J Bras Pneumol . 20 06 ;3 2(5):4 89 - 9 4
Prognostic factors for complications following pulmonary
resection: pre- albumin analysis, time on mechanical
ventilation, and other factors*
RENATA CRI STI ANE GENNARI BI ANCHI1, JULI ANA NALI N DE SOUZA2, CAROLINA DE ALM EI DA GI ACI ANI2, NEUCY FENALTI HÖEHR3, IVAN FELI ZARDO CONTRERA TORO4
*St u dy con du ct ed at t he Universidade Est adu al de Campinas (UNICAM P, St at e Universit y at Campinas) Hospit al de Clínicas -Cam pin as, Brazil.
1. M ast ers f rom t he Depart men t of Surgery of t he Universidade Est adual de Campinas (UNICAM P, St at e Universit y at Campinas) School of M edical Scien ces - Campinas, Brazil; Prof essor of Physical Therapy at t he São João da Boa Vist a Cen t ro Un iversit ário das Facu ldades Associadas de En sino (UNIFAE, Associat ed Schools of Learn in g Universit y Cent er) - São João da Boa Vist a, Brazil
2. Physical Therapist an d special M ast ers st u den t in t he Depart m en t of Su rgery of t he Un iversidade Est adu al de Cam pinas (UNICAM P, St at e Un iversit y at Cam pin as) School of M edical Scien ces - Cam pinas, Brazil
3. Prof essor in t he Clin ical Pat hology Depart ment of t he Universidade Est adual de Cam pin as (UNICAM P, St at e Un iversit y at Campin as) School of M edical Sciences - Cam pinas, Brazil
4. Head of t he Thoracic Su rgery Division of t he Depart men t of Surgery of t he Universidade Est adual de Campinas (UNICAM P, St at e Universit y at Campin as) School of M edical Sciences - Campinas, Brazil
Corresponden ce t o: Ren at a Crist ian e Gen nari Bian chi. Ru a Agost inho Pires de Agu iar, 610, apt 5, Bairro São Lázaro - CEP: 13870- 480, São João da Boa Vist a, SP, Brasil. Tel: 55 19 3631- 7116. Email: bian chirenat a@ hot mail.com
Submit t ed: 6 Oct ober, 2005. Approved, af t er review: 3 M arch, 2006.
ABSTRACT
Objective: To determine whether pre- operative nutritional status and post- operative time on mechanical ventilation, as well as others factors, are correlated with post- operative complications (general or pulmonary) in patients undergoing
elect ive thoracic surgery. M ethods: A prospective st udy was conducted, involving 71 pat ients undergoing elective
pulmonary resection. The data collected pre- operatively included gender, age, smoking status, pre- albumin level, lymphocyte count, and body mass index. The peri- operative data included type of surgery and surgical time, as well as post- operative
time on mechanical ventilation.Results: Post- operative complications were found to correlate with low pre- albumin
concentration, type of resection, surgical time, and post- operative time on mechanical ventilation. Surgical time and post- operative time on mechanical ventilation were also implicated in the post- operative pulmonary complications
observed in 22 (30.99%) of the patients studied.Conclusion: Our results suggest that pre- albumin concentration, type
of surgery and surgical time, as well as operative time on mechanical ventilation, serve as predictive indices of post-operative complicat ions in patient s undergoing elective pulmonary resect ion. In the analysis of the post- post-operative pulmonary complications, statistically significant correlations were found between such complications and increases in surgical time or post- operative time on mechanical ventilation.
