PREVALENCE OF POTENTIALLY REVERSIBLE
DEM ENTIAS IN A DEM ENTIA OUTPATIENT
CLINIC OF A TERTIARY UNIVERSITY-AFFILIATED
HOSPITAL IN BRAZIL
Leonel Tadao Takada
1, Paulo Caramelli
2, M arcia Radanovic
3,
Renat o Anghinah
4, Ana Paula B. J. Hart mann
4, Carla Crist ina Guariglia
4,
Valéria Sant oro Bahia
4, Ricardo Nit rini
5ABSTRACT - The im portance of investigating the etiology for dem entia lies in the possibility of treating potentially reversib le d em entias. The aim s of this retrosp ective stud y are to d eterm ine the p revalence of p otentially reversib le d em entias am ong 454 outp atients seen at the Cog nitive and Behavioral Neurolog y Unit, Hosp ital d as Clínicas, São Paulo University School of Med icine - Brazil, b etw een the years of 1991 and 2001, and ob serve their evolution in follow -up . Am ong the initial 454 p atients, 275 fulfilled the DSM-IV criteria for d em entia. Alzheim er´ s d isease w as the m ost freq uent d iag nosis (164 cases; 59.6%). Tw enty-tw o cases (8.0%) of p otentially reversib le d em entia w ere ob served , the m ost freq uent d iag noses b eing neurosyp hilis (nine cases) and hyd rocep halus (six cases). Full recovery w as ob served in tw o p atients and p artial recovery in 10 p atients. Tw o cases w ere not treated and eig ht cases w ere lost on follow -up . The p revalence found in the p resent stud y falls w ithin the rang e rep orted in p revious stud ies (0-30%).
KEY WORDS: d em entia, p revalence, Alzheim er´ s d isease, neurosyp hilis, hyd rocep halus.
Prevalência de dem ências pot encialm ent e reversíveis em am bulat ório especializado de hospit al universitário terciário no Brasil
RESUMO - A im p ortância d e se investig ar a etiolog ia d a d em ência encontra-se na p ossib ilid ad e d e se tratar d em ências p otencialm ente reversíveis. Os ob jetivos d este estud o retrosp ectivo são d eterm inar a p revalência d e d em ências p otencialm ente reversíveis em 454 p acientes atend id os no Grup o d e Neurolog ia Cog nitiva e d o Com p ortam ento d o Hosp ital d as Clínicas d a Faculd ad e d e Med icina d a Universid ad e d e São Paulo entre 1991 e 2001 e ob servar a sua evolução em seg uim ento. Entre os casos iniciais, 275 p reencheram os critérios d e d em ência d o DMS-IV. Doença d e Alzheim er foi o d iag nóstico m ais freq üente (164 casos; 59,6%). Vinte e d ois casos (8,0%) de dem ência potencialm ente reversível foram encontrados, sendo os diagnósticos m ais freqüentes neurossífilis (nove casos) e hid rocefalia (seis casos). Recup eração com p leta ap ós tratam ento foi ob servad a em d ois p acientes e p arcial, em d ez. Dois p acientes não receb eram tratam ento e oito não ad eriram ao seguim ento. A p revalência encontrad a neste estud o situa-se entre as relatad as em estud os anteriores (0-30%).
PALAVRAS-CHAVE: d em ência, p revalência, d oença d e Alzheim er, neurossífilis, hid rocefalia.
Beh avio ral an d Co g n it ive Neu ro lo g y Un it , Dep art m en t o f Neu ro lo g y, Ho sp it al d a Clín icas, Un iversit y o f São Pau lo Sch o o l o f Med icin e (USP) São Pau lo SP, Brazil: 1Un d erg rad u ate Stu d en t, USP; 2Assist an t Pro fesso r, USP; 3Co n su lt an t Neu ro lo g ist , USP; 4Po stg rad u ate Stu d en t, USP; 5Asso ciat e Pro fesso r, USP.
Received 16 Ap ril 2003. Accep t ed 1 Au g u st 2003.
