (17.9%) 1 (0.9%) 0 (0.0%)
Mode a e pain (n= 33; 31.1%) 14 (13.2%) 17 (16.0%) 2 (2.0%) 0 (0.0%)
Se e e pain (n= 14; 13.2%) 8 (7.5%) 2 (2.0%) 3 (2.8%) 1 (0.9%)
Wilcoxon ma ched-pai s signed- anks es (p< 0.001).
An impo an poin o be analyzed was he numbe o ad e se e en s and i is no e-
wo hy ha no in ec ions we e epo ed in any pa ien a e he HyFoSy p ocedu e. Fou
aso agal eac ions we e epo ed, in one case wi hou pain and in h ee cases wi h mild
pain du ing he p ocess. A painless spo ing episode was also desc ibed.
Finally, clinical esul s a e summa ized in Table 4. Compa ed wi h ou gene al pop-
ula ion ha unde wen an IUI-D du ing he s udy pe iod, clinical p egnancy a es we e
be e a e HyFoSy (27.3% s. 20.8%, p= 0.453); o IUI-H, he same end is obse ed
(
10.3% s. 14.8%
,p= 0.496), al hough, as expec ed, ou comes we e lowe han wi h IUI-D.
Table 4. Clinical ou comes a e ubal pa ency diagnosis.
IUI-D (n= 22) IUI-H (n= 29) To al (n= 51)
Clinical p egnancy a e a i s IUI 27.3% 10.3% 17.7%
Clinical p egnancy a e a e wo IUI 45.5% 17.2% 29.4%
Cumula i e clinical p egnancy a e 54.6% 17.2% 33.3%
IUI-D: in au e ine insemina ion wi h dono semen; IUI-H: in au e ine insemina ion wi h husband o pa -
ne ’s semen.
4. Discussion
An op imal ini ial in e ili y sc eening p o ocol would be a p ocess ha is diagnos-
ically accu a e, p o i able, eliable and as leas in asi e as possible. In addi ion, he
in es iga ion should p o ide he physician wi h use ul p ognos ic in o ma ion ega d-
ing possible u u e ea men . Cu en ly, he ex ensi e use o in asi e p ocedu es such
lapa oscopy o hys e oscopy a e he s anda ds a many e ili y cen e s bu ad ances in
gynecological ul asonog aphy ha e shown ha ul asounds could eplace ou ine in asi e
p ocedu es. An ul asound-based app oach would make he basic in e ili y diagnosis less
ime-consuming and less expensi e, bu a he same ime mo e accep able o mos pa ien s;
hus, i is i al o gynecologis s o implemen mode n non-in asi e ul asound modali ies
in daily p ac ice.
As we s a ed p e iously, ubal disease is an impo an cause o in e ili y and ubal
pa ency es ing is an impo an pa o he in e ili y in es iga ion [
1
]. The disad an ages
associa ed wi h con en ional es s such as LC and HSG pa ed he way o he de elop-
men o HyFoSy which is desc ibed in compa ison wi h he o he echniques as jus as
J. Clin. Med. 2021,10, 4169 6 o 8
accu a e, mo e pa ien - iendly and cos -e ec i e and less pain ul; in addi ion, i uses a
non-emb yo oxic con as and does no equi e o e e pa ien s o ano he cen e o ubal
pa ency e alua ion as i could no mally be pe o med a he e ili y cen e i sel , educing
he wai ing imes o s a ing an assis ed ep oduc i e ea men . Finally, indica ions o
his echnique include a basic in e ili y s udy, when in au e ine insemina ion o p o-
g ammed in e cou se a e p esc ibed as p e e en ea men s and o e i y ha he ubes a e
occluded a e a su gical p ocedu e [17].
Bea ing in mind hese conside a ions, we designed a diagnos ic accu acy s udy com-
pa ing a p e ious HSG wi h he esul s o he cu en HyFoSy es . P e ious esul s ha e
shown a o al conco dance wi h LC [
18
] and a highe p opo ion o ubes we e classi ied
as pa en when compa ed wi h HyCoSy [
12
]. In addi ion, HyFoSy p o ided a mo e ac-
cu a e diagnosis compa ed o HyCoSy wi h saline solu ion when bo h echniques we e
con on ed wi h LC [
19
]. As a as we know, his is he i s s udy whose esul s show a
high enough deg ee o conco dance be ween he wo echniques analyzed o be able o
in oduce HyFoSy as a i s -line clinic ubal pa ency es [20]. This s a emen is con i med
in cases whe e addi ional es ing is needed i he esul s a e abno mal du ing he i s
e alua ion. In his sense, we would ha e needed o pe o m a second complemen a y
es in hose pa ien s who p esen ed bila e al ubal obs uc ion wi h HyFoSy, bu as hese
women al eady had a p e ious HSG, we could con i m he ini ial diagnosis in wo o he
cases wi hou pe o ming a hi d p ocedu e. In ou case, he pe cen age o inconclusi e
esul s a e HyFoSy is lowe han in o he s udies [
11
,
14
]; he eason may be ound in he
implemen a ion o a p ope lea ning cu e, which will acili a e he es ablishmen o his
diagnos ic s a egy by educing he cases ha need o be con i med.