INTRODUCTION
When a pat ient is submit t ed t o surgery under general anest hesia, t here is a cert ain impact on p u l m o n ary f u n ct i o n , even i f t h e su r g er y i s ext rat horacic. This impact is undoubt edly great er in t horacic surgery, which can lead t o signif icant post - operat ive complicat ions (POCs).(1)
A prolonged anest hesia period, t he locat ion of t he incision , hypercapni a, severe dyspnea and advanced age accompanied by a long hist ory of cardiopulmonary illness are also considered risk f act ors f or post - operat ive pulmonary complicat ions (POPCs),(2)as are smoking, obesit y and abnormal
blood gas/ spiromet ry values.(3)Awareness of pat ient
nut rit ional st at us is crucial t o t he post - operat ive assessment since malnut rit ion implies great er int ra-operat ive and post - ra-operat ive risks.(4)General body
measurement s, such as weight and height , are easily assessed and can provide valuable inf ormat ion regarding nut rit ional st at us.(4)There also seems t o
be a correlat ion bet ween visceral prot ein def iciencies and morbidit y.(5)Laborat ory t est ing f or nut rit ional
st at u s v ar i ab l es,(5 ) u si n g m et h o d s su ch as
det ermining t he pre- albumin levels and perf orming lymphocyt e count s, can also be import ant .
St udies have shown t hat mechanical vent ilat ion (MV) and surgical t ime inf luence POCs. To maint ain respirat ory f unct ion during surgical int ervent ions, M V is ext ensively used during, and in some cases af t er, anest hesia. However, prolonged use of MV can lead t o POCs. Despit e being considered a support m et ho d, M V can ei t h er red u ce or aggr avat e pulmonary injury. High peak inspirat ory pressure val u es r esu l t i n p u l m o n ar y ed em a, al veol ar dest ruct ion, surf act ant dysf unct ion and deat h.(6)It
is est imat ed t hat POPCs account f or 24% of all deat hs occurring wit hin t he f ist six post - operat ive d ays.(7) Co n cep t u al l y, POPCs are def i n ed as
pulmonary abnormalit ies t hat occur during the post -operat ive period and produce an ident if iable disease or clinically significant dysf unct ions that unfavorably af f ect t he clinical evolut ion.(8) The predominant
POPCs are at el ect asi s an d pn eu m on i a.(9- 1 0) I n
addit ion, t he patient might present acut e respirat ory f ai l u r e, acu t e resp i r at o ry d i st r ess syn dr om e, pulmonary embolism or bronchopleural f ist ula.
The obj ect i ve of t hi s st u dy w as t o assess nut rit ional indices such as pre- albumin levels and lymphocyt e count s, as well as surgical t ime and t ime
on M V, in order t o charact erize t he inf luence of t hese f act ors on post - operat ive morbidit y.
M ETHODS
A prospect ive cohort st udy was conduct ed f rom M ay of 2002 t o Oct ober of 2003 in t he Thoracic Surgery Depart ment of t he Campinas St at e Universit y Hospit al de Clínicas.
A t otal of 71 consecutive pat ients, of both genders, submit t ed t o pulmonary resect ion met t he inclusion crit eria and comprised t he st udy sample. During t he dat a collect ion period, no modif icat ions t hat might int erf ere wit h pat ient post - operat ive evolut ion were made t o the basic int ra- operative treatment prot ocols. The f ollowing inclusion crit eria were applied: undergoing elect ive pulmonary resect ion surgery (p n eu m o n ect o m y, l o b ect o m y, b i l o b ect o m y, segment ect omy or nodulect omy); being 18 years of age or older; and giving writ t en inf ormed consent .
Pat ient s who died during t he int ra- operat ive period were excluded f rom t he analysis.
The st udy design was approved by t he Et hics Commit t ee of t he Campinas St at e Universit y School of M edicine (Opinion no., 231/ 2002).
The f ollowing pre- operat ive dat a were gat hered f rom pat ient medical chart s: gender; age; working diagnosis; smoking st at us; pre- albumin values and lymphocyt e count s (up to f ive days prior t o surgery); body mass index (BMI); and correlat ed morbidit ies, su ch as d i ab et es m el l i t u s, syst em i c ar t er i al hypert ension and alcoholism. All pat ient s underwent anest hesia administ ered by t he same team, using the same anest het ic met hods and involving select ive ventilation.
The following int ra- operat ive dat a were collected: Type and t ime (in hours) of t horacic surgery; t ype of su rgi cal i n ci si on; an d com pli cat i on s, su ch as hemorrhage, hypot ension or deat h.