Dr. Leonel Tadao Takada - Rua Dr. M ário Cardim 87 - 04019-000 São Paulo SP - Brazil. E-mail: lt t akada@hot mail.com
Acco rd in g t o Malet t a1, t h e co n cep t o f reversib le
d em en t ias, as it h as b een m o st freq u en t ly u n d ers-to o d , co vers th ree g ro u p s o f d istin ct co n d itio n s. Th e first o n e co n sist s o f d ep ressio n w it h asso ciat ed co g -n it ive im p a irm e -n t , w h ich is o ft e -n re fe rre d t o a s “p seu d o d em en t ia”. Th e seco n d g ro u p co m p risesis m ad e o f co n d it io n s w h ich m o re co m m o n ly cau se acu t e co n fu sio n al st at es o r d eliriu m , su ch as t o xic
t o id en t ify t h e p revalen ce o f p o t en t ially reversib le d em en t ias is t h e lack o f co n sist en t d efin it io n s fo r o f p o t en t ially reversib le cau ses o f d em en t ia acro ssa-m o n g vario u s stu d ies2. Fo r in stan ce, d ep ressio n m ay
h ave b een co n sid ered a t reat ab le d em en t ia in ear-lier st u d ies2-5. Ho w ever, t h isit m ay n o t fu lfill t h e cu
r-ren t crit eria fo r d em en t ia4.
The prevalence of potentially reversible dem entias has p reviously b een rep orted b y several authors, and the results have varied w id ely am ong stud ies2-10. One
of the first studies on potentially reversible dem entias is t h at o f Marsd en & Harriso n11, in w h ich 27 o u t o f
108 p atients p resented p otentially reversib le d em en-t ia s. Cla rfield3, in a n m et a -a n a lysis o f 32 st u d ies,
fo u n d t h at t h e p revalen ce o f p o t en t ially reversib le d em en t ias w as 13.2% (ran g in g fro m 0 t o 32.5%). The m ost freq uent causes found were d rug s, d ep ressio n an d m et ab o lic d ist u rb an ces. Barry an d Mo sko -w it z2 fo u n d t h e p revalen ce o f t reat ab le co n d it io n s
to ran g eran g in g fro m 1.3% to 30%, w h ile review in g 10 studies between the years of 1972 and 1986. Wey-th in g4, in a q u an t it at ive review o f 16 st u d ies p u b
lis-hed b etw een 1972 and 1994, found that 15.2% w as th e p revalen ce o f p o ten tially reversib le cau ses o f d e-m en t ia. Th e e-m o st freq u en t cau ses fo u n d w ere ag ain d ep ressio n an d d ru g in t o xicat io n . Th e p revalen ce o f p o t en t ia lly reversib le d em en t ia s in Bra zil h a s p re-vio u sly b een sh o w n in th ree stu d ies. On e12 in d icated
a p revalen ce o f p o t en t ially reversib le d em en t ias o f 2 3 .6 %. Of t h e se , 2 .7 % h a d p a rt ia lly re ve rsib le d em entia and 1.8% had fully reversed d em entia after t reat m en t o f t h e u n d erlyin g d isease. Th e m o st fre-q u en t cau se o f p o t en t ially reversib le d em en t ia w as lo w seru m vit am in B12 d o sag e. In a p revio u s st u d y within our outp atient unit7, eight out of 100 p atients
p resen t ed p o t en t ially reversib le cau ses o f d em en t ia, w h ich w ere h yd ro cep h alic d em en t ia (six cases, fo u r o f w h ich h ad n o rm al p ressu re h yd ro cep h alu s) an d neuroshyp hilis (two cases). Vale and Mirand a9 found,
am o n g 186 p at ien t s, p o t en t ially reversib le cau ses o f d em en t ia in 32 cases (16 cases o f alco h o lism , 10 cases o f n o rm al p ressu re h yd ro cep h alu s, 4 cases o f n eu ro syp h ilis an d t w o cases o f d ep ressio n ).
Th e im p o rt an ce o f in vest ig at in g p o t en t ially re-versib le d em en t ias an d d et erm in in g it s p revalen ce lies n o t o n ly in t h e o b vio u s o p p o rt u n it y t o lessen o n e´ s co g n it ive im p airm en t b y t reat in g t h e u n d er-lyin g cau se o f su ch a co n d it io n , b u t also in t h e d eci-sio n o f h o w t o in vest ig at e su ch d em en t ias. Given t h at t h e p ret est p ro b ab ilit y o f p o t en t ially reversib le d em en tia is h ig h o r lo w, o n e m u st co n sid er th e co st-benefit of each test and the burden those tests would b rin g t o t h e p at ien t s, sh o u ld a b ro ad er d iag n o st ic
a p p ro a ch t o d e m e n t ia b e u se d , a n d a lso t h e p rob ab ility of the occurrence of false p ositive tests2,4.