In a emp s o o e come he inabili y o examine he whole cou se o he allopian ube
in one scanning plane [
21
], o he echniques such as 3-dimensional ul asound (3D-US) and
dopple ha e been assessed ins ead o 2D-US o imp o e isualiza ion while pe o ming
HyFoSy; howe e , up o da e, i is he e o e ques ionable whe he hese echniques a e o
addi ional alue o HyFoSy. I has been epo ed ha , wi h o wi hou dopple , 3D-HyFoSy
does no seem o o e bene i s abo e eal- ime 2D-HyFoSy pe o med by an expe ienced
ul asonog aphe , so we could assume ha HyFoSy appea s o be an accu a e and well-
ole a ed i s -line diagnos ic p ocedu e and 3D-HyFoSy echnique is help ul o a less
quali ied ope a o [
19
,
22
]. The e o e, he ac o ha ing used 2D-HyFoSy, along wi h he
ac ha he p ocedu e has been pe o med by a quali ied sonog aphe , could also explain
why ewe con i ma o y es s a e needed in ou s udy han in o he o a simila na u e.
Jus as impo an as he isualiza ion echnique, is he choice o he app op ia e cannula
o pe o m he p ocedu e; some au ho s ha e ecommended he use o a pedia ic Foley
balloon ca he e o p e en e lux [
15
] bu based on ou expe ience, he use o an in au e ine
balloon-less ca he e is mo e use ul, while i is isible in he u e ine ca i y, in case o ha ing
di icul ies wi h he ExEm®Foam ca he e as hey a e less pain ul and cheape .
Once he p ecision o HyFoSy was accep ed o he assessmen o ubal pa ency, we
ocused on pa ien ’s pain. Ou esul s showed ha , in gene al, HyFoSy is a less pain ul
echnique compa ed wi h con en ional HSG; hese da a a e consis en wi h hose o a
p e ious s udy in ha he a e age ime equi ed o pe o m he p ocedu e is ela ed o he
in ensi y o pain [
11
]. Howe e , and despi e ou esul s being encou aging ega ding he
pain associa ed o HyFoSy, hey a e no as good om he poin o iew o ad e se e en s,
since we epo ed a highe incidence o aso agal eac ions compa ed o o he s udies [
13
].
I is impo an o emembe ha hese pa ien s eco e quickly a e changing posi ion.
Las ly, we con i med ha he clinical p egnancy a es om in au e ine insemina ions
ca ied ou a e pe o ming HyFoSy we e no a ec ed by an inco ec diagnosis since ou
ou comes we e like hose obse ed in daily clinical p ac ice, when HyFoSy was p e iously
used o diagnose ubal pa ency. In addi ion, he s udies published o da e ha e epo ed a
spon aneous p egnancy a e ha anges be ween 19–30% o a pe iod o app oxima ely
6 mon hs [10,23].
J. Clin. Med. 2021,10, 4169 7 o 8
In summa y, ul asound e ili y assessmen is an accu a e choice o a i s line in e -
ili y wo kup and i s use has been ising. This has allowed he de elopmen o ea men
s a egies such as Fe iliscan
©
, based on he ealiza ion o a high-quali y 3D-US ha in-
ol es he assessmen o ubal pa ency by pe o ming HyFoSy [
24
]. This in eg al app oach
is a ge ed o add ess speci ic issues conce ning he e ili y po en ial o he woman.
5. Conclusions
HyFoSy is a sui able echnique o assess ubal pa ency. Ou esul s sugges ha i
could be conside ed a p omising al e na i e o HSG ega ding accu acy and e ec i eness
in pa ien s a low isk o ubal disease. Fu he mo e, HyFoSy is cos -e ec i e, less ime-
consuming, well- ole a ed, can be pe o med in an exam oom equipped only wi h an
ul asound scanne , educes wai ing imes and migh no a ec clinical ou comes a e an
assis ed ep oduc i e ea men . The es ablishmen o an app op ia e diagnos ic s a egy
ha includes quali ied s a and he mos e ec i e ul asound echnique o ca y ou he
p ocedu e, has allowed us o educe he cases ha need o be con i med.