J Bras Pneumol . 20 06 ;3 2(5):4 89 - 9 4
In order t o describe t he sample prof ile according t o t he man y variables u nder st udy, descript ive st at ist ical t ables of t he cont inuous variables were prepared, as were t ables describing t he f requency of t he cat egori cal variabl es. For t he pu rposes of comparing POCs and POPCs in t erms of cat egorical variables, t he chi- square t est or, when necessary, Fisher's exact t est , was used. To compare POCs and POPCs in t erms of cont inuous variables, t he Mann-Whit ney non- paramet ric t est , which compares t he observat ion post s, was used. In order t o det ermine which f act ors inf luenced pulmonary complicat ions, logist ic regression was used via univariat e analysis, t oget her wit h st epwise mult ivariat e analysis.(12- 13) A signif icance level of 5% (i.e., p < 0.05) was adopted.
RESULTS
A t ot al of 63 pat ient s were diagnosed wit h pulmonary neoplasia, whereas 8 were diagnosed wit h pulmonary mycetoma. There were 44 males (61.97%). Ages ranged from 19 t o 77 years of age, with a mean of 55.69 years. Of t he 71 pat ient s evaluat ed, 24 (3 3 .8 % ) w er e sm o k er s, 2 6 ( 3 6 .6 2 % ) w er e nonsmokers, and 21 (29.58%) were f ormer smokers. The types of pulmonary resection were bilobectomy in 3 pat ient s (4.23%), lobect omy in 35 (49.3%), nodulectomy in 13 (18.31%), pneumonectomy in 14 (19.72%) and segmentectomy in 6 (8.45%). lobectomia eTypes of surgery were grouped as f ollows: lobect omy and bilobectomy; nodulectomy plus segment ectomy; and pneumonectomy.
In t he present st udy, t here was no st at ist ical signif icance f or t he occurrence of POCs or POPCs based on age or lymphocyt e count .
A t ot al of 28 pat ient s (39.44%) present ed POCs, whereas 22 (30.99%) present ed POPCs.
The present st udy compared POCs and POPCs in t erms of cat egorical variables (gender, smoking status
and t ype of surgery). Comparisons were also made in t erms of general int ra- operat ive complicat ions, int operat ive respirat ory complicat ions and int ra-operat i ve hemodyn am i c com pl i cat i on s. These variables (POCs and POPCs) were also compared wit h con t i n u ou s vari abl es (age, pre- al bum i n l evel , lymphocyt e count , surgical t ime, t ime on MV and BMI).
In ref erence t o t ime on M V, 63 pat ient s were ext u bat ed in t he operat i ng room , and 6 were ext ubat ed in t he int ensive care unit . For 2 pat ient s, it was not possible t o det ermine t he moment of ext ubat ion. The t ype of surgery was f ound t o have st at ist ical signif icance in t he comparison among t he POCs: pneumonect omy, lobect omy, bilobect omy, nodulect omy and segment ect omy (p = 0.01 f or all). There were also st at ist ically signif icant correlat ions f or t he f ollowing: POCs wit h surgical t ime (p = 0.004), POCs wit h t ime on M V (p = 0.01) and POCs wit h pre- albumin level (p = 0.009); POPCs wit h surgical t ime (p = 0.003); and POPCs wit h t ime on M V (p = 0.04). The remaining result s (f or gender, smoking st at us, BMI, int ra- operat ive complicat ions, int operat ive respirat ory complicat ions and int ra-operat ive hemodynamic complicat ions) were not st at ist ically signif icant . Tables 1 and 2 show t he most important result s, whereas Tables 3 and 4 show t he logist ic regression f or POCs and POPCs.
DISCUSSION
The majorit y of t he st udied pat ient s underwent resect ion of t he pulmonary parenchyma due t o neoplasia. According t o some aut hors,(14)lung cancer
is t he leading cause of deat h f rom cancer, f or men and women, in t he USA, despit e t he fact t hat surgical resect ion of f ers a bet t er chance f or cure in pat ient s wit h non- small cell lung cancer.