The actual reversib ility of p otentially reversib le d e-m en t ias h as b een review ed in st u d ies b y Clarfield3
an d Weyt in g h et al.4 Clarfield3 fo u n d t h at , in 11 st u
-d ies, 11% o f t h e cases o f su ch -d em en t ias sh o w e-d im p ro vem en t aft er t reat m en t (8% w it h p art ial reco -very an d 3 % w it h co m p let e reco -very). Weyt in g h et a l.4, fo u n d p art ial reversal t o ran g e fro m 0 t o 23%
o f d em en t ia cases (averag e 9.3%) an d fu ll reversal ran g in g fro m 0 t o 10% (averag e 1.5%). It w as also o b served t h at p art ially an d fu lly reversed d em en t ia cases h aves fallen o ver t h e p ast few years, an d t h e-refo re au g m en t in g t h e d iscu ssio n o ver an ad eq u at e ap p ro ach t o d em en t ia.
The aim of this study is to ascertain the prevalence o f p o t en t ially reversib le d em en t ias in t h e Beh avio ral an d Co g n it ive Neu ro lo g y Un it fro m t h e d ivisio n o f Ne u ro lo g y, a t t h e Ho sp it a l d a s Clín ica s o f t h e Un iversit y o f São Pau lo Sch o o l o f Med icin e, Brazil (USP), a clin ic d ed icat ed t o p at ien t s w it h co g n it ive im p airm en t , b y ret ro sp ect ively st u d yin g t h e cases o f outp atients seen over ten years’ of exp erience (19912001), as w ell as o b servin g t h e evo lu t io n o f p o t en -t ially reversib le d em en -t ia cases in fo llo w -u p .
M ETHOD
We retrospectively reviewed the files of 454 outpatients co n secu t ively seen co n secu t ively in t h e USP Co g n it ive an d Beh avio u ral Neu ro lo g y Un it o ver t h e p erio d 1991 t o 2001 p erio d .
The p atients´ clinical evaluation includ ed com p lete cli-n ical h ist o ry acli-n d p h ysical/cli-n eu ro lo g ical exam icli-n at io cli-n alo cli-n g with cognitive evaluation. A lab oratory evaluation was also p erfo rm ed an d in clu d ed co m p lete b lo o d co u n t, seru m so -d iu m an -d p o t assiu m , u rea, creat in in e, ch o lest ero l, t ryg li-cerid es, uric acid , calcium , p hosp horus, total p rotein, alb u-m in , g lo b u lin , b iliru b in , alkalin e p h o sp h at ase, γ-g lu t am yl transferase, transam inases concentrations, erythrocyte se-d im en t at io n rat e, seru m t h yro xin e, T3 an d t h yro id st iym u -lat in g h o rm o n e co n cen t rat io n s, seru m VDRL an d FTA-ABS an d co m p u t ed t o m o g rap h y o r m ag n et ic reso n an ce im a-g in a-g o f t h e h ea d . Ot h er t est s w ere p erfo rm ed b a sed o n t h e d ia g n o st ic h yp o t h esis co n sid ered fo r ea ch ca se.
In t ern a t io n a le p o u r la Rech erch e et l´ En seig n em en t en Neu ro scien ces (NINDS-AIREN)15 crit eria o f p ro b ab le an d p o ssib le vascu lar d em en t ia.
Th e crit eria u sed in t h e d iag n o sis o f d em en t ia w it h Lew y b od ies w as that of the consortium on DLB consensus g u id elin es16. Fro n t o t em p o ral d em en t ia w as reach ed fro -m ach ieved as a d iag n o sis b ased o n t h e -m o d ified Lu n d Man ch est er crit eria17. Parkin so n ´ s d isease w it h asso ciat ed d em en t ia w as d iag n o sed w h en p arkin so n ian syn d ro m e w a s m o re, o r a s, evid en t a s t h e d em en t ia syn d ro m e. Th e d iag n o sis o f d ep ressio n w as b ased o n t h e Diag n o st ic an d St at ist ical Man u al o f Men t al Diso rd ers - Fo u rt h Ed it io n13 crit eria o n d ep ressive d iso rd er. Ot h er d iag n o seis w ere m a-d e b asea-d o n u su al crit eria.