Au ho Con ibu ions:
J.R. was in ol ed in he s udy concep and design, da a collec ion and
managemen and d a ing he a icle. C.C. wo ked on he acquisi ion o da a. E.S.-L. pa icipa ed in
he analysis and in e p e a ion o he da a and d a ing he a icle. C.G.-R. wo ked on he c i ical
e iew o he a icle. N.P. was in ol ed in he da a managemen and analysis. F.C. pa icipa ed in
he acquisi ion o da a. V.B. was implica ed in d a ing he a icle and M.F.-S. wo ked on he s udy
concep and design and c i ical e iew o he a icle and inal d a . All au ho s ha e ead and ag eed
o he published e sion o he manusc ip .
Funding:
This esea ch did no ecei e any speci ic g an om unding agencies in he public,
comme cial, o no - o -p o i sec o s. Howe e , he Exem
®
FOAM ki s used in his s udy we e
p o ided ee o cha ge by GynaecologIQ.
Ins i u ional Re iew Boa d S a emen :
The s udy was conduc ed acco ding o he guidelines o he
Decla a ion o Helsinki, and app o ed by he Ins i u ional Re iew Boa d (o E hics Commi ee) o
Hospi al Uni e si a io Vi gen Maca ena (p o ocol code 2071 and da e o app o al 2nd o May 2013).
In o med Consen S a emen :
In o med consen was ob ained om all subjec s in ol ed in he s udy.
Acknowledgmen s:
The au ho s hank all he pa ien s o pa icipa ing in he s udy. The au ho s
also hank all he s a a IVI-RMA Se illa (Se ille, Spain) o hei con ibu ion o his wo k and
Ma ía C uz o he c i ical e iew o his manusc ip .
Con lic s o In e es : The au ho s decla e no con lic o in e es .
Re e ences
1.
Rajesh, H.; Lim, S.L.; Yu, S.L. Hys e osalpingo- oam sonog aphy: Pa ien selec ion and pe spec i es. In . J. Women’s Heal h
2016
,
ume 9, 23–32. [C ossRe ]
2.
Mol, B.W.J.; Lijme , J.; Dijkman, B.; an de Veen, F.; We heim, P.; Boss, P.M.M. The accu acy o se um chlamydial an ibodies in
he diagnosis o ubal pa hology: A me a-analysis. Fe il. S e il. 1997,67, 1031–1037. [C ossRe ]
3. Dun, E.C.; Nezha , C.H. Tubal Fac o In e ili y. Obs e . Gynecol. Clin. N. Am. 2012,39, 551–566. [C ossRe ] [PubMed]
4.
Saunde s, R.D.; Shwayde , J.M.; Nakajima, S.T. Cu en me hods o ubal pa ency assessmen . Fe il. S e il.
2011
,95, 2171–2179.
[C ossRe ]
5.
Adelusi, B.; Al-Nuaim, L.; Makanjuola, R.; Khashoggi, T.; Chowdhu y, N.; Kanga e, D. Accu acy o hys e osalpingog aphy and
lapa oscopic hyd o uba ion in diagnosis o ubal pa ency. Fe il. S e il. 1995,63, 1016–1020. [C ossRe ]
6.
Maheux-Lac oix, S.; Bou in, A.; Moo e, L.; Be ge on, M.-E.; Bujold, E.; Labe ge, P.; Lemy e, M.; Dodin, S. Hys e osalpingosonog a-
phy o diagnosing ubal occlusion in sub e ile women: A sys ema ic e iew wi h me a-analysis. Hum. Rep od.
2014
,29, 953–963.
[C ossRe ] [PubMed]
7.
Exacous os, C.; Zupi, E.; Ca uso i, C.; Lanzi, G.; Ma coni, D.; A duini, D. Hys e osalpingo-Con as Sonog aphy Compa ed wi h
Hys e osalpingog aphy and Lapa oscopic Dye Pe uba ion o E alua e Tubal Pa ency. J. Am. Assoc. Gynecol. Lapa osc.
2003
,10,
367–372. [C ossRe ]
8.
Lopes, V.M.; Ba guil, J.P.; Lace da, T.S.; Souza, A.L.M.; Filho, A.M.D.R.; Rolle , M.F.; Ba bosa, E.A.; Tie no, N.Z.; Lopes, J.R.C. An
o e iew o he esul s o hys e osonog aphy p io o in i o e iliza ion. JBRA Assis . Rep od. 2017,21, 302–305. [C ossRe ]
9.
Emanuel, M.H.; Exal o, N. Hys e osalpingo- oam sonog aphy (HyFoSy): A new echnique o isualize ubal pa ency. Ul asound
Obs e . Gynecol. 2011,37, 498–499. [C ossRe ]
J. Clin. Med. 2021,10, 4169 8 o 8
10.
Exal o, N.; Emanuel, M.H. Clinical Aspec s o HyFoSy as Tubal Pa ency Tes in Sub e ili y Wo kup. BioMed Res. In .
2019
,2019,
1–12. [C ossRe ]
11.