The POPC incidence f ollowing t horacot omy
TABLE 1
Principle variables with statistical significance for post- operative complications
Var iables Surgi cal t ime Tim e on M V Pre- albumin
(hours: minut es) (hours:minut es) (mg/ dl)
Pat ient s wi t h POCs (n) 28 28 21
M ean 4:15 h 8:55 h 11,37 mg/ dl
Pat ient s wit hout POCs (n) 38 38 27
M ean 3:30 h 4:52 h 15,86 mg/ dl
p 0,004 0,01 0,009
J Bras Pneumol . 20 06 ;3 2(6):4 89 - 9 4
accompanied by pulmonary resect ion st ands at approximat ely 30%. It has been report ed t hat t his occurs not only due t o t he removal of pulmonary t issue, but also as a result of an alt erat ion in t he nut rit ional st at us, as well as of alt erat ions in t he chest - wall mechanics, of t he t horacot omy it self , of t he anest hesia and of t he M V.(15) The nut rit ional
indices used herein were chosen due t o t heir ease
of applicat ion and low cost , as well as t o t he f act t hat t hey are considered sat isf act ory predict ors of post - operat ive morbidit y. This can be observed in t he current st udy, in which POPCs occurred at a rat e of 30.99%, compared wit h 39.44% f or POCs.
The highest rat e of respirat ory complications was associat ed wit h longer surgical t imes. According t o some aut hors,(16)t he most common post - operat ive
complicat ion f ollowing operat ions last ing over f our hours is pneumonia, regardless of which lung is af f ect ed.
Various ot her aut hors have conf irmed t hat being over t he age of 70 represent s an independent risk f act or f or pulmonary resect ion.(17)In cont rast , ot her
aut hors(18)have arrived at t he conclusion t hat , f or
malignant diseases in elderly pat ient s, pulmonary resect ion is benef icial. St ill ot her aut hors,(19) have
st at ed t hat elderly pat ient s present ing good general healt h st at us do not display an increased number of POCs and should t heref ore not be excluded f rom surgery exclusively on t he grounds of age. In t he present study, patient age was not predictive of POCs. We also f ound t hat smoking st at us had no inf luence on POCs, alt hough t he lit erat ure shows
TABLE 2
Principal variables of statistical significance for post- operative pulmonary complications
Var iables Su rgical t ime Ti me on M V
(hours:minut es) (hour s:minut es)
Pat ient s wit h POPCs (n) 22 22
M ean 4:26 h 6:25 h
Pat ient s wit hout POPCs (n) 44 44
M ean 3:35 h 6:22 h
p 0,003 0,04
POPC: post - operat ive pulmonary compl icat ions; M V: mechanical vent ilat ion
TABLE 3
Significant variables in the univariat e analysis of post- operative complications and post- operative
pulmonary complications
Post- operative complications
Var iabl e 95% CI p OR
Pre- albumin (0.988- 0.803) 0.0292 0.891
Type of surgery (23.515- 1.374) 0.0165 5.684
Surgical t ime (2.967- 1.160) 0.0099 1.855
Post- operative pulmonary complications
Variable 95% CI p OR
Surgical t ime (3.206- 1.181) 0.009 01.946
95% CI: 95% conf idence i nt erval; OR: odds rat io
TABLE 4
Significant variables in the univariate analysis of post- operative complications and post- operative pulmonary complications
Post- operative complications
Var iabl e 95% CI Est imat e EP chi- square p OR
Pre- albumin (0.680- 0.949) - 0.2194 0.0852 6.6381 0.0100 0.803
Lymphocytes (1.014- 2.059) 0.3681 0.1807 4.1486 0.0417 1.445
Surgical t ime (1.163- 5.348) 0.9138 0.3892 5.5120 0.0189 2.494
Post- operative pulmonary complications
Var iabl e 95% CI Est imat e EP chi- square p OR
Surgical t ime (1.181- 3.206) 0.6655 0.2549 6.8192 0.0090 1.946
95% CI: conf idence int erval; SE: st andard error; OR: odds rat io
J Bras Pneumol . 20 06 ;3 2(5):4 89 - 9 4
t hat smokers are at great er risk f or developing POPCs.(20)
Our result s show t hat t here was a st at ist ically si gn i f i can t corr el at i on b et w een pr e- al b u m i n alt erat ions and POCs, as evidenced by t he f inding t hat 43.75% of t he pat ient s present ing POCs had low levels of pre- albumin. Such correlat ions have also been report ed in t he lit erat ure,(21)underscoring