Th e o b servat io n o f im p ro vem en t (o r lack o f) in each case w as m ad e b ased o n clin ical im p ressio n w h en d at a w ere availab le. Wh en d at a w ere lackin g , p at ien t s an d /o r fam ilies were contacted b ythrough telep hone and the cog-n it ive o u t co m e w as o b t aicog-n ed fro m b y t h eir im p ressio cog-n s.
Th e an alysis o f t h e d at a o b t ain ed w as m ad e u t ilizin g -t h ro u g h -t h e p ro g ram SPSS fo r Win d o w s versio n 10.0.1.
RESULTS
Two hundred and seventy five patients fulfilled the criteria for the d iagnosis of d em entia. Of these, 79 had already been included in a form er report7. Am ong
the rem aining 179 that d id not have d em entia, d e-p ression was d iagnosed in 31 ind ivid uals.
Alzheim er´ s d isease (AD) was the m ost freq uently est ab lish ed d iag n o sis (Tab le 1). Am o n g t h e 164 ca-ses o f AD, t h e d iag n o sis o f d efin it e AD w as m ad e in four cases. Prob ab le AD w as found in 95 cases, w he-reas 65 cases o f p o ssib le AD w ere en co u n t ered . Th e second m ost freq uent d iag nosis w as that of vascular d em en t ia (VD). Pro b ab le VD w as t h e fin al d iag n o sis in five cases; the other 32 ind ivid uals b eing consid e-red t o b e p o ssib le VD ca ses (h yd ro cep h a lu s w a s fo u n d as a co m o rb id it y in o n e case o f p o ssib le VD). In 20 cases, n o sp ecific et io lo g y fo r d em en t ia co u ld b e est ab lish ed . Ot h er d iag n o seis m ad e are en list ed in Tab le 1.
In t h e p resen t st u d y, n eu ro syp h ilis, h yd ro cep h alu s, alco h o lic d em en t ia, Wern ickeKo rsako ff syn d ro -m e, Wilso n ´ s d isease an d su b d u ral h e-m at o -m a w ere consid ered p otentially reversib le causes of d em entia, t h u s t o t alin g 22 (8.0% o f all cases w it h d em en t ia an d 4.8% o f all p at ien t s seen ) p at ien t s in t h e p o t en -t ially reversib le d em en -t ia g ro u p . Th e -t w o m o s-t fre-q u en t d iag n o ses in t h is g ro u p w ere n eu ro syp h ilis (n in e cases) an d h yd ro cep h alu s (six cases). Hyd ro ce-p h alu s w as also n fo u n d as a co m o rb id it y in 2 cases (1 w it h p o ssib le VD p revio u sly d escrib ed an d o n e w it h n eu ro syp h ilis).
Th e p o t en t ially reversib le d em en t ia g ro u p h as it s d em o g ra p h ica l ch a ra ct erist ics (a g e a n d sch o o lin g
years) list ed in Tab le 2. Th e g en d er d ist rib u t io n w as as fo llo w : t h ree fem ale an d 22 m ale. Tab le 2 are also list sed t h e ch aract erist ics fo u n d fo r t h e irreversib le d e m e n t ia g ro u p , w h ich w a s co m p o se d o f 1 4 7 fem ales an d 105 m ales. Th e g ro u p s w ere d ifferen t co n cern in g o n g en d er (p ~ 0, Ch i-Sq u a re t est ), a s t h ere w ere m o re m a le p a t ien t s in t h e reversib le d em en t ia g ro u p . No st a t ist ica lly sig n ifica n t d ifferen ces w ere fo u n d b et w een t h e g ro u p s w h en sch o o lin g ye a rs w e re co n sid e re d (p = 0 .0 6 5 , Ma n n -Wh it n ey U t est ), b u t a sig n ifica n t d ifferen ce w a s found in ag e b etw een the g roup s (p ~ 0, Mann-Whit-ney U test). The potentially reversible dem entia group h ad a lo w er m ean ag e m ean t h an t h e irreversib le
Table 1. Et iology of dement ia.