D eye , K.; Ou , R.; Hompes, P.G.; Mija o ic, V. Hys e osalpingo- oam sonog aphy, a less pain ul p ocedu e o ubal pa ency
es ing du ing e ili y wo kup compa ed wi h (se ial) hys e osalpingog aphy: A andomized con olled ial. Fe il. S e il.
2014
,
102, 821–825. [C ossRe ]
12.
Lim, S.L.; Jung, J.J.; Yu, S.L.; Rajesh, H. A compa ison o hys e osalpingo- oam sonog aphy (HyFoSy) and hys e osalpingo-
con as sonog aphy wi h saline medium (HyCoSy) in he assessmen o ubal pa ency. Eu . J. Obs e . Gynecol. Rep od. Biol.
2015
,
195, 168–172. [C ossRe ]
13.
Engels, V.; Medina, M.; An olín, E.; Ros, C.; Ama o, A.; De-Gui io , C.; Manzou , N.; So illo, L.; De la Cues a, R.; Rod íguez, R.;
e al. Feasibili y, ole abili y, and sa e y o hys e osalpingo- oam sonog aphy (hy osy). mul icen e , p ospec i e Spanish s udy. J.
Gynecol. Obs e . Hum. Rep od. 2020,50, 102004. [C ossRe ]
14.
Emanuel, M.H.; Van Vlie , M.; Webe , M.; Exal o, N. Fi s expe iences wi h hys e osalpingo- oam sonog aphy (HyFoSy) o o ice
ubal pa ency es ing. Hum. Rep od. 2011,27, 114–117. [C ossRe ]
15.
Van Schoub oeck, D.; Bosch, T.V.D.; Ameye, L.; Boes, A.S.; D’Hooghe, T.; Timme man, D. Pain du ing Fallopian- ube pa ency
es ing by hys e osalpingo- oam sonog aphy. Ul asound Obs e . Gynecol. 2015,45, 346–350. [C ossRe ]
16. Landis, J.R.; Koch, G.G. The Measu emen o Obse e Ag eemen o Ca ego ical Da a. Biome ics 1977,33, 159. [C ossRe ]
17.
Luciano, D.E.; Exacous os, C.; Johns, D.A.; Luciano, A.A. Can hys e osalpingo-con as sonog aphy eplace hys e osalpingog-
aphy in con i ming ubal blockage a e hys e oscopic s e iliza ion and in he e alua ion o he u e us and ubes in in e ile
pa ien s? Am. J. Obs e . Gynecol. 2011,204, 79.e1–79.e5. [C ossRe ] [PubMed]
18.
Van Schoub oeck, D.; Bosch, T.V.D.; Meuleman, C.; Tomasse i, C.; D’Hooghe, T.; Timme man, D. The Use o a New Gel Foam o
he E alua ion o Tubal Pa ency. Gynecol. Obs e . In es ig. 2013,75, 152–156. [C ossRe ]
19.
Piccioni, M.; Riganelli, L.; Filippi, V.; Fugge a, E.; Colagio anni, V.; Impe iale, L.; Cacce a, J.; Panici, P.B.; Po po a, M.G.
Sonohys e osalpingog aphy: Compa ison o oam and saline solu ion. J. Clin. Ul asound 2016,45, 67–71. [C ossRe ]
20.
Exal o, N.; S assen, M.; Emanuel, M.H. Sa e y aspec s and side-e ec s o ExEm-gel and oam o u e ine ca i y dis ension and
ubal pa ency es ing. Rep od. Biomed. Online 2014,29, 534–540. [C ossRe ] [PubMed]
21.
Luciano, D.E.; Exacous os, C.; Luciano, A.A. Con as Ul asonog aphy o Tubal Pa ency. J. Minim. In asi e Gynecol.
2014
,21,
994–998. [C ossRe ]
22.
Ludwin, I.; Ludwin, A.; Wiechec, M.; Nocun, A.; Banas, T.; Bas a, P.; Pi ynski, K. Accu acy o hys e osalpingo- oam sonog aphy
in compa ison o hys e osalpingo-con as sonog aphy wi h ai /saline and o lapa oscopy wi h dye. Hum. Rep od.
2017
, 1–12.
[C ossRe ]
23.
Exacous os, C.; Tibe io, F.; Szabolcs, B.; Romeo, V.; Romanini, E.; Zupi, E. Can Tubal Flushing wi h Hys e osalpingo-Foam
Sonog aphy (HyFoSy) Media Inc ease Women’s Chances o P egnancy? J. Minim. In asi e Gynecol. 2015,22, S238. [C ossRe ]
24.
Le aillan , J.-M.; Pasquie , M.; Massin, N. A no el concep o emale in e ili y explo a ion: The Fe iliscan
©
, a dedica ed
all-in-one 3D ul asound explo a ion. J. Gynecol. Obs e . Hum. Rep od. 2019,48, 363–367. [C ossRe ] [PubMed]