t he import ance of assessing pre- albumin levels. In addi t ion, t he lit erat ure demon st rat es t hat pre-albumin is t he first serum protein t o be alt ered under acut e malnut ri t ion condit ions and is t he most sensit ive in t erms of ret urning t o it s normal level f ollowing nut ritional supplement at ion. The object ive of det ermining pre- albumin levels is t o indirect ly measure visceral prot ein mass. Pre- albumin present s quit e a small body reserve and a short half - lif e (of approximat ely t wo days).(22)Theref ore, one must be
caref u l w hen i n t erp ret i n g i t s l evel s p ri o r t o co n f i r m i n g a d i ag n o si s o f p r o t ei n - cal o r i e mal nut ri t ion, since hepat ic produ ct ion of pre-albumin drops in response t o systemic inflammation, such as t hat seen in t rauma or sepsis, t he end result being t hat serum pre- albumin levels f all rapidly.(21)
Due t o t hese charact erist ics, cert ain aut hors(23)
consider t his prot ein t he best nut rit ional assessment paramet er.
Various st udies have demonstrat ed a relationship bet ween POCs and low lymphocyt e count s. In order t o complement t he assessment of pat ient s wit h suspect ed prot ein- calorie malnut rit ion, one must det ermine serum prot eins such as pre- albumin, f urt her t o assessing t he number of lymphocyt es.(21)
In t he present st udy, lymphocyt e count was not suf f icient ly sensit ive t o predict POCs, a f inding t hat cont radict s t hose of t he art icles cit ed. However, pre-albumin level proved t o be a nut rit ional index t hat is predict ive of POCs, alt hough not specif ically predict ive of POPCs.
Li f e expect an cy is low er in obese pat i ent s, alt hough surgical mort alit y rat es are not higher.(24)
However, obese pat ient s are at great er risk f or pulmonary complicat ions.(24) Nevert heless, in t he
present st udy, BMI, which charact erizes obesit y, did not prove suf f icient ly sensit ive t o predict POPCs.
The t ype of surgery paramet er was an ef f ect ive predict or of POCs but not of POPCs. According t o some aut hors,(17)t he mort alit y rat e among pat ient s
undergoing pneumonect omy is t ypically t wice as high as t hat among t hose undergoing lobect omy.
In addit ion, segment ect omy or nodulect omy carry t he lowest risks, and pneumonect omy carries t he highest risk. Theref ore, t here is a clear relat ionship bet ween t he ext ent of resect ion and post - operat ive morbidit y/mort alit y.(19)
A gamut of adverse ef f ect s and complicat ions are associat ed wit h M V. These complicat ions occur wit h great f requency and yet are not f requent ly report ed in lit erat ure. The pot ent ial adverse ef f ect s include a decrease in t he cardiac index, respirat ory alkalosis, increased int racranial pressure and gast ric dist en si on. Compl icat i on s t hat are exclu sivel y respirat ory, such as pneumot horax, bronchopleural f ist u la an d n osocom i al pn eu moni a, can ari se. Complicat ions can also result f rom inappropriat e handling of t he mechanical vent ilat or, such as t he use of incorrect set t ings or not heat ing/ humidif ying t he inspired air.(25)
In a ret rospect ive analysis of t he incidence of int ra- operat ive and immediat e POCs, 65 pat ient s wit h pulmonary emphysema and submit t ed t o lung t ransplant were evaluat ed. The conclusion t hat t ime on MV > 48 hours and post - operat ive hemorrhage were t he variables t hat best indicat ed deat h during t he immediat e post - operat ive period.(26)
Some aut hors perf ormed a ret rospect ive st udy of 508 pat ient s undergoing gast roduodenal surgery, wit h t he purpose of invest igat ing risk f act ors f or POPCs. The conclusion was t hat t he int ra- operat ive/ post - operat ive t ime on M V cont ribut ed t o t he development of t hese complicat ions.(27)
In t he current st udy, t he int ra- operat ive t ime on MV correlat ed signif icant ly wit h POCs (28 pat ient s; p = 0.0198), as well as wit h POPCs (22 pat ient s; p = 0.0491). Alt hough our result s suggest t hat t here is a relat ionship bet ween t ime on M V and POCs, t here i s st il l a short age of st udi es in t he li t erat ure evaluat ing POCs in relat ion t o t i me on M V in pulmonary resect ions. Theref ore, more st udies are n eeded t o det ermi n e w het her a l on ger i n t ra-operat ive t ime on M V result s in POCs.