Et io lo g y o f Dem en t ia N Percen t ag e (%)
Alzh eim er´ s d isease 164 59.6
Vascu lar d em en t ia 37 13.4
Fro n t o t em p o ral d em en t ia 14 5.1
Neu ro syp h ilis 9 3.3
Dem en t ia w it h Lew y Bo d y 6 2.2
Hyd ro cep h alu s 5 1.8
Parkin so n ´ s d isease 4 1.5
Alco h o lic d em en t ia 3 1.1
Creu t zfeld t -Jako b d isease 3 1.1
Wern icke-Ko rsako ff 3 1.1
Hu n t in g t o n ´ s d isease 2 0.7
Wilso n ´ s d isease 1 0.4
Dem en t ia d u e t o h ead t rau m a 1 0.4
Su b d u ral h em at o m a 1 0.4
Mu lt ip le Syst em At ro p h y 1 0.4 Pro g ressive su p ran u clear p alsy 1 0.4
Un d et erm in ed 20 7.3
To t al 275 100
Table 2. Comparison betw een groups for age and schooling years.
Po t en t ially reversib le Irreversib le d em en t ias d em en t ias
Ag e 53.86 (SD 13.97) 68.95 (SD 9.66)
d em en t ia g ro u p . Th ere w ere 23 illit era t es in t h e irreversib le d em en t ia g ro u p an d o n e illit erat e in t h e p o t en t ially reversib le d em en t ia g ro u p .
Am o n g t h e p at ien t s in t h e p o t en t ially reversib le d em en t ia g ro u p , fu ll reco very w as o b served in t w o p at ien t s (o n e d iag n o sed w it h n eu ro syp h ilis an d t h e o t h er, w it h h yd ro cep h alu s) aft er p ro p er t reat m en t . Part ial reco very w as t reat m en t ´ s o u t co m e o f t reat -m ent in 10 p atients (nine w ith neurosyp hilis and one with sub d ural hem atom a). In two ind ivid uals (one with alcoholic d em entia and the other with hyd roce-phalus) specific treatm ent for the etiology of dem entia was not ind icated , and in follow up they were cog-nitively stab le. Eight cases were lost on follow-up .
DISCUSSION
The prevalence of potentially reversible dem entias in t h is sam p le, at 8%, is sim ilar t o t h e o n e fo u n d in a p revio u s st u d y b y o u r g ro u p7. A rem ark sh o u ld b e
m ad e reg ard in g t h e fact t h at , in co n t rast t o t h e p resen t st u d y, t h e p revio u s st u d y h ad n o d id n o t in clu -d e o n e cases o f alco h o lism (o u t o f o n e h u n -d re-d ) as a reversib le et io lo g y fo r d em en t ia., o p p o sed t o t h is o n e. Alco h o lic d em en t ia h as b een a su b ject o f d is-cu ssio n as t o it s act u al reversib ilit y18. In sp it e o f t h is,
it could fit within the concept of potentially reversible cau ses o f d em en t ia, an d t h erefo re it w as in clu d ed in t h is st u d y. Th e resu lt s o b t ain ed in t h is art icle are also co n sist en t w it h t h e p revalen ce ran g e fo r p o t en t ially reversib le d em en t ias assessed b y p revio u s st u -d ies18,19, b et w een 0 an d 30%.
The m ost frequent diagnoses for potentially rever-sib le cases w ere n eu ro syp h ilis an d h yd ro cep h alu s. In p ast st u d ies2-4 d ep ressio n an d d ru g in t o xicat io n
w ere t h e m o st freq u en t d iag n o ses fo r su ch cases. No n et h eless, d ep ressio n w as n o t co n sid ered a re-versib le d em en t ia in t h is st u d y. A p revalen ce st u d y b a sed o n a t ert ia ry h o sp it a l d em en t ia o u t p a t ien t clin ic p o p u lat io n is su b ject t o a select io n b ias, w h ich is b asically a co n seq u en ce o f t h e lo cal h ealt h syst em st ru ct u re an d t h e co m m u n it y fro m w h ich t h e cases are d raw n , an d t h erefo re, t h is kin d o f st u d y is a u n iq u e reflectio n o f th e g ro u p s´ exp erien ce. Fo r in stan -ce, n eu ro syp h ilis w as fo u n d t o b e t h e m o st freq u en t et io lo g y fo r p o t en t ially reversib le d em en t ia in t h is p articu lar stu d y. Ho w ever, th is d iag n o sis h asw as n o t been observed in previous series, including other Bra-zilian p revalen ce st u d ies9,12. Th is n o tw ith stan d in g ,
p revalence stud ies such as the p resent, p rove im p or-t an ce n o or-t o n ly fo r or-t h e reaso n s p revio u sly rep o ror-t ed , b ut also for contrib uting tow ard s estab lishing a g ro-u n d fo r ep id em io lo g ical d at a reg ard in g p o t en t ially
reversib le d em entias ins am ong developing countries, from which data rem ain are still scarce, It has been suggested that there is a higher prevalence of poten-tially reversible dem entias am ong individuals aged less t h an 65 years20. In d eed , in t h e p resen t st u d y a sig n
i-ficant d ifference in ag e d istrib ution b etw een the p o-t en o-t ially reversible dem eno-tia group (which had lower m edian for age) and the irreversible dem entia group was found. This finding could signify that some poten-tially reversible cases of dementia, such as neurosyphilis, are more prevalent among a younger population, while primary dementias such as AD haves a progressively higher incidence, the older the population is21.