ACKNOWLEDGMENTS
REFERENCES
1 . M irra AP, Just o FA. Part icularidades da ciru rgia pulm onar. In : Jorge Filho I, Andrade JI de, Ziliot t o Ju nior A, edit ores. Cirurgia geral: pré e pós- operat ório. São Paulo: At heneu; 19 95 . p.60 5.
2 . Jackson CV. Preoperat ive pulmonary evaluat ion. Arch Int ern M ed. 1988;148(10):2120- 7. Comment in: Arch Int ern M ed. 19 90; 15 0(5 ): 111 6.
3 . Tray n er E Jr, Cel l i BR. Po st o p erat i ve p u l m o n ar y com plicat ions. M ed Clin Nort h Am . 2001;85(5):1129- 39. 4 . Jo rg e Fi l h o I , Basi l e Fi l h o A, M ad u r ei ra Fi l h o D . Avaliação n u t ricion al. In : Jorge Filho I, An drade JI de, Zi li ot t o Ju n i or A, edit ores. Ciru rg ia g eral: p ré e pó s-op erat ório. São Pau l o: At hen eu ; 19 95. p.28- 9. 5 . Bryan t LR, M organ Ju n ior CV. Parede t orácica, pleu ra,
pu lm ão e m ediast in o. In : Schw art z SI, edit or. Prin cípios de ciru rgia. 4a ed. Rio de Jan eiro: Gu an abara Koogan . 1 9 8 5 . p .6 8 5 - 9 .
6 Halbert sma FJ, Vaneker M, Schef f er GJ, van der Hoeven JG. Cytokines and biot rauma in vent ilat or-induced lung injury: a cri t i cal revi ew o f t h e l i t erat u re. Net h J M ed . 2005; 63(10): 382- 92.
7 . Pierson DJ, Bran son RD. Prof essor's rou nds in respirat ory car e: p r ev en t i o n o f p o st o p erat i v e at el ect asi s an d pn eu m on i a [ vi deoco n f eren ce] . Irvin g, Texas: Am eri can Associat ion f or Respirat ory Care; Novem ber 17, 1992. 8 . O'Donohue WJ Jr. Post operat ive pulmonary complicat ions.
When are prevent ive and t herapeut ic measures necessary? Post grad M ed. 1992; 91(3): 167- 70, 173- 5.
9 . Peper EA, Conrad SA. Respirat ory com plicat ions of su rgery an d t horacic t rauma. In : George R, Light R, M at t hay M , M at t h ay R, ed i t o r s. Ch est m ed i ci n e: essen t i al s o f pu lmonary and crit ical care m edicin e. Balt im ore: Williams
& Wilkins; 1990. p.453- 73.
1 0 . Pesola G, Nashaa E, Kvet an V. Pu lmonary complicat ions an d respirat ory t herapy. In : Frost E, Goldin er P, Bryan -Br o w n C, ed i t o rs. Po st an est h et i c care. N o r w al k , Conn ect icu t : Applet on Lan ge; 1990. p.63- 79.
11 . Schu lak JA. Com plicações cirú rgicas. In : Sabist on Ju n ior DC, Lyerly HK, edit ores. Fu n dam en t os de ciru rgia. 2a ed. Rio de Jan eiro, Gu an abara Koogan ; 1996. p.116- 8. 1 2 . Fonseca JS, M art in s GA. Cu rso de est at íst ica. 5aed. São
Pau lo: At las. 1994.
1 3 . Hosmer DL, Lem eshow S. Applied logist ic regression. New York: John Wiley Sons; 1989.
1 4 . Borin g CC, Squ ires TS, Ton g T, M on t gom ery S. Can cer st at i st ics, 1 99 4. CA Can cer J Clin . 1 99 4; 4 4(1 ): 7- 2 6. 15. Wang J, Ult m an R, Olak J. Prospect ive t rial of dif f u sing
capacit y an d oxygen con su mpt ion in t he predict ion of
p u l m o n ary co m p li cat i o n s af t er l u n g resect io n . Chest . 1 99 7; 11 2: 15 3S.
1 6 . Garibaldi RA, Brit t M R, Coleman M L, Readin g JC, Pace NL. Risk f act ors f or post operat ive pneumonia. Am J M ed. 1 981; 7 0(3): 6 7 7- 80 .
1 7 . Bolliger CT, Perruchoud AP. Fu nct ion al evaluat ion of t he lu ng resect ion can didat e. Eu r Respir J. 1998; 11(1): 198-2 1 198-2 .
1 8 . Berggren H, Ekroth R, Malmberg R, Naucler J, William- Olsson G. Hospit al mort alit y and long- t erm survival in relat ion t o preoperative f unct ion in elderly patients wit h bronchogenic carcinom a. Ann Thorac Surg. 1984;38(6):633- 6.
1 9 . Damhuis RA, Schut t e PR. Resect ion rat es and post operat ive mort alit y in 7,899 pat ient s wit h lung cancer. Eur Respir J. 1996 ; 9(1): 7 - 10.
2 0 . N a k a g a w a M , Ta n a k a H , Tsu k u m a H , K i sh i Y. Relat ion ship b et w een t he du rat ion of t he preoperat ive sm oke- f ree period an d t he in ci den ce of post operat i ve p u l m o n ary co m p l i cat i o n s af t er p u l m o n ary su rg ery. Ch est . 2 0 01 ; 1 2 0 (3 ): 7 0 5 - 1 0 . Co m m en t i n : Ch est . 2 0 0 5 ; 1 2 7 (6 ): 1 8 7 3 - 5 .
2 1 . Ju n qu eira JC do s S. Fat ores de risco n u t rici on ai s n as co m p l i caçõ es p ó s- o p er at ó ri as em p aci en t es i d o so s su b m et i do s à ci ru rg ia el et i va d e g ran d e p ort e.[ t ese] . Cam p in as: Un iversid ad e Est adu al de Cam pin as. 2 00 2. 2 2 . Sullivan DH. What do t he serum prot eins t ell us about our el d erl y p at i en t s? J Gero n t o l A Bi o l Sci M ed Sci . 2001;56(2):M 71- 4. Comment on: J Gerontol A Biol Sci Med Sci. 2001;56(2): M 79- 82.
2 3 . M easu rem en t o f vi sceral p ro t ei n st at u s i n assessi n g p ro t ei n an d en er g y m al n u t ri t i o n : st an d ar d o f care. Pr eal b u m i n i n Nu t r i t i o n al Car e Co n sen su s Gr o u p . Nu t rit i o n . 1 9 95 ; 11 (2 ): 1 69 - 71 .
2 4 . Doyle RL. Assessing and modif ying t he risk of post operat ive pulmonary complicat ions. Chest . 1999;115(5 Su ppl):77S-81S.
2 5 . Pi erso n DJ. Com pl icat ion s associat ed w i t h m ech an ical vent ilat ion . Crit Care Clin . 1990; 6(3): 711- 24.
2 6 . M ayo- M ol des M , Vi llalai n - Perez C, Vicen t e- Gu ill en R, Ram os- Bri o n es F, Cal vo - M ed i n a V, M o rales- M arin P, e t a l . [ L u n g t r a n sp l a n t at i o n f o r e m p h y sem a : ret ro sp ect i ve st u d y o f 6 5 p at i en t s] M ed Cl in (Barc). 20 05; 125 (16 ): 618- 21. Sp an ish. Com m en t i n : M ed Cl in (Barc). 2 0 0 5 ; 1 2 5 (1 6 ): 61 6 - 7 .