Alzh eim er´ s d isease w as th e m o st freq u en t d iag -n o sis fo r t h e d em e-n t ia sy-n d ro m e i-n t h e sam p le h ere co n sid ered h ere. Th e p revalen ce fo u n d o f 59.6% is also co n sist en t w it h p revio u s series. Marsd en & Har-riso n11 d escrib ed a p revalen ce o f p resu m ed AD o f
57.1%. Nit rin i et al7 rep o rt ed 54% o f AD d iag n o sis
in 100 o u t p at ien t s, as w ell as 20% o f p revalen ce fo r vascu lar d em en t ia. Clarfield3, review in g 32 st u d ies
that investigated the p revalence of d em entias, found out that Alzheim er´ s disease was diagnosed in 56.8% o f t h e cases, w h ile. Am es et al.6 h ad 59 o u t o f 100
cases d iag n o sed w it h AD.
Am o n g p at ien t s w it h p o t en t ially reversib le d e-m en t ias, t w o h ad a fu ll reco very an d 10 h ad p art ial reco very aft er t reat m en t , rep resen t in g 9% w it h fu ll reco very an d 45.4% w it h p art ial reco very. Co n sid e-rin g t h e d at a d iscu ssed ab o ve, t h ese fin d in g s d o n o t lie within the range found in p revious stud ies. It m ust b e t aken in t o acco u n t t h at in t h e p resen t sam p le, u n like o t h er st u d ies, n eu ro syp h ilis w as t h e m o st freq u en t d iag n o sis am o n g p o t en t ially reversib le cau -ses o f d em en t ia (as w ell as t h e lead in g d iag n o sis am o n g p at ien t s in w h ich fu ll o r p art ial reco very w as ob served ), which could p rovid eb e an exp lanation for t h e d iscrep an cy fo u n d h ere.
Th e p re va le n ce o f n e u ro syp h ilis ca se s fo u n d , sh o u ld also p o in t o u t t h e im p o rt an ce o f syp h ilis sero lo g y as o n e o fam o n g t h e t est s t h at sh o u ld b e in -clu d ed in t h e lab o rat o ry evalu at io n o f d em en t ia. Al-t h o u g h iAl-t s p revalen ce h as fallen o ver Al-t h e p asAl-t years, n eu ro ssyp h ilis is st ill a relevan t cau se fo r p o t en t ially reversib le d em en t ia, as it can b e o b served fro m t h e resu lt s o f t h is st u d y, an d sh o u ld n o t b e o verlo o ked as a d iag n o sis, esp ecially in am o n g p o p u lat io n s o f d evelo p in g co u n t ries p o p u lat io n s.
res-sio n in a d em en t ia o u t p at ien t clin ic is en h an ced b y t h e fact t h at it h as b een p ro p o sed22 t h at p at ien t s
su fferin g fro m d ep ressio n alo n g w it h a co exist in g co g n it ive im p a irm en t (“reversib le d em en t ia ”), a re m o re p ro n e t o d evelo p in g irreversib le d em en t ia o n fo llo w -u p , t h an p at ien t s w it h d ep ressio n alo n e. Ac-co rd in g ly, t h is p o p u la t io n w a rra n t s a n a t t e n t ive fo llo w -u p .
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